Published in the United States of America
2022 * VOLUME 16 « NUMBER 2
AMPHIBIAN & REPTILE
CONSERVATION
amphibian-reptile-conservation.org
ISSN: 1083-446X eISSN: 1525-9153
Front cover: Black-webbed Treefrog (Rhacophorus kio Ohler & Delorme 2006), male, Xuan Nha Nature Reserve, Son La Province, Vietnam.
This frog is known to occur in China, Myanmar, Thailand, and Vietnam (Frost 2022). It is categorized as Endangered (EN) by the Vietnam Red
Data Book (2007). The Black-webbed Treefrog is a threatened species in Vietnam due to habitat degradation and severe habitat fragmentation.
This species was found at night, on trees, and near puddles in the evergreen forests. Photo by Anh Van Pha.
Introductory page. Smilisca cyanosticta (Smith, 1953). The Blue-spotted Treefrog occurs on the Atlantic slopes of
southern Mexico and northern Central America from Oaxaca and southern Veracruz through northern Chiapas, Mexico,
into Guatemala (https://amphibiansoftheworld.amnh.org). These individuals were located at Ejido Villa Guadalupe, in
the municipality of Huimanguillo, Tabasco. Wilson et al. (2013b) determined its EVS as 12, placing it in the upper
portion of the medium vulnerability category. Its conservation status has been considered as Least Concern (LC) by
the IUCN, but this species is not listed by SEMARNAT. Photo by Liliana Rios-Rodas.
Amphib. Reptile Conserv. 1 August 2022 | Volume 16 | Number 2 | e315
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
16(2) [General Section]: 1-61 (e315).
The herpetofauna of Tabasco, Mexico: composition,
distribution, and conservation status
‘Ma. del Rosario Barragan-Vazquez, *Liliana Rios-Rodas, *Lydia Allison Fucsko, Louis W. Porras,
‘Vicente Mata-Silva, *Arturo Rocha, ‘Dominic L. DeSantis, ’Eli Garcia-Padilla, Jerry D. Johnson,
and ®Larry David Wilson
'Centro de Investigacién para la Conservacion y Aprovechamiento de los Recursos Tropicales, Division Académica de Ciencias Bioldgicas,
Universidad Judrez Autonoma de Tabasco, Villahermosa, MEXICO *Facultad Maya de Estudios Agropecuarios, Universidad Aut6noma de Chiapas,
Carretera Catazaja-Palenque, Km 4, C.P. 29980, Catazaja, Chiapas, MEXICO +*Department of Humanities and Social Sciences, Swinburne
University of Technology, Melbourne, Victoria, AUSTRALIA +7705 Wyatt Earp Avenue, Eagle Mountain, Utah, 84005, USA °Department of
Biological Sciences, The University of Texas at El Paso, El Paso, Texas 79968-0500, USA °Department of Biological and Environmental Sciences,
Georgia College and State University, Milledgeville, Georgia 31061, USA ‘Oaxaca de Juarez, Oaxaca 68023, MEXICO *Centro Zamorano
de Biodiversidad, Escuela Agricola Panamericana Zamorano, Departamento de Francisco Morazan, HONDURAS and 1350 Pelican Court,
Homestead, Florida 33035-1031, USA
Abstract.—The herpetofauna of Tabasco, Mexico, consists of 170 species, including 39 anurans, five caudates,
one caecilian, two crocodylians, 111 squamates, and 12 turtles. We catalogued the distribution of these species
among the three physiographic regions we recognize in the state: the Gulf Coastal Plain (88 species), the
Sierras Bajas de Petén (93 species), and the Sierra Norte de Chiapas (145 species). The individual species are
found in either one, two, or all three regions (mean = 1.9). Approximately 68% of the herpetofauna in Tabasco
occupies only one or two of the three regions, which is of important conservation significance. The largest
number of single-region species is found in the Sierra Norte de Chiapas (50), followed by the Gulf Coastal
Plain (12) and the Sierras Bajas de Peteén (nine). Coefficient of Biogeographic Resemblance (CBR) calculations
indicate that the Sierra Norte de Chiapas and the Sierras Bajas de Peten share the greatest number of species
(79), followed by 71 species between the Sierra Norte de Chiapas and the Gulf Coastal Plain, and 61 between
the Gulf Coastal Plain and the Sierras Bajas de Peten. Fifty-five species occupy all three regions. A similarity
dendrogram based on the Unweighted Pair Group Method with Arithmetic Averages (UPGMA) illustrates that
the Sierras Bajas de Peteén clusters with the Gulf Coastal Plain at the 0.67 level and the Sierra Norte de Chiapas
clusters with the previous pair at the 0.64 level, and overall indicates an intermediate level of similarly. With
reference to distributional categories, the greatest number of species is represented by the non-endemic
species (146 of 170), followed by the country endemics (20), and the non-natives (five). Of the 146 non-endemic
species, the majority (95) are MXCA species (i.e., those found only in Mexico and Central America). The
principal environmental threats to the Tabasco herpetofauna are deforestation, agricultural activities, roads,
soil contamination and oil extraction, myths and cultural factors (gastronomy), illegal commerce, and forest
fires. We evaluated the conservation status of each of the native species by using the SEMARNAT, IUCN, and
EVS systems, of which the EVS system provided the most inclusive assessment of the state’s herpetofauna.
We also employed the Relative Herpetofaunal Priority (RHP) method to determine the rank order of the three
physiographic regions and found the highest values in the Sierra Norte de Chiapas. Most of the protected areas
in the state are located in the Gulf Coastal Plain, which is only the second or third most important region from
a conservation perspective. Nonetheless, about 95% of the native herpetofauna has been documented within
the system of protected areas. Finally, we provide a set of conclusions and recommendations for the future
protection of the Tabasco herpetofauna.
Keywords. Anurans, caecilians, caudates, conservation status, crocodylians, physiographic regions, protected areas,
protection recommendations, squamates, turtles
Resumen.—La herpetofauna de Tabasco, Mexico, consta de 170 especies, incluidos 39 anuros, cinco caudados,
un cecilido, dos crocodilianos, 111 escamosos y 12 tortugas. Catalogamos la distribuciOn de estas especies
entre las tres regiones fisiograficas que reconocemos, incluyendo la Llanura Costera del Golfo (88 especies), las
Sierras Bajas del Peten (93 especies) y la Sierra Norte de Chiapas (145 especies). Las especies individuales se
Correspondence. rosariobarragan@gmail.com (MRB), aril707@hotmail.com (LR), lydiafucsko@gmail.com (LAF), empub@msn.com
(LWP); vmata@utep.edu (VM); arocha3(@miners.utep.edu (AR); dominic.desantis@gcsu.edu (DLD); eligarcia_18@hotmail.com (EG); jjohn-
son@utep.edu (JDJ), bufodoc@aol.com (LDW)
Amphib. Reptile Conserv. 2 August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
encuentran de una a tres regiones (media = 1,9). Aproximadamente el 68% de la herpetofauna de Tabasco ocupa
solo una o dos de las tres regiones, lo que es de gran importancia para la conservacion. El mayor numero de
especies de una sola region se encuentra en la Sierra Norte de Chiapas (49) seguida por la Llanura Costera del
Golfo (12) y las Sierras Bajas del Petén (nueve). Los calculos del Coeficiente de semejanza biogeografica (CBR)
demuestran que la Sierra Norte de Chiapas y las Sierras Bajas de Petén comparten el mayor numero de especies
(79), seguidas de 71 entre la Sierra Norte de Chiapas y la Llanura Costera del Golfo y 61 entre la Llanura Costera
del Golfo y Sierras Bajas del Petéen. Cincuenta y cinco especies ocupan las tres regiones. Un dendrograma de
similitud basado en el metodo de grupos de pares no ponderados con promedios aritméticos (UPGMA) ilustra
que las Sierras Bajas del Petén se agrupan junto con Llanura Costera del Golfo en el nivel .67 y la Sierra Norte
de Chiapas se agrupa con el par anterior en el nivel .64, lo que indica un nivel generalmente intermedio de
similitud en general. Con referencia a las categorias de distribucion, el mayor numero de especies es el de las
especies no endémicas (146 de 170), seguido de las endémicas del pais (20) y no nativos (cinco). De las 146
especies no endemicas, la mayor parte (95) son especies MXCA. Las principales amenazas ambientales para
la herpetofauna de Tabasco son deforestacion, actividades agropecuarias, carreteras, contaminacion del suelo
y actividades petroleras, mitos y factores culturales (gastronomia), comercio ilegal, e incendios forestales. El
estado de conservacion de cada especie nativa se evaluo mediante el uso de los sistemas SEMARNAT, UICN y
EVS, de los cuales el sistema EVS fue de mayor utilidad. También se utilizo el método de Prioridad Relativa de
la Herpetofauna (RHP) para determinar el orden de importancia de las tres regiones fisiograficas y los valores
mas altos se encontraron en la Sierra Norte de Chiapas. La mayoria de las areas protegidas en el estado estan
ubicadas en la Llanura Costera del Golfo, que es solo la segunda o tercera region mas importante desde una
perspectiva de conservacion. No obstante, alrededor del 95% de la herpetofauna nativa se ha documentado en
el sistema de areas protegidas. Finalmente, se entregan un conjunto de conclusiones y recomendaciones para
la futura proteccion de la herpetofauna de Tabasco.
Palabras Claves. Anuros, areas protegidas, caudados, cecilidos, crocodilidos, escamosos, estatus de conservacion,
recomendaciones de proteccion, regiones fisiograficas, tortugas
Citation: Barragan-Vazquez MR, Rios-Rodas L, Fucsko LA, Porras LW, Mata-Silva V, Rocha A, DeSantis DL, Garcia-Padilla E, Johnson JD, Wilson LD.
2022. The herpetofauna of Tabasco, Mexico: composition, distribution, and conservation status. Amphibian & Reptile Conservation 16(2): 1-61 (e315).
Copyright: © 2022 Barragan-Vazquez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License
[Attribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction
in any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced,
are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Received: 9 May 2022; Accepted: 21 June 2022; Published: 8 August 2022
“The more we get done ourselves, the easier it will be for
our children and their children to move the world back
to sustainability. ”
Peter H. Raven (2021)
Introduction
Tabasco is an oddly shaped state in Mexico, in which a
western segment and an eastern segment are connected
to each other by a slender isthmus. With a total area of
24,731 km”, this state is relatively small (the 24" smallest
of the 32 federal entities in Mexico, http://inegi.org;
accessed 5 May 2022). The state’s area constitutes only
about 1.3% of the country’s area. The coastal region of
Tabasco lies adjacent to the southwesternmost corner of
the Gulf of Mexico. To the southwest, Tabasco 1s bordered
by the state of Veracruz, to the northeast by the state of
Campeche, to the south by the state of Chiapas, and to the
southeast by a small portion of the northwestern border
of Guatemala. To the west, much of the state lies in the
Gulf Coastal Plain, where it merges with part of this
Amphib. Reptile Conserv.
physiographic region in Veracruz, and to the east, this
plain merges with the lowlands of the Yucatan Peninsula.
The two principal portions of the state are connected by
a slender segment of land at least 6 km in width between
Campeche and Chiapas, through which passes a portion
of the Usumacinta River (Google Earth, https://earth.
google.com, accessed: 9 May 2022).
The hydrography of Tabasco is dominated by the
presence of portions of the first and second largest
watersheds in Mexico, those of the Grijalva and the
Usumacinta rivers, which arise from divergent points in
the central highlands of Chiapas (the Grijalva) and the
central highlands of Guatemala (Usumacinta) and join
together in a common delta before entering the Gulf of
Mexico near the town of Frontera.
Tabasco is partitioned into 17 municipalities and its
capital is Villahermosa. As of 2020, its population was
2,402,598, which ranks 20" in the country. More recently
its density was noted as 97 people/km?’, ranking 12" in
the country (http://inegi.org; accessed 5 May 2022). This
figure is 1.6 times the average density for Mexico.
August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
The southeasternmost portion of the state contains
the highest elevation (http://inegi.org; accessed 5 May
2022), between 1,140 and 1,150 m on an unnamed peak
located at 17°24’38”N, 92°50’22”W near the border
with Chiapas, more or less south of Villahermosa (http://
peakbagger.com; accessed 7 June 2021). As expected,
the lowest elevation in the state is sea level, all along the
198.8 km of shoreline (http://inegi.org; accessed 5 May
2022).
Materials and Methods
Our Taxonomic Position
In this paper we follow the same taxonomic position
as detailed in previous works on other portions of
Mesoamerica (Johnson et al. 2015a,b; Mata-Silva
et al. 2015; Teran-Juarez et al. 2016; Woolrich-Pifia
et al. 2016, 2017; Nevarez-de los Reyes et al. 2016;
Cruz-Saenz et al. 2017; Gonzalez-Sanchez et al. 2017;
Lazcano et al. 2019; Ramirez-Bautista et al. 2020;
Torres-Hernandez et al. 2021; Cruz-Elizalde et al.
2022). Johnson (2015a) can be consulted for a formal
statement of this position, with special reference to the
subspecies concept.
System for Determining Distributional Status
We employed the same system developed by Alvarado-
Diaz et al. (2013) for the herpetofauna of Michoacan
to ascertain the distributional status of members of the
herpetofauna of Tabasco. Subsequently, Mata-Silva et
al. (2015), Johnson et al. (2015a), Teran-Juarez et al.
(2016), Woolrich-Pifia et al. (2016, 2017), Nevarez-de
los Reyes et al. (2016), Cruz-Sanchez et al. (2017),
Gonzalez-Sanchez et al. (2017), Lazcano et al. (2019),
Ramirez-Bautista et al. (2020), Torres-Hernandez et
al. (2021), and Cruz-Elizalde et al. (2022) utilized
this system, which consists of four categories: SE =
endemic to Tabasco; CE = endemic to Mexico; NE
= not endemic to Mexico; and NN = non-native in
Mexico.
Systems for Determining Conservation Status
To assess the conservation status of the herpetofauna
of Tabasco, we employed the same three systems (-e.,
SEMARNAT, IUCN, and EVS) used by Alvarado-Diaz
et al. (2013), Mata-Silva et al. (2015), Johnson et al.
(2015a), Teran-Juarez et al. (2016), Woolrich-Pifia et al.
(2016, 2017), Nevarez-de los Reyes et al. (2016), Cruz-
Sanchez et al. (2017), Gonzalez-Sanchez et al. (2017),
Lazcano et al. (2019), Ramirez-Bautista et al. (2020),
Torres-Hernandez et al. (2021), and Cruz-Elizalde et
al. (2022). Detailed descriptions of these three systems
appear in the earlier papers of this series, and thus are not
repeated here.
Amphib. Reptile Conserv.
The Mexican Conservation Series
The Mexican Conservation Series (MCS) was initiated
in 2013, with a study of the herpetofauna of Michoacan
(Alvarado-Diaz et al. 2013), as a part of a set of five papers
designated as the “Special Mexico Issue” published in
Amphibian & Reptile Conservation. The basic format
of the entries in the MCS was established in this paper,
1.e., providing an examination of the composition,
physiographic distribution, and conservation status of
the herpetofauna of a given Mexican state or group of
states. Two years later, the MCS resumed with a paper
on the herpetofauna of Oaxaca (Mata-Silva et al. 2015).
That same year, Johnson et al. (2015a) presented a paper
on the herpetofauna of Chiapas. The following year,
three entries in the MCS appeared, on Tamaulipas (Teran-
Juarez et al. 2016), Nayarit (Woolrich-Pifia et al. 2016),
and Nuevo Leon (Nevarez-de los Reyes et al. 2016).
Thereafter, three entries were published in 2017, on Jalisco
(Cruz-Saenz et al. 2017), the Mexican Yucatan Peninsula
(Gonzalez-Sanchez et al. 2017), and Puebla (Woolrich-
Pifia et al. 2017), followed by subsequent entries on
Coahuila (Lazcano et al. 2019), Hidaldo (Ramirez-
Bautista et al. 2020), Veracruz (Torres-Hernandez et al.
2021), and most recently one on Querétaro (Cruz-Elizalde
et al. 2022). Therefore, this paper on the herpetofauna of
Tabasco is number 14 in this series.
Physiography and Climate
Physiographic Regions
To analyze the distribution of the herpetofauna of Tabasco,
we used the classification system of physiographic
regions of INEGI (1986 and 2016). According to these
studies, two physiographic regions are distinguished, one
with two subregions (Fig. 1), which are described here.
Gulf Coastal Plain (GCP). This province (Fig.
2) comprises 95.7% of the state’s area. Located in
southeastern Mexico, it encompasses the states of
Campeche, Chiapas, Oaxaca, Tabasco, and Veracruz; and
its average length in each state is between 125 and 150
km. To the north, its limits are defined by the Gulf of
Mexico; to the east, by the Yucatan Peninsula and Belize:
to the south, by the Central American Cordillera and the
Sierras de Chiapas and Oaxaca; and to the west by the
Sierra Madre del Sur and Sierra Volcanica Transversal or
Eye Neovolcanico.
The Gulf Coastal Plain was formed by alluvium
carried by the Papaloapan, Coatzacoalcos, Grijalva,
and Usumacinta rivers, which cross the province
before emptying into the Gulf of Mexico. In the central
part of this plain, the lower basins of the Griyalva and
Usumacinta rivers (the largest basins in the country)
meet and then converge south of the port of Frontera,
Tabasco, to exit into the Gulf of Mexico. The Usumacinta
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
3315000 3400000 3485000 3570000
3655000
Gulf of Mexico
SNC Chiapas
So
Qo
ao
uw
nn
w
Oaxaca
Physiographic regions
Mi Gulf Coastal Lowlands
™ Sierras del Norte de Chiapas y Guatemala
Physiographic subregions
M™) Sierras del Norte de Chiapas (SNC)
™) Sterras Bajas del Petén (SBP)
Guatemala
100 km
a
3315000 3400000 3485000 3570000
3655000
Fig. 1. Physiographic regions in the state of Tabasco, Mexico, and location of the state in Mexico.
and Grijalva rivers contribute about 27% of Mexico’s
hydrologic resources (West et al. 1985). Throughout
most of this province, relatively young sedimentary
rocks form extensive alluvial plains and coastal plains
with an almost flat relief at elevations below 100 m. This
relief creates extensive flood plains and lagoons, among
which La Machona, Mecoacan, Sitio Grande, and El
Rosario are the most prominent (INEGI 2006; SAHOP
1980). Two types of climates are evident: (1) warm humid
with abundant rainfall in summer, which covers 76.0% of
the surface area and is distributed from the coastal zone
to the vicinity of the mountains in the southern portion
of the state, and (11) warm subhumid with summer rains,
which is present toward northeastern Tabasco, in the
municipality of Balancan. This region is the least humid
in the state, with an average annual temperature of 26.4
°C (INEGI 2016).
Grasslands used for grazing livestock have displaced
the natural vegetation in this physiographic region, as they
cover 30.6% of the area; and additional agricultural areas
occupy 25.8% of this region. The third most common
type of vegetation is the Tular-popal association, which
forms dense patches that cover 26.6% of the swampy
areas. In addition, some forests are dominated by a single
species (16.2%), such as Cashan (7erminalia amazonia),
laurel (Nectandra sp.), Mulato (Bursera simaruba) or
Chicozapote (Achras zapota). To a lesser degree, the
mangroves (2.8%), which are composed of a group of
halophilic plants, are characterized by such dominant
species as Red Mangrove (Rhizophora mangle), Black
Mangrove (Avicennia germinans), or White Mangrove
(Laguncularia racemosa) (INEGI 2016).
Sierras Bajas del Petén (SBP). This province (Fig. 3)
only covers 4.3% of the area of the state, and includes
the mountains that extend from southeastern Mexico to
Guatemala. This region is characterized by a parallel
Amphib. Reptile Conserv.
arrangement of folded mountain ranges with rounded
summits, steep flanks, and wide intermontane valleys
at its base (Zavala-Cruz and Ortiz-Pérez 2019). To the
north, this province is limited by the occurrence of the
Gulf Coastal Plain, to the east by Belize, to the south
by Guatemala, and to the west it borders the Central
American Mountain Cordillera. This province is divided
into five physiographic subprovinces, two of which
occur in Tabasco: the northern Sierras of Chiapas and the
Lower Sierras of Petén.
Sierras del Norte de Chiapas (SNC). In Tabasco, this
region (Fig. 4) is composed of two small portions to
the south that together cover an area of 986.0 km? and
comprise parts of the municipalities of Huimanguillo,
Macuspana, Tacotalpa, and Teapa (INEGI 1986). In
these areas, the highest elevations are the hills of La
Pava and La Ventana (at elevations of 880 and 560 m,
respectively); and the Madrigal, Tapijulapa, and Poana
Mountains (at elevations from 560 to 900 m). The lower
hills are La Campana, La Corona, Cocona, Mono Pelado,
and El Tortuguero (CONAFOR 2013). Limestone rocks
such as dolomites and marls dominate this region, and
they alternate with shales and sandstones, but there
also are many types of ancient alluvium, igneous rocks
formed from volcanic clasts, andesites, and volcanic ash.
The lithological diversity gives these mountain ranges
a “complex character” (INEGI 1989; Zavala-Cruz and
Ortiz-Pérez 2019), and karst features are prominent.
Climate
Temperature. Here, we present the monthly minimum,
mean, and maximum temperatures for a single locality
in each of the three recognized physiographic regions
in Tabasco (Table 1). The elevations for these three
localities range from 10 m at Villahermosa in the Gulf
August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Fig. 2. Gulf Coastal Plain. Mangroves in the municipality
Paraiso, Tabasco. Photo by José del Carmen Geronimo-Torres.
Fig. 4. Sierra Norte de Chiapas. Mountain Cloud Forest
fragment in the municipality of Huimanguillo, Tabasco. Photo
by Liliana Rios-Rodas.
Coastal Plain to 34 m at Huimanguillo in the Sierra Norte
de Chiapas.
The mean annual temperature (MAT) is highest at
Tenosique (elevation 19 m) in the Sierras Bayas del Petén
(SBP) at 26.7 °C. The MAT for the other two localities
in the Gulf Coastal Plain (GCP) and the Sierra Norte de
Chiapas (SNC) differ by only 0.1 °C (26.4 °C for the GCP
and 26.3 °C for the SNC). These values are reflective of
the limited variation in elevational range in Tabasco.
The minimum annual temperatures range from 21.6
°C in the SBP and the SNC to 23 °C in the GCP, which
only represents a difference of 1.4 °C (Table 1). The
mean minimum monthly temperatures peak in May in
the GCP and SBP (at 25.6 °C in the former, and 23.6
°C in the latter) and in June in the SNC (at 23.7 °C).
The mean maximum monthly temperatures are highest
in May in all three regions, respectively 34.8 °C, 35 °C,
and 35.4 °C in the GLC, SNC, and SBP. The monthly
maximum temperatures are lowest in January in the GCP
(at 26.7 °C) and SBP (at 28.0 °C), and in December and
January in the SNC (at 26.9 °C).
Precipitation. Naturally, monthly precipitation is lowest
during the dry season in February (in the SBP), March (in
the GCP), or April (in the SNC), and highest during the
rainy season in September in all three regions (Table 2).
The data in Table 2 demonstrate that 63.0—76.3% of the
Amphib. Reptile Conserv.
Fig. 3. Sierras Bajas del Petén. Panoramic view of the Sierras
Bajas del Petén, Ejido Nuevo Progreso, municipality of
Tenosique, Tabasco, near the border with Guatemala. Photo by
Nelly del Carmen Jiménez-Pérez.
yearly precipitation falls during the rainy season, from
May to October. The annual rainfall ranges from 1,476.0
mm in the SBP to 2,316.8 mm in the SNC (Table 2).
Composition of the Herpetofauna
Families
The members of the native and non-native herpetofauna
of Tabasco are arranged among 45 families, including
10 families of anurans, one of salamanders, one of
caecilians, one of crocodylians, 24 of squamates, and eight
of turtles (Table 3). The total of 45 families includes 72.6%
of the 62 families with native, non-native, and introduced/
questionable members represented in Mexico (J. Johnson,
unpublished, 26 March 2022). Among the 12 amphibian
families, 51.1% of the species (Tables 4 and 5) are
classified in the families Craugastoridae (seven species)
and Hylidae (16 species). Among the 33 reptile families,
59.5% of the species (Tables 4 and 5) are classified in the
families Dactyloidae (14 species), Phrynosomatidae (five),
Colubridae (20), Dipsadidae (30), and Viperidae (six).
Genera
The genera of amphibians and reptiles represented in
Tabasco number 104, including 24 genera of anurans, one
of salamanders, one of caecilians, one of crocodylians, 67
of squamates, and 10 of turtles. These 104 genera include
48.8% of the 213 recorded for Mexico (J. Johnson,
unpublished, 26 March 2022). Among the amphibians
(Table 4), the largest numbers of species are classified in
the genera Craugastor (seven species) and Bolitoglossa
(five); among the reptiles (Table 4), the most speciose
genera are Norops (14 species), Sceloporus (five), and
Coniophanes (Six).
Species
The herpetofauna of Tabasco consists of 170 species,
including 39 anurans, five salamanders, one caecilian,
two crocodylians, 111 squamates, and 12 turtles (Tables 3
August 2022 | Volume 16 | Number 2 | e315
August September October November December Annual
July
June
April May
February March
January
Table 1. Monthly minimum (Min), mean (Mean, in parentheses), maximum (Max), and annual temperature data (in °C) for the three physiographic regions of Tabasco, Mexico. The selected
localities for each region and their elevations are as follows: Gulf Coastal Plain—Cardenas (29 m asl), Centla (4 m), Villahermosa (10 m); Sierra Norte de Chiapas—Huimanguillo (29
Physiographic
region
m), Teapa (41 m), Macuspana (13 m); and Sierras Bajas del Petén—Tenosique (19 m). Data were taken from https://es.climate-data.org and https://smn.conagua.gob.mx/es/climatologia
(Accessed: 16 June 2021).
Amphib. Reptile Conserv.
pee
(26.4)
30.4
24.5 23.6 21.9 20.8
(26.9) (25.9) (24.4) (23.5)
30.5 29.1 O17 27.0
25.2
(28.1)
32.1
25.2 25.2
(28.1) (28.4)
32.1 32.5
25.8
(29.5)
34.3
24.4
(28.6)
33.9
22.4
(26.2)
319
21.0
(24.1)
28.4
20.1
(22.8)
26.5
Gulf Coastal Plain
23.1 22.1 20.3 19.1 21.5
(26.8) (25.6) (24.0) (22.8) (25.8)
31.0 29.5 28.0 26.9 30.5
23.3
(27.6)
39 2
23.7 23.3
(28.1) (27.8)
32.8 32.6
23.7
(28.9)
34.3
22.2
(27.7)
33.4
19.0 20.2
(23.4) (25.3)
28.1 30.9
18.3
(22.2)
26.5
Sierra Norte de
Chiapas
Barragan-Vazquez et al.
21.6
(26.7)
31.9
19.4
(23.9)
28.5
20.7
(25.2)
29.8
22.3
(26.7)
BD
22.9
(27.8)
32.7
22.9
(28.2)
33.5
22.9
(28)
33.1
23.5
(28.6)
33.7
23.6
(29.5)
35.4
22.5
(28.6)
34.8
20.4
(26.3)
32.1
19.4
(24.6)
29.7
18.8
(23.4)
28
Sierras Bajas del
Petén
and 4). The current numbers of native species in Mexico
for these six groups are, respectively, 258, 155, 3, 3, 902,
and 51 (J. Johnson, unpublished, 26 March 2022). The
165 native species in Tabasco comprise 12.0% of the
1,372 species in the entire native Mexican herpetofauna
(J. Johnson, unpublished, 29 May 2021).
Three states in Mexico border Tabasco, and all have
been evaluated in the Mexican Conservation Series
(Chiapas: Johnson et al. 2015a; Campeche: Gonzalez-
Sanchez et al. 2017; Veracruz: Torres-Hernandez et al.
2021). Based on these works, the total figures for the
native taxa in these states are as follows: Chiapas, 326;
Campeche, 125; and Veracruz, 351. The number of native
species in Tabasco (165) is closest to that in Campeche,
essentially another lowland state in the western portion
of the Yucatan Peninsula. As expected, the two larger and
more montane states to the north (Veracruz) and south
(Chiapas) contain 2.1 and 2.0 times as many species,
respectively, as Tabasco.
Patterns of Physiographic Distribution
We used a system of three regions (Fig. 1) to analyze
the physiographic distribution patterns of members of the
Tabasco herpetofauna. The results for the 170 species are
tabulated in Table 4 and summarized in Table 5.
The total number of taxa in each of the three regions we
recognize ranges from 88 in the Gulf Coastal Plain to 145
in the Sierra Norte de Chiapas. The total for the remaining
area (Sierras Bajas del Petén) is 93. The average of these
three values 1s 108.7, or 63.9% of the number for the total
herpetofauna (170). The lowest value (88) is 51.8% of the
total value (170), and the corresponding percentages for
the other two regions in numerical order are 54.7 (93/170)
and 85.3 (145/170). These results indicate that the higher
elevations in the state, as in the Sierra Norte de Chiapas
(see above), exhibit much greater herpetofaunal diversity
than the corresponding lower elevations. This situation
is consistent with the recognition that herpetofaunal
diversity in Mexico is highest in the nearby or bordering
states of Oaxaca and Chiapas (Mata-Silva et al. 2015;
Johnson et al. 2015a) to the south.
Six herpetofaunal groups are represented in Tabasco,
i.e., anurans, salamanders, caecilians, crocodylians,
squamates, and turtles. As is typical for the state
herpetofaunas in Mexico, anurans and squamates
contain the largest numbers of species and the caecilians
and crocodylians the fewest, while the salamanders
and turtles are represented by intermediate numbers.
The largest numbers of anurans (36 of 39, or 92.3%),
salamanders (four of five, or 80.0%), and squamates
(96 of 111, or 86.5%) and of the herpetofauna in
general (145 of 170, or 85.4%) occupy the Sierra Norte
de Chiapas. Nonetheless, turtles do not follow this
pattern, inasmuch as all 12 of the species in Tabasco
occur on the Gulf Coastal Plain, with only six of them
(50.0%) occurring in the Sierra Norte de Chiapas, and
August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
No. 1. Hyalinobatrachium viridissimum (Taylor, 1942). The
Northern Glassfrog is a non-endemic species distributed
from Guerrero and Veracruz, Mexico, through Guatemala
and Belize to northwestern Honduras, and possibly to the
departments of Santa Ana and Cabafias in El Salvador (https://
amphibiansoftheworld.amnh.org/). This individual is from
Muku Chem, in the municipality of Tacotalpa, Tabasco. Torres-
Hernandez et al. (2021) calculated its EVS as 11, placing it
in the lower portion of the medium vulnerability category. Its
conservation status has not been assessed by either the IUCN or
SEMARNAT. Photo by Manuel Herndndez- May.
No. 2. Craugastor alfredi (Boulenger, 1898). Alfred’s Rain
Frog is distributed from central Veracruz, northern Oaxaca, and
southward to the states of Tabasco and Chiapas, Mexico (https://
amphibiansoftheworld.amnh.org/). This individual was located
at Muku Chem, in the municipality of Tacotalpa, Tabasco.
Wilson et al. (2013b) determined its EVS as 9, placing it at the
upper limit of the low vulnerability category. Its conservation
status has been considered as Least Concern (LC) by the IUCN,
but this species is not listed by SEMARNAT. Photo by Liliana
Rios-Rodas.
No. 3. Craugastor berkenbuschii (Peters, 1870). Berkenbusch’s
Robber Frog ranges along the Atlantic slopes of southern San
Luis Potosi, Hidalgo, Puebla, Veracruz, Tabasco, and northern
Oaxaca, north of the Isthmus of Tehuantepec, Mexico (https://
amphibiansoftheworld.amnh.org/). This individual was located
at Muku Chem, in the municipality of Tacotalpa, Tabasco.
Wilson et al. (2013b) assessed its EVS as 14, placing it at the
lower limit of the high vulnerability category. Its conservation
status has been considered as Least Concern (LC) by the IUCN
and as a species of Special Protection (Pr) by SEMARNAT.
Photo by Marco Antonio Torrez-Pérez.
Amphib. Reptile Conserv.
No. 4. Duellmanohyla chamulae (Duellman, 1961). The
Chamula Mountain Brook Frog is known only from a few
localities at elevations above 1,600 m on the northern slopes
of the Central Highlands of Chiapas and into adjacent extreme
southwestern Tabasco, Mexico (https://amphibiansoftheworld.
amnh.org/). This individual was encountered at Ejido Villa
Guadalupe, in the municipality of Huimanguillo, Tabasco.
Wilson et al. (2013b) determined its EVS to be 13, placing
it at the upper limit of the medium vulnerability category.
Its conservation status has been evaluated as Endangered
(EN) by IUCN, and as a species of Special Protection (Pr) by
SEMARNAT. Photo by José del Carmen Geronimo-Torres.
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 2. Monthly and annual precipitation data (in mm) for the three physiographic regions of Tabasco, Mexico. The selected
localities for each of the regions, with elevation given in parentheses) are as follows: Gulf Coastal Plain—Cardenas (29 m asl),
Centla (4 m), Villahermosa (10 m); Sierra Norte de Chiapas—Huimanguillo (29 m), Teapa (41 m), Macuspana (13 m); Sierras Bajas
del Petén—Tenosique (19 m). Data were taken from https://es.climate-data.org and https://smn.conagua.gob.mx/es/climatologia
(Accessed: 16 June 2021). The shaded area indicates the months of the rainy season.
Physiographic Jan Feb Mar Apr May Jun
region
GulfCoastal 76g 4g5 0303353 i
Plain
picwa deh None, “Ase wat Ween TA 120 2573
de Chiapas
Sierras Bajas del 62 34 eye 54 95 227
Petén
an intermediate number of nine (75.0%) occurs in the
Selvas Bayas del Petén.
The members of the Tabasco herpetofauna are
distributed in either one, two, or three physiographic
regions (Table 4), as follows: one (69 of 170 species;
40.6%); two (46; 27.1%); and three (55, 32.4%). The
mean regional occupancy figure is 1.9, which is slightly
higher than the 1.6 value for Querétaro, another state
with three physiographic regions that was assessed
in the Mexican Conservation Series (Cruz-Elizalde
et al. 2022). A sizable portion of the 170 species in
Tabasco (115; 67.6%) occurs in only one or two of the
three physiographic regions, which is of considerable
conservation significance (see below).
The number of species occupying a_ single
physiographic region ranges from eight in the Sierras
Bajas del Petén (SBP) to 50 in the Sierra Norte de
Chiapas (SNC).
The 50 single-region species in the SNC (Table 7) are
as follows (numbers refer to distributional categories as
reported by Wilson et al. [2017], and asterisks indicate
the country endemics):
Incilius macrocristatus 4
Hyalinobatrachium viridissimum 4
Craugastor berkenbuschii*
Craugastor pelorus*
Charadrahyla chaneque*
Duellmanohyla chamulae*
Exerodonta bivocata*
Ptychohyla macrotympanum 4
Quilticohyla zoque*
Rheohyla miotympanum*
Triprion spinosus 4
Gastrophryne elegans 4
Agalychnis moreletii 4
Bolitoglossa platydactyla*
Bolitoglossa rufescens 4
Bolitoglossa veracrucis*
Norops barkeri*
Norops capito 4
Norops compressicauda*
Norops laeviventris 4
Amphib. Reptile Conserv.
Jul Aug Sept Oct Nov Dec
136.5 193.3 2105 foe «125.8 79.8
L938 247.8 341.5 299 210.3. 178.3
141 206 261 196 104 60
Norops petersi 4
Lepidophyma tuxtlae*
Xenosaurus rackhami 4
Dendrophidion vinitor 4
Ficimia publia 4
Phrynonax poecilonotus 6
Senticolis triaspis 7
Stenorrhina freminvillii 4
Tantilla rubra 4
Tantilla schistosa 4
Tantillita lintoni 4
Adelphicos quadrivirgatum 4
Amastridium sapperi 4
Coniophanes piceivittis 4
Dipsas brevifacies 4
Geophis carinosus 4
Geophis laticinctus*
Geophis sanniolus 4
Leptodeira maculata 4
Leptodeira septentrionalis 4
Ninia diademata 4
Oxyrhopus petolarius 6
Rhadinaea decorata 6
Sibon dimidiatus 4
Sibon nebulatus 6
Xenodon rabdocephalus 6
Micrurus elegans 4
Scaphiodontophis annulatus 4
Amerotyphlops tenuis 4
Bothriechis schlegelii 6
Order Families Genera
Anura 10 24
Caudata 1 1
Gymnophiona 1 1
Subtotal 12 26
Crocodylia l 1
Squamata 24 67
Testudines 8 10
Subtotal 33 78
Total 45 104
Annual
1,489.8
2,316.8
1,476
Table 3. Taxonomic composition of the native and non-native
herpetofauna of Tabasco, Mexico.
Species
39
5
1
45
August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
No. 5. Exerodonta bivocata (Duellman and Hoyt, 1961). The
Chiapan Highlands Treefrog is distributed along the Atlantic
slopes of extreme southwestern Tabasco, Oaxaca, and Chiapas
in southern Mexico (https://amphibiansoftheworld.amnh.org/).
This individual was located in Ejido Villa Guadalupe, in the
municipality of Huimanguillo, Tabasco. Wilson et al. (2013b)
assessed its EVS as 15, placing it in the lower portion of the
high vulnerability category. Its conservation status has been
judged as Endangered (EN) by the IUCN, but this species is not
listed by SEMARNAT. Photo by Liliana Rios-Rodas.
No. 6. Ptychohyla macrotympanum (Tanner, 1957). The Pine
Forest Stream Frog is distributed in humid montane and pine-
oak forest, on the northern slopes of the Chiapan Highlands of
Tabasco and Chiapas in Mexico (https://amphibiansoftheworld.
amnh.org/). This individual was found in the Ejido Villa
Guadalupe of Huimanguillo, Tabasco. Wilson et al. (2013b)
assessed its EVS as 11, placing it in the lower portion of the
medium vulnerability category. Its conservation status has been
considered as Vulnerable (VU) by the IUCN, but this species
is not listed by SEMARNAT. Photo by Jenny del Carmen
Estrada- Montiel,
No. 7. Quilticohyla zoque (Canseco-Marquez, Aguilar-Lopez,
Luria-Manzano, Pineda-Arredondo, and Caviedes-Solis, 2017).
The Zoque Treefrog is distributed in evergreen tropical forest at
three localities in southern Mexico in the Selva Zoque, two in
southern Veracruz (Paso del Moral and Arroyo Zarco), one in
extreme southwestern Tabasco near the Veracruz and Chiapas
borders, and one in northeastern Oaxaca (Chalchijapa) (https://
amphibiansoftheworld.amnh.org/). This individual was located
in Ejido Villa Guadalupe, in the municipality of Huimanguillo,
Tabasco. Torres-Hernandez et al. (2021) assessed its EVS as 14,
placing it at the lower limit of the high vulnerability category.
Its conservation status has been judged as Endangered (EN) by
the IUCN, but this species is not listed by SEMARNAT. Photo
by Liliana Rios-Rodas.
Amphib. Reptile Conserv.
No. 8. Zriprion spinosus (Steindachner, 1864). The Coronated
Treefrog occurs in humid forests, primarily in the premontane
zone of eastern Mexico in the states of Tabasco, Veracruz,
Puebla, Oaxaca, and Chiapas, and on into Central America
south into Panama (https://amphibiansoftheworld.amnh.org/).
This individual is from Cerro El Madrigal, in the municipality
of Teapa, Tabasco. Wilson et al. (2013b) calculated its EVS as
10, placing it in the lower portion of the medium vulnerability
category. Its conservation status has been considered as Near
Threatened (NT) by IUCN, but this species is not listed by
SEMARNAT. Photo by Marco Antonio Torrez-Pérez.
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 4. Distribution of the herpetofauna of Tabasco, Mexico, by physiographic region. No asterisk = non-endemic; * = country
endemic; ** = non-native.
Physiographic region
Sierras de Chiapas y Guatemala Number of
Taxon Gulf Coastal Plain regions
(GCP) Sierra del Norte de Sierras Bajas del
Chiapas (SNC) Petén (SBP)
| Total herpetofauna(170 species) |
| AMPHIBIA(4Sspeciesy) |
| Anura(39speciesy |
| Bufonidae(3species) |
| Incilius macrocristaus |
| Centrolenidae(I species) |
| Hyalinobatrachium viridissimum |
| Craugastoridae(7speciesy |
| Craugastoralfred’ |
| Craugastor berkenbuschit* |
| Craugastorlaticeps |
| Craugastorloki |
| Craugastorpalenque |
| Craugastorpelorus* |
ECraugasior@hodoy se ee || =e
| Eleutherodactylidae(2 species) |
| Eleutherodactylusleprus |
| Eleutherodactylusplanirostris** | +
| Hylidae (16 species) |
| Charadrahylachaneque® |
| Dendrosophusebraccatus | HP
| Dendrosophus microcephalus | HT 8
| Duellmanohyla chamulac* |
| Exerodontabivocata® |
| Ptychohyla macrotympanum |
| Quilticohylazoques |
| Rheohyla miotympamum® |
Se AAD AE Ss |
| Smiliscabaudini | 8
| Smilisca cyanosticta |
| Talocohylaloquax | 8
| Talocohylapicta |
| Trachycephalus vermiculatus | HT 8
| Triprionpetasatus |
| Triprion spinosus |
| Leptodactylidae(3 species) |
| Engystomopspustulosus |
| Leptodactylusfragilis |
| Microhylidae(2 species) |
| Gastrophyrneelegans |
| Hypopachusvariolosus |
| Phyllomedusidae(2 species) |
| Agalychnismoreletii |
| Ranidae(2 species) |
AA
{i
THEFT ITE
Amphib. Reptile Conserv. 11 August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Table 4 (continued). Distribution of the herpetofauna of Tabasco, Mexico, by physiographic region. No asterisk = non-endemic;
* = country endemic; ** = non-native.
Physiographic region
Sierras de Chiapas y Guatemala Number of
Taxon Gulf Coastal Plain regions
(GCP) Sierra del Norte de Sierras Bajas del
Chiapas (SNC) Petén (SBP)
Lithobates vaillanti
Rhinophrynidae (1 species)
Caudata (5 species)
Plethodontidae (5 species)
Bolitoglossa alberchi*
Rhinophrynus dorsalis
Bolitoglossa mexicana
Bolitoglossa rufescens
Bolitoglossa veracrucis*
Gymnophiona (1 species)
Dermophis mexicanus
Reptilia (125 species)
Squamata (111 species)
Norops biporcatus
Norops lemurinus
Norops petersii
O
Norops capito
Norops compressicauda*
Norops sericeus
Norops laeviventris
Norops sagrei**
Norops tropidonotus
Norops uniformis
Ctenosaura similis +
+
+
+
+
+
+
+
+
+
+
+
+
3
Amphib. Reptile Conserv. 12 August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 4 (continued). Distribution of the herpetofauna of Tabasco, Mexico, by physiographic region. No asterisk = non-endemic;
* = country endemic; ** = non-native.
Physiographic region
Sierras de Chiapas y Guatemala Number of
Taxon Gulf Coastal Plain regions
(GCP) Sierra del Norte de Sierras Bajas del
Chiapas (SNC) Petén (SBP)
Amphib. Reptile Conserv. 13 August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Table 4 (continued). Distribution of the herpetofauna of Tabasco, Mexico, by physiographic region. No asterisk = non-endemic;
* = country endemic; ** = non-native.
Physiographic region
Sierras de Chiapas y Guatemala Number of
Taxon Gulf Coastal Plain regions
(GCP) Sierra del Norte de Sierras Bajas del
Chiapas (SNC) Petén (SBP)
| Stenorrhina degenhardtii__—— |
| Stenorrhina freminvillii__— |
| Tantillarubra |
| Tantillaschistosa |
| Tantillitalinton’ |
| Dipsadidae(30 species) |
| Adelphicos quadrivirgatum |
| Amastridium sapperi_ |
[Celia seytalina |
| Coniophanes bipunctatus |
| Coniophanesfissidens |
| Coniophanes imperialis | 8
| Coniophanespiceivitis |
| Coniophanes quinquevittatus | HT 8
| Coniophanes schmidti |
-ConophisHineatus FP
Dipsas brevifacies
+]+]+
+/+]+]+]+]4+]4]+
N Je PRO JR PRO PN TN IN JR fe
Enulius flavitorques
Geophis carinosus
Geophis laticinctus* _ SSS SSS ea SSS Ee
Geophis sanniolus pf
Geophis sartorii
+
NTH
ee | (A
| Imantodes gemmistraus | CC CU Cid tT
Leptodeira renata
| Leptodeiramaculaa | —C—“‘iLSCSCC“‘(S+TOTCOUWT CC
| Leptodeira septentrionalis | CE CU CS CC
Ninia diademata
mT
HH
ttt
|
++
Ninia sebae
Oxyrhopus petolarius _——S_——
Pliocercus elapoides SSE Se LS a es | ee
Rhadinaea decorata SSE ISS _ ee
Sibon dimidiatus
i |
+ tHe
Sibon nebulatus
Vanes
| Tretanorhinus nigroluteus |
| Xenodonrabdocephalus |
| Elapidae(2 species) |
| Micrurusdiastema* |
| Micruruselegans |
| Leptotyphlopidae(I species) |
| Epictiaphenops |
| Natricidae(3 species) |
| Nerodiarhombifera |
| Thamnophismarcianus |
| Thamnophisproximus |
| Sibynophiidae(I species) |
| Scaphiodontophisannulaus |
| Typhlopidae(2speciesy |
| Amerotyphlopstenuis |
+ ]+
— |r
Amphib. Reptile Conserv. 14 August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 4 (continued). Distribution of the herpetofauna of Tabasco, Mexico, by physiographic region. No asterisk = non-endemic;
* = country endemic; ** = non-native.
Number of
Physiographic region
Sierras de Chiapas y Guatemala
Taxon Gulf Coastal Plain
(GCP) Sierra del Norte de Sierras Bajas del
Chiapas (SNC) Petén (SBP)
Viperidae (6 species)
Agkistrodon russeolus
Virgotyphlops braminus**
Cheloniidae (2 species)
Thirteen of these 50 species (26.0%) are country
endemics and 37 (74.0%) are non-endemics. Thirty of
the 37 non-endemics (81.1%) are MXCA species, and
Dermatemydidae (1 species) _—_ _)
regions
Oxybelis fulgidus 6
Stenorrhina freminvillii 4
Enulius flavitorques 6
thus are distributed some distance from Mexico into Epictia phenops 4
Central America. Six of these non-endemics (16.2%) Nerodia rhombifera 3
are MXSA species, and thus range from Mexico through Virgotyphlops braminus**
Central America and into South America. Finally, one Chelonia mydas 9
non-endemic (2.7%) is a USCA species, and thus ranges Lepidochelys kempii 9
from the United States to Central America.
The 11 single-region species in the GCP (Table 7) are as
follows (numbers refer to the distributional categories as
designated by Wilson et al. [2017]; one asterisk indicates
a country endemic species; and two asterisks a non-
native species):
Eleutherodactylus planirostris**
Aspidoscelis guttatus*
Amphib. Reptile Conserv.
Dermochelys coriacea 9
Note that only one of these 11 species (9.1%) is a country
endemic, two (18.2%) are non-natives, and eight (72.7%)
are non-endemics. Of the eight non-endemics, one is a
MXUS species (12.5%), the only one in Tabasco that
ranges northward from Mexico into the United States.
Two of these are MXCA species (25.0%), two are MXSA
species (25.0%), and three are OCEA (or oceanic) species
(37.5%; the sea turtles).
August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
lipped Frog is distributed from the Lower Rio Grande Valley
of southern Texas (USA) through eastern and southern Mexico
(southeast from Colima), and into Central America through
northern and western Colombia (https://amphibiansoftheworld.
amnh.org/). This individual was found in the Ejido Villa
Guadalupe of Huimanguillo, Tabasco. Wilson et al. (2013b)
calculated its EVS as 5, placing it in the lower portion of the
low vulnerability category. Its conservation status has been
considered as Least Concern (LC) by the IUCN, but this
species is not listed by SEMARNAT. Photo by José del Carmen
Geronimo-Torres.
No. 11. Lithobates vaillanti (Brocchi, 1877). Vaillant’s Frog
ranges from “low and moderate elevations from north-central
Veracruz and northern Oaxaca to the central Rio Magdalena
region in Colombia on the Atlantic versant and on the Pacific
versant in southeastern Oaxaca and northwestern Chiapas,
Mexico, and from northwestern Nicaragua to southwestern
Ecuador” (https://amphibiansoftheworld.amnh.org/). This
individual was located in the Ejido Villa Guadalupe of
Huimanguillo, Tabasco. Wilson et al. (2013b) determined its
EVS as 9, placing it at the upper limit of the low vulnerability
category. Its conservation status has been considered as Least
Concern (LC) by the IUCN, but this species is not listed by
SEMARNAT. Photo by José del Carmen Geronimo-Torres.
Amphib. Reptile Conserv.
16
No. 10. Agalychnis taylori Funkhouser, 1957. Taylor’s Leaf
Frog occurs on the Atlantic slopes and lowlands from southern
Veracruz and northern Oaxaca in Mexico, through the more
humid portions of Tabasco, Campeche, Quintana Roo and
Yucatan, and on through Guatemala to west-central Honduras
(https://amphibiansoftheworld.amnh.org/). This individual was
found in the municipality of Centro, Tabasco. Torres-Hernandez
et al. (2021) calculated its EVS as 11, placing it in the lower
portion of the medium vulnerability category. Its conservation
status has been considered as Least Concern (LC) by the IUCN,
but this species is not listed by SEMARNAT. Photo by José del
Carmen Geronimo-Torres.
No. 12. Bolitoglossa mexicana Dumeéril, Bibron, and Dumeéril,
1854. The Mexican Mushroom-tongued Salamander is
distributed from the “Atlantic slope from southern Veracruz
(Mexico) across the base of the Yucatan Peninsula, with an
isolated population in the northern part of Yucatan Peninsula, to
Honduras (extending to the Pacific versant in the Ocotepeque)
and El Salvador (Departamento de Chalatenango, municipio
de La Palma, Cerro La Palma)” (https://amphibiansoftheworld.
amnh.org/). This individual was encountered in Villa Luz, in
the municipality of Tacotalpa, Tabasco. Wilson et al. (2013b)
assessed its EVS as 11, placing it in the lower portion of
the medium vulnerability category. Its conservation status
has been considered as Least Concern (LC) by the IUCN
and it is allocated to the Special Protection (Pr) category by
SEMARNAT. Photo by Liliana Rios-Rodas.
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 5. Distribution of herpetofaunal families in Tabasco, Mexico, by physiographic province. See Table 4 header for an explanation
of the abbreviations.
Distribution among physiographic regions
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Amphib. Reptile Conserv. 17 August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Table 6. Pair-wise comparison matrix of Coefficient of Biogeographic Resemblance (CBR) data of the herpetofaunal relationships
for the three physiographic regions in Tabasco, Mexico. Underlined values = number of species in each region; upper triangular
matrix values = species in common between two regions; and lower triangular matrix values = CBR values. The formula for this
calculation is: CBR = 2C/N, + N, (Duellman, 1990), where C is the number of species common to both regions, N, is the number of
species in the first region, and N, is the number of species in the second region. See Table 4 for an explanation of the abbreviations,
and Fig. 12 for the UPGMA dendrogram produced from the CBR data.
Gulf Coastal Plain Sierra Norte de Chiapas Sierras Bajas del Petén
Gulf Coastal Plain 88 71 61
Sierra Norte de Chiapas 0.61 145 79
Sierras Baja de Petén 0.67 0.66 93
The eight single-region species inthe SBP (Table 7) areas 79 between the SNC and the SBP. The average value of
follows (numbers refer to the distributional categories as — shared species among all three regions is 70.3.
designated by Wilson et al. [2017]; an asterisk indicates The CBR data in Table 6 demonstrate values ranging from
country endemics): 0.61 to 0.67 (see below), with a mean value of 0.65. This
range of CBR values is limited and the values are relatively
Triprion petasatus 4 high, indicating that many of these species are widespread.
Engystomops pustulosus 6 We determined the numbers of species inhabiting one,
Bolitoglossa alberchi* two, and three of the recognized physiographic regions
Scincella gemmingeri* (Table 7). In each of the two smaller herpetofaunas for
Coniophanes schmidti 4 the Gulf Coastal Plain and the Sierras Bajas del Petén
Leptodeira frenata 4 subregion the numbers of species found in one, two,
Agkistrodon russeolus 4 and three regions increase from the lowest to the highest
Crotalus tzabcan 4 value. However, in the area with the largest herpetofauna
(145 species), the Sierra de Norte de Chiapas, the number
Two of these eight species (25.0%) are country endemics __ of single-region species (50) is higher than the number
and the remaining six are non-endemics. Of the six non- — of the double-region species (40), and is closer to the
endemic species, one is an MXSA species and the other number of species occupying all three regions (55).
five are MXCA species. Of the 170 total herpetofaunal species in Tabasco, 101
In summary, of the 69 single-region species distributed (59.4%) are found in two or three physiographic regions,
in Tabasco, 51 (73.9%) are non-endemics, 16 (23.2%) leaving 69 (40.6%) with a distribution in only a single
are country endemics, and two (2.9%) are non-natives. region (see above). Thus, 50 of these 69 single-region
Of the three physiographic regions in Tabasco, the SNC __ species are restricted to the Sierra Norte de Chiapas.
is of greatest conservation importance, given that it The highest CBR value (0.67) is that between the
supports the largest overall number of species (145), as | GCP and the SBP, and the lowest value (0.61) is between
well as the largest numbers of single-region species (50) — the GCP and the SNC. We expected a relatively high
and country-endemics (13). level of resemblance among these three areas, since the
two higher-elevation regions are adjacent to the lower-
We constructed a Coefficient of Biogeographic elevation region, and all three regions contain relatively
Resemblance (CBR) matrix for establishing the —lowelevations (see above).
herpetofaunal similarity relationships among the three The overall CBR values among the three physiographic
physiographic regions in Tabasco (Table 6). The SNC _ regions are as follows, arranged from the highest to
supports the highest level of species richness at 145 — lowest value (species numbers in parentheses):
species, followed by 93 in the SBP, and 88 in the GCP.
The mean species richness for the three regions is 108.7. GCP (88) — 0.61 — SNC (145)
The numbers of shared species among all regional SBP (93) — 0.66 — SNC (145)
pairs range from 61 between the GCP and the SBP to GCP (88) — 0.67 — SBP (93)
Table 7. Counts of the number of species within each of the three physiographic regions in Tabasco, Mexico, which occupy one,
two, or three of the physiographic regions.
Physiographic Number of regions inhabited
region One Two Three Total
Gulf Coastal Plain 1] 22 55 88
Sierra del Norte de 50) AO 55 145
Chiapas
Sierras Baja del Petén 8 30 55 93
State total 69 46 55 170
Amphib. Reptile Conserv. 18 August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
pes ae SF
No. 13. Bolitoglossa veracrucis Taylor, 1951. The Veracruz
Salamander previously was known only from the type
locality (Veracruz, Mexico), at 100 to 1,000 m elevation
(https://amphibiansoftheworld.amnh.org/). In 2008, however,
a population of this species was recorded for the first time
in the state of Tabasco, from Cuevas de Muku Chem, in the
municipality of Tacotalpa (Geronimo-Torres et al. 2022).
Wilson et al. (2013b) calculated its EVS as 17, placing it
in the middle portion of the high vulnerability category. Its
conservation status has been considered as Endangered (EN)
by IUCN, and as a species of Special Protection (Pr) by
SEMARNAT. Photo by Marco Antonio Torrez-Pérez.
No. 15. Corytophanes hernandesii (Wiegmann, 1831).
Hernandez’s Helmeted Basilisk occurs at low and moderate
elevations on the Atlantic versant from southeastern San Luis
Potosi, Mexico, to northwestern Honduras (McCranie et al.
2004). This individual was encountered in the Ejido Villa
Guadalupe of Huimanguillo, Tabasco. Wilson et al. (2013a)
determined its EVS as 13, placing it at the upper limit of the
medium vulnerability category. Its conservation status has not
been determined by the IUCN, but this species was provided
Special Protection (Pr) status by SEMARNAT. Photo by José
del Carmen Geronimo-Torres.
Amphib. Reptile Conserv.
No. 14. Corytophanes cristatus (Merrem, 1820). The Smooth
Helmeted Iguana is found at low and intermediate elevations
on the Gulf and Caribbean slopes from central Veracruz to
Colombia (Lee 1996). This lizard ranges from central Veracruz
and the southern part of the Yucatan Peninsula in Mexico,
southward on the Atlantic versant and lowlands of Central
America through northern Guatemala and Belize to Costa Rica,
where it occurs on both the Atlantic and Pacific slopes into
northwestern Colombia (Campbell 1998). This individual was
found in the municipality of Tacotalpa, Tabasco, in secondary
vegetation. Its EVS has been determined as 11, placing it in
the middle portion of the medium vulnerability category, and
its IUCN status has been assessed as Least Concern (LC). This
species was allocated to the Special Protection (Pr) category
by SEMARNAT. Photo by Marco Antonio Torrez-Pérez.
No. 16. Norops barkeri Schmidt, 1939. Barker’s Anole is a
semiaquatic anole endemic to southern Mexico. This species
is known from states of Veracruz, Chiapas, Oaxaca, and
Tabasco (Powell and Birt 2001). This individual was found
in the Ejido Villa Guadalupe of Huimanguillo, Tabasco.
This lizard’s EVS has been assessed as 15, placing it in the
lower portion of the high vulnerability category (Wilson et al.
2013a). Its IUCN status has been determined as Vulnerable
(VU), and it is considered a species of Special Protection (Pr)
by SEMARNAT. Photo by Jenny del C.-Estrada- Montiel.
August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
SBP GCP SNC
1.00
90
80
10 ss .64
60
0
AO
30
.20
10
OO
Fig. 5. UPGMA-generated dendrogram illustrating the simi-
larity relationships of species richness among the herpetofau-
nal components in the three physiographic regions of Tabasco
(based on the data in Table 6; Sokal and Michener 1958). Simi-
larity values were calculated using Duellman’s (1990) Coef-
ficient of Biogeographic Resemblance (CBR).
Based on the data in Table 6, we created a UPGMA
dendrogram (Fig. 5) to demonstrate the herpetofaunal
resemblance patterns among the three physiographic
regions in Tabasco (see map, Fig. 1). The dendrogram
indicates that the CBP and GCP cluster at the 0.67 level
and the SNC clusters to the previous pair at the 0.64
level. This overall pattern indicates that all three regions
are closely aligned together at an intermediate level of
resemblance.
Distribution Status Categorizations
We utilized the same system as Alvarado-Diaz et al.
(2013) to examine the distribution status of members
of the Tabasco herpetofauna, and this system has been
used in all the subsequent entries in the MCS (see above).
The categories in this system are non-endemic, country
endemic, state endemic (of which none occur in Tabasco),
and non-native. These categorizations are listed in Table
8 and summarized in Table 9.
The numbers of species in each of the three applicable
categories, in decreasing order of size, are as follows:
non-endemics, 145 (85.3% of total of 170 species):
country endemics, 20 (11.8%); and non-natives, five
(2.9%). As with the states of Oaxaca (Mata-Silva et
al. 2015), Chiapas (Johnson et al. 2015a), Tamaulipas
(Teran-Juarez et al. 2016), Nuevo Leon (Nevarez-de los
Reyes et al. 2016), Coahuila (Lazcano et al. 2019), and
Veracruz (Torres-Hernandez et al. 2021), as well as the tri-
state Yucatan Peninsula (Gonzalez-Sanchez et al. 2017),
Amphib. Reptile Conserv.
most of the herpetofaunal taxa in Tabasco fall within the
non-endemic category. In the other six states evaluated
in the Mexican Conservation Series, the largest number
falls within the country endemic category: Michoacan
(Alvarado-Diaz et al. 2013); Nayarit (Woolrich-Pifia
et al. 2016); Jalisco (Cruz-Saenz et al. 2017); Puebla
(Woolrich-Pifia et al. 2017); Hidalgo (Ramirez-Bautista
et al. 2020); and Querétaro (Cruz-Elizalde et al. 2022).
Twenty country endemic species are present in
Tabasco, and perhaps this relatively low number was
expected because the state lies largely on the Gulf
Coastal Plain and adjacent to relatively low-elevation
areas, which generally are not known for significant
herpetofaunal endemism. No state endemic species
occur in Tabasco. In the 13 previous entries in the MCS
(including the Oaxaca update; Mata-Silva et al. 2021),
the number of state endemic species ranges from one
in Nayarit and Nuevo Leon (Woolrich-Pifia et al. 2016;
Nevarez-de los Reyes 2016) to 105 in Oaxaca (Mata-
Silva et al. 2021).
Five non-native species have been recorded from
Tabasco, including Eleutherodactylus _ planirostris,
Norops sagrei, Hemidactylus frenatus, H. turcicus, and
Virgotyphlops braminus. Two of these five species (7.
frenatus and V. braminus) are the most widespread of the
non-native species recorded in the 13 entries in the MCS
(Cruz-Elizalde et al. 2022), and to date they have been
reported in 13 states or tri-state regions.
Wilson et al. (2017) introduced a system for the
distributional categorization of the Mesoamerican
herpetofauna. The data for the categories applicable to this
work are summarized in Table 10. Previously, we noted
that 145 species are non-endemic to Tabasco, and we
allocated them to six of the nine categories developed by
Wilson et al. (2017), including MXUS, MXCA, MXSA,
USCA, USSA, and OCEA. As expected, the greatest
number and proportion of species fall into the MKCA
category (95, or 65.5%), given the proximity of Tabasco
to Central America and since a significant portion of its
eastern border is shared with Guatemala. Interestingly,
the next largest number and proportion of species are
allocated to the MXSA category (34, or 23.4%). Oddly,
only a single species (0.7%) is assigned to the MXUS
category. By way of comparison, this category contains
29 species, or 17.2%, in the herpetofauna of the adjacent
state to the west (1.e., Veracruz; Torres-Hernandez et al.
2021). The remaining 15 species are in the USCA (eight,
or 5.5%), USSA (four, or 2.7%), and OCEA (three, or
2.1%) categories.
Principal Environmental Threats
Deforestation
Deforestation in southeastern Mexico is a serious matter
that has worsened over time, and the state of Tabasco is
no exception (Fig. 6). The continuous loss of vegetational
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
No. 17. Norops compressicauda Smith and Kerster, 1955. The
Malposo Scaly Anole is endemic to Mexico. This anole has
been reported from the states of Oaxaca, Veracruz, and Chiapas.
Here we present the first records of this species from the state
of Tabasco, from the municipalities of Teapa and Tacotalpa,
in montane areas at elevations from 100 to 700 m (Rios
Rodas et al. 2017). Wilson et al. (2013a) calculated its EVS
as 15, placing it in the lower portion of the high vulnerability
category. Its conservation status has been considered as Least
Concern (LC) by the IUCN, but this species is not listed by
SEMARNAT. Photo by Liliana Rios-Rodas.
a Geer ea
y
No. 19. Ctenosaura similis (Gray, 1831). The Common
Spiny-tailed Iguana occurs at low and moderate elevations
from southern Veracruz and Oaxaca southward to Panama
(Lee 1996). The native range of this species extends along
the Atlantic versant from the Isthmus of Tehuantepec
southeastward to northeastern Nicaragua, and on the Pacific
versant from the Isthmus of Tehuantepec southeastward
to Panama (Kohler 2003). This individual was found in
rainforest at an elevation of 200 m, in the municipality of
Tenosique, Tabasco. Wilson et al. (2013a) calculated its EVS
as 8, placing it in the upper portion of the low vulnerability
category. Its conservation status has been considered as Least
Concern (LC) by the IUCN. This species was allocated to the
Threatened (A) category by SEMARNAT. Photo by Maria del
Rosario Barragan-Vazquez.
Amphib. Reptile Conserv.
21
No. 18. Coleonyx elegans Gray, 1845. The Yucatan Banded
Gecko is distributed on the Gulf and Pacific slopes in the
states of the southeastern region of Mexico. In Tabasco, this
species has been recorded in the municipalities of Tacotalpa,
Huimanguillo, and Teapa. This individual is from Muku
Chem, in the municipality of Tacotalpa, Tabasco. Its EVS has
been determined as 9, placing it at the upper limit of the low
vulnerability category (Wilson et al. 2013a). Its IUCN status
has been assessed as Least Concern (LC), and as Threatened
(A) by SEMARNAT. Photo by Manuel Herndndez-May.
— S ee _
No. 20. Sceloporus teapensis Ginther, 1890. The Teapen
Rosebellied Lizard occurs at low elevations on the Atlantic
slopes from southern Veracruz and Oaxaca, eastward through
Chiapas, Tabasco, and Campeche, and through the Petén region
of Guatemala to Belize, and south to Coban, Alta Verapaz,
Guatemala (Lee 1996). This individual was encountered in the
Ejido Villa Guadalupe of Huimanguillo, Tabasco. Wilson et al.
(2013a) determined its EVS as 13, placing it at the upper limit
of the medium vulnerability category. Its conservation status
has been assessed as Least Concern (LC) by the IUCN, but
has not been determined by SEMARNAT. Photo by Jenny del
Carmen Estrada- Montiel.
August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Fig. 6. Deforestation due to road construction in the vicinity
of Paraiso, Tabasco. Photo by José del Carmen Geronimo-
Torres.
cover in tropical forest has been precipitated primarily by
a shift in land use for livestock and agricultural activities,
lumber extraction, an increasing number of roads, oil
production-related activities, and the direct effect of
human population growth (Maldonado-Sanchez et al.
2016). To date, Tabasco has lost more than 90% of its
original vegetational cover (Zavala-Cruz and Castillo
2003), and more recent data indicate that approximately
only 2% of this vegetation remains (Sanchez-Munguia
2005). In the basins of the Grijalva and Usumacinta
rivers, the tropical forest cover has been reduced from
36% in 1993 to only 9% in 2007 (Kolb and Galicia 2012).
The above numbers reveal the somber panorama
that Tabasco currently faces, which directly affects the
prospects for conserving biodiversity, including its
herpetofauna. The last remnants of forest in Tabasco
are distributed mostly in the municipalities of Teapa,
Tenosique, Huimanguillo, and Macuspana (Castillo and
Zavala 1996); ironically, these are the same geographic
entities where various extension records of amphibians
and reptiles have been reported in recent years. Species
such as the Northern Glass Frog (Hyalinobatrachium
viridissimum), the Chiapan Highlands Treefrog
(Exerodonta bivocata), the Smooth-headed Helmeted
Basilisk, locally known as Turipache (Corytophanes
cristatus), Barker’s Anole (Norops barkeri), and the
Keeled Earth Snake (Geophis carinosus) are just a few
worthy of mention. These records highlight the need for
continuous and urgent exploration, especially in areas
that still contain tropical forest.
Agricultural Activities
As mentioned earlier, one of the main drivers of
deforestation is farming (Fig. 7) and livestock activities.
In this regard, Alejandro-Montiel et al. (2010) stated
that these activities are responsible for 94% of the land
change that has taken place in Tabasco. Noteworthy
agricultural policies for Tabasco were developed in the
1960s and 1970s (Plan Chontalpa and Plan Balancan-
Amphib. Reptile Conserv.
22
Fig. 7. Conversion of land use for agricultural purposes in
the community of Villa Luz, in the municipality of Tacotalpa,
Tabasco. Photo by Liliana Rios-Rodas.
Tenosique), and have affected more than 200,000 ha,
resulting in the complete elimination of evergreen
tropical forest and the desiccation of wetlands for the
later development of urban communities (Barkin 1978).
For example, immediately after the completion of one of
these projects, a subsequent study revealed that only 8%
of the forests remained in the municipalities of Balancan
and Tenosique, which increased flooding and soil erosion
in those areas (Tudela 1989; Torres-Masuera 2021).
These programs did not have the promised results, but
on the contrary were responsible for the loss of forest
and biodiversity that have not recovered thus far. This
infamous action was never reported; therefore, there are
no actual numbers that can reveal the specific amount of
biodiversity affected.
Currently, Tabasco dedicates more than 253,000 ha
to the cultivation of banana, sugarcane, cocoa, corn,
and oil palm. Unfortunately, these large-scale crops
are damaging to the remaining natural ecosystems in
the state, whose effects are exacerbated by the large
amount of associated chemicals. The municipalities of
Huimanguillo and Balancan have the largest amount of
land used for cultivation, and Huimanguillo also has the
largest livestock production (Infografia Agroalimentaria
2017). Atthe same time, the municipality of Huimanguillo
contains remnants of evergreen tropical forest where
additional species have been reported in recent times,
expanding their geographic distributions. The current
and historical situation regarding the development of
agriculture in the state also indicates the continuous
damage inflicted on natural ecosystems and, therefore,
all of the species they harbor.
Roads
Roads represent an important contributor to the
intensification of productivity in communities, and
simultaneously are an instrumental component for social,
economic, and cultural integration. According to INEGI
(2009), Tabasco has an extensive system of roads, and is
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
No. 21. Sphaerodactylus continentalis Werner, 1896. The
Upper Central American Geckolet occurs at “low and
moderate elevations from the Isthmus of Tehuantepec in
northern Oaxaca, Mexico, to about the Catacamas, Olancho,
region of east-central Honduras;” this species “also occurs
on Utila Island in the Honduran Bay Islands and possibly
on Cozumel Island, Quintana Roo, Mexico” (McCranie and
Hedges 2012). This individual is from Muku Chem, in the
municipality of Tacotalpa, Tabasco. Mata-Silva et al. (2021)
determined its EVS as 10, placing it at the lower limit of the
medium vulnerability category. Its conservation status has
been evaluated as Least Concern (LC) by the IUCN, but it
has not been assessed by SEMARNAT. Photo by Liliana Rios-
Rodas.
ee
Ab si ares
No. 23. Lepidophyma flavimaculatum Dumeril, 1851. The
Yellow-spotted Night Lizard is found at low and moderate
elevations on the Atlantic slope from Veracruz eastward
through northern Guatemala, Belize, and northern Honduras.
In the Yucatan Peninsula it is known from northeastern
Chiapas, El Petén, Belize, and southern Quintana Roo
(Lee 1996). This individual was located in the Ejido Villa
Guadalupe of Huimanguillo, Tabasco. Wilson et al. (2013a)
assessed its EVS as 8, placing it in the upper portion of the
low vulnerability category. Its conservation status has been
evaluated as Least Concern (LC) by the IUCN, and this
species was placed in the Special Protection (Pr) category by
SEMARNAT. Photo by José del Carmen Gerénimo-Torres.
Amphib. Reptile Conserv.
No. 22. Holcosus stuarti Smith, 1940. The Rainbow Ameiva
occurs on the “Atlantic slopes of Mexico from the middle of
the Isthmus of Tehuantepec eastward in the lowlands to the
southern borders of Laguna de Términos and to Tenosique,
Tabasco; southward up the valley of the Rio Grijalva at least
as far as Tuxtla Gutiérrez, Chiapas” (Meza-Lazaro and Nieto-
Montes de Oca 2015). This individual was located in the
Ejido Villa Guadalupe of Huimanguillo, Tabasco. Wilson et
al. (2013a) determined its EVS as 7, placing it in the middle
limit of the low vulnerability category. Its conservation status
has been evaluated as Least Concern (LC) by the IUCN, but
this species is not listed by SEMARNAT. Photo by Jenny del
Carmen Estrada- Montiel.
No. 24. Leptophis mexicanus Duméril, Bibron, and Dumeéril,
1854. The Mexican Parrot Snake is distributed in southeastern
Mexico, including Chiapas, Veracruz, Oaxaca, Tabasco,
Yucatan, Campeche, San Luis Potosi, Querétaro, Tamaulipas,
Puebla, Hidalgo, Nuevo Leon, Guerrero, and Yucatan
Peninsula, into Guatemala, Honduras, Belize, El Salvador,
Nicaragua, and Costa Rica. In Guatemala it occurs from near
sea level to about 1,360 m in elevation (Lee 1996; Campbell
1998). This individual was found in the municipality of
Tacotalpa, Tabasco, in secondary vegetation (acahual). Its
EVS has been determined as 6, placing it in the middle portion
of the low vulnerability category. Its conservation status has
been considered as Least Concern (LC) by the IUCN and it
is allocated to the Threatened (A) category by SEMARNAT.
Photo by Marco Antonio Torrez-Pérez.
August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Fig. 8. Roads. A Boa imperator dead on the road in the Pantanos
de Centla Biosphere Reserve, in the municipality of the same
name, Tabasco. Photo by Coral J. Pacheco-Figueroa.
among the three best-served states in the country, with
an index of 248 m/km? (Vidal-Garcia and Negrete 2019).
The construction and functioning of roads are elements
that have drastic and long-term consequences on the
natural landscape, as they significantly affect the survival
of the native herpetofauna (Trombulak and Frissell 2000;
Coffin 2007). The building and maintenance of roads
implies the unavoidable removal of native vegetation
cover, thus enabling a series of linked processes that
ultimately lead to the detriment of adjacent habitats.
With respect to the mortality of fauna on roads (Fig.
8), Pozo-Montuy et al. (2019) reported 111 individuals
killed by vehicles on the road from Villahermosa to
Zacatal; of those, 22.5% were reptiles and 20.7%
amphibians. The species affected more frequently were
in the families Iguanidae, Boidae, Colubridae, Viperidae,
and Geoemydidae; more specifically for lizards they
included Green Iguanas ([guana rhinolopha) and Black
Iguanas (Ctenosaura similis) (Canales-Delgadillo et al.
2020). Other studies carried out in the state reported the
killing of 1. rhinolopha on highway 186 (Villahermosa-
Aeropuerto) and the Cane Toad (Rhinella horribilis) on
the Tabascan plains. Lastly, a survey conducted at Reserva
de la Bidsfera Pantanos de Centla showed that 43% of the
road-kills were amphibians, primarily Brown’s Leopard
Frog (Lithobates brownorum) (Pacheco-Figueroa 2021).
Soil Pollution and Ojil-related Activities
In Tabasco, the municipalities with the highest numbers
of oil spills that affected numerous hectares of land
from 1995 until 2001 were Cardenas, Huimanguillo,
Cunduacan, and Comalcalco (Ochoa-Gaona et al.
2011). The long history of oil spills and gas explosions
in Tabasco (Fig. 9) has led to serious consequences in
many communities, because this activity also resulted in
the pollution of soils and vegetation such as grasslands
(Zavala-Cruz et al. 2005). Some studies have identified
approximately 7,500 ha that are affected, more than 90%
of which are located in wetlands (Adams-Schroeder
Amphib. Reptile Conserv.
24
Fig. 9. Deforestation due to oil activities in the vicinity of
Paraiso, Tabasco. Photo by José del Carmen Geronimo-
Torres.
1999; Beltran-Paz 2006). It was estimated that 0.07% of
the state was polluted with fossil fuels (Rivera-Cruz and
Trujillo-Narcia 2004; Ferrera-Cerrato et al. 2006). All
amphibian groups found in Tabasco have been affected
by the oil industry, although a study by Reynoso-Rosales
(1999) in southeastern Mexico, including Tabasco,
determined that the detriment to amphibians ts the result
of a combined effect from both farming and the oil
industry. With respect to the latter activity, this includes
consecutive processes such as exploration, perforation,
and production. Among the direct effects from the oil
industry are the disturbances caused by permanent
light sources at all installations, which likely affect
the behavior of species present around these industrial
facilities. For instance, toads (Rhinella and Incilius)
congregate at light sources to search for food.
Myths and Cultural Factors
With respect to the herpetofauna, ethnozoological
knowledge includes symbolic, spiritual, and social
meanings in indigenous societies (Avila-Najera et
al. 2018), although few studies have addressed this
subject in Tabasco. Among the most frequent uses of
native herpetofauna are for food (iguanas, turtles, and
crocodiles, Hernandez-Lopez et al. 2012) and magic-
religious uses in conjunction with medicinal application.
For example, rattlesnakes (Crotalus) are used to treat
cancer, diabetes, acne, and skin health issues (GOmez-
Alvarez and Pacheco 2010). On the other hand, snakes
generally are considered as dangerous, and _ their
encounters usually result in their immediate elimination.
A similar situation 1s experienced by amphibians, which
are considered mostly as undesirable.
People in Tabasco have consumed native terrestrial
vertebrates for millennia, primarily reptiles, birds,
and mammals as food, as well as for skins, pets, and
medicinal purposes (Pozo-Montuy et al. 2019). To date,
16 species of reptiles have been identified as traditionally
consumed in Tabasco, such as iguanas, turtles, snakes,
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
© Marco A. Torrez Pérez
No. 25. Oxybelis potosiensis (Taylor, 1941). The Gulf Coast
Vine Snake is distributed from San Luis Potosi and northern
Veracruz, southward to Yucatan, Mexico, and Belize (Jadin
et al. 2020). This individual was found in the municipality
of Huimanguillo, Tabasco. Its EVS has been determined as
5 (Cruz-Elizalde et al. 2022), placing it in the lower portion
of the low vulnerability category. Its conservation status has
not been evaluated (NE) by the IUCN, and it is considered
as having No Status (NS) by SEMARNAT. Photo by Marco
Antonio Torrez-Pérez.
ae
= = aa
j ©Maseo A. TorreZ érez
No. 26. Coniophanes imperialis (Baird and Girard, 1859). The
Black-striped Snake occurs at low and moderate elevations
on the Atlantic slope from southern Texas southward on
the Atlantic watershed through eastern Mexico, Yucatan,
Belize, and northern and eastern Guatemala to Honduras;
it also occurs locally on Pacific slopes in Oaxaca, Chiapas,
Yucatan, Campeche, and Quintana Roo (Lee 1996; Campbell
1998). This individual was found in the municipality of
Huimanguillo, Tabasco. Its EVS has been determined as
8, placing it in the upper portion of the low vulnerability
category. Its conservation status has been established as Least
Concern (LC) by the IUCN, but has been assigned No Status
(NS) by SEMARNAT. Photo by Marco Antonio Torrez-Pérez.
No. 27. Enulius flavitorques (Cope, 1868). The Pacific Long-
tailed Snake occurs at low and moderate elevations on the
Pacific versant from Jalisco, Mexico, to Panama, and on the
Atlantic versant in Chiapas, Mexico, Honduras (including Isla
Utila in the Islas de la Bahia), Panama, northern Colombia,
and northwestern Venezuela (Hernandez- Valadez et al. 2016).
This individual was found in a coconut plantation in Playa
Chiltepec, in the municipality of Paraiso, Tabasco. Its EVS
has been determined as 5, placing it in the lower portion of
the low vulnerability category. Its conservation status has been
evaluated as Least Concern (LC) by the IUCN, but its status
remains undetermined (NS) by SEMARNAT. Photo by Marco
Antonio Lopez-Luna.
Amphib. Reptile Conserv.
No. 28. Jmantodes cenchoa (Linnaeus, 1758). The Neotropical
Blunt-headed Treesnake occurs at low and moderate elevations
in Mexico, from Chiapas on the Pacific slope and Tamaulipas
on the Atlantic slope, southward throughout most of the
Petén region in Guatemala and the northeastern portion of
Yucatan Peninsula, through the remainder of Central America
to Argentina and Paraguay (Lee 1996; Campbell 1998). This
individual was found in Muku Chem, in the municipality of
Tacotalpa, Tabasco. Wilson et al. (2013a) determined its EVS
as 6, placing it in the middle portion of the low vulnerability
category. Its conservation status has been considered as Least
Concern (LC) by the IUCN, and as a species of Special
Protection (Pr) by SEMARNAT. Photo by José del Carmen
Geronimo-Torres.
August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Table 8. Distributional and conservation status measures for members of the herpetofauna of Tabasco, Mexico. Distributional
status: CE = endemic to country of Mexico; NE = not endemic to state or country; and NN = non-native. The numbers suffixed
to the “NE” category signify the distributional categories developed by Wilson et al. (2017) and implemented in the taxonomic
list at the Mesoamerican Herpetology website (http://mesoamericanherpetology.com), as follows: 3 (species distributed only in
Mexico and the USA); 6 (species ranging from Mexico to South America); 7 (species ranging from the USA to Central America);
and 8 (species ranging from the USA to South America). Environmental Vulnerability Score (taken from Wilson et al. 2013a,b):
low (L) vulnerability species (EVS of 3-9); medium (M) vulnerability species (EVS of 10—13); and high (H) vulnerability species
(EVS of 14-20). IUCN Categorization: CR = Critically Endangered; EN = Endangered; VU = Vulnerable; NT = Near Threatened;
LC = Least Concern; DD = Data Deficient; NE = Not Evaluated. SEMARNAT Status: A = Threatened; P = Endangered; Pr =
Special Protection; and NS = No Status. See Alvarado-Diaz et al. (2013), Johnson et al. (2015a), and Mata-Silva et al. (2015) for
explanations of the EVS, IUCN, and SEMARNAT rating systems.
Distributional | Environmental IUCN SEMARNAT
Taxa Vulnerability ce
Status categorization status
Category (score)
Amphib. Reptile Conserv. 26 August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 8 (continued). Distributional and conservation status measures for members of the herpetofauna of Tabasco, Mexico.
Distributional status: CE = endemic to country of Mexico; NE = not endemic to state or country; and NN = non-native. The numbers
suffixed to the “NE” category signify the distributional categories developed by Wilson et al. (2017) and implemented in the
taxonomic list at the Mesoamerican Herpetology website (http://mesoamericanherpetology.com), as follows: 3 (species distributed
only in Mexico and the USA); 6 (species ranging from Mexico to South America); 7 (species ranging from the USA to Central
America); and 8 (species ranging from the USA to South America). Environmental Vulnerability Score (taken from Wilson et al.
2013a,b): low (L) vulnerability species (EVS of 3—9); medium (M) vulnerability species (EVS of 10-13); and high (H) vulnerability
species (EVS of 14-20). IUCN Categorization: CR = Critically Endangered; EN = Endangered; VU = Vulnerable; NT = Near
Threatened; LC = Least Concern; DD = Data Deficient; NE = Not Evaluated. SEMARNAT Status: A = Threatened; P = Endangered;
Pr = Special Protection; and NS = No Status. See Alvarado-Diaz et al. (2013), Johnson et al. (2015a), and Mata-Silva et al. (2015)
for explanations of the EVS, IUCN, and SEMARNAT rating systems.
Distributional. | E2vironmental IUCN SEMARNAT
Taxa Vulnerability ahee
status categorization status
Category (score)
Amphib. Reptile Conserv. 27 August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Table 8 (continued). Distributional and conservation status measures for members of the herpetofauna of Tabasco, Mexico.
Distributional status: CE = endemic to country of Mexico; NE = not endemic to state or country; and NN = non-native. The numbers
suffixed to the “NE” category signify the distributional categories developed by Wilson et al. (2017) and implemented in the
taxonomic list at the Mesoamerican Herpetology website (http://mesoamericanherpetology.com), as follows: 3 (species distributed
only in Mexico and the USA); 6 (species ranging from Mexico to South America); 7 (species ranging from the USA to Central
America); and 8 (species ranging from the USA to South America). Environmental Vulnerability Score (taken from Wilson et al.
2013a,b): low (L) vulnerability species (EVS of 3—9); medium (M) vulnerability species (EVS of 10-13); and high (H) vulnerability
species (EVS of 14-20). IUCN Categorization: CR = Critically Endangered; EN = Endangered; VU = Vulnerable; NT = Near
Threatened; LC = Least Concern; DD = Data Deficient; NE = Not Evaluated. SEMARNAT Status: A = Threatened; P = Endangered;
Pr = Special Protection; and NS = No Status. See Alvarado-Diaz et al. (2013), Johnson et al. (2015a), and Mata-Silva et al. (2015)
for explanations of the EVS, IUCN, and SEMARNAT rating systems.
Distributional. | Environmental IUCN SEMARNAT
Taxa Vulnerability aoe
status categorization status
Category (score)
Amphib. Reptile Conserv. 28 August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 8 (continued). Distributional and conservation status measures for members of the herpetofauna of Tabasco, Mexico.
Distributional status: CE = endemic to country of Mexico; NE = not endemic to state or country; and NN = non-native. The numbers
suffixed to the “NE” category signify the distributional categories developed by Wilson et al. (2017) and implemented in the
taxonomic list at the Mesoamerican Herpetology website (http://mesoamericanherpetology.com), as follows: 3 (species distributed
only in Mexico and the USA); 6 (species ranging from Mexico to South America); 7 (species ranging from the USA to Central
America); and 8 (species ranging from the USA to South America). Environmental Vulnerability Score (taken from Wilson et al.
2013a,b): low (L) vulnerability species (EVS of 3—9); medium (M) vulnerability species (EVS of 10-13); and high (H) vulnerability
species (EVS of 14-20). IUCN Categorization: CR = Critically Endangered; EN = Endangered; VU = Vulnerable; NT = Near
Threatened; LC = Least Concern; DD = Data Deficient; NE = Not Evaluated. SEMARNAT Status: A = Threatened; P = Endangered;
Pr = Special Protection; and NS = No Status. See Alvarado-Diaz et al. (2013), Johnson et al. (2015a), and Mata-Silva et al. (2015)
for explanations of the EVS, IUCN, and SEMARNAT rating systems.
Distributional | Environmental IUCN SEMARNAT
Vulnerability Aa
status categorization status
Category (score)
NS
[wes mc) COdOCitSCS”
NEA
NEA
NE6
NEA
NEA
NET
Amphib. Reptile Conserv. 29 August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
—
No. 29. Ninia sebae (Duméril, Bibron, and Duméril, 1854). The
Redback Coffee Snake occurs at low and moderate elevations
on the Atlantic slope from Veracruz and the Pacific slope
from Oaxaca, Mexico, southeastward and eastward through
Central America to Costa Rica (Lee 1996). In Panama it has
been recorded in Changuinola district (Ponce et al. 2008).
In Guatemala it ranges from near sea level to about 2,000
m in elevation (Campbell 1998). This individual was found
in a cornfield in the municipality of Tenosique, Tabasco. Its
EVS has been determined as 5 (Wilson et al. 2013a), placing
it in the lower portion of the low vulnerability category. Its
conservation status has been assessed as Least Concern (LC)
by the IUCN, but as Not Evaluated (NS) by SEMARNAT.
Photo by Maria del Rosario Barragan-Vazquez.
No. 31. Micrurus elegans Jan, 1858. The Elegant Coral
Snake is distributed from Mexico to southwestern Guatemala.
In Mexico it has been reported from the states of Chiapas,
Oaxaca, Puebla, Veracruz, and in the municipality of Teapa,
Tabasco (Soto-Huerta and Clause 2017). This species ranges
from 100 to 1,700 m in elevation. This individual was found
in the municipality of Tacotalpa, Tabasco. Its EVS has been
determined as 13 (Torres-Hernandez et al. 2021), placing it
at the upper limit of the medium vulnerability category. Its
conservation status has been considered as Least Concern
(LC) by the IUCN, but it is considered a species of Special
Protection (Pr) by SEMARNAT. Photo by Marco Antonio
Torrez-Pérez.
Amphib. Reptile Conserv.
a ~ a J
‘ ~~ ae
aot wail Be SEF sa
No. 30. Sibon dimidiatus (Gunther, 1872). The Slender Snail
Sucker occurs at low, moderate, and intermediate elevations
on the Pacific slope of Guatemala, and in premontane areas
from northern Veracruz, Mexico, southward through Central
America to northern Brazil, Colombia, Peru, Venezuela,
Guyana, and Ecuador west of the Andes (Lee 1996; Espinal
et al. 2021). This individual is from Muku Chem, in the
municipality of Tacotalpa, Tabasco. Wilson et al. (2013a)
determined its EVS as 10, placing it at the lower limit of
the medium vulnerability category. Its conservation status
has been assessed as Least Concern by the IUCN, but it has
not been assessed by SEMARNAT. Photo by Marco Antonio
Torrez-Pérez.
© Marco A. Torrez Pérez Cal
No. 32. Epictia phenops (Cope, 1875). The distribution of
the Slender Threadsnake extends “from southern Mexico to
western Honduras” (Wallach 2016: 254). This individual was
found in the city of Villahermosa. The EVS of this blindsnake
has been calculated as 4 (Mata-Silva et al. 2021), placing it
in the lower portion of the low vulnerability category. The
conservation status of this species has not been assessed by
either the IUCN or SEMARNAT. Photo by Marco Antonio
Torrez-Pérez.
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 9. Summary of the distributional status data for herpetofaunal families in Tabasco, Mexico.
Distributional status
Number of
species Non-endemic (NE) oe ae Non-native (NN)
fF
Bifonidie | as | a eS
| CCentrolenidae | CC
| —sCrangastoridae | C‘iEC“ M4 8
| _Eleutherodactylidae | 2 ed
Hylidae
| CSubtotal | 8 8 8
(SBP lcthodont ass S| ee ee
| CSubtotal | SC“<C~d 8
| Dermophiidae TE
| Subtotal aT eee
LOSS SS EE EEE Ee a ae SS)
| Crocodylidae PE
| Subtotal
| Corytophanidae | 4 4
| Dactyloidae a
| —SDiploglossidae | CC CE
| —sEublepharidae |
| Gekkonidae |
SSS an se ST EES ee
| Mabuyidae Td
| __Phrynosomatidae | C“C~*dC“($R USC
| Phyllodactylidae | ECE ee
Te oSeicidae To a SE ee
| _Sphaerodactylidae | Ci
| Sphenomorphidae | t—<C~ss
Ss a a a a ee) eer
|e ExXaniiiidaes ee
| Xenosauridae PE
Sabicea PE Ee | Sea Ee ese se
I = 0c: nD ee
ME Echidne UE
| CdDipsadidae | Ci CD
ee eee Ne Sa
| _Leptotyphlopidae | Ce
ee aaa | (0:
| ——sSSibynophiidae |
——— ih prlopidas —— | | | |__|
ho Vipera
| CSubtotal |G eT
rnd CHeloniidie. car | ros ie ee eee
| Chelydridae Te
| Ss Dermatemyidae | CE
Emydidae
__——— |
| CSubtotal Te
SS a ee: |S | an: | 7a i, | |i: | iil
| CC Sum Total] iO eT HS OO te
NIN]; eyo
pm fr |
HPO fHPOPN[ofefutefolryo]—|—|R]aTE]y
BSleEfPofelrmolrmo]—e[nfelr
ott Leet LO)
tl Rot BNO)
}
Amphib. Reptile Conserv. 31 August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
BA ons ~ i Jie ne ~ x ~ on pa ey. :
No. 33. Thamnophis marcianus (Baird and Girard, 1853).
The Checkered Garter Snake occurs at low and moderate
elevations throughout the southwestern United States and
northern Mexico, and on the Pacific slope of the Isthmus of
Tehuantepec. On the Atlantic slope, it ranges from northern
Chiapas and eastern Tabasco through the Yucatan Peninsula
and southward to Costa Rica (Lee 1996). This individual was
found in the municipality of Huimanguillo, Tabasco. Its EVS
has been determined as 10 (Wilson et al. 2013a), placing it
at the lower limit of the medium vulnerability category. Its
conservation status has been assessed as Least Concern (LC)
by the IUCN, and it has been allocated to the Threatened (A)
category by SEMARNAT. Photo by Marco Antonio Torrez-
Pérez.
No. 34. Agkistrodon russeolus Gloyd, 1972. The distribution
of the Mexican Moccasin primarily extends along the outer
part of the Yucatan Peninsula, from west-central Campeche
and the northern portion of Yucatan and Quintana Roo
on the Gulf side, and in northern Belize on the Caribbean
side, although isolated records are available from extreme
southeastern Campeche and central Petén, Guatemala (Porras
et al. 2013). This individual was found at Nuevo Pochote, in
the municipality of Emiliano Zapata, Tabasco (Charruau et
al. 2014). Its EVS has been determined as 15 (Porras et al.
2013), placing it in the lower portion of the high vulnerability
category (Gonzalez-Sanchez et al. 2017). Its conservation
status has been evaluated as Near Threatened (NT) by the
IUCN and it has been allocated to the Special Protection (Pr)
category by SEMARNAT. Photo by Marco Antonio Lopez-
Luna.
No. 35. Crotalus tzabcan Klauber, 1952. The Yucatan
Neotropical Rattlesnake occurs in the Yucatan Peninsula,
including Campeche, northeastern Chiapas, Quintana Roo,
Tabasco, and Yucatan, México, northern Belize and El Petén,
Guatemala (Lee 1996; Campbell 1998; Campbell and Lamar
2004). This individual was found in the village of El Triunfo
in the municipality of Balancan, Tabasco. Its EVS has been
determined as 16 (Gonzalez-Sanchez et al. 2017), placing it
in the middle portion of the high vulnerability category. Its
conservation status has been designated as Least Concern
(LC) by the IUCN, but as No Status (NS) by SEMARNAT.
Photo by Marco Antonio Lopez-Luna.
Amphib. Reptile Conserv.
No. 36. Metlapilcoatlus mexicanus (Dumeéril, Bibron, and
Dumeril, 1854). The Central American Jumping Pitviper
occurs at low, moderate, and intermediate elevations on
the Atlantic slope “from southern Mexico through Central
America south to Costa Rica and Panama, where it is also
found on the Pacific versant” (Heimes 2016). This individual
was found in the municipality of Tacotalpa, Tabasco, in
secondary vegetation. Its EVS has been determined as 12
(Wilson et al. 2013a), placing it in the upper portion of the
medium vulnerability category. Its conservation status has
been assessed as Least Concern (LC) by the IUCN and it is
allocated to the Threatened (A) category by SEMARNAT.
Photo by Marco Antonio Lopez-Luna.
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 10. Summary of the distributional categories of the herpetofaunal families in Tabasco, Mexico, containing non-endemic
species. The categorizations are as follows: MXUS, species distributed only in Mexico and the United States (except perhaps for
a few also found in Canada); MXCA (species found only in Mexico and Central America); MXSA (species ranging from Mexico
to South America); USCA (species ranging from the United States to Central America (except perhaps for a few also found in the
Antilles); USSA (species ranging from the United States to South America); and OCEA (oceanic species).
Number of Distributional status
Family non-endemic | = MXU MXCA MXSA USCA USSA OCEA
species species 3) species (4) | species (6) species (7) | species (8) | species (9)
|
°
-
°
no a el et
i ———
| Phyllomedusidae | 2 | Oo | 2
Ranidaes ee
| Rhinophrynidae | | CO
| Subtotal | 30 |
| Plethodontidae | 3 | 8
Subtotal ees ee ee
| Dermophiidae |
[Subtotal | |
Total | HA
| Crocodylidae_ | 2 | COT
|Subtotal | 2 CO
| Corytophanidae |] 4 |
|Dactyloidae | |
| Diploglossidae | |
| Eublepharidae | |
|Iguanidae | | CT
Re a Ss ee ee
| Phrynosomatidae | S| ST
| Phyllodactylidae | |
|Scincidae | | CC
| Sphaerodactylidae | 2 | SO | 2
| Sphenomorphidae_ | 1 |
|Teiidae |
|Xantusiidae | EE
(uimne2 ceo |
OTR | NW] ete
RINE MIN
Xenosauridae
Subtotal
Boidae
Colubridae
Dipsadidae
Elapidae
Leptotyphlopidae
Natricidae
a
Typhlopidae
Viperidae
|Subtotal | |
|Cheloniidae [| 2 CT
|Chelydridae
| Dermatemyidae |] |
| Dermochelyidae | |
semyidae S|) eS |e
|Geoemydidae | tt
| Kinosternidae | 3
| Staurotypidae |] 2 |
[Subtotal | |
[Total A § | a
|Sumtotal | 45 TS
Amphib. Reptile Conserv. 33 August 2022 | Volume 16 | Number 2 | e315
ae
=a
ps — 1 — os
a a
—S— i —
ee ee Ol
Pe
Pt Oe _
Se ee ee
en a
| 36
Wye tRelRe|Re|TRe [Nb
The herpetofauna of Tabasco, Mexico
= J
»
ae 3
a oe
“ oe - ae 2 fe “ Cae
- - ie Me “a i %
" ' Las Te at Ray ae ‘ = ‘all
A isto pes | Sab af chen © = aed
Fig. 10. The human consumption of meat from iguanid lizards
of the genus Crenosaura documented in the municipality of
Paraiso, Tabasco. Photo by Liliana Rios-Rodas.
and crocodiles. Among the turtles, the species most
affected are the MHicotea (Trachemys_ venusta),
Pochitoque Tres Lomos (Kinosternon scorpioides),
Pochitoque Jahuactero (Kinosternon acutum), and
Chiquiguao (Chelydra rossignonii). Furthermore, the
Lagarto or Cocodrilo (Crocodylus moreletii) and the
Iguana Verde (/guana rhinolopha) also are in frequent
demand (Pozo-Montuy et al. 2019). The consumption
of these species varies according to the region and
season of the year. For instance, the consumption of
freshwater turtles is a tradition for numerous Tabascan
families during Lent.
Illegal Trade
Unfortunately, the illegal trafficking of reptile species
in Tabasco is a common activity due to the high
demand for meat (iguanas and crocodiles) and turtle
eggs (Figs. 10-11). More specifically, many turtles in
the state have been part of the Tabascan gastronomy
(Guevara-Chumacero et al. 2017). Among _ turtles,
people primarily eat Dermatemys mawii due to its size
and meat quality, and consequently this consumption
has pushed the species to near extinction (Zenteno-Ruiz
et al. 2004). Although this species is consumed mostly
in local communities, the species also 1s sold outside
its distributional range, with prices varying according
to the time of year (Guichard-Romero 2006). The
crocodile (C. moreletii) is desired for its fat, since local
communities use it for treating asthma. Furthermore,
all of the species reported above often are purchased
by people to keep as pets in tanks within their homes.
With regard to amphibians, individuals of the treefrog
Agalychnis taylori are sold as pets due to their attractive
coloration, and often are advertised on websites by
people lacking legal documentation. A similar situation
is happening with the Central American Boa (Boa
imperator), of which individuals usually are kept as
pets, but also are sacrificed for their skin.
Amphib. Reptile Conserv.
-
4 *
a £
vy : =, = —6mw©w
ry me = Itty 7
~ » a Ae
_— : a ' | = " = \ - — ¥ e
_—c : ,
2 a ok. Ww. -3 a ee i } a 4 f
ae “ . ~~ : .. : af wt y « ¥ 2 4
Fig. 11. Illegal trafficking of turtle species in the municipality
of Centla, Tabasco. Photo by Liliana Rios-Rodas.
Fig. 12. Forest fires caused by agricultural activities, Laguna
San Isidro, Reserva de la Biosfera Pantanos de Centla, Tabasco.
Photo by Marco Antonio Torrez-Pérez.
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
No. 37. Dermatemys mawii (Gray, 1847). The Central American
River Turtle occurs in the Caribbean lowlands of southern
Mexico from central Veracruz southeastward through the
southern portion of the Yucatan Peninsula (Campbell 1998). In
Tabasco this species is distributed practically throughout the
state; however, wild populations have decreased considerably
because it is hunted as a food source and its habitat has been
severely modified (Rangel-Mendoza and Weber 2015). This
individual belongs to the management unit of the Academic
Division of Biological Sciences at the Universidad Juarez
Auténoma de Tabasco. Its EVS has been determined as 17
(Wilson et al. 2013a), placing it in the middle portion of the
high vulnerability category, and its IUCN status has been
assessed as Critically Endangered (CR). It was allocated to the
Endangered (P) category by SEMARNAT. Photo by Liliana
Rios-Rodas.
No. 39. Claudius angustatus Cope, 1865. The Narrow-bridged
Musk Turtle occurs at low elevations on the Gulf versant of
Mexico from southeastern Veracruz, Tabasco, and Campeche,
and it is restricted to the base of the Peninsula de Yucatan,
through northern Guatemala and northern Belize (Lee
1996). This individual was located at Division Académica
de Ciencias Biologicas of Universidad Juarez Autonoma de
Tabasco, in the municipality of Centro. Wilson et al. (2013a)
assessed its EVS as 14, placing it at the lower limit of the high
vulnerability category. Its conservation status was evaluated
as Near Threatened (NT) by the IUCN, and it was placed
in the Endangered (P) category by SEMARNAT. Photo by
Liliana Rios-Rodas.
Amphib. Reptile Conserv.
No. 38. Kinosternon leucostomum (Duméril, Bibron, and
Dumeril, 1851). The White-lipped Mud Turtle occurs at low
elevations from southern Veracruz, Mexico, southeastward
through Central America to Colombia and the Pacific lowlands
of Ecuador (Lee 1996). This individual was located at Division
Académica de Ciencias Biologicas of Universidad Juarez
Autonoma de Tabasco, in the municipality of Centro. Wilson
et al. (2013a) assessed its EVS as 10, placing it at the lower
limit of the medium vulnerability category. Its conservation
status has not been evaluated by the IUCN, but was assessed
as Special Protection (Pr) by SEMARNAT. Photo by Liliana
Rios-Rodas.
. wey, 5 a Ce | x
No. 40. Staurotypus triporcatus (Wiegmann, 1828). The
Mexican Giant Musk Turtle occurs at low elevations on
the Atlantic slope from central Veracruz, northern Oaxaca,
northern and eastern Chiapas, western Campeche, Mexico, as
well as southward and eastward through northern Guatemala
and Belize (Lee 1996; Reynoso et al. 2016). This individual
was located at Division Académica de Ciencias Bioldgicas of
Universidad Juarez Autonoma de Tabasco, in the municipality
of Centro. Wilson et al. (2013a) assessed its EVS as 14,
placing it at the lower limit of the high vulnerability category.
Its conservation status has been evaluated as Near Threatened
(NT) by the IUCN, and as Threatened (A) by SEMARNAT.
Photo by Liliana Rios-Rodas.
August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Wildfires
In general, farming activities cause most wild fires
in Tabasco. The deliberate burning of grasses before
cultivation is a frequent practice by farmers who burn the
land to eliminate undesirable plants in order to benefit
their grasslands. Furthermore, the resulting ashes from
these fires are regarded as valuable fertilizer for their
grasses (Camara-Cabrales et al. 2019). Unfortunately,
these practices are performed without any regulations,
and may end up accidently burning a larger area than
originally planned, including entire forest plantations
(Camara-Cabrales et al. 2019). In addition, remnant
areas of tropical forest also are burned, since many
farms are located within this vegetation type. Fires
have caused communities such as Villa de Guadalupe in
Huimanguillo, Sierra El Madrigal in Teapa, and Sierra de
Tenosique, to eradicate large tracts of tropical forest, and
consequently many animals are killed, impeded by their
slow movement. Another important area that has suffered
the consequences of wildfires is Reserva de la Bidsfera
Pantanos de Centla, where local villagers traditionally
use fires to capture turtles during the dry season; and
these fires not only kill the turtles, but also burn their
nests and eggs (Beauregard-Solis et al. 2010; Zenteno-
Ruiz et al. 2004).
Conservation Status
We used the same three systems of conservation
assessment as in the previous entries in the Mexican
Conservation Series (see above), 1.e., SEMARNAT
(2010), the IUCN Red List (http://tucnredlist.org), and
the EVS (Wilson et al. 2013a, b). We have continued
to update the assessments from these three systems as
necessary.
The SEMARNAT System
The Secretaria del Medio Ambiente y Recursos Naturales
(SEMARNAT) of the federal government of Mexico
developed a system of conservation assessment for
the national fauna (SEMARNAT 2010), which is used
by many Mexican herpetologists. Three categories are
employed in the SEMARNAT system: endangered (P),
threatened (A), and under special protection (Pr). We
allocated the species remaining unassessed in this system
to date into a “No Status” (NS) category. The ratings
available for the Tabasco herpetofauna are given in Table
8 and summarized in Table 11.
As noted in previous entries in the Mexican
Conservation Series (see above), only a small portion
of the herpetofauna of Tabasco has been assessed using
this system. Of the 165 native species occurring in
Tabasco, only 56 species (33.9%) have been provided
with SEMARNAT ratings and are placed in the three
categories as follows: Endangered (P), four (2.4%);
Amphib. Reptile Conserv.
Threatened (A), 10 (6.1%); and Special Protection (Pr),
42 (25.5%). The majority of the species native to Tabasco
(109, or 66.1%), however, have a No Status (NS) rating
by the SEMARNAT system. In our opinion, until and
unless all the species occurring in the state are assessed
this system will be of little help in understanding the
conservation needs of the herpetofauna of Tabasco.
Assuming that the SEMARNAT personnel have
placed a greater emphasis on assessing endemic species
in Mexico, then this should be evident by comparing the
distributional category assignments and the SEMARNAT
assessments. To ascertain whether such a bias exists, the
pertinent data in Table 12 indicate that the majorities of
species in Tabasco are non-endemic and have not been
assessed (98, or 59.4%), and the evaluated species are
also largely non-endemic (47, or 28.5%). Thus, these
data indicate no bias toward the assessment of country
endemic species.
The IUCN System
The system of conservation assessment developed
and implemented by the International Union for
Conservation of Nature is used broadly, but it has been
criticized in earlier entries of the Mexican Conservation
Series for several reasons, as discussed in Johnson et al.
(2015b). Still, the assessments available for the Tabasco
herpetofauna are collated in Table 8 and summarized in
Table 13.
Of the 165 native herpetofaunal species in Tabasco,
114 (69.1%) have been evaluated using the IUCN system
(Table 13). Of these 114 species, 19 have been allocated
to the three threat categories of CR (four, or 3.5%); EN
(four, or 3.5%); and VU (11, or 9.6%). The four CR
species are the anurans Ptychohyla macrotympanum and
Agalychnis moreletii and the turtles Lepidochelys kempii
and Dermatemys mawii;, and all four are non-endemic.
The four EN species are the anurans Charadrahyla
chaneque and Duellmanohyla chamulae, the salamander
Bolitoglossa veracrucis, and the turtle Chelonia mydas,
and the anurans and the salamander are country endemics
while the turtle is non-endemic. The 11 VU species are the
anurans Incilius macrocristatus, Craugastor alfredi, C.
rhodopis, and Eleutherodactylus leprus, the salamander
Bolitoglossa alberchi, the caecilian Dermophis
mexicanus, the crocodylian Crocodylus acutus, the lizard
Norops barkeri, and the turtles Chelydra rossignonii,
Dermochelys coriacea, and Trachemys venusta. The
three anurans are non-endemic, except for C. rhodopis,
which is a country endemic, the salamander is a country
endemic, the caecilian and crocodylian are non-endemic,
the lizard is a country endemic, and the three turtles are
non-endemic.
The remaining 95 species are placed in the “lower
risk” categories of NT (10, or 6.1% of the total of 165
species) and LC (85, or 51.5%). The 10 NT species are the
anurans Craugastor berkenbuschii, C. laticeps, Rheohyla
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 11. SEMARNAT categorizations for the herpetofaunal species in Tabasco, Mexico, arranged by families. Non-native species
are excluded.
Number SEMARNAT categorizations
Family of Speci
pecial No status
species adangered)(F). .|"Ehreavened'(’) “| irotection< Py) (NS)
i el 3
ee — eet |
Hylidae
Leptodactylidae
Microhylidae
Phyllomedusidae
Ranidae
Rhinophrynidae
Subtotal
Plethodontidae Sarr EEE SSE _ EES EE
| Dermophiidac TP
Sibit) a E SSS
Gr eS Ee ee ae
|Crocodylidae TS
USS iAD5E05 a | 2 || LN | = SN | NI? | L=—~
| Corytophanidae | A 8
pDaciviodact i | Ss eS eS CoB
i i a a eee eee eee eee
CESS | | [ee eee
Viguatidsd ss (| 22 | Sa ts) ee |
Lab uyides <a
| Phrynosomatidae | S| SS
| Phyllodactylidae |] St | CO
[SCE A ets [fs Sel | lc) neal | = fos |e tll ee ee
| Sphaerodactylidae | 2
| Sphenomorphidae | 2
Ci i, i ce i Saar ae ee ee eee
pXantusiidae J Sf
CXensaitdde nl | Oe. Olim on | ke |
| Subtotal a 8
ea, a a a ee eee eee
|Colubridae | 2 CC ZS
|Dipsadidae | 8
cele | | |
| Leptotyphlopidae | tS
Notice | ee eee |S a eel
psibynophiidaess |S er Sle CU
C—O ee ee ee ee ee
DS SS ESE ESS SSS ee Eee
|Subtotal | SS
ecidomidasis ih Be ee Ee ee
Chel ditdie | | Pees eS Se
|Dermatemyidae | dt
Isbensochelyidace i) eS
u
| Kinosternidae | 3
BO lAPmofuolrm]—|nf—frmolel_]|7
elole[p
Amphib. Reptile Conserv. 37 August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Table 12. Comparison of the SEMARNAT and distributional categorizations for the Tabasco herpetofauna. Non-native species are
excluded.
Distributional categories
Endangered (P)
Non-endemic species (NE) 4
Country-endemic species (CE) —
Total 4
miotympanum, and Smilisca cyanosticta (two country
endemics and two non-endemics), the salamander
Bolitoglossa platydactyla (a country endemic), the
lizard Celestus rozellae (a non-endemic), and the
turtles Rhinoclemmys areolata, Kinosternon acutum,
Claudius angustatus, and Staurotypus triporcatus (all
non-endemics). The 85 LC species comprise the largest
group of the native species (Table 13), but whether this
large portion of the native species are in reality of “Least
Concern” is a question we examine below.
Of the remaining 51 species in the herpetofauna, four
are allocated to the DD category (2.4% of the total of 165
species) and 47 are in the NE category (28.5%). In the
next section, we examine the status of these 51 species
using the EVS system. To determine the relationship
between the application of the IUCN categories and the
distribution categories, the data on these correlations are
assembled in Table 14. These data indicate that of the
20 country endemic species, six (30.0%) are allocated
to the “threat categories.” None of these six species
is placed in the CR category, thus three species are in
the EN category, including the anurans Charadrahyla
chaneque and Duellmanohyla chamulae, and _ the
salamander Bolitoglossa veracrucis. The other three
species are consigned to the VU category, including
the anuran Craugastor rhodopis, the salamander
Bolitoglossa alberchi, and the anole Norops barkeri. The
remaining CE species, numbering 14, are distributed
rather uniformly among the other IUCN categories, with
the highest number (five) placed in the LC category. As
expected, the majority of the 145 non-endemic species
(80, or 55.2%) are also allocated to the LC category.
The next largest number (44, or 30.3%) was placed in
the Not Evaluated (NE) category. The remaining non-
endemic species (21, or 14.5%) are distributed among
the remaining IUCN categories, with 13 placed in the
“threat categories” (CR, EN, and VU). Based on the
data in Table 14, no correlation 1s evident between the
placements of the country endemic or non-endemic
species among the IUCN’s “threat categories.” More to
the point, as commonly found in earlier entries of the
Mexican Conservation Series, most species of either
distribution category (country endemic or non-endemic)
are placed either in the LC category or are not assessed
using the IUCN system. In the case of Tabasco, these
species amount to 124 of the 145 non-endemic species
(85.5%) and eight of the 20 country-endemic species
Amphib. Reptile Conserv.
SEMARNAT categories
Special No Status
Threatened (A) Protection (Pr) (NS) Total
9 34 98 145
9 10 20
10 43 108 165
38
(40.0%). In total, 132 of the 165 total native herpetofaunal
species in Tabasco (80.0%) are placed either in the Least
Concern or NE categories using the IUCN system. At this
juncture, the IUCN assessment system has demonstrated
that the majority of the evaluated herpetofauna is either
of little concern (1.e., is in reasonably good shape from
a conservation perspective) or simply has been ignored
(i.e., non-evaluated). We further examine these LC and
NE species in the next section.
The EVS System
The EVS (Environmental Vulnerability Score) system of
conservation evaluation initially was created as a means
for assessing the conservation status of the amphibians
and reptiles of Honduras (Wilson and McCranie 2004).
Subsequently, it has been used for the same purpose with
other segments of the Mexican and Central American
herpetofaunas (e.g., Townsend and Wilson 2010,
2013a,b; Johnson et al. 2015b, 2017; Mata-Silva et al.
2015, 2019; and all entries in the MCS [see above]). In
this study, the EVS values for all 162 native non-marine
Species occurring in Tabasco are given in Table 8 and
summarized in Table 15.
The EVS values range from 3 to 19, one less than the
entire theoretical range of 3—20. The most frequent values
(applied to 10 or more species) are 6 (13 species), 7 (12),
8 (13), 9 (16), 10 (21), 11 (16), 12 (15), 13 (17), 14 (11),
and 15 (10). These 10 values are applied to 144 native
non-marine species (88.9% of the total of 162 species).
The lowest possible score of 3 was established for two
anuran species (Rhinella horribilis and Smilisca baudini)
and the highest score of 19 for one turtle (7rachemys
venusta).
As with previous MCS reports, herein the EVS scores
are aggregated into three categories of low (EVS of 3-9),
medium (10-13), and high (14-19) vulnerability. On the
basis of this categorization, the species counts increase
slightly from low (66) to medium (69) and then decrease
markedly to high (27). This sort of pattern is emblematic
of herpetofaunas that contain more non-endemic species
(145 in the case of Tabasco) than endemic species (20),
as was previously determined in Chiapas (Johnson et al.
2015a), Tamaulipas (Teran-Juarez et al. 2016), Nuevo Leon
(Nevarez-de los Reyes et al. 2016), Jalisco (Cruz-Saenz
et al. 2017), the Mexican Yucatan Peninsula (Gonzalez-
Sanchez et al. 2017), and Coahuila (Lazcano et al. 2019).
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 13. IUCN Red List categorizations for the herpetofaunal families in Tabasco, Mexico. Non-native species are excluded. The
shaded columns to the left are the “threat categories,” and those to the right are the categories for which too little information on
conservation status exists to allow the taxa to be placed in any other IUCN category, or they have not been evaluated.
IUCN Red List categorization
Number 7
Family of Critically Eendanoered! | Walners bis Near Least Data Not
species Endangered 8 Threatened | Concern | Deficient | Evaluated
(NE)
1
3
Dactyloidae
—
—
Xantusiidae
Xenosauridae
N
—)
| Colubridae | 2
| Dipsadidae | 3
| Total | 12
1
6
N
Subtotal 4
Corytophanidae
1
_
al
2
l
0
0
2
6
8
Sum total 5
Category total 165 19 95 51
Amphib. Reptile Conserv. 39 August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Table 14. Comparison of IUCN and distributional categorizations for the Tabasco herpetofauna. Non-native species are excluded.
IUCN category
a LP Critically Near Least Data Not
ee eae Endangered ee aaa Threatened Concern Deficient Evaluated Total
(CR) (NT) (LC) (DD) (NE)
Non-endemic species
4 1 8 Ti 80 1 44 145
(NE)
Country-endemic
species (CE) _ 4 ; : 2 2 A ae
Total 4 4 11 10 85 4 47 165
The results of applying the IUCN categories to the
Tabasco herpetofauna are compared to those obtained
from using the EVS system in Table 16. This comparison
demonstrates that only 16 of the 27 high vulnerability
species (59.3%) are placed in the three IUCN “threat
categories.” These 16 species are the anurans /ncilius
macrocristatus (VU 11), Craugastor alfredi (VU 11),
C. rhodopis (VU 14), Eleutherodactylus leprus (VU
12), Charadrahyla chaneque (EN 13), Duellmanohyla
chamulae (EN 13), Ptychohyla macrotympanum (CR
11), Agalychnis moreletii (CR 7), the salamanders
Bolitoglossa alberchi* (VU 15) and _ Bolitoglossa
veracrucis* (EN 17), the caecilian Dermophis mexicanus
(VU 11), the crocodylian Crocodylus acutus (VU 14), the
anole Norops barkeri* (VU 15), and the turtles Chelydra
rossignonii (VU 17), Dermatemys mawii (CR 17), and
Trachemys venusta (VU 19). At the other extreme, the
65 low vulnerability species constitute 75.6% of the 86
LC species (Table 16). As demonstrated in the other
MCS studies, there is a general lack of correspondence
between the application of the IUCN and EVS assessment
systems.
Only four of the 162 native non-marine species
in the Tabasco herpetofauna are allocated to the DD
category (Table 17), which are the anurans Craugastor
palenque, C. pelorus*, and Exerodonta bivocata*, and
the night lizard Lepidophyma tuxtlae*. Based on similar
arguments presented in previous MCS studies (e.g.,
Torres-Hernandez et al. 2021), we suggest that the three
anurans, each with an EVS of 15, would be better served
by being placed in the EN category and the lizard, with
an EVS of 11, in the NT category.
Forty-seven species still remain to be evaluated using
the IUCN system, and thus we allocated them to the NE
category (Tables 8 and 18). Only three of these species
are country endemics (the anuran Quilticohyla zoque and
the lizards Holcosus amphigrammus and H. stuarti). The
remaining 44 species are all non-endemics. The EVS
values range from 3—15, which allocates a certain number
of species to each of the three summary categories (Table
8). Twenty-four species have a low EVS score, 19
have medium scores, and four have high scores. When
these species are assessed by the IUCN, we suggest
that the four high vulnerability species (Quilticohyla
zoque, Oxybelis potosiensis, Oxyrhopus petolarius, and
Amphib. Reptile Conserv.
40
Agkistrodon russeolus), with an EVS of 14 or 15, should
be placed in one of the three “threat categories.” The 10
species with an EVS of 11, 12, or 13 should be allocated
to the NT category. The remaining 33 species, with an
EVS of 3-10, can be placed in the LC category.
As with all the previous entries in the Mexican
Conservation Series, in this entry we ascertained that
IUCN has placed a rather large segment of the Tabasco
herpetofauna in the Least Concern category (Table 19).
This includes 85 species, or 52.5% of the total of 162
native non-marine species. Since over half of the species
in Tabasco have been judged by IUCN to be of Least
Concern, one might conclude that the conservation status
of this herpetofauna is in reasonably good shape. To
examine whether this is the case, the determinations of
the EVS values for these 85 species are shown in Table
19. Given that the majority of the Tabasco herpetofauna
is comprised of non-endemic species, one might expect
that a large portion of these species should be assigned to
the LC category, which proves to be the case. Only five
(5.9%) of these LC species are country endemics. The
EVS values for the 85 LC species range from 3 to 17, or
only three fewer than the entire theoretical range for the
EVS (1.e., 3-20). This range is two fewer than the entire
range for Tabasco (3-19). Allocation of the EVS values
for the 85 LC species into the three summary categories
indicates the following: low (3-9), 40 species; medium
(10-13), 38 species; and high (14-20), 7 species. On
the basis of these allocations, we suggest that a more
realistic evaluation would position the seven high
vulnerability species in one of the three threat categories,
as: CR (Micrurus diastema), EN (Crotalus tzabcan),
and VU (Triprion spinosus, Norops compressicauda,
Sceloporus lundelli, Dipsas brevifacies, and Porthidium
nasutum). The 40 medium vulnerability species most
logically should be allocated to the NT category, and
the 40 low vulnerability species should be retained in
the LC category, at least until more up-to-date, targeted
conservation status surveys can be completed.
Relative Herpetofaunal Priority
Johnson et al. (2015a) developed the concept of Relative
Herpetofaunal Priority (RHP) in the third entry of the
MCS. This device is a simple means for measuring the
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 15. Environmental Vulnerability Scores (EVS) for the herpetofaunal species in Tabasco, Mexico, arranged by family. The
and the one to the right indicates the high vulnerability scores. Non-
P.
shaded area to the left encompasses low vulnerability scores
native species are excluded.
)
pe
S
3
N
>>
=
ra)
%
ze
5)
=
=
>
S
—_
=|
o
=
=
S
=
>
—|
a
Number
of
lossidae
Eublepharidae
astoridae
Iguanidae
Eleutherodactylidae
Sphenomorphidae
Sibynophiidae
Typhlopidae
Viperidae
Subtotal
Chelydridae
Geoemydidae
Kinosternidae
Subtotal
Sum total
Subtotal
Corytophanidae
Phyllomedusidae
Dactyloidae
Phrynosomatidae
Sphaerodactylidae
Phyllodactylidae
Scincidae
Leptotyphlopidae
Natricidae
Dermatemyidae
Plethodontidae
Dermophiidae
Subtotal
Crocodylidae
Xenosauridae
Subtotal
Emydidae
Rhinophrynidae
Subtotal
Bufonidae
Centrolenidae
Leptodactylidae
Microhylidae
Subtotal
Mabuyidae
Xantusiidae
Colubridae
Dipsadidae
Elapidae
Crau
Diplo
Category total
August 2022 | Volume 16 | Number 2 | e315
41
Amphib. Reptile Conserv.
The herpetofauna of Tabasco, Mexico
Table 16. Comparison of Environmental Vulnerability Scores (EVS) and IUCN categorizations for members of the herpetofauna of
Tabasco, Mexico. Non-native species and marine species are excluded. The shaded area at the top encompasses low vulnerability
category scores, and the one at the bottom includes the high vulnerability category scores.
IUCN category
Least Data Not Total
Concern Deficient | Evaluated
Critically
Endangered Vulnerable
Endangered
ne en ee ee eee ee
—_
is)
relative importance of the herpetofaunal components
of the physiographic regions in any given geographic
entity, such as states in Mexico in the case of the MCS.
Ascertaining the RHP is accomplished by using two
metrics, 1.e., (1) the proportions of state and country
endemics (only country endemics in the case of Tabasco)
among the physiographic regional herpetofaunas, and
(2) the absolute quantity of high vulnerability category
species in each physiographic regional herpetofauna.
The data resulting from these calculations are presented
in Tables 20 and 21, respectively.
The data in Table 20 are based on the relative number
of country endemics (since there are no state endemic
species in Tabasco). These data demonstrate that the first
rank is occupied by the SNC with 17 species of a total of
145 species (11.7%). The second rank is held by the GCP
with five country endemics among a total of 89 species
(5.6%), and the third rank is the SBP with three country
endemics among a total of 93 species (3.2%).
The data in Table 21 show the relative numbers
of high vulnerability species, but the rankings differ
Threatened
Near
somewhat from those seen in Table 20. The first rank
is the same in both instances, 1.e., the Sierra Norte de
Chiapas, with 23 high vulnerability species among a
total of 142 species (16.2%). The second rank relative
to the high vulnerability species, however, 1s held by the
Sierras Bajas de Petén with 15 such species among a total
of 91 (16.5%), although it holds rank number three with
respect to country endemics. The third rank in Table 21
is for the Gulf Coastal Plain, with 10 high vulnerability
species among a total of 79 (12.7%), while this region’s
status is rank two relative to country endemics.
Based on the results of the RHP analyses, the
physiographic region with the highest priority is clearly
the SNC, since it supports the highest numbers of both
country endemics (Table 20) and high vulnerability
species (Table 21). The 17 country endemics, as
indicated by the asterisks in Table 4, include eight
anurans (Craugastor berkenbuschii, C. pelorus, C.
rhodopis, Charadrahyla chaneque, Duellmanohyla
chamulae, Exerodonta bivocata, Quilticohyla zoque, and
Rheohyla miotympanum), two salamanders (Bolitoglossa
Table 17. Environmental Vulnerability Scores (EVS) for members of the herpetofauna of Tabasco, Mexico, allocated to the IUCN
Data Deficient category. * = country endemic.
Environmental Vulnerability Score (EVS)
Species Geographic Ecological Reproductive mode/Degree Total
distribution distribution of persecution score
Craugastor palenque i a ae a | ae |
Craugastor pelorus* lo el
| Exerodontabivocata* | OTS
Lepidophyma tuxtlae*
Amphib. Reptile Conserv. 42 August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 18. Environmental Vulnerability Scores (EVS) for members of the herpetofauna of Tabasco, Mexico, currently Not Evaluated
(NE) by the IUCN. Non-native species are excluded. * = country endemic.
Environmental Vulnerability Score (EVS)
Species ‘ : Reproductive
Geographic Ecological
distribution distribution more Degree Ol
persecution
|Rhinellahorribilis | 8
ee
a
cS
| Noropsbiporcats | Et
E
Ce
| Noropstemurims 88
Norops rodriguezii 10
ce
| Norops tropidonoms | 8
|Noropsuniformis, TA
a
‘iguinavkinotopha ———=—~S~SC‘iaSSSCdYS Cd Cd
| Marisoralineola | 8 8
| Sceloporusvariabilis |
eC
10
|Scincellacherrieg | 8 8
| Holcosus amphigrammus® | SL
[Hotcomssuri® ———=S=~=~“‘is;CSC*‘( UBT dUATCOCdSOC“‘SUSSOOOUOCO#*d;SCO*~‘<(‘ia]R
|Xenosaurusrackhami | 8
|Boaimperator 8
| Drymobius margaritiferus |
Lampropeltis polyzona
| Onybelis potosiensis | SS
a
a
| Coniophanesfissidens | 8 TT
ee
Cimantodes cenchea—=—=~—CSC‘ SSCS) COC‘
| Imantodes gemmisrams | 8
| Leptodeira septenrionalis, | |
[Onrhopus peters ———=S~C~wSC“‘ TUSSCdTSOOUéCUdOOC~<“ RSSCC‘*dSC“‘éNM#
[Rhadinaea decoraa ——=~=~sC~SCiS| Cd Cd
|Sibonnebulas
Epictia phenops
Wlul]ey_nftre
Aa
WW} ute |e
ies)
ios)
t
ios)
N
ies)
i
t
+
HEE er
AA N | GW
HA Ww | Go] Go | Go
|
tHE
HHH
HHH
Bothrops asper
Kinosternon leucostomum
Kinosternon scorpioides
Amphib. Reptile Conserv. 43 August 2022 | Volume 16 | Number 2 | e315
—
The herpetofauna of Tabasco, Mexico
Table 19. Environmental Vulnerability Scores (EVS) for members of the herpetofauna of Tabasco, Mexico, assigned to the IUCN
Least Concern (LC) category. Non-native species are excluded. * = country endemic.
Environmental Vulnerability Score (EVS)
ppecics Geographic Ecological Reproductive mode/Degree Total
distribution distribution of persecution score
3 2
Mesoscincus schwartzei
ne Kee)
—
os)
—
—
—
—
—
N
—
—
ie)
N
—
N
—
ies)
—
—
— — — — tee
Amphib. Reptile Conserv. 44 August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 19 (continued). Environmental Vulnerability Scores (EVS) for members of the herpetofauna of Tabasco, Mexico, assigned
to the IUCN Least Concern (LC) category. Non-native species are excluded. * = country endemic.
Environmental Vulnerability Score (EVS)
ppecics Geographic Ecological Reproductive mode/Degree Total
distribution distribution of persecution score
2 ]
—
N
1
—
ies)
N
ne Kak Kom)
—
a a a a ae
i a rr a
EE i Lee eee ee
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12
14
platydactyla and B. veracrucis), five lizards (Norops Bolitoglossa veracrucis*
barkeri, N. compressicauda, Holcosus amphigrammus, Crocodylus acutus
H.. stuarti, and Lepidophyma tuxtlae), and two snakes Norops barkeri*
(Geophis laticinctus and Micrurus diastema). The 23 Norops compressicauda*
high vulnerability species found in the SNC are identified Sceloporus lundelli
in Table 8 and are listed here for emphasis: Oxybelis potosiensis
Dipsas brevifacies
Craugastor berkenbuschii* Oxyrhopus petolarius
Craugastor palenque Micrurus diastema*
Craugastor pelorus* Porthidium nasutum
Craugastor rhodopis* Chelydra rossignonii
Exerodonta bivocata* Dermatemys mawii
Quilticohyla zoque* Trachemys venusta
Triprion spinosus Kinosternon acutum
Bolitoglossa platydactyla* Staurotypus triporcatus
Amphib. Reptile Conserv. 45 August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Table 20. Number of herpetofaunal species in the three distributional status categories among the three physiographic regions of
Tabasco, Mexico. Rank order is based on the number of country endemics.
Distributional categories
Physiographic region : Country
Non-endemics ‘
Endemics
Gulf Coastal Plain 78 5
Sierra Norte de Chiapas 125 17
Sierras Baja del Petén 88 3
Of these 23 species, 10 are country endemics (*) with
EVS values ranging from 14 to 19.
The GCP includes five country endemics: the anuran
Craugastor rhodopis, the lizards Aspidoscelis guttatus,
Holcosus amphigrammus, and H. stuarti, and the snake
Micrurus diastema. The GCP also harbors 10 high
vulnerability species, which are indicated in Table 8 and
listed here for emphasis:
Craugastor rhodopis*
Crocodylus acutus
Oxybelis potosiensis
Micrurus diastema*
Chelydra rossignonii
Dermatemys mawii
Trachemys venusta
Kinosternon acutum
Claudius angustatus
Staurotypus triporcatus
Only two of these 10 species are country endemics (*),
but the EVS values for all ten range from 14 to 19.
Finally, the SBP contains only three country
endemics: the anuran Craugastor rhodopis, the
salamander Bolitoglossa alberchi, and the lizard
Scincella gemmingeri. This region, however, supports
15 high vulnerability species that are listed in Table 8
and here for emphasis:
Craugastor palenque
Craugastor rhodopis*
Bolitoglossa alberchi*
Crocodylus acutus
Sceloporus lundelli
Oxybelis potosiensis
Agkistrodon russeolus
Crotalus tzabcan
Porthidium nasutum
Total Rank order
Non-natives
88 2
145
93 3
Chelydra rossignonii
Dermatemys mawii
Trachemys venusta
Kinosternon acutum
Claudius angustatus
Staurotypus triporcatus
Only two of these 15 species are country endemics (*),
but the EVS values for all 15 species range from 14
to 19.
In each of the three physiographic regions we
recognize in Tabasco, the largest distributional group,
as expected, 1s comprised of the non-endemic species.
Similarly, the high vulnerability species in each region
are non-endemic species. As a result, unlike the many
states surveyed thus far in the MCS, the group of
principal conservation concern in Tabasco is the non-
endemic segment. Consequently, this group of species is
examined more closely below in an effort to protect the
herpetofauna of Tabasco.
Natural Protected Areas in Tabasco
The ostensible purpose for the establishment of natural
protected areas in any location is to protect key portions
of the ecosystems contained within them from the
depredations of societal elements outside them for
perpetuity. Basically, there are two types of issues, i.e.,
agriculturalization and urbanization. To be maximally
effective, such protected areas should include functionally
capable segments of the ecosystems originally present
in a given entity (e.g., a state), whose size and extent
is sufficient to support viable populations of all the
organisms found within the designated protected area.
Most often, however, such areas are established without
the completion of the requisite work to demonstrate
the existence of survivable populations of anything
more than a handful of the resident creatures. When
Table 21. Number of herpetofaunal species in the three EVS categories among the three physiographic regions of Tabasco, Mexico.
Rank order is determined by the relative number of high EVS species. Non-native and marine species are excluded.
Physiographic province
Gulf Coastal Plain 39
Sierra Norte de Chiapas 60
Sierras Baja del Petén 38
Amphib. Reptile Conserv.
Low
Medium High Total Rank order
31 10 79 3
59 23 142 1
38 15 91 2
August 2022 | Volume 16 | Number 2 | e315
an-Vazquez et al.
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August 2022 | Volume 16 | Number 2 | e315
47
Amphib. Reptile Conserv.
The herpetofauna of Tabasco, Mexico
Table 23. Distribution of herpetofaunal species in the Natural Protected Areas of Tabasco, Mexico, based on herpetofaunal surveys.
Abbreviations are as follows: * = species endemic to Mexico and ** = non-native species. The numbers signifying the 14 Natural
Protected Areas in Tabasco are as follows: 1 = Pantanos de Centla; 2 = Cafion del Usumacinta; 3 = Agua Blanca; 4 = La Sierra de
Tabasco; 5 = Laguna del Camaron; 6 = CICN Yumka; 7 = Reserva Ecoldgico de la Chontalpa; 8 = Laguna de las Ilusiones; 9 =
Yu-Balcah; 10 = Cascadas de Reforma; 11 = Rio Playa; 12 = Grutas del Cerro Cocona; 13 = Laguna Mecoacan; and 14 = Guaritec.
Pita Ts [sts [s [ofa [> Pola fetafie
CEE a GG
PBufonidaeGspets) | | | | |. | |. 1117) 1—
‘inciins macrocrisans | | | {+} | | | | | | [+/ | _
[Centrotenidae specs) | | || ilar
[Avainobatrachium virdssimum | + | | [+]
[Craugastoridae species) |_| |
Be
Craugastor laticeps
Craugastor loki
Craugastor palenque [sl
Craugastor pelorus*
ard
Craugastor rhodopis*
=
[Eleutherodactylidae (2 species) | || ||
[Eleutherodactylusteprus | TE + | +L +L
[Eleutherodactylus planirostris*® ||| TL
Hylidae(15 species) | TT
[Charadrahylachaneque* | TT +H |
LDendrosophus ebraceams | | | TL
[Dendrosophus microcephalus | + | + | | + | ||
ial
Duellmanohyla chamulae*
Exerodonta bivocata*
Ptychohyla macrotympanum
QOuilticohyla zoque*
Rheohyla miotympanum*
Scinax staufferi
Smilisca baudinii a
Smilisca cyanosticta aa
Tlalocohyla loquax
Tlalocohyla picta
el elelet
Trachycephalus vermiculatus a5
rr
Triprion spinosus (ele
[Leptodactylidae @speciesy | |_|
Eneystomops pustiosus | [+ |
Leptodacryius fagiis | + [+ |
[Microhylidae(2 species) || ||
[Gasrophyrne elegans | | | [+
[ial
eee
Es
ean
Amphib. Reptile Conserv. 48 August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 23 (continued). Distribution of herpetofaunal species in the Natural Protected Areas of Tabasco, Mexico, based on herpetofaunal
surveys. Abbreviations are as follows: * = species endemic to Mexico and ** = non-native species. The numbers signifying the 14
Natural Protected Areas in Tabasco are as follows: 1 = Pantanos de Centla; 2 = Cafion del Usumacinta; 3 = Agua Blanca; 4 = La Sierra
de Tabasco; 5 = Laguna del Camaron; 6 = CICN Yumka; 7 = Reserva Ecoldgico de la Chontalpa; 8 = Laguna de las Ilusiones; 9 =
Yu-Balcah; 10 = Cascadas de Reforma; 11 = Rio Playa; 12 = Grutas del Cerro Cocona; 13 = Laguna Mecoacan; and 14 = Guaritec.
iT? Ts [+ ts[s [7 [e [> Pola fetafie
[popacmasverotous _|+{+| | | 111111111
PPaylomedusione@speey | | | | ||. |. |} )) 11
[Agalychnismoreens | [| | | | | —
[niobate brownorm «t+ | | t+le|
PRhinophrynidae (Tepeciesy) |__| ||
[Rhinophymus dorsais—_———~st + ||
Caudata (5 species) =
Plethodontidae (5 species) =
Bolitoglossa alberchi* [airy
Bolitoglossa mexicana |
Bolitoglossa platydactyla* =|
=
Bolitoglossa rufescens
=
[Bolitoglossaveracrucis* | | LT
[Gymnophiona (I species) | || TT
[Dermophiidae (I species) ||| TT
[Dermophis mexicanus | + | LTT
Sree S|
Crocodylia (2 species)
Crocodylidae (2 species)
Crocodylus acutus
Crocodylus moreletii
Squamata (110 species)
Corytophanidae (4 species)
Basiliscus vittatus
Corytophanes cristatus
Corytophanes hernandezii
[iaemanctustongives | +|+|_
TDactyloidae 4 specs) | |__| _
[Norops barter «did
[Norops becterh |_| [+
Novbpstipersans—||[[
ops aio
Norops capito
Norops compressicauda*
—
[Norops laevis i
[Norapsredriguecii [| __
Amphib. Reptile Conserv. 49 August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Table 23 (continued). Distribution of herpetofaunal species in the Natural Protected Areas of Tabasco, Mexico, based on herpetofaunal
surveys. Abbreviations are as follows: * = species endemic to Mexico and ** = non-native species. The numbers signifying the 14
Natural Protected Areas in Tabasco are as follows: 1 = Pantanos de Centla; 2 = Cafion del Usumacinta; 3 = Agua Blanca; 4 = La Sierra
de Tabasco; 5 = Laguna del Camar6én; 6 = CICN Yumka; 7 = Reserva Ecoldgico de la Chontalpa; 8 = Laguna de las Ilusiones; 9 =
Yu-Balcah; 10 = Cascadas de Reforma; 11 = Rio Playa; 12 = Grutas del Cerro Cocona; 13 = Laguna Mecoacan; and 14 = Guaritec.
Pet [s[*ts[s [oe [> Pola fetafie
[Noropstropidonoms | oT +L +] +] oT | | t+] | t+] ft
[Noropspetersi | TT dT + TT CT CT ET
[Noropsuniformis | CT +L +] +] Tt tT TT eT
[Noropsunilobams | tT +L TT UT CT CE ET
Diploglossidae(Ispeciesy |_| | | | TT
Celestus rozellae a |
[Eublepharidae(1speciesy |_| ||
Coleonyx elegans
Gekkonidae (2 species)
Hemidactylus frenatus**
Hemidactylus turcicus**
Iguanidae (2 species)
Ctenosaura similis
Iguana rhinolopha
Mabuyidae (1 species)
Marisora lineola +
/Phrynosomatidae(Sspecies) ||| |
[Sceloporustundelli |
[Sceloporusserrifer |
[Sceloporusteapensis || |
+
Sceloporus variabilis afr | + |
Phyllodactylidae (1 species) [aa]
Thecadactylus rapicauda
Scincidae (2 species) (|
-
=
Sphaerodactylus glaucus
Sphaerodactyius milepuncianes |__| + [|
[Sphenomorphidae @ species) | | [|
er
Treiidae Sepecisy | | | |
[Aspidosels depot =i + | [+
[Aspidoscelisgutans® ++ +
Mesoscincus schwartzei
Plestiodon sumichrasti
Sphaerodactylidae (2 species)
Amphib. Reptile Conserv. 50 August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 23 (continued). Distribution of herpetofaunal species in the Natural Protected Areas of Tabasco, Mexico, based on herpetofaunal
surveys. Abbreviations are as follows: * = species endemic to Mexico and ** = non-native species. The numbers signifying the 14
Natural Protected Areas in Tabasco are as follows: 1 = Pantanos de Centla; 2 = Cafion del Usumacinta; 3 = Agua Blanca; 4 = La Sierra
de Tabasco; 5 = Laguna del Camarén; 6 = CICN Yumka; 7 = Reserva Ecologico de la Chontalpa; 8 = Laguna de las Ilusiones; 9 =
Yu-Balcah; 10 = Cascadas de Reforma; 11 = Rio Playa; 12 = Grutas del Cerro Cocona; 13 = Laguna Mecoacan; and 14 = Guaritec.
Pita Ts [*ts[s [7 [a] Pola feta fie
SNR a GC
Lepidophyma fvinacuam | [+ [*|*|| | ||| | [+] | _
[Lepidophyma nates | | | | |_|
PXenossuridae speci) | | | ||| _
Taottaeigpcisy —-| | | | | | |
ee
=
1
[Pseudelaphefiairgs |_| | [+*| | | | | | |_
[Senicoisriaps [+ {*{ f+; | | | | [+] _
amis II ale) Saleen
Stenorrhina degenharatii ==)
Stenorrhina freminvillii
Tantilla schistosa
Tantilla rubra
Tantillita lintoni
Dipsadidae (27 species)
Adelphicos visoninum
Clelia scytalina
rN
S
3
a
&
=
S
iS
S
ies)
sf
[Coniophanes quinguevinatus | + | + | | + |
[Coniophanes schmidti | TE + | TL
[Conophistineams LH T+ LT
Dipsasbrevifacies | TH LT
[Geophiscarinous | TEL |
[Geophislaticinctus® | EE + TE CE
Amphib. Reptile Conserv. 51 August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
Table 23 (continued). Distribution of herpetofaunal species in the Natural Protected Areas of Tabasco, Mexico, based on herpetofaunal
surveys. Abbreviations are as follows: * = species endemic to Mexico and ** = non-native species. The numbers signifying the 14
Natural Protected Areas in Tabasco are as follows: 1 = Pantanos de Centla; 2 = Cafion del Usumacinta; 3 = Agua Blanca; 4 = La Sierra
de Tabasco; 5 = Laguna del Camaron; 6 = CICN Yumka; 7 = Reserva Ecologico de la Chontalpa; 8 = Laguna de las Ilusiones; 9 =
Yu-Balcah; 10 = Cascadas de Reforma; 11 = Rio Playa; 12 = Grutas del Cerro Cocona; 13 = Laguna Mecoacan; and 14 = Guaritec.
PieT2 Ts [*ts[s [7 [a] Pola fetafie
|Geophissartorit | Ct + TT +] OT UT +]
Imantodescenchoa | oT Cd HT +] oT LT
LImantodes gemmistratus | + | | oT +] TL
[Leptodeirafrenata | CE +H TL +P +] oT UL PT UT HT OT eT
[Leptodeiramacuata | TL E+] UT UT UE
[Leptodeira seprentrionalis | + | =o +] +] +] +t+} +) P+] f+] |
[Niniadiademaa | Et TT + TT UT
Niniaseboe dt + TP + t+] oT PT oT TP UT TT eT
[Oxyrhopus perolarius | + | Hc el
[Pliocercus elapoides | * ||
-Rhadinaeadecoraa | + | +
Sibon dimidiatus
Micrurus diastema*
a
[Micruruselegans | TL |
[Leptotyphlopidae (I species) ||| TT
Epictiagoudo’ LH TL + | |
Thamnophismarciams | *# | LT + LT
Thamnophisproximus | *# TL TL
[Sibynophiidae(I species) ||| =
[Scaphiodontophisannulatus |_| + | + | + io
=
Lt
ie
Typhlopidae (2 species) |
Amerotyphlops tenuis
Indotyphlops braminus** = ar
Viperidae (7 species) Li
Agkistrodon russeolus | + |
Bothriechis schlegelii
+
Chelonia mydas
[iepidecheystenpa |_| | | [| |
[chetyaritacaspeas) | | | 1.111...) ?P?f?t. I
Amphib. Reptile Conserv. 52 August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
Table 23 (continued). Distribution of herpetofaunal species in the Natural Protected Areas of Tabasco, Mexico, based on herpetofaunal
surveys. Abbreviations are as follows: * = species endemic to Mexico and ** = non-native species. The numbers signifying the 14
Natural Protected Areas in Tabasco are as follows: 1 = Pantanos de Centla; 2 = Cafion del Usumacinta; 3 = Agua Blanca; 4 = La Sierra
de Tabasco; 5 = Laguna del Camaron; 6 = CICN Yumka; 7 = Reserva Ecoldégico de la Chontalpa; 8 = Laguna de las Ilusiones; 9 =
Yu-Balcah; 10 = Cascadas de Reforma; 11 = Rio Playa; 12 = Grutas del Cerro Cocona; 13 = Laguna Mecoacan; and 14 = Guaritec.
Taxon
Natural Protected Area
put 2tsitat stot 7} sf 9 | wo] nm | 2] a3 | 1 |
[Chelydrarossignonii | + TL TE + | TT
Dermatemydidae (I species) ||| TTT
LDermatemysmawii | # T+] TL TE Ee
PDermocteyidae tspeces) | | | | | | | | |
Dermochelys coriacea SSS SaaS aaa
Emydidae (1 species)
Trachemys venusta
Geoemydidae (1 species)
Rhinoclemmys areolata
Kinosternidae (3 species)
Kinosternon acutum
Kinosternon leucostomum
Kinosternon scorpioides
Staurotypidae (2 species)
Claudius angustatus
Staurotypus triporcatus
Total
+
+
such information is available, generally it is assembled
in a sufficiently detailed management plan that, in the
best-case scenario, is used to justify the recognition of
a given natural protected area. Oftentimes, however,
the management plan is drawn up after the official
designation of the protected area, or does not exist at the
time of the designation. This scenario often is the case
with herpetofaunal surveys.
In order to assess the extent to which the natural
protected areas of Tabasco are able to protect the state
herpetofauna, we collected a variety of data on these
areas (Table 22). The number of these areas in Tabasco is
rather substantial, amounting to 14 entities, which is the
same number as seen in the state of Puebla (Woolrich-
Pifia et al. 2017). The Mexican Federal government
administers two of these 14 areas, 11 are administered at
the state level, and one 1s a private reserve. The 14 areas
range in size from seven to 302,707 ha. Their total area is
743,808.5 ha or 7,438.1 km, which is 30.1% of the total
area of the state and close to three times the proportion
occupied by the 14 areas located in Puebla (Woolrich
et al. 2017). In Tabasco, these areas were established
relatively recently, during the 33-year period from 1988
to 2019. The representation of these areas among the
physiographic regions of Tabasco is skewed toward the
Llanura Costera de Golfo Sur or Gulf Coastal Lowlands,
with 10 of the 14 located there. Three areas are found
Amphib. Reptile Conserv.
+
=
within the Sierras del Norte de Chiapas and only one in
the Sierras Baja del Petén.
With respect to the range of facilities available in
these 14 protected areas, eight have the full range (Table
22), and the remaining six have fewer. A major concern
for the stability of the state’s protected areas is that, to
some degree, landowners occupy nine of the 14 (64.3%)
areas. Unfortunately, the nine occupied areas include all
of the largest ones, and the largest area not occupied by
landowners encompasses only 572 hectares (5.72 km”).
Also unfortunate is that only five of the 14 areas have
had management plans developed for them. Fewer than
half (six) of the 14 areas have had herpetofaunal surveys
conducted for them. Below we examine the impact of this
situation on the protection of the state’s herpetofauna.
Of the 165 native species known from Tabasco, all but
seven (158, or 95.8%) have been recorded from one or
more of the state’s natural protected areas (Table 23). In
addition, all five non-native species have been recorded
from one or more of these areas (Table 24). The number
of species recorded from these 14 areas ranges from
18 in PE Laguna del Camarén and ADVC Guaritec to
112 in PE La Sierra de Tabasco (Table 23). The seven
species that are not represented in any of the 14 areas
are: Rheohyla miotympanum*, Bolitoglossa veracrucis* ;
Lepidophyma tuxtlae*; Xenosaurus rackhami;, Chelonia
mydas, Lepidochelys kempii;, and Dermochelys coriacea.
August 2022 | Volume 16 | Number 2 | e315
The herpetofauna of Tabasco, Mexico
These seven species include three country endemics, and
all three of the sea turtles known from the state.
Unlike the situation commonly encountered in the
other states surveyed in the MCS, a high percentage of the
known herpetofauna in Tabasco has been documented in
the 14 natural protected areas in the state (Table 24). To
date, of the 162 species thus far recorded from these areas,
most (141, or 87.0%) are non-endemic species, which is a
similar percentage (85.3%) for the representation of non-
endemic species in the herpetofauna as a whole (Table
9). In Tabasco, 16 of the 162 (9.9%) species known from
these areas are country endemics, again similar to the
percentage (11.8%) for the state as a whole (Table 9). All
five of the non-native species (100%) have been shown
to occur in the natural protected areas in the state, which
is not desirable, as these species have been recorded in
from one to all 14 of these areas. Nonetheless, the goal
of complete representation of the native herpetofauna in
the established natural protected areas is within reach,
as only seven species need to be added. As noted above,
however, four of these seven species are country endemics
and three are sea turtles. All but one of these species have
been recorded from only a single physiographic region
(Table 4), with the four terrestrial species documented
from the Sierra del Norte de Chiapas and the three marine
species from the Gulf Coastal Plain. Apparently, a special
effort must be undertaken to incorporate all seven species
within the existing system of natural protected areas.
Conclusions and Recommendations
Conclusions
A. The herpetofauna of Tabasco presently consists of 165
native species, including 38 anurans, five salamanders,
one caecilian, two crocodylians, 107 squamates, and 12
turtles. In addition, five non-native species have been
recorded from the state, including one anuran and four
squamates.
B. We recognize three physiographic regions in Tabasco:
the Gulf Coastal Plain (GCP), the Sierras Bajas del Petén
(SBP), and the Sierra Norte de Chiapas (SNC).
C. The three physiographic regions we recognize in
Tabasco support from 88 species in the Gulf Coastal
Plain (GCP) to 145 in the Sierra del Norte de Chiapas
(SNC), with an intermediate number of 93 in the Sierra
Bajas del Petén (SBP).
D. The numbers of species shared among. the
physiographic regions range from 61 between the GCP
and the SBP to 79 between the SNC and the SBP. The
Coefficient of Biogeographic Resemblance (CBR) values
range from 0.61 between the GCP and the SNC to 0.67
between the GCP and the SBP. The UPGMA dendrogram
(Fig. 5) indicates that the SBP and GCP cluster at the
Amphib. Reptile Conserv.
54
0.67 level, while the SNC clusters to the previous pair at
the 0.64 level. This pattern indicates that all three regions
are closely aligned at a relatively intermediate level of
overall resemblance.
E. The level of herpetofaunal endemism in Tabasco
is relatively low. Of the 165 recorded native species,
only 20 are country endemics (12.1%), including eight
anurans, three salamanders, and nine squamates. No state
endemics are known from this state.
F. The distribution status of the 170 species comprising
the Tabasco herpetofauna is as follows (in decreasing
order of species numbers): non-endemics (145, 85.3%);
country endemics (20, 11.8%); and non-natives (5,
2.9%). Of the 145 non-endemic species, their allocation
among six of the nine distributional categories are as
follows: MXCA (95, 65.5%); MXSA (34, 23.4%); USCA
(eight, 5.5%); USSA (four, 2.7%); OCEA (three, 2.1%);
and MXUS (one, 0.7%).
G. The principal environmental threats to the herpetofauna
of Tabasco are deforestation, agricultural activities, roads,
soil contamination and oil extraction, myths and cultural
factors (gastronomy), illegal commerce, and forest fires.
H. The conservation status of the Tabasco herpetofauna
was evaluated by using the SEMARNAT, IUCN, and EVS
systems. As in previous MCS entries, the SEMARNAT
system was determined to be of limited value, given
that of 165 native species distributed in Tabasco, only
56 (33.9%) have been assessed using this system. A
comparison of the SEMARNAT and _ distributional
categorizations demonstrates that the majority of the
species in Tabasco that have not been evaluated (98,
59.4%) are non-endemic species. Otherwise, the species
that have been assessed also are primarily non-endemic
species (47 or 28.5%), indicating no bias toward the
consideration of country endemic species.
I. The results of the application of the IUCN system (by
category and proportion) are: CR (four, 2.4% of 165
native species); EN (four, 2.4%); VU (11, 6.7%); NT
(10, 6.1%); LC (85, 51.5%); DD (four, 2.4%); and NE
(47, 28.5%).
J. A comparison of the IUCN and _ distributional
categorizations illustrates that most of the 165 native
species (132, 80.0%) are either allocated to the LC
category (85, 51.5%) or Not Evaluated (NE; 47, 28.5%).
K. The application of the EVS system of conservation
assessment to the 162 native non-marine species of Tabasco
demonstrates that the categorical values increase slightly
from low vulnerability (66, 40.7% of 162 native non-marine
species) to medium vulnerability (69, 42.6%), and then
decrease markedly at high vulnerability (27, 16.7%).
August 2022 | Volume 16 | Number 2 | e315
Barragan-Vazquez et al.
L. A comparison of the IUCN and EVS conservation
status categorizations demonstrates that only 16 of the
27 high vulnerability species (59.3%) are placed in
the three “threat categories” (CR, EN, or VU), while
66 low vulnerability species or 77.6% are among the
85 species in the IUCN LC category. As found in
previous MCS studies, these two conservation systems
lacked correspondence when applied to the Tabasco
herpetofauna.
M. An examination of the conservation status of the
species allocated to the IUCN DD, NE, and LC categories
indicates that many of these 136 species (82.4% of the
165 native species) have not been assessed adequately
compared to their respective EVS values. Thus, we
strongly recommend that these species be reassessed to
better demonstrate their propects for future survival.
N. The Relative Herpetofaunal Priority (RHP) measure
was utilized to determine the conservation significance
of the three regional herpetofaunas in Tabasco. This
analysis demonstrates that the herpetofauna of the
Sierra del Norte de Chiapas is the most significant
among the three regions, inasmuch as it supports the
greatest numbers of country endemic species and high
vulnerability species. The two other areas differ in their
rankings (i.e., the rankings are reversed) based on these
two RHP measures.
O. The number of protected areas in Tabasco 1s 14, of
which the Mexican Federal Government administers
two, while 11 are administered at the state level, and one
is a private reserve. These 14 areas have been established
relatively recently, from 1988 to 2019. Collectively,
these areas comprise 30.1% of the total area of the state.
Most of these areas (10 of the 14) are located in the Gulf
Coastal Plain, while three are found in the Sierra del
Norte de Chiapas, and only one ts in the Sierras Baya del
Petén. Landowners occupy nine (64.3%) of the 14 areas,
an undesirable situation with respect to the protection
of the included herpetofaunal species. Unfortunately,
only five of the 14 areas have developed management
plans. In addition, only six of the 14 have completed
herpetofaunal surveys.
P. One highly desirable aspect, however, is that 158
(95.8%) of the 165 native species from the state have
been recorded from one or more of the 14 areas. On the
other hand, however, all five non-native species known
from the state also are found in one or more of these
areas. Of the 158 native species, 141 are non-endemics
and 17 are country endemics.
Q. Future conservation efforts should be directed toward
either locating sustainable populations of the seven
unrecorded species within existing natural protected
areas or establishing new areas, or perhaps enlarging
Amphib. Reptile Conserv.
existing areas to encompass these species. In addition,
herpetofaunal surveys need to be prepared for the eight
areas presently lacking them.
Recommendations
A. Our principal interest in preparing this 14" entry in
the MCS is to document the composition, physiographic
distribution, and conservation status of the 165 native
Species constituting the herpetofauna of Tabasco. The
use of the EVS conservation system demonstrates that
the categorical values increase only slightly from low
vulnerability (66 species) to medium vulnerability
(69 species), and then decrease markedly at high
vulnerability (27). The Relative Herpetofaunal Priority
measure indicates that the herpetofauna of the Sierra del
Norte de Chiapas is the most significant among the three
physiographic regions in Tabasco, because it supports
the highest numbers of country endemic species and high
vulnerability species.
B. The most important conservation challenge in Tabasco
is to conduct the herpetofaunal surveys for eight of the
14 protected areas, with the hope that populations of the
Species not known to be represented within this system
can be found in one or more of the areas located in the
Gulf Coastal Plain and Sierra del Norte de Chiapas.
C. Once the presence of the entire native herpetofauna
has been ascertained in the system of natural protected
areas, then the next step will be to establish monitoring
programs for all native species in order to guarantee their
long-term survival. We submit that these steps need to
be taken with the greatest speed, given that Tabasco is
the 20" most populous state in Mexico and the 12" most
densely populated.
“Living wild species are like a library of books still
unread. Our heedless destruction of them is akin to
burning the library without ever having read its books.”
John D. Dingell (1991)
Acknowledgments.—We are grateful to the following
individuals for providing their photographs for this
article: Jenny del Carmen Estrada-Montiel, Coral J.
Pacheco-Figueroa, José del Carmen Geronimo-Torres,
Manuel Alberto Hernandez-May, Marco Antonio Torrez-
Pérez, Manuel Hernandez-May, and Marco Antonio
Lopez-Luna. We also are very thankful to Guillermo
Woolrich-Pifia for his perceptive and helpful review of
the manuscript.
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Amphib. Reptile Conserv.
México. 116 p.
Ma. Del Rosario Barragan-Vazquez graduated with a Master’s degree in Environmental
Sciences from the Universidad Juarez Autonoma de Tabasco (UJAT) in Villahermosa, Tabasco,
Mexico. She is a full-time Research Professor at UJAT in the Biology and Environmental
Management degree programs. She is interested in the study of amphibians and reptiles at the
community level, and from ecological, taxonomic, and management and utilization points of
view. She has undertaken academic appointments at CINVESTAV-Merida, Faculty of Sciences,
UNAM, and at the Universidad Veracruzana, with work on amphibian cultivation, taxonomy,
and behavior. She has participated in research projects on the herpetofauna in the municipalities
of the Sierra de Tabasco, and has authored or co-authored various articles, notes, and book
chapters, primarily on the community level biodiversity and population genetics in turtles. She
is in charge of the Coleccion de Anfibios y Reptiles de Tabasco (CART), curated within the
Division Académica de Ciencias Bioldgicas de la UJAT.
Liliana Rios-Rodas has a degree in Biology from the Universidad Juarez Autonoma de Tabasco
(UJAT), a Master’s degree in Agricultural Sciences and Natural Resources from the Universidad
Autonoma de México, and a Ph.D. in Ecology and Management of Tropical Systems from UJAT.
Her main research topics involve the ecology of communities and populations of amphibians
and reptiles of Tabasco, focusing on riparian ecosystems of tropical environments. She has
worked on the ecomorphology of the genus Sce/oporus, geometric morphometry in Dryophytes
plicatus, and trophic ecology in Craugastor berkenbuschii. Liliana has participated in genetic
conservation projects for Dermatemys mawii and Trachemys venusta, and in updating the
Tabasco Amphibian and Reptile Collection (CART). She is the author or co-author of several
articles on the distribution, diversity, and conservation of the herpetofauna of Tabasco.
Lydia Allison Fucsko, who resides in Melbourne, Australia, is an environmental activist and
amphibian conservationist. As a photographer with international publications, she has taken
countless amphibian photographs, including photo galleries of frogs mostly from southeastern
Australia. Dr. Fucsko has a Bachelor of Humanities from La Trobe University (Bundoora, Victoria,
Australia) and a Diploma in Education from the University of Melbourne (Parkville, Victoria,
Australia). She has postgraduate diplomas in computer education and in vocational education and
training from the University of Melbourne (Parkville). Additionally, Dr. Fucsko has a Master’s
degree in Counseling from Monash University (Clayton, Victoria, Australia). She received her
Ph.D. in Environmental Education, which promoted habitat conservation, species perpetuation, and
global sustainable management, from Swinburne University of Technology (Hawthorn, Victoria,
Australia), while being mentored by the late Australian herpetologist and scholar Dr. Michael
James Tyler (Order of Australia recipient). As a sought-after educational consultant, Dr. Fucsko has
academic interests that include: clinical psychology, focusing on psychopathology; neuroscience
and empathy; environmental education for sustainable development; sentient ecology; academic
writing; and creative writing, which includes poetry and creative non-fiction books for children
and young adults. Dr. Fucsko also is the senior author (with Boria Sax) of a chapter in the 2019
Springer Encyclopedia of Sustainability in Higher Education entitled “Learning activities for
environmental education for sustainable development.” Recently, Dr. Fucsko has co-authored an
obituary of Jaime D. Villa, a study of the introduced Mesoamerican herpetofauna, a treatment of
the conservation prospects of the Mesoamerican salamander fauna, papers on the herpetofauna
of Veracruz and Querétaro, Mexico, a review of the book Advances in Coralsnake Biology, and a
study on the biological and cultural diversity of Oaxaca, Mexico, among several other academic
papers. In 2020, the species Zantilla lydia, with the suggested common name of Lydia’s Little
Snake, was named in her honor.
59 August 2022 | Volume 16 | Number 2 | e315
Amphib. Reptile Conserv.
The herpetofauna of Tabasco, Mexico
Louis W. Porras graduated in 1971 with a degree in Biology from what today is known as Miami-
Dade College in Miami, Florida, USA. Over his career he has authored or co-authored over 60
academic publications, including the descriptions of two new species, and two taxa have been
named in his honor. Louis developed an interest in herpetology at an early age in his native Costa
Rica. His passion for the field led him to travel to many remote areas, including throughout the
Bahamas, the United States, Mesoamerica, and parts of South America. In 1968, he worked at the
Houston Zoological Gardens, and from 1982 to 1984 at Utah’s Hogle Zoo. In 1976, he attended
the inaugural meeting of the International Herpetological Symposium (IHS), and later served the
group as Vice-President and President. In 1993, along with Gordon W. Schuett, he helped launch
the journal Herpetological Natural History, and for IHS’ 20" anniversary, in recognition of his
contributions, three former Presidents dedicated the book Advances in Herpetoculture in his honor.
Louis’ career in publishing began in 1995, when as a member of Canyonlands Publishing Group
he helped publish Fauna magazine. In 2002 he founded Eagle Mountain Publishing, LC, which
has published such herpetological titles as Biology of the Vipers (2002), Biology of the Boas and
Pythons (2007), Amphibians, Reptiles, and Turtles in Kansas (2010), Conservation of Mesoamerican
Amphibians and Reptiles (2010), and Amphibians and Reptiles of San Luis Potosi (2013). From
2014 to 2018 he was the Publisher and Managing Editor of the journal Mesoamerican Herpetology,
and recently he was the Publisher and Co-editor of the book Advances in Coralsnake Biology: with
an Emphasis on South America.
Vicente Mata-Silva is a herpetologist originally from Rio Grande, Oaxaca, Mexico. His interests
include ecology, conservation, natural history, and biogeography of the herpetofaunas of Mexico,
Central America, and the southwestern United States. He received a B.S. degree from the Universidad
Nacional Autonoma de México (UNAM), and MLS. and Ph.D. degrees from the University of Texas
at El Paso (UTEP). Vicente is an Assistant Professor of Biological Sciences at UTEP, in the Ecology
and Evolutionary Biology Program, and Co-Director of UTEP’s Indio Mountains Research Station,
located in the Chihuahuan Desert of Trans-Pecos, Texas, USA. To date, Vicente has authored or co-
authored over 100 peer-reviewed scientific publications. He also was the Distribution Notes Section
Editor for the journal Mesoamerican Herpetology, and is currently Associate Editor for the journal
Herpetological Review.
Arturo Rocha is a Ph.D. student in the Ecology and Evolutionary Biology program at the
University of Texas at El Paso. His interests include the study of the biogeography, physiology, and
ecology of amphibians and reptiles in the southwestern United States and Mexico. A graduate of
the University of Texas at El Paso, his thesis centered on the spatial ecology of the Trans-Pecos Rat
Snake (Bogertophis subocularis) in the northern Chihuahuan Desert. To date, he has authored or
co-authored over 20 peer-reviewed scientific publications.
Dominic L. DeSantis is an Assistant Professor of Biology at Georgia College and State University,
Milledgeville, Georgia, USA, in the Department of Biological and Environmental Sciences.
Dominic’s research interests broadly include the behavioral ecology, conservation biology, and
natural history of herpetofauna. In addition to ongoing collaborative projects associated with the
“| Mesoamerican Research Group, much of Dominic’s current research focuses on using novel animal-
borne sensor technologies to study the behavior of snakes in the field. While completing his Ph.D.
at the University of Texas at El Paso, Dominic accompanied Vicente Mata-Silva, Eli Garcia-Padilla,
and Larry David Wilson on survey and collecting expeditions to Oaxaca in 2015, 2016, and 2017,
and is a co-author on numerous natural history publications produced from those visits, including
an invited book chapter on the conservation outlook for herpetofauna in the Sierra Madre del Sur
of Oaxaca.
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Barragan-Vazquez et al.
Eli Garcia-Padilla is a Social Biologist and Professional Photographer with more than 12 years
of experience in the formal study and photo documentation of the biological and cultural diversity
of Mexico. He has published one book, entitled Mexican Biodiversity: the Snake, the Jaguar and
the Quetzal, and more than 100 formal contributions on knowledge, the communication of science
and the conservation of Mesoamerican biodiversity. Since 2006, he has been exploring Oaxaca
and Chiapas, which are the most biodiverse and multicultural states in Mexico. In 2017, he began
to enter the mythical region of Los Chimalapas in the Isthmus of Tehuantepec, which is the most
biologically rich region in all of Mexico, under a community social conservation scheme. Eli has
published his photographic work in prestigious magazines such as National Geographic in Spanish
and Cuartoscuro. In 2020, he co-founded the Mesoamerican Biodiversity initiative with the aim of
creating a community around the dissemination of the most important wealth of Mexico, which is
its biodiversity and its culture. His writings are published regularly in Oaxaca Media, the Jornada
Ecologica and the Ojarasca Supplement of La Jornada.
Jerry D. Johnson is Professor of Biological Sciences at The University of Texas at El Paso, and
has extensive experience studying the herpetofauna of Mesoamerica, especially that of southern
Mexico. Jerry is the Director of the 40,000-acre Indio Mountains Research Station, and was a co-
editor on the book Conservation of Mesoamerican Amphibians and Reptiles and co-author of four of
its chapters. He was also the senior author of the recent paper “A conservation reassessment of the
Central American herpetofauna based on the EVS measure” and is Mesoamerica/Caribbean editor for
the Geographic Distribution section of Herpetological Review. Jerry has authored or co-authored over
130 peer-reviewed papers, including two 2010 articles, “Geographic distribution and conservation
of the herpetofauna of southeastern Mexico” and “Distributional patterns of the herpetofauna
of Mesoamerica, a Biodiversity Hotspot.” One species, Zantilla johnsoni, has been named in his
honor. Presently, he is an Associate Editor and Co-chair of the Taxonomic Board for the journal
Mesoamerican Herpetology.
Larry David Wilson is a herpetologist with lengthy experience in Mesoamerica. He was born
in Taylorville, Illinois, USA, and received his university education at the University of Illinois at
Champaign-Urbana (B.S. degree) and at Louisiana State University in Baton Rouge (M.S. and
Ph.D. degrees). He has authored or co-authored more than 460 peer-reviewed papers and books on
herpetology. Larry was the senior editor of Conservation of Mesoamerican Amphibians and Reptiles
and a co-author of seven of its chapters. His other books include The Snakes of Honduras, Middle
American Herpetology, The Amphibians of Honduras, Amphibians & Reptiles of the Bay Islands
and Cayos Cochinos, Honduras, The Amphibians and Reptiles of the Honduran Mosquitia, and
Guide to the Amphibians & Reptiles of Cusuco National Park, Honduras. To date, he has authored
or co-authored the descriptions of 75 currently-recognized herpetofaunal species, and seven species
have been named in his honor, including the anuran Craugastor lauraster, the lizard Norops wilsoni,
and the snakes Oxybelis wilsoni, Myriopholis wilsoni, and Cerrophidion wilsoni. In 2005, he was
designated a Distinguished Scholar in the Field of Herpetology at the Kendall Campus of Miami-
Dade College in Miami, Florida, USA. Currently, Larry is a Co-chair of the Taxonomic Board for the
website Mesoamerican Herpetology.
61 August 2022 | Volume 16 | Number 2 | e315
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
16(2) [General Section]: 62—68 (e316).
Reproductive characteristics of the Burmese Narrow-headed
Softshell Turtle, Chitra vandijki, in captivity
‘Hong Xiaoyou, *2*Zhu Xinping, ‘Chen Chen, ‘Cai Xiaodan, *Li Yongming, and ‘Li Xinping
'Key Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture, Pearl River Fisheries Research
Institute, Chinese Academy of Fishery Sciences, Guangzhou, CHINA *College of Life Science and Technology, Shanghai Ocean University, Shanghai,
CHINA 3Xishuangbanna Indigenous Fish Research and Breeding Center, Dai Autonomous Prefecture of Xishuangbanna, CHINA +Xishuangbanna
Dai Autonomous Prefecture Fishery Technology Extension Station, Dai Autonomous Prefecture of Xishuangbanna, CHINA
Abstract.—The purpose of this study was to provide basic data for the breeding biology of Chitra vandijki and
to contribute to the conservation of this species. The Burmese Narrow-headed Softshell Turtle, Chitra vandijki,
is a CITES Appendix I-listed species, and biological information on wild and captive C. vandijki is relatively
scarce. In 2019, we studied the reproductive biology of two C. vandijki specimens (a female and a male) that
had been in captivity for approximately 25 years. The oviposition period of the domesticated female C. vandijki
was from June to August. The female laid eggs at night, and no egg protection behavior was observed. The
female C. vandijki laid five clutches of eggs in a year representing 564 eggs in total, with 100-131 eggs/clutch,
and the interval between successive clutches was 9-28 d. The fertilization rate of C. vandijki was 90.4%, and
the hatching rate was 38.6%. The eggs were spherical and rigid, with an average mass of 15.04 + 0.65 g and
an average diameter of 2.96 + 0.22 cm. The average hatching period of C. vandijki was 65.3 d at 28.0—29.0 °C,
and the average accumulated incubation temperature was 44,688.6 °C-h. The average mass of newly hatched
neonates was 10.51 + 0.57 g, and the average mass of juvenile C. vandijki reached 150.37 + 53.86 g after one
year of feeding live fry in a greenhouse.
Keywords. Burmese Narrow-headed Softshell Turtle; captive-breeding; Chitra vandijki, conservation; egg laying;
juvenile; threatened species
Citation: Hong X, Zhu X, Chen C, Cai X, Li Y, Li X. 2022. Reproductive characteristics of the Burmese Narrow-headed Softshell Turtle, Chitra vandijki,
in captivity. Amphibian & Reptile Conservation 16(2) [General Section]: 62-68 (e316).
Copyright: © 2022 Hong et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Accepted: 22 February 2022; Published: 1 September 2022
Introduction
The Burmese Narrow-headed Softshell Turtle, Chitra
vandijki, is a large turtle with a straight-line carapace
length of up to 1 m. It is listed on CITES Appendix I and
classified as Critically Endangered (CR) on the JUCN
Red List of Threatened Species (Rhodin et al. 2018; Platt
et al. 2021). It is mainly distributed in rivers in Myanmar
and Thailand (Platt et al. 2014). The abundance and
distribution of C. vandijki have been sharply reduced
because of human hunting and habitat destruction
(Kuchling et al. 2004; Platt et al. 2005, 2014). Because
little 1s known about the turtle’s ecological habits,
successful cases of artificial breeding are very few and
knowledge of its breeding biology is extremely lacking
(Platt et al. 2018, 2020).
Because the external appearance of C. vandijki 1s
similar to the Asian Giant Softshell Turtle, Pelochelys
cantorii, and given the demands of the Chinese wild
animal market, C. vandijki has been illegally traded
to China as food or for rearing in the last century.
Although P. cantorii in China is Critically Endangered
(Gong et al. 2017; Hong et al. 2019; Wu et al. 2020),
we have successfully carried out artificial breeding of
six P. cantorii (three females and three males) turtles
since 2014 (Zhu et al. 2015; Hong 2020). At present,
we have bred more than 800 P. cantorii between 1
and 6 years old (Ministry of Agriculture and Rural
Affairs of People’s Republic China 2020). Based on
our successful experience in the artificial breeding
of captive P. cantorii, we carried out research on the
reproductive biology of two captive C. vandijki, and
the mitochondrial genomes of the individual hatched
offspring confirmed their identity as Burmese Small-
headed Turtles (Chen et al. 2021). The findings of this
study enrich the basic biological data of C. vandijki
and provide a theoretical basis for its conservation
biology.
Correspondence. hongxiaoyoul216@163.com (HX); zhuxinping_1964@163.com (ZX), chenchen3729@163.com (CC), cxd430@163.com
(CX); 1258313402@qq.com (LY); 13988165908@163.com (LX)
Amphib. Reptile Conserv.
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Hong et al.
Materials and Methods
Captive Care, Conditions, and Management
Two C. vandijki, one male and one female, were
accidentally captured and rescued from the waters of
the Mekong River at the border between Myanmar,
Laos, and Guanli Town, Mengla County, Xishuangbanna
Prefecture, Yunnan Province, China in 1995. Their body
weights at the time of capture were approximately 3 kg
and 7 kg, respectively.
The two C. vandijki were raised in an outdoor fish
pond at an elevation of 570 m asl (21°35’40.84’"N
101°14’5.02”E) in Xishuangbanna Prefecture, Yunnan
Province, China. This region has a north tropical and
south tropical humid monsoon climate, which includes
a long summer without winter. The annual average
temperature 1s between 18.6 and 21.9 °C, and the annual
average precipitation 1s between 1,200 and 1,700 mm.
The dimensions of the pond were 30 m =< 25 m, the water
depth was 1.2 m, and the bottom mud was 30-40 cm
thick (Fig. 1A). In 2012, a 25 m x 2 m nesting sand pond
with a depth of 60 cm was built on the side of the main
pond, and there was a shed above the sand pool for shade.
Tiles were used to build an incline of about 30° so the
turtles could climb up from the water to the sand pond
(Fig. 1A—B). In the pond, Tilapia Oreochromis niloticus,
Carp Cyprinus carpio, and Crucian Carp Carassius
auratus were cultured together, and the C. vandijki lived
by feeding on these fish.
box, (D) rearing facilities.
Amphib. Reptile Conserv.
Fig. 1. Artificial rearing facility of Burmese Narrow-headed Softshell Turtles: (A) breeding pond, (B) nesting area, (C) incubation
In December 2018, the fish pound was cleared, and the
large fish were removed. From February to May 2019,
200 kg of live fish fry, including Carp, Crucian Carp, and
Mud Carp (Cirrhinus molitorella) with body lengths of
3—5 cm, were regularly added to the pond to serve as the
food for improving the cultivation of C. vandijki.
Collection and Hatching of Eggs
In April 2019, the stones and plants in the spawning sand
pool were cleared, and the sand was raked loose and
sieved. From May to July, water was sprayed irregularly
into the spawning sand pond to ensure that the sand
remained damp. A surveillance camera was installed
above the spawning pool to observe the oviposition
activity of C. vandijki. For the first clutch, the eggs
were incubated in situ for 25 days, the clutch was dug
manually, and artificial incubation was continued. For
the other clutches, within 16—24 h after the turtle had laid
the eggs, they were collected by excavating the nest. The
numbers of eggs and fertilized eggs were counted and
recorded. The diameter of each egg was measured with
a Vernier caliper (+ 0.01 cm), and the egg weight was
measured using an electronic balance (+ 0.01 g).
The incubators for fertilized eggs were plastic boxes
with dimensions of 57 x 41 x 36 cm. The medium was
sieved fine river sand, and the moisture content of the
sand was 8—10% (weight ratio, Fig. 1C). The thickness
of the sand pile was approximately 15 cm. The fertilized
eggs in a given clutch were arranged on the sand pile in
>)
—
September 2022 | Volume 16 | Number 2 | e316
Reproductive characteristics of the Burmese Narrow-headed Softshell Turtle
the incubator and covered with 2 cm of fine sand with
the same dampness. The incubator was then covered.
The temperature of the incubator was controlled by an
indoor air conditioner, and maintained at 28.0—29.0 °C.
Water was sprayed regularly onto the sand to control the
humidity.
Cultivation of Hatchlings
After emergence, the hatchlings were observed and
photographed. The body mass of each hatchling was
obtained using an electronic balance (+ 0.01 g). The
length and width of the carapace and the length and
width of the snout of each juvenile were measured using
a caliper (+ 0.01 cm). Hatchlings were reared according
to the rearing method of Asian Giant Softshell Turtle
(P. cantorii) hatchlings (Hong et al. 2018), and cultured
in six custom-designed round buckets with a diameter
of 1.2 m and a water depth of 0.5 m. The cultivation
density was 25-30 individuals/m’, the bottom of the
bucket contained 15 cm of fine sand, and the water was
filtered through circulation (Fig. 1D). The pH of the
water was measured regularly and adjusted to 7.0—7.5
with quicklime. The neonates were fed live Mosquito
Fish, Gambusia affinis. The temperature was controlled
by air conditioning and the water temperature was
maintained at 26.0—31.0 °C. In July 2020, five juvenile
a
C. vandijki were randomly selected from each barrel.
The body mass and length and width of the carapace of
30 hatchlings were measured.
Statistics
The data shown below and labeled as “this study”
are expressed as the mean + SD, and were compared
and analyzed using ANOVA. Statistical analysis was
conducted using IBM SPSS 23.0 software. All statistical
tests were two-tailed, and the significance level was set
as P<0.05.
Results and Discussion
Morphology of the Parents
In 2012, the body mass of the female C. vandijki was
38.0 kg. On 6 December 2018, the body masses of the
female and male parental C. vandijki were 59.2 kg and
40.0 kg, respectively.
There were irregular, slightly fuzzy yellow stripes
on the adult carapace (Fig. 2A). The longitudinal stripes
on the neck and back merged behind the head, and the
neck stripes were more obvious than the stripes on the
back (Fig. 2B). The neck was not obviously separated
from the anterior edge of the carapace. The neck of the
Fig. 2. Characteristics of Burmese Narrow-headed Softshell Turtles: (A) back; (B) head and neck, close-up; (C) male, ventral view;
(D) female, ventral view.
Amphib. Reptile Conserv.
September 2022 | Volume 16 | Number 2 | e316
Hong et al.
Table 1. Egg laying and hatching data of Burmese Narrow-headed Softshell Turtles in 2019.
Number of
Date of egg laying Clutch size fertilized eggs/
clutch
3 June 2019 101 69
1 July 2019 131 117
18 July 2019 110 105
27 July 2019 122 120
9 August 2019 100 99
Total 564 510
adult C. vandijki was slightly short and could not turn to
the middle or rear of the carapace. The front edge of the
carapace was flat, without folds or warts. The head of
the adult C. vandijki was small, and the snout was short
(Fig. 2A—B).
The main morphological difference between the males
and females was the tail. The tail of male C. vandijki was
thick and long, extending out from the edge of carapace,
while the tail of female C. vandijki was thin and short,
extending no longer than the edge of the carapace (Fig.
2C-D).
Egg Laying
In 2004 and 2006, 10 and 20 eggs were laid, respectively,
in the culture pond water of the parent C. vandijki.
After the construction of the spawning sand pond, 98 C.
vandijki hatchlings were collected from the fish pond in
September 2018. However, they all died within 30 d of
captive feeding following the cultivation method of the
Chinese Softshell Turtle Pe/odiscus sinensis (Zhao et al.
1997).
Beginning in June 2019, the female turtle was
observed climbing up the sand dunes at night, looking
for nesting sites. On the nights of 3 June to 9 August, the
female turtle laid five clutches of eggs, for a total of 564
eges. The four intervals between the five clutches were
28 d, 17 d, 9 d, and 13 d, respectively (Table 1), and the
average interval was 16.75 + 8.18 d.
The C. vandijki eggs were nearly round and rigid,
and the calcareous layer of the eggshell was thin. The
number of eggs in each clutch varied from 100 to 131
(Table 1), with an average of 112.8 + 13.5 eggs/clutch.
We randomly selected 40 eggs from the first clutch and
another 40 eggs from the second clutch for measurements.
Fertilization rate Number of hatchings/ Hatching rate
(%) clutch (%)
69.3 43 62.3
85.4 80 80.0
95.5 54 68.4
98.4
20 9.1
99.0
90.4 197 38.6
The egg masses were 13.37—16.47 g (15.04 + 0.65 g)
and egg diameters were 2.76—3.15 cm (2.96 + 0.22 cm).
According to the average egg weight, the total weight of
the five clutches of eggs could be estimated as 8,482.56
g, accounting for 14.335% of the maternal body weight.
Hatching and Characteristics of Hatchlings
The five clutches included 510 fertilized eggs, and the
fertilization rate was 90.4%. In total, 197 hatchlings
emerged, for a hatching rate of 38.6% (Table 1).
The average incubation period of the fertilized
eges was 65.3 + 5.4 d, and the average accumulated
incubation temperature was 44,688.6 °C-h at a room
temperature of 28.0—29.0 °C (28.51 °C on average) based
on the hatching data of the second clutch. Under artificial
conditions, the hatching rate for the last four clutches of
eggs was 34.9%.
The carapace of the newly hatched neonate C. vandijki
was approximately round, with obvious yellow stripes on
the neonate’s back, neck, and limbs. The carapace was
covered with small protuberances and the posterior edge
was yellow without stripes (Fig. 3). The newly hatched
neonate C. vandijki weighed 9.44—11.75 g (10.51 + 0.57
g, n = 60, 30 neonates in the first clutch and another 30
neonates in the second clutch). The length of the neonate
C. vandijki carapace was 4.18—4.70 cm (4.41 + 0.13 cm),
and the width of the carapace was 3.75—4.24 cm (4.01 +
0.10 cm). The length of the snout of neonate C. vandijki
was 0.14—0.22 cm (0.16 + 0.02 cm) and the width of the
snout was 0.15—0.24 cm (0.19 + 0.02 cm).
The reproductive biology data for four species of
softshell turtles bred in captivity are shown in Table 2.
C. vandijki, P. cantorii, and the Siamese Narrow-headed
Softshell Turtle (Chitra chitra) are all large Trionychidae
Table 2. Comparison of the reproductive biology of four species of softshell turtles in captivity.
Burmese Narrow- Siamese Narrow- Asian Giant Softshell Chinese Softshell Turtle
headed Softshell headed Softshell Turtle Turtle (Hong et al. 2018; (Yang et al. 1999; Zhou
Turtle (this study) (Kitimasak et al. 2003) Hong 2020) 2004)
Parent sample size (9, 3) Vol 2,4 Io >800, >100
Number of clutches/year 5 3-4 46 5-7
Clutch size 100-133 40-88 32-55 8-25
Egg diameter (cm) 2.96 + 0.22 3.32+40.15 3.10+0.18 2.00-2.40
Egg mass (g) 15.04 + 0.65 19.00 + 1.67 16.82 + 1.99 3.55-6.77
Mass of neonate (g) 10.51 + 0.57 13.10 + 1.03 13.60 + 0.85 2.33-4.83
HCC UnUar Mn UpaLlon 44,688.60 Not reported 44,886.50 36,000
temperature (°C-h)
Amphib. Reptile Conserv. 65 September 2022 | Volume 16 | Number 2 | e316
Reproductive characteristics of the Burmese Narrow-headed Softshell Turtle
iW BN) ut Wi
i{ (Ct AAV HAN (NM iil :
AC (i |
quae «6
Fig. 3. Hatchling of Burmese Narrow-headed Softshell Turtle.
animals with similar breeding biology, but they are very
different from the Chinese Softshell Turtle, Pelodiscus
sinensis. There are very limited breeding data for wild C.
vandijki. Platt et al. (2020) reported that the numbers of
eggs in four collected clutches were 58, 76, 89, and 102;
and the diameter of the eggs was 2.01—3.66 cm (2.60—2.95
cm on average). The length of the carapace of the hatchlings
was 2.73-4.10 cm (3.52 + 0.35 cm), and the width of the
carapace was 2.75—3.86 cm (3.39 + 0.26 cm). However,
data for the parent C. vandijki were not reported in that
study. In general, in our study, the clutch size, diameter of
eggs, and body size of neonate C. vandijki were all higher
than those reported by Platt et al. (2020), suggesting that
the maternal size in our study might be larger and/or that
the nutritional status of C. vandijki in captivity is better
than that in the field (Gibbons et al. 1990; Litzgus et al.
2008; Hong et al. 2018).
Based on the egg laying and hatching data, we found
that the number of eggs in each clutch was relatively
constant and the fertilization rate remained at a high
level. However, the hatching rates of the last two clutches
were relatively low (Table 1). The total mass of the five
clutches of eggs accounted for approximately 14% of
the body mass of the female C. vandijki. We considered
that the low hatching rate of the last two clutches may
be due to the influence of oviposition frequency and
the availability of reproductive resources for the female
C. vandijki (Jackson and Prange 1979; Ferguson et al.
1982). We speculate that too much of the energy of
the female C. vandijki had been consumed by the late
stage of oviposition, and the spawning intervals between
the last two clutches were short (9 d and 13 d), which
may have resulted in an insufficient energy supply
for the development of the eggs, leading to improper
development of the embryos. This phenomenon has been
reported for P. cantorii (Hong et al. 2018).
Growth of Juveniles
By July 2020, 180 juvenile C. vandijki survived, for a
survival rate of 91.4%. The body weight of juvenile C.
Amphib. Reptile Conserv.
vandijki was 49.80-311.10 g (150.37 + 53.86 g, n = 30),
the length of the juvenile carapace was 7.54—13.19 cm
(11.05 + 1.66 cm), the width of the carapace was 7.56—
12.87 cm (10.84 + 1.53 cm), the length of the juvenile
snout was 0.22—0.40 cm (0.29 + 0.05 cm), and the width
of the snout was 0.23—-0.43 cm (0.31 + 0.06 cm). The
living habits of P. cantorii and C. vandijki are similar;
thus, the juvenile breeding method of P. cantorii is also
suitable for C. vandijki and 1s ideal in terms of survival
rate and growth rate.
P. cantorii is endangered due to overhunting and
habitat destruction, and China has increased its artificial
conservation efforts to gradually restore wild resources,
which has achieved initial results (Ministry of Agriculture
and Rural Affairs of People’s Republic China 2020).
Currently, the C. vandijki population has been greatly
reduced, and so it is also in a critical condition state. For
this reason, referring to the Chinese protection strategy
for P. cantorii, we can use the limited captive population
of C. vandijki to carry out conservation biological
research in order to achieve the artificial conservation of
this species, and subsequently release the captive turtles
into the wild to restore the wild population.
Acknowledgments.—Thanks are due to the staff of
Xishuangbanna Dai Autonomous Prefecture Fishery
Technology Extension Station for the breeding turtles for
more than 25 years. We also thank all those who have
contributed to the conservation of Pelochelys cantorii
and Chitra vandijki. The financial support for this work
was provided by the Foshan City Financial Special
Fund-2020, the Guangdong Agricultural Science and
Technology Demonstration City Project, and the Central
Public-interest Scientific Institution Basal Research Fund,
CAFS (#2019ZD04, #2020TD35 and #2020ZJTDO1).
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Reproductive characteristics of the Burmese Narrow-headed Softshell Turtle
Amphib. Reptile Conserv.
Hong Xiaoyou completed his B.A. degree at Huazhong Agriculture University, People’s Republic of
China, and his M.S.A. and Ph.D. degrees in Conservation Biology from Shanghai Ocean University,
People’s Republic of China. In 2011, he joined the Pearl River Fisheries Research Institute, Chinese
Academy of Fishery Sciences in Guangzhou, where his research is focused on the exploitation,
conservation of genetic resources, artificial breeding, and genetic improvement of turtles. In particular,
Dr. Hong has successfully bred Pe/ochelys cantorii in captivity for the first time in China.
Zhu Xinping received his Ph.D. degree in Genetics from the Institute of Hydrobiology, Chinese
Academy of Sciences, People’s Republic of China, in 2004. He has worked at the Pearl River Fisheries
Research Institute, Chinese Academy of Fishery Sciences in Guangzhou since 1988. Prof. Zhu is now
the Deputy Director of the Research Institute. The research scope of the team he leads focuses on
conservation and breeding of Pelochelys cantorii, the developmental mechanisms of turtle germ cells
and transplantation technology, breeding of high-fecundity Mauremys mutica, and early propagation
and breeding of fast-growing Pelodiscus sinensis.
Chen Chen completed his B.A. degree at Ludong University, People’s Republic of China, and
his M.S. and Ph.D. degrees at the Ocean University of China, People’s Republic of China. After
graduation, Dr. Chen joined the Laboratory of Aquatic Germplasm Resources and Genetic Breeding
at the Chinese Academy of Fishery Sciences, Pearl River Fisheries Research Institute in Guangzhou.
Recently, his research direction is in turtle population genetics, focusing on the allele distributions of
turtle populations and metapopulation dynamics.
Cai Xiaodan received her M.S. degree in Fishery Resources at Nanjing Agricultural University,
People’s Republic of China. She joined the Pearl River Fisheries Research Institute, Chinese Academy
of Fishery Sciences in Guangzhou in 2007, where her work is focused on river fisheries management
and aquatic life protection, with a special interest in Endangered aquatic wildlife protection.
Li Yongming graduated in 1988 from the Yunnan Agricultural School, People’s Republic of China,
majoring in Freshwater Aquaculture, and has been engaged in the domestication and breeding of
indigenous fishes in the Lancang River. As a government employee, Mr. Li conducts fishery supervision
and management as well as aquatic wildlife protection work.
Li Xinping is a farmer who cultivates aquatic seedlings, with a special interest in the protection and
breeding of turtles. Mr. Li has been rearing the two captive Chitra vandijki specimens used in this
study for more than 25 years.
68 September 2022 | Volume 16 | Number 2 | e316
Amphibian & Reptile Conservation
16(2) [General Section]: 69-87 (e317).
Official journal website:
amphibian-reptile-conservation.org
Applying population genetics to define the units for
conservation management in the European Tree Frog,
Hyla arborea
‘Astrid Krug, ‘?Jana Auffarth, and '*Heike Prohl
‘Institute of Zoology, University of Veterinary Medicine, Biinteweg 17, 30559 Hannover GERMANY *AquaEcology GmbH & Co. KG, Steinkamp
19, 26125 Oldenburg, GERMANY
Abstract.—Population genetic analyses are a powerful tool for obtaining information about cryptic genetic
lineages, population structure, and the distribution of intra- and interpopulation genetic diversity across the
landscape. This knowledge is crucial for establishing units for the conservation management of endangered
species. Species with limited dispersal capacities, such as amphibians, are particularly affected by habitat
fragmentation and reductions in gene flow among isolated populations. The European Tree Frog, Hyla
arborea, has suffered from dramatic population declines in the last decades and is categorized as Vulnerable
to Critically Endangered in its north-western distribution range. In Lower Saxony (Germany), the current
distribution of the tree frog is fragmented. In this study, we aimed to assess the population structure, genetic
diversity, gene flow, and migration rates in order to define the units for conservation management. Across
a distribution area of 250 km’, frogs were sampled at 14 localities and genotyped at seven microsatellite
loci, and the mtDNA cytochrome b gene was sequenced for a subsample. Whereas microsatellite pairwise
D,,,and F,, values showed genetic differentiation among nearly all sampled populations, Bayesian analyses
assigned the 14 localities to two distinct genetic clusters including seven subclusters. Together with a
slight correlation between geographic and genetic distance, the population structure indicates ongoing
fragmentation. The cytochrome b haplotype distribution does not indicate divergence into mtlineages, but
highlights the former connection of populations along the river Elbe. The results of this study suggest that the
intense anthropogenic pressures in this area over the last decades have had negative genetic consequences
for this species. The fragmented population structure calls for reconnection of the isolated occurrences by
the implementation of conservation measures.
Keywords. Amphibian, Bayesian assignment, conservation genetics, genetic diversity, population fragmentation,
population structure
Citation: Krug A, Auffarth J, Préhl H. 2022. Applying population genetics to define the units for conservation management in the European Tree Frog,
Hyla arborea. Amphibian & Reptile Conservation 16(2) [General Section]: 69-87 (e317).
Copyright: © 2022 Krug et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Accepted: 14 September 2022; Published: 24 October 2022
When reconnection of the habitats of endangered
Introduction
Genetic diversity and connectivity mediated by migrating
individuals between populations are critical for the
maintenance of many threatened species and can be
evaluated by population and landscape genetic analyses
(Shaffer et al. 2015). Loss of connectivity disrupts gene
flow between formerly connected habitats and leads to
the isolation of populations. Isolation in turn imposes a
more rapid erosion of genetic diversity, exacerbating the
effects of genetic drift and inbreeding on local gene pools
(Andersen et al. 2004; Crnokrak and Roff 1999; Hedrick
and Kalinowski 2000; Luquet et al. 2011).
Species 1S necessary, it 1s essential to determine the
genetic structures and migration patterns for effective
conservation management. This information can be used
to delineate conservation units (e.g., Palsboll et al. 2007),
even though the concepts that are applied to define them
are somewhat uneven among studies and taxa (Shaffer
et al. 2015). While Evolutionary Significant Units
(ESUs) are used to delineate entities which possess a
long (evolutionary) history (Crandall et al. 2000; Moritz
1994), management efforts are often restricted to a more
recent and regional space. In such cases, population
boundaries need to be identified among which gene
flow is limited. To achieve this, both mitochondrial
Correspondence. “heike.proehl@tiho-hannover.de (HP, corresponding author); krug_astrid@gmx.de (AK); auffarth.jana@gmail.com (JA)
Amphib. Reptile Conserv.
October 2022 | Volume 16 | Number 2 | e317
Conservation management units of Hyla arborea
and nuclear markers are informative. Mitochondrial
DNA has been widely used to analyze the phylogenetic
relationships of amphibian populations (Dufresnes et
al. 2013; Stock et al. 2012), while nuclear markers like
microsatellites are well suited for detecting fine-scale
structuring of populations and recent loss of genetic
variation (Selkoe and Toonen 2006). Population genetic
approaches such as Bayesian assignment tests use
population allele frequencies to group individuals into
genetic clusters. Together with information on genetic
divergence between genetic clusters, this approach can
be used to denote conservation units (Olsen et al. 2014;
Rowe and Beebee 2007).
In Europe, habitat loss, fragmentation, and degradation
— mostly due to anthropogenic pressure (Cushman 2006;
Pimm and Raven 2000) — are the most significant threats
to endangered wildlife populations (Fahrig and Merriam
1994; Sih et al. 2000; Stuart et al. 2004). Amphibian
populations are especially vulnerable to fragmentation
and loss of genetic variation due to their low dispersal
capabilities (as reviewed in Smith and Green 2006). For
safeguarding vulnerable species of this most endangered
vertebrate group (Stuart et al. 2004), it 1s necessary to
counteract genetic depletion by maintaining the exchange
of individuals among populations.
The European Tree Frog has shown long-term decline
in much of its Western European distribution, mainly
caused by habitat fragmentation (Andersen et al. 2004;
Dubey et al. 2009; Krug and Prohl 2013). The highest
genetic diversity of this species has accumulated in
South-eastern Europe, where it survived in refugia during
glaciations. After late-Pleistocene diversification on the
Balkan Peninsula, one of several major genetic groups
recolonized North and Western Europe. Postglacial
expansions resulted in decreasing genetic diversity across
the range and therefore increased the vulnerability of
populations towards North-Western Europe (Dufresnes
et al. 2013; Stock et al. 2012). Indeed, the tree frog is
not categorized as threatened in South-Eastern Europe,
while it is reported to have declined and is now classified
as Vulnerable to Critically Endangered in different
areas in the north-west (see review in Dufresnes et al.
2013, Table S1). In Lower Saxony in Germany, where
the current distribution is patchy with some main
occurrences in the lowlands (Fig. 1), the conservation
status of the tree frog 1s Endangered (see the Red List at
http://www.amphibienschutz.de). Although the species
was widespread in the past, severe declines have been
observed mainly in the second half of the last century
(Manzke and Podloucky 1995). In some places, measures
for conservation management have been successful
(Brandt and Liiers 2017; Buschmann et al. 2006; Richter
and Mugge 2012).
For supporting further conservation activities,
analyses of the genetic structure are required for
assessing the genetic clusters as a way to delineate the
units for conservation management (Rowe and Beebee
Amphib. Reptile Conserv.
2007). So far, several studies have measured the genetic
structure and diversity in more or less fragmented
metapopulation systems (Andersen et al. 2004; Angelone
and Holderegger 2009; Arens et al. 2006; Dubey et al.
2009; Edenhamn et al. 2000; Krug and Prohl 2013). The
aim of this study was to perform a conservation genetic
survey of the European Tree Frog across its distribution in
Lower Saxony and adjacent areas. The specific intention
was to assess significant genetic differentiation in order
to define those conservation units among which dispersal
is restricted. The obtained information was then used to
identify population management goals and to provide
specific recommendations about conservation priorities
to ensure the long-term survival of the tree frog in this
region.
In this study, we tested hypotheses regarding
population genetic structure, differentiation, and diversity
in the Endangered European Tree Frog by analyzing
mitochondrial sequence and nuclear microsatellite data
with a series of statistical techniques. First, we tested
for the existence of diverged genetic lineages. We
further predicted that past population expansion and
recent habitat fragmentation 1) reduced the migration
among localities; 2) reduced genetic diversity as well as
genetic population size within localities; and 3) resulted
in significant genetic structure among the remaining
tree frog localities. Therefore, 4) we expected a small
to moderate effect of geographic distance on genetic
differentiation as a result of the ongoing population
disconnection. This work reveals ongoing population
fragmentation with moderate genetic diversity for the
populations of the European Tree Frog in Lower Saxony.
Materials and Methods
Sample Collection and Preparation
Fourteen sites were sampled across the tree frog
distribution in Lower Saxony and adjacent distributions
in North Rhine Westphalia and Saxony-Anhalt, all in
Germany. We chose one sample site within each main
occurrence of the tree frog in this region (Fig. 1). In the
occurrence near Hannover, however, we sampled four
sites: two in the west of Hannover (KZ, KO, see Table
1 for site definitions) and two in the east of Hannover
(KH, BH) for a comparison of smaller scaled spatial
distances. In total, 237 individuals were sampled with
5—22 individuals per sample site (Table 1). Genetic
material was collected from the tips of tadpole tails and
buccal swabs of adult frogs. The adults were collected
from the choruses during the breeding seasons in spring
2007 and 2008. Tadpoles were sampled in summer 2007
at three localities. In this year, the climatic conditions for
breeding where unfavorable and adult catch rates were
low at these sites. To avoid bias in the results from tadpole
samples representing offspring from only one breeding
pair, tadpoles were sampled in different breeding ponds.
October 2022 | Volume 16 | Number 2 | e317
Krug et al.
heel
\
0 10 20 30 40 ad
Sa er aS
oe
Fig. 1. Current distribution of the European Tree Frog, and the distribution of cyt b haplotypes in Lower Saxony and adjacent areas
on the basis of TK25-quadrants (grey squares) during 1994—2010 in Lower Saxony (NLWKN 2011), 1993-2006 in North Rhine
Westphalia (LANUV 2011), and 1990-2000 in Saxony Anhalt (Meyer et al. 2004). Dashed lines denote state borders, dots denote
sample sites. Inset in upper left corner: Haplotype network of 11 distinct haplotypes of cyt 6 of H. arborea (901 bp) in Lower
Saxony and adjacent areas. Each haplotype is represented by one circle and color. The size of a circle corresponds to the haplotype
frequency. Lines between haplotypes denote mutational steps between sequences.
The genetic diversity for these localities was similar to
other locations, suggesting that relatedness among samples
did not bias the results (Table 1). DNA from the tail clips
was fixed in 99% ethanol and extracted using a proteinase
K digestion followed by a Phenol-Chloroform protocol
(Sambrook et al. 1989), and then stored at -20 °C. DNA
was extracted from the buccal swabs with an Invisorb Spin
Swab Kit (Invitek) following the manufacturer’s protocol,
and stored at -20 °C. Another study confirmed that buccal
swabbing is a very efficient method for obtaining DNA of
adequate quality for microsatellite amplification (Broquet
et al. 2007).
A total of seven polymorphic microsatellite loci
(WHA1-9, WHA1-20, WHA1-25, WHA1-67, WHAI1-
103, WHA1-104, and WHA1-140) previously isolated
by Arens et al. (2000) were amplified following the
author’s protocol, except that the annealing temperature
for WHA1-20 was changed to 64.6 °C. The PCR
products were genotyped using the capillary sequencer
MegaBace 1000 (Amersham Bioscience). Allele scoring
was performed using the software Genetic Profiler v.
Amphib. Reptile Conserv.
71
2.2. The genotyping results can be found in the file that
accompanies this article (Supplementary file 1).
Because earlier analyses (Stock et al. 2012) included
only four samples of mt DNA from Germany, we also
sequenced cytochrome 5 (cyt b) fragments of 901 bp for
5—20 individuals from each sample site, excluding KO and
BH from the Hannover population. The cyt 5 fragment
was amplified via PCR using the primers MVZ 15-L (5'-
GAACTAAT GGCCCA CACWWTACGNAA -3') and
cyt b AR-H (TAWAAGGGTCTTCTACTGGTTG) from
Moritz et al. (1992) and Goebel et al. (1999). The PCR
reaction (25 ul) consisted of 20-100 ng DNA, | ul of
each primer (10 uM), 0.8 ul dNTPs (10 mM, 5PRIME),
2.5 ul 10x advanced Buffer (SPRIME), 1.25 U Taq DNA
Polymerase (SPRIME), and 17.45 ul H,O. The PCR
conditions were as follows: an initial denaturation at 94 °C
for 3 min; 35 cycles at 94 °C for 45 s, annealing temperature
of 50 °C for 45 s, and extension at 65 °C for 1 min. The
PCR products were sent to the Macrogen Company
(Seoul, South Korea) for purification and sequencing with
an ABI3730XL genetic analyzer (Applied Biosystems).
October 2022 | Volume 16 | Number 2 | e317
Conservation management units of Hyla arborea
Table 1. Overview of data from the various sample sites. *: Samples from adult frogs, '' samples from tadpoles, H,: observed
heterozygosity, H,: expected heterozygosity, SD: standard deviation, F’,: inbreeding coefficient, with bold values for significant
differences after 1,000 permutations, R: mean allelic richness over all loci, 4: haplotype diversity, 2: nucleotide diversity, NV: number
of sampled individuals, N,: mean number of alleles over all loci.
ID Sample site mean H, + SD mean H, + SD Fs IN’. R h m [%| N
QU Quakenbriick * 0.786 + 0.248 0.741 0.143 -0.070 4.00 ~ 0.00 0.00 5
WK Westerkappeln* 0.661 + 0.187 0.579 + 0.158 -0.154 3.43 - 0.54 0.06 8
EK Espelkamp* 0.796 + 0.169 0.754 + 0.087 -0.058 S29 5.18 0.00 0.00 12
KZ Kananohe Zentrum * 0.667 + 0.169 0.666 + 0.134 -0.001 5.14 4.65 0.00 0.00 20
KO Kananohe Ost? 0.701 + 0.208 0.684 + 0.089 -0.027 4.57 4.53 - - 11
KH Kolshorn# 0.754 + 0.131 0.713 + 0.094 -0.059 6.29 3.37 0:53 0.13 20
BH Beinhorn* 0.693 + 0.089 0.693 + 0.093 -0.001 S57 4.84 - - 20
BA Bassum ' 0.771 + 0.099 0.748 + 0.092 -0.032 5.43 4.98 0.41 0.05 20
RU Ruschwedel * 0.731 + 0.064 0.721 + 0.050 -0.015 5.00 4.50 0.68 0.14 18
WG Wolfsburg-Gifhorn * 0.790 + 0.158 0.799 + 0.080 -0.011 7.71 6.65 0.61 0.08 20
ST Strothe 0:735,+ 0.153 0.708 + 0.126 -0.039 6.29 5.34 OAQ 0.02 21
AN Amt Neuhaus # 0.708 + 0.111 0.750 + 0.090 0.057 6.43 5.50 0.66 0.15 22
SW Salzwedel ' 0.600 + 0.227 0.687 + 0.181 0.130 6.00 5.01 0.57 0.11 20
PW Pevestorfer Wiesen* 0.793 + 0.110 0.764 + 0.091 -0.039 6.43 5.55 0.42 0.05 20
Statistical Analysis
Analysis of mtDNA
Both directions of the cyt b sequences were assembled
using the computer software SeqMan™ I (DNASTAR,
Inc., Konstanz, Germany). Multiple sequence
alignments were performed in MEGA 4 (Tamura et al.
2007) using the Muscle algorithm (Edgar 2004), and
all variable sites were confirmed by visual inspection
of the chromatograms. The EMBL-EBI sequence
analytical tool (Madeira et al. 2022) was used to
convert the sequences to the corresponding amino acid
sequences in order to assure that nuclear copies were
not sequenced. The program MEGA was applied to
calculate p-distances between sample sites (Tamura
et al. 2004). Haplotype diversity (4) and nucleotide
diversity (ma) (Nei 1987) were determined with
ARLEQUIN ver. 3.11 (Excoffier et al. 2005). A haplotype
network of the cyt 6 data set was constructed via the
statistical parsimony analysis of the program TCS
1.21 (Clement et al. 2000) using the default settings.
Analysis of Microsatellites
Microsatellite data were checked for null alleles,
stuttering, and allelic dropout using Micro-CHECKER
(Van Oosterhout et al. 2004). The program Fstar v.
2.9.3 (Goudet 1995) was used to test for genotypic
disequilibrium of all pairs of loci in each sample and to
calculate average allelic richness per population. For the
calculation of average allelic richness, sample sites with
less than ten individuals (QU and WK) were excluded.
For each sample site and locus, the observed and
Amphib. Reptile Conserv. 72
expected heterozygosity (Nei 1987) and deviation from
Hardy-Weinberg equilibrium (HWE) (Guo and Thompson
1992) were determined with ARLEQUIN Ver. 3.11 (Excoffier
et al. 2005). Genepop ver. 4.1 (Rousset 2008) was used to
test for a global deviation from HWE in each sample site.
The inbreeding coefficient fF’. per sample site (Weir and
Cockerham 1984) was calculated using Genetix ver. 4.05
(Belkhir et al. 2004) and the significance was tested with a
permutations test (1,000 permutations).
Genetic differentiation between the sample sites was
calculated as global F’,.and pairwise F’,. values (Weir and
Cockerham 1984) in ARLEQuUIN (Excoffier et al. 2005). In
addition, pairwise D_., (Jost 2008), a substitute measure
of genetic differentiation, was calculated using the R
package DEMEtics (Gerlach et al. 2010). Significance
was calculated by 10,000 bootstraps.
The data were also tested for Isolation By Distance
in sampled populations (IBD; Storfer et al. 2010; Wright
1943). IBD occurs when gene flow occurs but declines
with increasing distances between pairs of populations,
and is typical for the genetic population structure of
many animal species (Hitchings and Beebee 1997; Spear
et al. 2005; Vergara et al. 2015). To test for IBD, a Mantel
test for correlation between pairwise genetic distances
(F,, and D,.) and pairwise geographic distances was
conducted, implemented in IBDWS 3.23 (Jensen et al.
2005). As proposed by Rousset (1997) for populations
in two-dimensional habitats, geographical distance was
log-transformed and genetic distance was expressed
as F. (1 — F,,), and D,,, (1 — D,,). Significance for
tr > 0 was assessed via 10,000 bootstraps. The linear
geographic distances among sample sites were calculated
in ArcView GIS 3.3 using the Distance Matrix extension
(Jenness 2005).
October 2022 | Volume 16 | Number 2 | e317
Krug et al.
Even though the Mantel test is widely used in
landscape genetic studies, an evaluation of different
methods revealed that Mantel tests exhibit high type-
1 error rates (Balkenhol et al. 2009). Those authors
recommended applying a combination of statistical
methods to avoid inaccurate conclusions derived from
only one method. Therefore, two additional hierarchical
Bayesian methods, GESTE (Foll and Gaggiotti 2006) and
BIMr (Faubet and Gaggiotti 2008), were applied here for
evaluating the effect of distance by means of generalized
linear models. Both BIMr and GESTE perform well for
moderate samples sizes and limited numbers of loci, as in
our study (Balkenhol et al. 2009).
GESTE estimates the genetic distance (F.,. values)
for each local population pair from multilocus genotypes
and correlates them to environmental factors. Posterior
probabilities associated with each factor allow the
identification of factors with the highest effect on genetic
structure. The regression coefficient estimate (Alpha)
indicates whether a factor reduces or enhances genetic
differentiation. The estimation of model parameters 1s
performed by using a combination of Markov Chain
Monte Carlo (MCMC) and Reversible-Jump MCMC
(RJMCMC) (Green 1995). As environmental factors,
we included latitude (G1) and longitude (G2; geographic
coordinates in GK3 format) as approximations of the
effect of distance among population pairs.
The software BIMr 1.1 estimates contemporary gene
flow and assesses the influence of genetic distance on gene
flow. This program quantifies the gametic disequilibrium
from multilocus genotypes (here, microsatellite alleles)
generated by the progeny of recent migrants to calculate
the proportion of the population that immigrated during
the last generation (Faubet and Gaggiotti 2008). Five
replicates (= runs) were run with a total of 1,020,000
iterations (burn-in: 1,000,000, sample size: 20,000) and
a thinning interval of 50 iterations. For each replicate,
first 20 short pilot MCMC runs of 1,000 iterations
were conducted, and the run with the lowest Bayesian
deviance (De) and the highest posterior probability
was selected to extract the parameter estimates (Faubet
et al. 2007; Faubet and Gaggiotti 2008). Two models
were calculated: model 0 did not include environmental
factors and model 1 included factor G1 which is the
geographic distance between pairs of populations. As
an alternative, the BayesAss software (Rannala 2007;
http://www.rannala.org/software/) was also used to
infer contemporary migrations rates. The software
was run with 10,000,000 iterations (i), a burn-in (b) of
1,000,000 repetitions, and the interval between samples
(n) was set to 1,000. The default values were used for all
other parameters at first. Then, we adjusted the mixing
parameters for migration rate (m), allele frequencies
(a), and inbreeding coefficients (f) to maintain their
acceptance rates between 20% and 60% as recommended
in the Manual.
Amphib. Reptile Conserv.
To infer genetic clusters, individual assignments to
populations were conducted by means of a combination
of non-spatial and spatial Bayesian algorithms with
STRUCTURE Version 2.3.3 (Pritchard et al. 2000) and TESS
version 2.3 (Chen et al. 2007; Francois et al. 2006).
Simulation data suggested the combination of TESS and
STRUCTURE as a reliable approach for deducing the spatial
population structure (Chen et al. 2007), outperforming
other Bayesian clustering programs. All StrucTURE runs
used 500,000 iterations after a burn-in period of 100,000.
An admixture ancestry model and correlated allele
frequencies were used between populations. STRUCTURE
was run both without and with information about the
sampling location (prior population information) and the
results were compared as recommended by Pritchard etal.
(2000; see also Dufresnes et al. 2013; Olsen et al. 2014).
Hierarchical analyses were performed by repeating the
STRUCTURE runs with each of the major clusters. Twenty
runs were conducted for each K. The range of possible
Ks tested spanned from | to 14, according to the number
of sampled breeding sites. The average log likelihood
Pr(X|K) (given by the estimated Ln Prob of data = Ln
P(D) in the software result output, see Table 4) was
calculated for each K across all runs. Since detecting
the true number of K is not always straightforward, we
included the AK statistics proposed by Evanno et al.
(2005), using STRUCTURE HARVESTER V.0.6.8 (Earl and von
Holdt 2012).
TESS uses a Bayesian method to detect population
structure, but it considers the spatial information
(geographical coordinates) of the individuals. After
assessing the preliminary runs as recommended in the
software manual, the maximum number of allowed
genetic clusters (K,.) was varied from 2 to 10. One
hundred independent runs for each K_ were conducted
under the admixture model, with 50,000 sweeps and a
burn-in period of 10,000 sweeps for each run.
Finally, the NeEstimator v2 software was used
to estimate the contemporary effective population
sizes at all sample sites (Do et al. 2014). Three single
sample estimators were implemented: the linkage
disequilibrium method, the heterozygote-excess method,
and the molecular coancestry method. The lowest allele
frequencies (P....) were set to 0.05, 0.02, 0.01, and 0+.
Crit
Results
Genetic Diversity
Genetic diversity was estimated for each population based
on the microsatellite alleles and the cyt 6 haplotypes (Table
1). While genetic diversity indices based on microsatellites
(H,, H,, N,, and R) are moderate to high across the range,
they are always highest in WG (except for H.); while the
indices based on cyt b (h, 2) tend to increase from west
(WK/QU) to east (PW) (Table 1; Fig. 1).
October 2022 | Volume 16 | Number 2 | e317
Conservation management units of Hyla arborea
Table 2. Pairwise D
est
Table 1 for sample site acronym definitions.
values (lower matrix) and pairwise F’,. values (upper matrix) between sample sites; ns = not significant. See
QU WK EK KZ KO KH
QU 0 0.120 0.066 0.111 0.113 0.110
WK 0.208 0 0.114 0.064 0.107 0.117
EK 0.195 0.286 0 0.041 0.031"° 0.069
KZ 0.284 0.145 0.102 0 0.002" 0.090
KO 0.324 0.243 0.097 0.001" 0 0.092
KH 0.412 0.301 0.222 0.279 0.290 0
BH 0.387 0.372 0.230 0.284 0.311 0.059
BA 0.189 0.230 0.220 0.199 0.189 0.172
RU 0.424 0.449 0.285 0.382 0.386 0.173
WG 0.139 0.309 0.296 0.230 0.306 0.237
ST 0.299 0.208 0.329 0.281 0.308 0.175
AN 0.265 0.315 0.230 0.248 0.263 0.245
SW 0.238 0.391 0.289 0.233 0.228 0.368
PW 0.213 0.365 0.278 0.278 0.322 0.350
BH BA RU WG ST AN SW PW
0.103 0.039 0.117 0.043 0.086 0.086 0.084 0.052
0.154 0.097 0.191 0.107 0.083 0.119 0.162 0.147
0.076 0.060 0.090 0.061 0.095 0.065 0.097 0.071
0.099 0.066 0.139 0.081 0.092 0.081 0.095 0.105
0.104 0.059 0.130 0.081 0.092 0.074 0.091 0.106
0.025 0.053 0.062 0.064 0.056 0.074 0.110 0.094
0 0.074 0.092 0.082 0.076 0.102 0.118 0.100
0.225 0 0.074 0.037 0.072 0.070 0.083 0.066
0.252 0.235 0 0.068 0.079 0.072 0.110 0.073
0.283 0.142 0.252 0 0.056 0.071 0.086 0.061
0.238 0.239 0.222 0.201 0 0.057 0.110 0.070
0.316 0.242 0.238 0.290 0.211 0 0.097 0.065
0.367 0.272 0.347 0.287 0.369 0.343 0 0.078
0.337 0.253 0.267 0.249 0.226 0.241 0.253 0
Mitochondrial Sequence Analysis
The analysis revealed 11 haplotypes of the cytochrome
b fragment which differed by ten variable sites and
nine parsimony informative sites (Fig. 1). There was no
evidence for any diverged haplotype groups that would
correspond to different genetic lineages. Most haplotypes
were closely related but unique to one sample site, except
for haplotypes Hy-1, Hy-2, and Hy-5. While Hy-1 (blue)
and Hy-5 (red) showed a broad distribution over almost
the complete sampling area, Haplotype Hy-2 (green)
was restricted to five sample sites in the northeast (Fig.
1). Eight haplotypes were found at only a single locality:
Hy-3 (white) in AN, Hy-4 (orange) in BA, Hy-6 (light
blue) in EK, Hy-7 (yellow) and HY-8 (brown) in KH,
Hy-9 (dark blue) in RU, and Hy-10 (grey) and Hy-11 (dark
grey) in WG. In WG and RU, four different haplotypes
were detected, while in QU, EK, and KZ (all in the west of
Hannover) only one haplotype was found. The p-distances
among localities were low, varying between O and 0.4
% (Supplementary Table S1). The GenBank accession
numbers can be found in Supplementary Table S3.
Microsatellite Analysis
The seven microsatellite markers examined were
polymorphic with seven to 16 alleles per locus. The
analysis with Micro-CHECKER uncovered signs of null
alleles for locus WHA1-67 in sample site KO and for
locus WHA1-140 in sample site SW. As null alleles for
these two loci were found at only a single sample site, we
did not adjust for null alleles. Furthermore, this analysis
revealed no evidence for large allele dropout or scoring
errors due to stuttering.
Deviation from Hardy-Weinberg-Equilibrium (HWE)
was found for WHA1-104, with a significant excess of
heterozygotes in sample site KH. The global test for
Amphib. Reptile Conserv.
HWE over all loci in each population resulted in no
significant deviation from HWE. Significance values
for the inbreeding coefficient F, were obtained for the
sample sites SW (F,, = 0.130) and WK (F,, = -0.154,
Table 1). No linkage (genetic) disequilibrium was found
between any pair of loci.
The global F’,. value across all localities was 0.083 and
highly significant (P > 0.0001). Genetic differentiation
calculated as pairwise D,_ and pairwise F’,. values were
significant in all cases except between the two sample
sites in the West of Hannover (KZ and KO), as well as EK
and KO regarding the F’,. values (Table 2). The Mantel
test for IBD showed a significant but low correlation
between the genetic and geographic distances (Fig. 2;
Der =Q:28eP O01 Eh. F029: 20,0 1S see
also Supplementary Table S2), indicating that genetic
differentiation is only partially explained by geographic
distances among the sites.
GESTE calculated five different models (Table 3). The
probability of a model was not improved by including
either latitude (G1) or longitude (G2) without interaction.
The model with the highest posterior probability was model
4, which included the constant, latitude, and longitude as
well as their interaction. The Alpha values were low for the
effects of both factors, while the Alpha value of the inter-
action indicates a significant effect on genetic differentiation.
All five replicates of the BIMr analysis showed a
De of 0.0. The highest posterior probability for the null
model was 0.79 (run 1), and the lowest was 0.55 (run
4). The posterior probabilities for model 1 (including
G1) were lower than the posterior probabilities of the
null model (Table 4); i.e., the geographic distance did
not seem to affect recent gene flow or migration among
sample sites. Mean migration rates were extremely low
and varied from 2.88e"" to 1.1le°; while the highest
mean migration rate was observed among PW and
WG, and the lowest was among AN and QU. Also, the
October 2022 | Volume 16 | Number 2 | e317
Krug et al.
Genetic Distance [D,,/(1-D...)1
Genetic Distance [F,,/(1-F;,)]
“0.0 0.6 4:2 1.8 2.4 3.0 =<010 0.6 1.2 1.8 2.4 3.0
Geographic Distance (Log km) Geographic Distance (Log km)
Fig. 2. Isolation By Distance plots. (a) D,, /(1 — D.,,) versus log geographic distance; and (b) F’,./(1 — F,,,) versus log geographic
est est
distance. The lines are the RMA (Reduced Major Axis) regressions.
migration rates between two close population pairs inthe by TESS (see below). Within each cluster, a fine
surroundings of Hannover were very low. For example, — substructuring could be detected, and the two approaches
the mean migration rates between KH to BH and vice — (with/without prior population information) provided
versa were only 1.66e!° and 2.34e!°, and those between __ slightly different clustering solutions. In those runs where
KZ and KO were 1.92e'° and 2.24e'° even though the __ the sampling location was used as prior information, the
distances between these pairs were only 3.94 km and 2.6 — western/central cluster was split along Hannover with
km, respectively. The analysis with BayesAss provided some admixed populations in the western part of the
very similar results for the runs with default and adjusted region (K =3, Fig. 3B). The Structure runs without prior
parameters. The migration rates were higher than those — population information supported the existence of two
calculated with BIMr, most of which fluctuated around genetic subclusters within this region (Supplementary
0.01. Interestingly, the migration rates between EK and Fig. S1B). Inthe northern/eastern cluster, both approaches
KZ, KO and KZ, as well as KH and BH were considerably provided similar results (Fig. 3C and Supplementary Fig.
higher (0.14, 0.16, and 0.20, respectively) and more SIC). RU was differentiated from WG and ST, which in
consistent with the genetic population structure (Fig. 3) — turn differed from the populations lying 1n the eastern
as well as the above-mentioned geographic distances. part of the study area in Saxony Anhalt. More detailed
Bayesian assignments conducted by Structure _ results of log likelihood Pr(X|K) values and AK statistics
suggested two major groups (K = 2), separating the — are provided in the Supplementary figures (Figs. S2 and
western/central populations (WK-BA-EK-KZ-KO-BH- __ S3, respectively).
KH) and the northern/eastern populations (RU-WG-ST- The TESS analysis supported the two major genetic
AN-PW-SW, Figs. 3A and 4, see also Supplementary —§ groups separated into a western/central cluster and a
Fig. SIA). The population QU appeared to be admixed, __ northern/eastern cluster (Fig. 5). Increasing the number
but was unambiguously assigned to the western group _ of K,. resulted in only a slight decrease in the Deviance
Table 3. Posterior probabilities for five possible models calculated with GESTE explaining the genetic differentiation of European Tree
Frogs as a function of the environmental factors latitude (G1) and longitude (G2). Constant is the intercept of the regression model. The
regression coefficients (Alpha) for different environmental factors used in the models are given in the right side of the table.
Model Factors included Posterior probability Factors Regression coefficients
ModelO — Constant 0.19 Constant Alpha 0 -3.69
Model 1 Constant, G1 0.19 Gl Alpha 1 0.06
Model2 — Constant, G2 0.18 G2 Alpha 2 -0.07
Model 3 Constant, G1, G2 0.17 G1*G2 Alpha 3 -2.14
Model 4 Constant, G1, G2, G1*G2 0.26
Amphib. Reptile Conserv. 75 October 2022 | Volume 16 | Number 2 | e317
Conservation management units of Hyla arborea
A
es § Y & F F F F&F YF F FF F F
Fig. 3. Estimation of the number of Hy/a arborea populations using the program Structure ver 2.3.1 (Pritchard et al. 2000) for the
admixture model with prior population information; QU, WK, EK, etc. = sample sites, separated by fine black lines. Each individual
is represented by a single vertical line broken into colored segments, with lengths proportional to the corresponding clusters. (A)
Plot for K = 2 in the analysis of the entire data set, (B) plot for K = 3, and (C) K = 4 for hierarchical analysis on each of the two
main clusters.
Information Criterion (DIC) of the models while the
resulting population structure was not consistent among
runs for each K, or in comparison with the STRUCTURE
results (data not shown). STRUCTURE as Well as TESS
revealed that frogs from WG in the eastern group (Fig.
3A) are of admixed origin from both genetic groups as
the assignment results from the two were similar.
Effective Population Sizes
Mean effective population sizes (N.) varied among the
sample sites and statistical methods applied. The results
also differed between P.,.. = 0.05 and the other P.,.. but
were the same for P,,,, = 0.02, 0.01, and 0+ (Table 5). The
large confidence intervals indicate that the results might
not be very reliable. However, most calculated N, values
were small (100 individuals or less). Only three sample
sites (KO, AN, and PW) showed consistently high values
for N (500 or higher, or infinite) for most methods.
Discussion
The analyses presented here provide valuable information
for the conservation management of the Endangered
European Tree Frog species, Hyla arborea, which suffers
from population isolation in its northern distribution
range. In Lower Saxony, a weak correlation between
genetic and geographic distances suggests a low level of
recent gene flow among localities, and further analyses
indicate a lack of current migration at least during the last
generation. Two major genetic clusters, one in the east
and one in the west, were found with some admixture
in a central population. Both main clusters were further
subdivided into several distinct regional clusters. The
substantial population structure, verified by significant
genetic distances among localities, suggests that the
populations are currently isolated to a large extent.
Consequently, conservation management is needed to
ensure the long-term persistence of this species in Lower
Saxony with suitable effective population sizes and high
levels of genetic diversity that are necessary to counteract
the reductions in fitness and adaptive potential (Andersen
et al. 2004; Frankham 2005; Allentoft and O’ Brien 2010;
Angelone 2010).
Isolation by Geographic and Genetic Distances
In addition to the Mantel test, the landscape genetic
analysis in GESTE provided some insight into the role
of geographic distance on genetic differentiation. While
the models including latitude and longitude alone did
not offer a better explanation for genetic differentiation
than the null model, the most complex model including
the interactions between latitude and longitude did. We
interpret this as the effect of the geographic distance
Table 4. Results of BIMr analysis (means of posterior probability and Alpha for run 1) for estimating migration rates among
localities with European Tree Frogs in Lower Saxony. The factor G1 is the geographic distance. Alpha 0 and Alpha | represent
estimates of the constant term and factor G1, respectively.
Model Factor Posterior probability Alpha 0 Alpha 1
Model 0 0.79 1.64
Model 1 G1 = geographic distance 0.21 1.48 0.14
Amphib. Reptile Conserv. 76 October 2022 | Volume 16 | Number 2 | e317
Krug et al.
A
Mean of estimated Ln probability of data ~~
Delta K
oOo NM fF OO
2 4 .6 -8 -10 12. 44
K
Fig. 4. Mean values of estimated Ln probability of data (LnPD) for each K (a) and delta K (b) when prior population information
was implemented.
on genetic dissimilarity between localities. Overall,
however, the posterior probability and alpha values
illustrate that the distance effect 1s not very large.
Habitat fragmentation might play a more important role
in shaping the genetic structure of the tree frogs in this
area. According to Podloucky and Fischer (2013), habitat
fragmentation in Lower Saxony is mainly caused by the
loss of summer habitat, breeding ponds, and corridors
suitable for migration. This is in accordance with the
disconnected distribution (Fig. 1) and significant genetic
distances (F,.and D, ) among most tree frog populations.
A significant population structure as a result of
limited dispersal between isolated populations 1s
typically accompanied by a slight to moderate effect of
isolation by distance. Isolation by distance was detected
in some European amphibian species (Rana dalmatina,
Sarasola-Puente et al. 2012; Bombina_ variegata:
Weihmann et al. 2009; Hantzschmann et al. 2020), but
not others (Bufo calamita: Allentoft et al. 2009; Bombina
bombina: Dolgener et al. 2012). For the tree frogs in
Lower Saxony, the small positive correlation (7 ~ 0.28)
between genetic and geographic distances suggests
a very low level of recent gene flow among localities.
This finding is in accordance with earlier studies on
tree frogs, which reported small to moderate correlation
coefficients between both distances and significant
population structure (Andersen et al. 2004; Angelone and
Holderegger 2009; Arens et al. 2006). In all these studies,
limited gene flow was explained by habitat fragmentation,
particularly the loss of breeding ponds. In contrast,
in those frog species which occur in more continuous
habitats or that have higher dispersal capacities, the
Fig. 5. Map of geographic-genetic cluster membership for A, = 2 as inferred by TESS.
Amphib. Reptile Conserv. 77 October 2022 | Volume 16 | Number 2 | e317
Table 5. Results for effective populations sizes (NV) calculated with the NV Estimator for three different methods and different P
Conservation management units of Hyla arborea
Crit
values. N. values were the same for P.,,, = 0.02, 0.01, and 0+. Only 0+ is used in the Molecular Coancestry method. Mean values
(N.) and Confidence Intervals (CIs) are given for each sample site, method, and P
Crit
The three methods
option.
Linkage disequilibrium Heterozygote excess Molecular
coancestry
Sample site Pre 0.05 0.02/0.01/0+ 0.05 0.02/0.01/0+ 0+
QU N, D5:7. 55.7 78 78 9.5
Cls 1.4 — inf. 1.4 — inf. 3.7 — inf. 3.7 — inf. 5.1-—15.2
Wk N, 1.3 13 5.1 5/1 2h
Cls 0.7 —2.7 0.7-2.7 2.5 — inf. 2.5 — inf. 2.0 —3.5
EK N, 16.3 33:5 9.9 9.9 8.2
ClIs 5.6 — inf. 8.7 — inf. 4.5 — inf. 4.5 — inf. 2.7—-16.9
KZ N, 46.3 28.2 34.7 34.7 5.6
CIs 15.8 — inf. 12.1 —319.2 7.5 — inf. 7.5 — inf. 2.3-—10.5
KO N, inf. 611.3 2515 2515 inf.
CIs 11.4 — inf. 10.4 — inf. 4.3 — inf. 4.3 — inf. inf. — inf.
KH N, 3193 159.7 inf. 443 59
CIs 30.5 — inf. 30.2 — inf. 5.8 — inf. 6.0 — inf. 3.2-8.9
BH N, 83.5 735 PORT inf. inf.
Cls 21.0 — inf. 21.3 — inf. 7.2 — inf. 7.7 — inf. inf. — inf.
BA N, W772 188.0 322.0 322.0 10.8
Cls 26.5 — inf. 26.8. inf. 6.5 — inf. 6.5 — inf. 1.8 —27.7
RU N, 19.3 27:5 67.7 81.9 inf.
Cls 8.4 — 106.4 10.8 — inf. 6.8 — inf. 7.1 — inf. inf.
WG N, 31.1 65.5 inf. inf. 9.1
CIs 16.0 — 113.5 26.0 — inf. 8.1 — inf. 9.3 — inf. 3.8 — 16.6
ST N, 34.7 TLS 39.7 51.0 inf.
Cls 15.7-315.7 25.4 — inf. 6.4 — inf. 7.2 — inf. inf. — inf.
AN Ny inf. inf. inf. inf. inf.
Gis 41.7 — inf. 74.0 — inf. 30.9 — inf. 57.8 — inf. inf. — inf.
SW N, StS 36.0 inf. inf. 43.4
CIs 15.2 — inf. 16.1 — inf. inf. — inf. 280 — inf. O-—217.7
PW N, 631.9 inf. inf. inf. inf.
CIs 36.2 — inf. 73.1 — inf. 6.1 — inf. 6.6 — inf. inf. — inf.
correlation between geographic and genetic distance 1s
higher (e.g., Prohl et al. 2006) or disappears in case of
panmixia (Leblois et al. 2000).
The BIMr analysis revealed that contemporary
migration (1.e., during the last generation) was practically
absent among the sample sites of tree frogs in Lower
Saxony. This is in contrast to the migration rates calculated
with BayesAss and the results of the SrRuCTURE analysis
(see below), which imply that individuals of mixed
ancestry exist in the different genetic clusters. However,
gene flow over the last few tree frog generations may
have suffered due to the expanding habitat fragmentation,
while some decades ago far more tree frog localities were
reported for lower Saxony, thus, the connectivity among
them was much better (Manzke and Podloucky 1995).
Amphib. Reptile Conserv.
Therefore, the signals for gene flow are still apparent in
the results of some analyses (StrucTURE, BAYESAss) but
not in those where the calculations are restricted to the
most recent years (BIMr).
Genetic Diversity
The expected microsatellite heterozygosity (H,) has been
measured in a number of previous population genetic
studies of the European Tree Frog. Interestingly, H, was
higher in the current study area (H,: 0.60 — 0.79) than in
most other northern areas where the genetic situation of
the tree frog was investigated (e.g., H, values in Denmark:
0.35—0.54, Andersen et al. 2004; Switzerland: 0.27—0.71,
Angelone and Holderegger 2009; and the Netherlands:
October 2022 | Volume 16 | Number 2 | e317
Krug et al.
0.39-0.59, Arens et al. 2006). As expected, the more
peripheral populations, such as those in Denmark and
the Netherlands, show lower genetic diversity values. In
comparison, the mthaplotypes diversity (mean h= 0.38, n
= 14 populations) is lower in the Lower Saxony area than
in the southern part of the distribution range (Greece,
Albania, Croatia, Serbia, and Romania) were the average
h amounts to 0.7 (n = 20 populations, calculated from
Dufresnes et al. 2013, Table S2). From all cumulative
data within the framework of this study, we can conclude
that in central and northern Europe, human induced
fragmentation processes involving habitat destruction
in a previously widely distributed frog species are
contributing to the depletion of genetic diversity.
Genetic Structure and Conservation Units
The Bayesian cluster analyses conducted with STRUCTURE
and TESS support the division of the tree frog populations
into two major geographic-genetic clusters, one in the
west and one in the east. One population in the south-
east of the area (WG) shows admixture between the two
groups and therefore a relatively high genetic diversity.
Thus, it seems that both groups were previously connected
by migrating animals when habitat fragmentation was
less severe. This result is consistent with the moderate
correlation between geographic distance and genetic
distances. Both analyses also provide evidence for
further fragmentation within both groups. In contrast, the
haplotype network does not indicate any older, distinct
(e.g., postglacial) lineages supporting the finding of
Dufresnes et al. (2013), that only one evolutionary unit is
present in this area.
Microsatellite pairwise D, and F.,. values all showed
significant genetic differentiation except for the two closest
sites (KZ and KO) in the West of Hannover. However,
mthaplotype distribution and Bayesian analyses of the
microsatellites suggest distinct relationships among the
currently fragmented localities. In the Northeast of Lower
Saxony, the distribution of the mthaplotypes indicates a
former connection of the populations along the river Elbe.
Interestingly, the easternmost occurrences at AN, PW,
and SW in the current and former distributions display a
relatively well-connected area, nonetheless the presently
distinct genetic sub-clusters in the Bayesian analyses and
pairwise F’. values are relatively high. The significant
F’, value found for SW indicates that the separation of
this site may have resulted in inbreeding in an isolated
population. Altogether, the available microsatellite data
point to recent fragmentation of tree frog populations
in this area, while similar mthaplotypes provide some
evidence for a former connection.
Interestingly, there is a significant genetic divergence
between the sample sites KZ and KO in the West and
the sample sites KH and BH in the East of Hannover.
One possible explanation is that recently constructed
motorways in combination with genetic drift contributed
Amphib. Reptile Conserv.
79
to population differentiations, which are also apparent in
the mthaplotype frequencies. Roads have been identified
as barriers to gene flow in some other amphibians (Arens
et al. 2007; Lesbarreéres et al. 2006). One central question
is whether these relatively young barriers (motorways
expanding in the 1960s, and dense urban areas) are the
only reason for the differentiation of these formerly
linked tree frog localities (Manzke and Podloucky 1995).
The low haplotype diversity in KZ, EK, and QU points to
a loss of genetic diversity as a consequence of increased
genetic drift in isolated occurrences.
In summary, the genetic analyses point to a highly
structured population, as was observed in other surveys
of European amphibians (Dolgener et al. 2012; Rowe and
Beebee 2007; Sarasola-Puente et al. 2012; Hantzmann et
al. 2020). The risks of fragmentation include population
reduction, loss of genetic diversity and declining fitness,
and finally extinction (Hitchings and Beebee 1997;
Cushman 2006). To reverse such negative processes,
conservation management that takes the genetic
population structure into account is important (Allentoft
et al. 2009; Olsen et al. 2014). For this endangered and
fragmented frog species, we suggest delineating the two
major genetic clusters as conservation units; and then
within those, intense reconnection efforts should be
undertaken by creating suitable habitats for migrating
frogs. Moreover, there is clear evidence of admixture in
WG, and gene flow along this route could be reestablished
between both clusters.
Conservation Measures
In our opinion, future conservation management should
be directed towards two aims. The first aim is to maintain
high genetic diversity in large and stable populations
within each conservation unit. In this context, it has been
argued that an effective breeding size (N_) of at least 50
animals is necessary to avoid inbreeding in the short
term and that an N, of 500 is necessary to maintain the
evolutionary potential that would allow adaptations to
environmental changes and assure long term viability
(Jamieson and Allendorf 2012). Most of our isolated
sample sites (e.g., BA, Fig. 3B—C) or sub-clusters (e.g.,
KH-BH) do not reach these effective population sizes.
For tree frogs, the ratio of effective breeding size (N_) to
census size (N) is ~ 0.5 (Broquet et al. 2009). Therefore,
we recommend the monitoring of population sizes and
maintaining population sizes of at least 100 breeding frogs
in isolated populations, 1.e., each sub-cluster, for short
term conservation goals, but increasing the population
sizes to 1,000 or more embedded in each of several meta-
population systems in every conservation unit (see also
Andersen etal. 2004; Frankham etal. 2014). Incases where
populations within a conservation unit are genetically and
geographically separated, genetic rescue can be attained
by establishing corridors to stimulate dispersal (e.g.,
in AN-SW-PW). Dense networks of suitable spawning
October 2022 | Volume 16 | Number 2 | e317
Conservation management units of Hyla arborea
ponds have been destroyed by habitat conversion but are
of great importance for the maintenance of large tree frog
populations and the connection of subpopulations. There
are several reports that tree frogs not only respond well
to new suitable water bodies, but also depend on them
for migrations exceeding several km and often colonize
them in subsequent breeding seasons (e.g., Angelone
and Holderegger 2009; Brandt and Ltiers 2017; Hansen
2004; Schwartze 2002; Zumbach 2004).
The second aim is to maintain overall genetic diversity
among the genetic clusters within the species and to
protect local co-adapted gene complexes (Savolainen et
al. 2013). To achieve this second goal, we recommend
the re-establishment of gene flow between genetic
clusters where possible, but at a lower level than within
them. This particularly applies to the western and eastern
clusters between which (former) gene flow is evidenced
by the Structure analysis (Fig. 3). Habitat reconnection
between these areas would allow a few frogs to travel
between the breeding ponds of different clusters, thereby
refreshing genetic diversity and counterbalancing the loss
of genetic diversity through drift, while diverse selection
pressures would sustain local adaptation. Levels of genetic
diversity inferred from neutral markers are not necessarily
correlated with variation in locally adapted traits. In this
context, more research is necessary to understand which
traits are locally adapted and how their variation affects
the fitness of a population. Very isolated and small
populations might benefit from translocations, 1.e., the
introduction of individuals from other populations. In
such cases, translocations should be restricted to within
the conservation unit to avoid causing outbreeding
depressions that have sometimes been observed between
distantly related populations (Sagvik et al. 2005).
Conclusions
Populations of the European Tree Frog in Lower Saxony
are highly fragmented geographically and genetically, and
therefore endangered. We identified two major genetic
clusters and recommend that they should be considered as
local conservation units. Conservation efforts should entail
areconnection of the populations within these conservation
units, and to a lesser degree between them. Moreover,
the maintenance of large and stable meta-populations
within genetic sub-clusters (mostly consisting of isolated
populations) needs to be achieved for long-term survival.
For translocations of individuals to recovering very small
and inbred populations or for reintroduction, we suggest
a mixing of individuals from different populations within
the same conservation unit to increase genetic diversity
and enhance the adaptive capacity regarding changing
environmental conditions. This study offers one example
of how population genetic studies can help to delineate
conservation units, and our recommendations might apply
just as well to other endangered species where declines are
connected to increasing habitat fragmentation.
Amphib. Reptile Conserv.
Acknowledgements.—This research was supported by
grants from the German Federal Environmental Foundation
(DBU), Heidehof-Stiftung, and MHans-Schiemenz-
Fonds - Deutsche Gesellschaft fiir Herp-etologie und
Terrarienkunde (DGHT). We thank the following nature
conservation authorities for permission to collect the tree
frogs: Kreis Minden Ltibbecke, Kreis Steinfurt, Landkreis
Diepholz, Landkreis Gifhorn, Landkreis Ltneburg,
Landkreis Osnabriick, Landkreis Stade, Landkreis Uelzen,
Region Hannover, and Stadt Wolfsburg. We are especially
grateful to the many people who helped during field work,
and R. Podloucky for providing distribution maps. Finally,
we thank our technician Sabine Sippel for her assistance in
the molecular lab, Sonke von den Berg for help by creating
the figures, Tjard Bergmann for submitting the Cyt b
sequences to Genbank, and Oscar Gaggiotti for providing
advice on BIMr.
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Populationen der Gelbbauchunke (Bombina _ v.
variegata) im stidlichen Niedersachsen. Zeitschrift fiir
Feldherpetologie 16: 183-200.
Weir BS, Cockerham CC. 1984. Estimating F-statistics
for the analysis of population-structure. Evolution 38:
1,358—1,370.
Wright S. 1943. Isolation by distance. Genetics 28: 114.
Zumbach S. 2004. Die Laubfrosche (Hyla arborea
und Hyla intermedia) in der Schweiz — Verbreitung,
Gefahrdung, und Schutz. Zeitschrift fiir Feld-
herpetologie (Supplement 5): 183-192.
October 2022 | Volume 16 | Number 2 | e317
Amphib. Reptile Conserv.
Conservation management units of Hyla arborea
Astrid Krug has a Ph.D. in Biology from the University of Veterinary Medicine
Hannover in Germany. During the time of her Diploma and Ph.D. theses, Astrid worked
on several herpetological projects with a focus on molecular genetic analyses in the
European Tree Frog. Since then, working in the field of clinical research, her unabated
and keen interest in herpetology remains.
Jana Auffarth holds a Ph.D. in Veterinary Research and Animal Biology from
University of Veterinary Medicine Hannover in Germany. At the time of this study,
she was a Postdoctoral Research Assistant at the Institute of Zoology, University
of Veterinary Medicine Hannover, where her research centered around amphibian
population ecology, conservation, and management on a molecular level. Currently,
she is working on assessments of aquatic systems in line with the EU water framework
directive and national regulations.
Heike Préhl discovered her interest in studying frogs in the wild while she studied
Biology at the University of Hannover, and while spending a year studying tropical
biology at the Universidad de Costa Rica. During that appointment, she benefitted
from a wide range of field courses, including herpetology. After sampling field data on
Neotropical frog behavior and ecology for her Diploma and Doctoral theses, as well
as her Postdoctoral project, she started to work as a Junior Professor at the Veterinary
University of Hannover (TiHo) in Germany. Heike is currently an apl. Professor for
Zoology and teaches courses related to Zoology, Ecology, and Evolution to biology and
veterinary students. Her research focuses on the behavior, ecology, and conservation of
Neotropical and European amphibians.
84 October 2022 | Volume 16 | Number 2 | e317
Krug et al.
e@ g¢ ¢ Ff ¢ €&
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HT War
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Supplementary Fig. S1. Estimation of the number of Hyla arborea populations using the program STRUCTURE ver. 2.3.1 (Pritchard
et al. 2000) without prior population information; QU, WK, EK, etc. = sample sites, separated by fine black lines. Each individual
is represented by a single vertical line broken into K-colored segments, with lengths proportional to each of the K-inferred clusters.
(A) Plot for K = 2 in the analysis of the entire data set, (B) plot for K = 4, and (C) K = 4 for hierarchical analysis on each of the two
main clusters.
‘@)
Mean of estimated Ln probability of data" Mean of estimated Ln probability of data~—~
2 3 4 o
K K
Supplementary Fig. S2. Mean values of estimated Ln probability of data (LnPD) for each K (A, C) and delta K (B, D) calculated
from STRUCTURE runs with STRUCTURE HARVESTER (20 replicates per K) in those analyses where prior population information was
implemented. (A—B), graphs for hierarchical analysis of the red cluster; (C—D), corresponding graphs for the green cluster (compare
to Fig. 3 in the main text).
Amphib. Reptile Conserv. 85 October 2022 | Volume 16 | Number 2 | e317
Conservation management units of Hyla arborea
B)
-5,600
-5,800 a 20
6,000} . 15
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-6,200 : 2140
-6,400 \
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Mean of estimated Ln probability of data Mean of estimated Ln probability of data~—~
2 3 4 5 6 Fé
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Supplementary Fig. S3. Mean values of estimated Ln probability of data (LnPD) for each K (A, C, E) and delta K (B, D, F) without
prior population information. (A—B), results for the entire data set. (C—D), graphs for hierarchical analysis of the red cluster. (E—F),
corresponding graphs for the green cluster.
Amphib. Reptile Conserv. 86 October 2022 | Volume 16 | Number 2 | e317
Krug et al.
Supplementary Table S1. Estimates of evolutionary divergence over cyt b sequence pairs between sample sites (p-distances).
QU WK EK KZ KH BA RU WG ST AN SW PW
QU 0
WK 0.001 0
EK 0.001 0.002 O
KZ 0.000 0.001 0.001 0
KH 0.003 0.002 0.004 0.003 O
BA 0.001 0.001 0.003 0.001 0.002 O
RU 0.001 0.001 0.002 0.001 0.003 0.002 O
WG 0.001 0.001 0.002 0.001 0.002 0.001 0.001 0
St 0.001 0.001 0.002 0.001 0.002 0.000 0.001 0.001 0
AN 0.001 0.001 0.002 0.001 0.003 0.001 0.002 0.001 0.001 0
SW 0.001 0.001 0.002 0.001 0.003 0.001 0.002 0.001 0.001 0.001 0
PW 0.001 0.001 0.002 0.001 0.002 0.001 0.001 0.001 0.000 0.001 0.001 0
Supplementary Table S2. Geographic distances (km) among sample sites.
QU WK EK KZ KO KH BH BA RU WG ST AN SW PW
QU 0 24.89 59.36 118.51 121.07 138.45 138.18 59.60 145.74 186.98 194.94 225.27 21432 244.29
WK 24.89 0 55.80 121.60 124.18 140.04 140.47 77.42 165.05 189.68 206.53 236.57 221.51 254.05
EK 59.36 55.80 0 66.97 69.52 84.52 85.18 57.94 135.51 134.27 158.58 187.71 168.42 203.12
KZ 118.51 121.60 66.97 0 2.59 20.80 19.80 79.20 107.70 68.55 98.15 125.14 101.84 138.06
KO 121.07 12418 69.52 2.59 0 18.53 17.33 81.32 107.77 65.97 96.27 123.05 99.39 = 135.75
KH 138.45 140.04 84.52 20.80 18.53 0 3.94 99.81 118.84 49.76 93.08 117.07 88.33 126.83
BH 138.18 140.47 85.18 19.80 17.33 3.94 0 98.08 115.08 49.22 89.62 114.01 86.17 124.28
BA 59.60 77.42 57.94 79.20 81.32 99.81 98.08 0 87.65 142.67 137.64 167.94 161.85 188.28
RU 145.74 165.05 135.51 107.70 107.77 118.84 115.08 87.65 QO 134.01 84.08 108.84 12469 133.14
WG 186.98 189.68 134.27 68.55 65.97 49.76 49.22 14267 134.01 0 73.62 86.47 47.60 88.04
ST 194.94 206.53 158.58 98.15 96.27 93.08 89.62 137.64 84.08 73.62 0 30.35 43.49 51.77
AN 225.27 236.57 187.71 125.14 123.05 117.07 114.01 167.94 108.84 86.47 30.35 0 42.06 24.53
SW 214.32 221.51 168.42 101.84 99.39 88.33 86.17 161.85 124.69 47.60 43.49 42.06 0 40.48
PW 24429 25405 203.12 138.06 135.75 126.83 12428 188.28 133.14 88.04 51.77 24.53 40.48 0
Supplementary Table S3. GenBank accession numbers for Hyla arborea CytB haplotypes Hy 1 to Hy 11.
Sequence ID GenBank accession number
BankIt2634361 Seql OP690610
BankIt2634361 Seq2 OP690611
BankIt2634361 Seq3 OP690612
BankIt2634361 Seq4 OP690613
BankIt2634361 Seq5 OP690614
BankIt2634361 Seq6 OP690615
BankIt2634361 Seq7 OP690616
BankIt2634361 Seq8 OP690617
BankIt2634361 Seq9 OP690618
BankIt2634361 Seq10 OP690619
BankIt2634361 Seq11 OP690620
Amphib. Reptile Conserv.
87
October 2022 | Volume 16 | Number 2 | e317
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
16(2) [General Section]: 88-103 (e318).
New biological data for two rare reedfrog species, Hyperolius
nimbae Laurent, 1958, and H. chlorosteus (Boulenger, 1915)
(Anura: Hyperoliidae)
‘Basseu Aude-Inés Gongomin, ‘*N’Goran Germain Kouameé, ‘Konan Laurent Agoh,
‘Kouassi Philippe Kanga, and *Mark-Oliver Rodel
‘Université Jean Lorougnon Guédé, UFR Environnement, Laboratoire de Biodiversité et Ecologie Tropicale (BioEcoTrop), Daloa, BP 150, COTE
D'IVOIRE *Museum fiir Naturkunde - Leibniz Institute for Evolution and Biodiversity Science, Invalidenstr. 43, 10115 Berlin, GERMANY
Abstract.—Our recent surveys have generated new biological data on Hyperolius nimbae and H. chlorosteus,
two little-known West African reedfrog species of conservation concern. During fieldwork at the eastern
foothills of the Ivorian part of the Nimba Mountains, H. nimbae and H. chlorosteus individuals were found
by acoustic and visual encounter surveys. In addition, various natural history data were recorded, including
clutch size and egg-deposition sites. Hyperolius nimbae males were found at the edges of a permanent swamp.
The area was dominated by cocoa and coffee plantations, and used in small-scale subsistence farming, i.e.,
growing plantains, cassava, and rice. A new locality is reported here for the species, but our surveys failed
to confirm its presence at some previously known sites. The entire range of the species is now confined to
a small, non-protected, human-impacted area. Under these conditions, this species is facing high extinction
risk. Hyperolius chlorosteus was found in a patch of dense, broadleaf and evergreen primary forest at a mid-
elevation along a torrent stream, and in a degraded lowland forest edging a large stream. The habitats of both
species are suffering from forest degradation and deforestation along streams, so we urgently recommend the
strict protection of the habitats of both species. Given these concerns, we suggest that the IUCN threat status
of H. nimbae should be updated to Critically Endangered. Considering the large range of H. chlorosteus, the
current IUCN categorization of this species as Least Concern seems to be correct. However, based on the fact
that in Ivory Coast it only occurs in the westernmost parts of the country, several of the few known national
populations have been lost, and the remaining forest habitats are declining, so we feel that H. chlorosteus
should be regarded as Endangered nationally.
Keywords. Biodiversity hotspot, endemic, habitat protection, Mount Nimba Reedfrog, Threatened species, Upper
Guinean forest area
Citation: Gongomin BA-I, Kouamé NG, Agoh KL, Kanga KP, Rédel M-O. 2022. New biological data for two rare reedfrog species, Hyperolius nimbae
Laurent, 1958, and H. chlorosteus (Boulenger, 1915) (Anura: Hyperoliidae). Amphibian & Reptile Conservation 16(2) [General Section]: 88-103
(e318).
Copyright: © 2022 Gongomin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Accepted: 23 August 2022; Published: 24 October 2022
Introduction
Ivorian montane areas, such as Mount Péko, Mount
Sangbé, and Mount Nimba, are small in extent but
comprise a high diversity of amphibian species (e.g.,
Rodel 2003; Rodel and Ernst 2003; Kanga et al. 2021).
Mount Nimba, in particular, hosts the richest amphibian
fauna of West Africa including various rare and
endemic species (Kanga et al. 2021; Rodel et al. 2021).
For instance, this mountain is the only known region
where the matrotrophic Nimba Toad, Nimbaphrynoides
occidentalis (Angel, 1943), and the Mount Nimba
Reedfrog, Hyperolius nimbae Laurent, 1958, are found.
Correspondence. *ngoran_kouame@yahoo.fr
Amphib. Reptile Conserv.
The biology of N. occidentalis has been investigated in
detail (Lamotte 1959; Lamotte and Sanchez-Lamotte
1999; Xavier 2009; Sandberger et al. 2010; Sandberger-
Loua et al. 2017, 2018), and this toad is considered to be
the flagship species for the conservation of the Nimba
mountains (Hillers et al. 2008a; Sandberger-Loua et al.
2016).
Much less attention has been directed toward
various other little-known amphibian species which
are, nevertheless, of high conservation concern in Ivory
Coast. These include, two notable reedfrogs, the Mount
Nimba Reedfrog Hyperolius nimbae and the Large Green
Reedfrog H. chlorosteus (Boulenger, 1915), for which
October 2022 | Volume 16 | Number 2 | e318
Gongomin et al.
we know very little concerning their life histories.
Hyperolius nimbae is currently classified as
Endangered on The IUCN Red List of Threatened
Species (IUCN 2021). It is endemic to the lowlands of
the eastern slopes of the Ivorian part of Mounts Nimba.
After Schiotz (1967) last collected this frog on 28 July
1963, the species was only recently rediscovered by
Kouamé et al. (2016). This species is rare throughout
its limited range in some swamp forests near Danané
(Schiotz 1967; Kouamé et al. 2016; Kanga et al. 2021).
By contrast, H. chlorosteus inhabits rainforests in Sierra
Leone, Guinea, Liberia, and western Ivory Coast (Rédel
et al. 2004; Channing and Rodel 2019) and is categorized
as Least Concern on the IUCN Red List (IUCN 2021).
Despite a broad distribution, H. chlorosteus is confined
to the edges of rivers in primary lowland forests (Schiotz
1967; Rodel and Glos 2019), and thus must be regarded
as threatened in Ivory Coast due to the decline of those
habitats. A previously known population in Lakota
(south-central Ivory Coast; Schietz 1967) no longer
exists, and more may have been lost due to deforestation.
For instance, Ivorian records of H. chlorosteus have been
published from the classified forests (managed forests) of
Cavally and Haute Dodo (Rodel and Branch 2002), and
the national parks of Mount Sangbé (Rédel 2003), Mount
Péko (Rodel and Ernst 2003), and Tai (e.g., Ernst and
Rodel 2008; Kpan et al. 2021), as well as from Mount
Nimba (Kanga et al. 2021), which are all situated in the
south-western part of the country. However, during a
decade of conflict, the gallery forests in Mount Péko as
well as both classified forests have been destroyed (NG
Kouameé, pers. obs.). These losses restrict the remaining
known Ivorian range of H. chlorosteus to the southern
part of Mount Sangbé, the lowland forests of Mount
Nimba, and the Tai National Park.
The aim of this study was to search for the persisting
populations of H. nimbae and H. chlorosteus at Mount
Nimba, and to collect additional data on the morphology,
call characteristics, breeding sites, and potential threats
for these poorly-known species.
Material and Methods
Study site. Fieldwork was conducted in the Mount Nimba
Integrated Nature Reserve (MNINR: 07°25’-07°45’N,
008°20’—008°35’W; Fig. 1) during both the rainy and dry
seasons, and was carried out on 84 days between 2 August
2019 and 8 July 2020. The MNINR covers 5,000 ha of
various habitats ranging from altered and former forests
in the lowlands, through dense, broadleaf and evergreen
forests stretching from the lower to mid-elevations, and
montane grasslands at the highest elevations (Lamotte et
al. 2003a,b; Lauginie 2007). Mean annual temperatures
vary from 22—27 °C on the mountain bases, and 16-21
°C on the mountain ridge. The rainy season extends
from eight to nine months and is only interrupted by a
short dry season from November/December to February/
Amphib. Reptile Conserv.
March. The precipitation is highest on the mountain
top, where it may reach up to 3,500 mm. During the dry
season, the humidity is usually below 30%, but exceeds
80% in the rainy season (Lauginie 2007). The dry season
is characterized by a warm, dry, and dusty wind known
as Harmattan. For a detailed description of MNINR’s
amphibian fauna see Kanga et al. (2021).
Sampling. As previous research has shown that these
two reedfrog species are only active at night (Kanga et
al. 2021), searches took place from 1800-2200 h GMT.
All searches were conducted by three people, totalling
a search-effort of 1,008 person-hours. Search techniques
focused on visual scanning of the terrain, supplemented
by acoustic surveying to find the males, and examination
of potential calling and breeding sites. Particular attention
was given to searching the vegetation around and/or
along forest streams and swamps. We investigated the
area seven times per month and counted only individuals
that were captured.
Hyperolius nimbae was found at one site at Yéalé,
while H. chlorosteus was collected at one site at MNINR
and another site at Yéalé. We visited each site 56 times
in the rainy season and 28 times in the dry season (Table
1; Appendices 1 and 2). Frogs were photographed,
measured, and sexed. To avoid re-counting frogs,
individuals that were not collected were marked as
vouchers by toe clipping following the recommendations
of Grafe et al. (2011), and released at their respective
sites of capture. Areas close to four villages (Dagbonpleu,
Danipleu, Kouan-Houlé, and Zéalé), within the formerly
known range of H. nimbae, were re-investigated seven
times. These visits were in the rainy season, which is the
presumed reproductive period of the species. We recorded
potential threats to H. nimbae and H. chlorosteus, defined
here as any anthropogenic activity that may negatively
impact the two species and/or their habitats.
Although the panzootic chytrid fungus Batracho-
chytrium dendrobatidis (Bd) seems to be absent from
West Africa, west of the Dahomey Gap (Penner et al.
2013), newly sterilized equipment was always used
at each site. Geographical coordinates were recorded
with a GPS (datum: WGS84). A few vouchers were
euthanized in a_ 1,1,1-trichloro-2-methyl-2-propanol
hemihydrate (MS222) solution and thereafter preserved
in 80% ethanol. These frogs are deposited in the research
collection of NGK at the Université Jean Lorougnon
Guédé, Daloa, Ivory Coast, and will serve as the bases
of a national reference collection and for research and
teaching purposes.
Morphological characteristics and advertisement
calls. Measurements of morphological features (in mm)
were taken by one person (BAIG) with a dial calliper
(accuracy + 0.1 mm), and are given as means (X) with
standard deviations (SD). They comprise: snout-urostyle
length, head width and length both at the level of jaw
October 2022 | Volume 16 | Number 2 | e318
Biology and conservation of Hyperolius nimbae and H. chlorosteus
10°W o°w
GUINEA
LIBERIA
City
Village
Road
Stream
State boundaries
0123 4km
Lit jj
8°W
8°N
OAST
ouan-Houlé
Danané
Fig. 1. Geographical location of the Mount Nimba Integrated Nature Reserve within the westernmost extension of Ivory Coast at
the border crossing point with Guinea and Liberia. The altered forest area where Hyperolius nimbae and H. chlorosteus were found
at Yéalé is represented by a purple star; the habitats of H. chlorosteus ranged from dense, broadleaf and evergreen forests from
lower to mid-elevations (yellow star). The inset figure indicates the location of Ivory Coast (green patch) on the African continent.
articulation, interorbital space, distance between eye and
nostril, distance from nostril to tip of snout, eye diameter,
internarial distance, tympanum diameter, crus length,
thigh length, and foot length including the tarsus and the
longest toe.
Other characters recorded included color pattern
variation following the definitions by Schiotz (1967)
and Channing and Rodel (2019). To ensure that clutches
of H. nimbae and H. chlorosteus could not be confused
with those of other sympatric reedfrogs, couples were
collected and kept separately in a plastic terrarium (25 x
Amphib. Reptile Conserv.
15 cm, 16 cm depth) with water (8.5 cm) and submerged
and floating vegetation until eggs were laid. Egg numbers
and diameters (accuracy + 0.1 mm) were determined
for each clutch. For comparison, further H. chlorosteus
clutch data collected between 1999 and 2001 in Tai
National Park by MOR are also reported here.
Hyperolius nimbae was not included in a phylogeny
of the genus (Portik et al. 2019), but is assumed to be a
member of the H. viridiflavus complex (Schietz 1999;
Channing 2022). Very recently, this was confirmed by
genetic data, and it was shown to be the sister species to
October 2022 | Volume 16 | Number 2 | e318
Gongomin et al.
Table 1. Numbers of daily searches for Hyperolius nimbae and H. chlorosteus, during the 84-night period from 2 August 2019 to 8
July 2020, in Mount Nimba Integrated Nature Reserve and Yéaleé.
; if HAyperolius nimbae HAyperolius chlorosteus
Sire oh eantite Yéalé (07°31.928’N, MNINR (07°34.652’N, Yéalé (07°31.932’N,
P 008°25.401’W; 425 m asl) 008°24.966’ W; 716 m asl) 008°25.508’ W; 387 m asl)
season
season
the Central African H. tuberculatus (Kouamé et al.2022). (Fig. 3). The calling males were mostly well concealed,
Nine sequential advertisement calls were collected from —§ perching between thick branches and leaves of cocoa
one male, in order to compare these data with those and coffee trees at ~1.80—2.10 m above the ground.
presented by Schietz (1967). Five advertisement calls | Througout the study, a total of 305 frogs were captured
were also recorded from a H. chlorosteus male. (Fig. 3; Appendix 1). They comprised 277 individuals,
All calls were recorded with a Huawei recorder (44.1 including one couple, caught in the rainy season and 28
kHz sample ratio, 16 bits of resolution, FFT length=256) males caught in the dry season. Generally, additional
and analyzed with the software Soundruler 0.9.6 (Gridi- —_ calling males were inaccessible, calling from high up in
Papp 2007; Kohler et al. 2017; Emmrich et al. 2020). For tall trees close to the deep pond.
each advertisement call, the following measurements Sympatric amphibian species in Yéalé were the White-
were recorded: call duration (s), dominant frequency — lipped Frogs Amnirana sp. “albolabris west”, Afrixalus
(Hz), fundamental frequency (Hz), minimum frequency dorsalis, A. fulvovittatus, Hyperolius concolor, H.
(Hz), maximum frequency (Hz), duration intervals fusciventris fusciventris, H. picturatus, Phrynobatrachus
between calls (s), duration intervals between notes (s), gutturosus, and P. latifrons, thus representing a typical
and overall frequency bandwidth (Hz). composition of a farmbush anuran community (Schietz
1967).
Results
Morphology of H. nimbae. We retained 13 males and
Observations on H. nimbae one female H. nimbae as vouchers. Snout-urostyle
lengths of the voucher males ranged from 28.8—35.0
Habitat, population size, and activity of H. nimbae. mm (32.3 + 1.8 mm), thus slightly exceeding the known
The Mount Nimba Reedfrog was found only in the range of H. nimbae (Schiotz 1967). The head was slightly
Yéalé village (07°31.928’N, 008°25.401’W; 425 masl) — longer (12.0 + 1.1 mm; range: 10.0—13.5 mm) than broad
at the periphery of MNINR. Our efforts to confirm the (10.8+0.8 mm; range: 9.9-12.5 mm); interorbital space
species around village forests at Dagbonpleu, Danipleu, ranged from 5.0—7.5 mm (6.4 + 0.7 mm); the distance
Kouan-Houlé, and Zéalé were unsuccessful. The forest between eye and nostril (2.1 + 0.3 mm; range: 2.0—3.0
areas formerly at these sites were destroyed and replaced =mm) approximated the distance from nostril to tip of
by roads and new settlements. At Yéalé, the habitat snout (2.2 + 0.3; range: 1.5—2.0 mm); eye diameter (4.6
comprised altered forest bordered by patches of bamboo, +0.4 mm; range: 4.0—-5.1 mm) was larger than internarial
intact forests, degraded forests with large clearings, space (3.2 + 0.3 mm; range: 3.0-4.0 mm) and tympanum
and thick grassy and shrubby vegetation around the diameter (2.3 + 0.3 mm; range: 2.0—3.0 mm); crus length
settlement. Large parts of the village’s surroundings were (16.5+1.0 mm; range: 15.1—18.9 mm) slightly exceeded
dominated by small-scale subsistence farming, mainly _ thigh length (15.0 +0.8 mm; range: 13.5—16.1 mm); and
plantings of corn, cassava, plantains, cocoa, and coffee, foot length including the longest toe ranged from 21.0-
as well as rice in swamps. During the entire study, the 26.9 mm (23.1 + 1.6 mm).
vegetation around swamps was checked at seven sites The female measured 34.0 mm SUL (Fig. 4A). Its
without detecting any sign of H. nimbae’s presence. head was slightly longer (14.0 mm) than broad (12.1
Specimens of H. nimbae were found only ina mixed mm); the interorbital space reached 8.0 mm; the
cocoa and coffee plantation (including plantains) edging —_ distance between eye and nostril (3.4 mm) was longer
a large and deep pond (greater than 100 x 70 m; Fig. 2), than the distance from nostril to tip of snout (1.8 mm);
where males started calling at dusk, usually around 1810 — eye diameter (5.0 mm) was larger than internarial space
h GMT. Calling males were active in each month of our = (3.0 mm) and tympanum diameter (2.9 mm); crus length
study and congregated in large choruses, particularly (18.0 mm) slightly exceeded thigh length (17.1 mm);
during the rainy season. Calling activity never stopped, and foot length including the tarsus and the longest toe
but was low during the dry season, as indicated by the —_ reached 24.5 mm.
much lower numbers of frogs caught during that time Mount Nimba reedfrogs have a brief and truncated
Amphib. Reptile Conserv. 91 October 2022 | Volume 16 | Number 2 | e318
Biology and conservation of Hyperolius nimbae and H. chlorosteus
Fig. 2. Habitats of Hyperolius nimbae at the foo
in heavily degraded habitats at the edge of large swamps.
snout and rough to warty dorsal skin with a varied color
pattern. The basic dorsal pattern varied from silver-grey
to chocolate brown. The dark pattern on the back varied
in intensity, but the general pattern was always similar
and recognizable (Fig. 4). The female coloration was
within the variation of the males (Fig. 4), but the discs
on toes and fingers were more reddish than in most males
(Fig. 4A). Likewise, the ventral color differed slightly
between individuals, but the female was not different
from the males (Fig. 5). However, instead of a dark
Amphib. Reptile Conserv.
hills of the Ivoria
92
n part of the Nimba Mountains. In Yéalé, the species was foun
i - Babee
vocal sac and yellowish gular gland, the female had a
white throat, with the edges beset by orange and black
speckles. The armpits and inner parts of limbs including
webbing were blood red (Fig. 5C). Some males had
similarly reddish skin parts (Fig. 5A), areas which are
used for water uptake, see Rddel (2000), whereas others
had blue-grey skin instead (Fig. 5B).
Reproduction of H. nimbae. At Yéalé, a couple of H.
nimbae in amplexus was captured on a Raphia Palm in
October 2022 | Volume 16 | Number 2 | e318
Gongomin et al.
w ~ eal (op)
(oe) jo) fo) jo)
Number of captured frogs
N
oO
Aug Sep Oct Nov Dec — Jan Feb Mar Apr
Months
May Jun Jul
Fig. 3. Number of Hyperolius nimbae individuals recorded
from 2 August 2019 to 8 July 2020 at Yéalé.
deeper water (> 1 m). The couple was placed into a terrarium,
and the following morning, 227 eggs were found attached
to a leaf above the water surface. The eggs had a dark and
light green pole that was surrounded by a thin transparent
jelly (Fig. 5D). Egg diameter varied from 1.6—2.5 mm, with
a mean value of 1.99 mm (SD: + 0.18 mm).
Vocalization of H. nimbae. The acoustic properties of
nine advertisement calls of one H. nimbae male were
analyzed (Fig. 6). Hyperolius nimbae call in a long,
fast series of pulse groups (notes), thus confirming the
call descriptions provided by Schiotz (1967). The call
duration averaged 2.77 + 0.56 s (range: 1.89-3.25 s). The
duration intervals between calls averaged 0.44 + 0.23
S (range: 0.22-0.87 s, N = 8). Intervals between notes
within each call were 0.15 + 0.03 s (range: 0.09-3.48 s, NV
= 131). The mean fundamental frequency was 1,359.37
Hz (N = 9), while the dominant frequency reached
2,718.75 Hz (N = 9). The maximum frequency intensity
was at 2,906.25 Hz (N = 9), and the minimum frequency
intensity averaged 2,718.75 Hz (N=9).
Threats to H. nimbae. We failed to confirm the species
presence at all sites where we had recorded it only a few
years before (see above). In addition, we observed various
signs of habitat degradation in the habitats of H. nimbae
at Yéalé. Aside from the close proximity to a human
settlement, the frogs’ habitats were dominated by cocoa
and coffee plants, and used for small-scale subsistence
farming, i.e., plantains and cassava. Large parts of the
breeding area of H. nimbae were used to establish rice
paddies. Bamboo patches were steadily harvested by the
local human population as construction materials. The
rainforest edges were impacted by logging (Fig. 2).
Observations on H. chlorosteus
Habitat, population size, and activity of H. chlorosteus.
Specimens of H. chlorosteus were found in MNINR ina
patch of dense, broadleaf and evergreen primary forest
at a mid-elevation along a torrent stream (07°34.652’N,
008°24.966’W; 716 m asl; Fig. 7A), as well as in a
Amphib. Reptile Conserv.
degraded forest edging a large stream at Yéalé village
(07°31.932’N, 008°25.508°W; 387 m asl; Fig. 7B).
From April—November, the rainy season, a total of 341
H. chlorosteus were captured in the two sites, always
at night along the streams (Fig. 8; Appendix 2). In the
dry season, from December to March, no signs of the
Species’ presence were observed. Males started calling at
around 1800 h GMT, most often after heavy rainfall. In
a patch of primary forest, 327 calling males perched on
leaves and branches of small shrubs at ~1.5—2.0 m height
above the ground (e.g., Fig. 7C) were captured. The other
recorded males were heard calling from very high up in
tall trees along the forest stream. A few calling males (V
= 11) were also found in a degraded forest, edging a large
stream at Yéalé village (07°31.932’N, 008°25.508’W;
387 m asl; Fig. 7B). There, they called on shrubs, with
the calling sites ranging from 1.80 m above the ground to
much higher. Sympatric frogs were Leptopelis macrotis,
Hyperolius picturatus, and White-lipped Frogs Amnirana
sp. “albolabris west.”
Morphology of H. chlorosteus. The snout-urostyle
lengths of 15 males, retained as vouchers, ranged from
31.5-35.0 mm (33.8 + 1.3 mm), thus occurring within
the known range of H. chlorosteus (Schiotz 1967). The
head was slightly longer (12.0 + 0.1 mm; range: 12.0-
12.2 mm) than broad (11.5 + 0.7 mm; range: 10.5—13.0
mm); the interorbital space ranged from 5.9—7.2 mm (6.5
+ 0.4 mm); the distance between eye and nostril (3.0 +
0.2 mm; range: 2.5—3.5 mm) was approximately twice
the distance from nostril to tip of snout (1.4 + 0.6; range:
0.6—-2.4 mm); the eye diamter (5.1 + 0.3 mm; range:
4 4-5.5 mm) was larger than internarial space (2.6 + 0.4
mm; range: 2.1—3.0 mm) and tympanum diameter (2.8 +
0.2 mm; range: 2.2-3.0 mm); the crus length (17.0 + 0.7
mm; range: 15.4—-18.1 mm) slightly exceeded the thigh
length (15.9 + 0.8 mm; range: 14.9—-16.9 mm); and foot
length including the longest toe ranged from 21.5—23.5
mm (22.2 + 0.8 mm).
Two females measured 36.8 and 37.5 mm in SUL.
As in the males, their heads were slightly longer (13.5
mm) than broad (13.2 mm); interorbital spaces were
7.0 and 7.2 mm; the distance between eye and nostril
was longer (3.3 + 0.3 mm; range: 3.1—3.5 mm) than the
distance from nostril to tip of snout (1.9 + 0.1 mm; range:
1.9-2.0 mm); the eye diamter (5.0 + 0.1 mm; range:
5.0—5.1 mm) exceeded the internarial space (2.9 + 0.1
mm; range: 2.9-3.0 mm) and tympanum diameter (2.9
+ 0.1 mm; range: 2.8-3.0 mm); the crus length (17.7 +
0.3 mm; range: 17.5—-17.9 mm) slightly exceeded thigh
length (16.9 1.5 mm; range: 15.9-18.0 mm); and foot
length including the tarsus and longest toe ranged from
23.5—23.8 mm (23.6 + 0.2 mm).
The color pattern of H. chlorosteus showed some
variations (see Figs. 7 and 9), however, all were within
the range known for the species (compare Schiotz 1967;
Rodel 2003; Channing and Rodel 2019).
October 2022 | Volume 16 | Number 2 | e318
Biology and conservation of Hyperolius nimbae and H. chlorosteus
Fig. 4. Benoa views of the Tapers nimbae fantale (A) ra males (B—H) from Yéalé, western oe Coast. Note the
variation in coloration.
Reproduction of H. chlorosteus. One female perched
on a broad leaf of a shrub overhanging a forest stream, at
~1.5 m height, was captured. Eggs were visible through
its ventral skin (Figs. 7D and 9F). An amplectant couple
was seen sitting on low vegetation in this site (Fig. 7E).
This couple was placed in a terrarium and a clutch of
62 eggs was present the next morning. The eggs were
attached to the glass above the water. They had beige and
dark poles surrounded by a thin transparent capsule (Fig.
Amphib. Reptile Conserv.
7F). Egg diameters varied from 2.0—2.5 mm, mean 2.2
mm (SD: + 0.25 mm). The jelly of H. chlorosteus eggs
is slightly opaque. Six additional H. chlorosteus clutches
observed in Tai National Park, south-west of Ivory Coast,
ranged from 54-122 eggs (86.2 + 28.8 eggs; Table 2).
Vocalization of H. chlorosteus. Five advertisement calls
were recorded from one male (Fig. 10). The calls were
repeated 2—7 times (Fig. 10B). The acoustic impression
October 2022 | Volume 16 | Number 2 | e318
Gongomin et al.
Table 2. Data for Hyperolius chlorosteus clutches from Tai National Park, Ivory Coast.
Clutch number | Date | Number of eggs Location of clutch Remarks
16 March 1999 pene canaen Clutch looks like a blackberry
above stream
above stream
Egg size 3-6 mm, nucleus 1.9—2
eo ene ae Bourecolded mm; clutch looks like a blackberry
4 February 71 Clutch on stone covered Egg size 3-6 mm, nucleus 2.2 mm;
1999 with mosses above water looks like a blackberry
Fig. 5. Ventral views of Hyperolius nimbae males (A and B) and fnate (C) adults, and the eggs (D) from Yéalé, western Ivory
Coast.
of the call is a low-pitched, far ranging metallic click | Hz, N = 5). The maximum frequency intensity was at
with a mean duration of 0.87 + 0.34 s (range: 0.51-1.41 2,643.75 + 167.70 Hz (range: 2,531.25—2,906.25 Hz, N
s). The duration intervals between calls averaged 2.90+ =5), and the minimum frequency intensity averaged at
1.27 s (range: 1.36-4.0 s, N=4). The mean fundamental 2,531.25 + 229.64 Hz (range: 2,343.75—2,906.25 Hz, N
frequency was 1,303.12 + 83.85 Hz (range: 1,265.62—. _=5).
1,453.12 Hz, N = 5), while the dominant frequency
reached 2,606.3 + 167.70 Hz (range: 2,531.25—2,906.25 Threats to H. chlorosteus. Major threats to H.
Amphib. Reptile Conserv. 95 October 2022 | Volume 16 | Number 2 | e318
Biology and conservation of Hyperolius nimbae and H. chlorosteus
Ampl (Pa)
oO
2 4 6
Time (s)
Frequency (kHz)
O-NWAH OH
T
eT ey a aD DT Ea RI RSI SU PI A UT Dy DS 0D Ds 0 |
0.25
Amplitude
2 4 6
Time (s)
1 2 3 4 ce)
Frequency (kHz)
Fig. 6. (A) Hyperolius nimbae usually calls perched between branches and leaves of trees. (B) Waveform (above), spectogram
(center), and powerspectrogram (below) of the advertisement calls of a H. nimbae male from Yéalé, western Ivory Coast.
chlorosteus were observed at Yéalé, where some forest
pockets along streams had been cleared and converted to
cocoa and coffee plantations, as well as rice cultivation.
Discussion
This study gathered new data on the biology and
distribution of two rare reedfrog species, Hyperolius
nimbae and H. chlorosteus, living in different forest
habitats in the western Upper Guinea forest zone
(Channing and Rodel 2019). Hyperolius nimbae has been
documented only from a few individuals and populations
on the Ivorian part of the Nimba Mountains (Schiotz
1967; Kouamé et al. 2016; Kanga et al. 2021), and little
was known about its phenotypic variation, biology, and
habitat requirements prior to this study. A recent study
based on 16S rRNA sequences of members of the H.
viridiflavus clade revealed that H. nimbae is a member of
the H. viridiflavus clade and sister species to the Central
African H. tuberculatus (Kouameé et al. 2022).
At Yéalé, a relatively large population of H. nimbae
was found in patches of heavily degraded forest area,
partly neighboring human settlements. This habitat fit well
with the earlier habitat description, 1.e., from the villages at
Dagbonpleu, Danipleu, Kouan-Houleé, and Zéalé (Kouamé
et al. 2016). However, an alarming result of this study is
that due to ongoing development of the area, all formerly
known sites have been destroyed, restricting the currently
known range of H. nimbae to Yéalé alone.
Our morphological assessments of a larger number of
individuals confirmed former descriptions, but slightly
increased our knowledge about color variability (Schiotz
1967; Kouamé et al. 2016; Figs. 3 and 4). Hyperolius
nimbae apparently is another reedfrog species that lacks
Amphib. Reptile Conserv.
sex specific color dimorphism (compare Schigtz 1967;
Veith et al. 2009; Portik et al. 2019). The new data herein
also confirms previous descriptions of the advertisement
calls of H. nimbae (Schigetz 1967). In contrast to most
other Hyperolius (Schigetz 1967, 1999), H. nimbae males
always produce a succession of continuous clicks and
thus much longer calls.
Most Hyperolius species are “prolonged breeders”
(Schiotz 1967, 1999: Lotters et al. 2004; Rodel et al.
2006; Kouamé et al. 2015). Hyperolius nimbae 1s no
exception to that rule, with males calling during all
months of the rainy season, usually at the edges of large
and permanent water bodies. We documented the first
known clutch for this species (Fig. 5D). The eggs were
attached to a leaf above the water surface, a feature which
is common to forest species within Hyperolius. Savannah
dwelling Hyperolius species deposit eggs under water,
most likely as a response to the higher desiccation risk
(Rodel 2000). We take the egg deposition above water as
a further hint that this species depends on forest, at least
to some extent.
It remains a mystery why H. nimbae apparently
tolerates degraded forests but only occurs in the Ivorian
foothills of Mount Nimba, as comparable habitats are
available beyond its range (Schiotz 1967). Most likely
this species was trapped at these sites when the Nimba
mountains were surrounded by savannah during drier
periods, representing a refugium for the survival of
forest species during unfavorable Pleistocene periods
(Maley 1996).
The new Hyperolius chlorosteus data reported herein
confirmed previous descriptions of the morphology and
advertisement call (Schiotz 1967, 1999; Channing and
Rodel 2019). This species is morphologically similar to
October 2022 | Volume 16 | Number 2 | e318
Gongomin et al.
=
ae,
é gi
es
Fig. 7. (A—B) Typical forest streams in the Mount Nimba Integrated Nature Reserve where Hyperolius chlorosteus breeds. A calling
be
al f
a
male (C), a female (D), a couple in amplexus (E), and their clutch (F) which was deposited on a leaf above a forest stream.
H. laurenti (from the eastern parts of the Upper Guinea
forest zone; Schiotz 1967, 1999: Channing and Rodel
2019), with which it also shares habitat requirements,
i.e., perching on branches above small to medium-sized
streams in primary or only slightly degraded forests,
often at considerable height (Rodel et al. 2005; Kouamé
et al. 2014). The breeding period of H. chlorosteus is
confined to the rainy season, and clutches are attached
at various heights on leaves, branches, and stones above
flowing water.
The habitat characteristics
of H. chlorosteus
Amphib. Reptile Conserv.
97
encountered in MNINR were similar to those reported
from previous sites, 1.e., dense forests with streams or
small rivers (Schiotz 1967; Rodel 2003; Ernst and Rodel
2008). Unfortunately, some of the known Ivorian sites
for H. chlorosteus no longer exist, such as Lakota (e.g.,
Schiotz 1967), the Mount Péko National Park (Rédel and
Ernst 2003), and the Cavally and Haute Dodo lowland
forests in the western part of the country (R6édel and
Branch 2002). In MNINR, the species was still found in
abundance, but this study also registered the increasing
and continuous degradation of its forest habitat.
October 2022 | Volume 16 | Number 2 | e318
Biology and conservation of Hyperolius nimbae and H. chlorosteus
wow fF u DBD
oO CO O Oo
Number of captured frogs
N
io)
Jan Feb Jul
Months
Mar Apr May = Jun
Fig. 8. Number of Hyperolius chlorosteus captured from 2
August 2019 to 8 July 2020 along lowland forest streams at
Mount Nimba.
Sa
4)
=e xs
“~< % *
, = a ¥
Fig. 9. Variation of color pattern o
Amphib. Reptile Conserv.
a } Te
of .
ii
Nee |
Hae
4
4
an
f Hyperolius chlorosteus from Mount Nimba Integrat
98
Conclusions and Threat Status
This study revealed the most viable and_ largest
population of H. nimbae known thus far. However, it
also revealed that formely known sites are most likely
gone, and the one reported herein might be the last site
where the species is thriving. Amphibians currently
have no official protection status in Ivory Coast, and no
dedicated conservation policies apply to them. The only
existing conservation measures for their protection are
the designations of protected areas (Rodel et al. 2021).
Unfortunately, the small pocket of forest zone where H.
nimbae was found falls entirely within a non-protected
area, and consequently it is exposed to increasing and
: wy sees
ed Nature Reserve, western Ivory Coast.
October 2022 | Volume 16 | Number 2 | e318
Gongomin et al.
Ci
=
ron 0
E
xt
-1|
Time (s)
® SP
z 4}
B 3p ,
Cc
g 2r
Si}
Ww OE | |
5 10
Time (s)
1
o
Tc
= |
= 0.57
acai ee
xt
0 1
0 2 3 4 5
Frequency (kHz)
Fig. 10. Calling male of Hyperolius chlorosteus (A) with (B) waveform (above), spectogram (centre) and powerspectrogram (below),
of the species’ advertisement call, from Mount Nimba Integrated Nature Reserve. Note that the data for five calls are shown.
ongoing human influence. This species is thus facing
an alarming risk of extinction, and the long-term
persistence of its population in the forthcoming years
is unlikely. The most important conservation action
would be the immediate protection of its habitat at Yéalé,
possibly accompanied by the establishment of a captive
rescue population. Currently, H. nimbae is classified as
Endangered (IUCN 2017). However, based on JUCN
Red List of Threatened Species criteria Al(a) (population
decline directly observed, only one known population
remaining), B1 (extent of occurrence less than 100 km/7),
and B2 (area of occupancy less than 10 km7?, a: only one
population known, b: population globally declining), we
believe that the threat status of this species should be
updated to Critically Endangered.
The second study species, H. chlorosteus, is similarly
exposed to habitat loss due to intensive deforestation. The
few remaining primary forests on which it depends do not
enjoy sufficient protection or sustainable management
(e.g., Chatelain et al. 1996; Wood 2003; Bakarr et al.
2004). The MNINR, Mount Sangbé, and the lowland
rainforest of Tai National Park remain the three known
Ivorian sites of H. chlorosteus at present (R6del 2003;
Ernst and Rodel 2008; Kanga et al. 2021). The recent
IUCN Red List (2020) classifies H. chlorosteus as Least
Concern. Given its large range, that category appears
to be correct. However, based on the facts that in Ivory
Coast the species only occurs in the westernmost parts
of the country, several of the few national populations
are gone, and the remaining forest habitats are declining,
we think that H. chlorosteus should be regarded as
Endangered nationally.
In summary, we urgently recommend the strict
protection of the habitats of both species.
Amphib. Reptile Conserv.
Acknowledgments.—We are greatly indebted to the
Ministere de |’Environnement et du Développement
Durable, and the Office Ivoirien des Parcs et Réserves,
Direction de Zone Ouest, Céte d’Ivoire, for permitting
the research. We would like to acknowledge the local
populations of Danané villages for their hospitality, and
are especially grateful for the support and collaboration
from Paul Seu, elder of Kouan-Houlé. We thank Nicolas
Granier, a conservationist of the Biotope Foundation
France, for facilitating the relationships between the local
people of Yéalé and our team. We are thankful to our
local assistants and field guides Droh David Gueu and
Zoda Alphonse Tokpa, for their invaluable help during
the field expedition. Alan Channing and Lucinda Lawson
improved our manuscript greatly with their constructive
comments. We are grateful to Michael L. Grieneisen for
his valuable comments.
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Sandberger L, Hillers A, Doumbia J, Loua NS, Brede C,
Rodel MO. 2010. Rediscovery of the Liberian Nimba
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(Amphibia: Anura: Bufonidae), and reassessment of
its taxonomic status. Zootaxa 2355: 56-68.
Sandberger-Loua L, Doumbia J, Rodel MO. 2016.
Conserving the unique to save the diverse. Identifying
key environmental determinants for the persistence of
the viviparous Nimba toad in a West African World
Heritage Site. Biological Conservation 198: 15—21.
Sandberger-Loua L, Miller H, Rodel MO. 2017. A
review of the reproductive biology of the only
known matrotrophic viviparous anuran, the West
African Nimba Toad, Nimbaphrynoides occidentalis.
Zoosystematics and Evolution 93(1): 105-133.
Sandberger-Loua L, R6del MO, Feldhaar H. 2018. Gene-
flow in the clouds: landscape genetics of a viviparous,
montane grassland toad in the tropics. Conservation
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Schiotz A. 1967. The treefrogs (Rhacophoridae) of
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1-346.
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Chimaira, Frankfurt am Main, Germany. 351 p.
Veith M, Kosuch J, Rodel MO, Hillers A, Schmitz A,
Burger M, Lotters S. 2009. Multiple evolution of
sexual dichromatism in African reed frogs. Molecular
Phylogenetics and Evolution 51: 388-393.
Woods D. 2003. The tragedy of the cocoa pod: rent-
seeking, land, and ethnic conflic in Ivory Coast. The
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Xavier F. 2009. La belle histoire du petit crapaud vivipare
du Mont Nimba. Bulletin de la Société Zoologique de
France 134: 13-21.
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Biology and conservation of Hyperolius nimbae and H. chlorosteus
ee |
CHASSE, P
Amphib. Reptile Conserv.
Basseu Aude-Inés Gongomin is a Ph.D. candidate at the Universté Jean Lorougnon Guédé (Daloa,
Ivory Coast). Her current research topic focuses on taxonomy, and the population ecology of
endemic amphibians of the Ivorian part of the Nimba Mountains.
N’Goran Germain Kouamé is an Ivorian herpetologist and biologist. He is a Senior Lecturer
at the Jean Lorougnon University (Daloa, Ivory Coast), and is also the current Chair of the West
African region of the IUCN SSC Amphibian Specialist Group (ASG). He holds a Diploma and
a Ph.D. in natural sciences from the Université d’Abobo-Adjamé (actually Université Nangui
Abrogoua), Abidjan, Ivory Coast, where he used leaf-litter frogs (Phrynobatrachus spp.) as models
to determine the conservation status of the Banco National Park, one of the rare remaining primary
forests situated in the midst of a West African mega-city. His current research interests mainly focus
on the taxonomy, ecology, distribution, and conservation of rare, threatened, and new amphibian
species in Ivory Coast.
Konan Laurent Agoh is a postgraduate student at the Université Jean Lorougnon Guédé (Daloa,
Ivory Coast) with an M.Sc. in Herpetology. His research interest focuses on the diversity and ecology
of amphibian assemblages in forest fragments of the valley of the Bandama River, an area which lies
between Lamto Faunal Reserve (central Ivory Coast) and Azagny rainforest (southern Ivory Coast).
Kouassi Philippe Kanga is a recent graduate of the Université Jean Lorougnon Guédé (Daloa,
Ivory Coast) with a Ph.D. in Herpetology. His work emaphsized amphibian diversity and its spatio-
temporal dynamics in the Ivorian part of Mount Nimba. His research was under the direction of Dr.
N’Goran Germain Kouamé, and aimed at linking amphibian assemblages with species function and
assessing how species react in response to environmental changes in Mount Nimba.
Mark-Oliver Rédel works with his team at the Museum fir Naturkunde, Berlin, Germany,
where he is the Curator of Herpetology. He has studied the systematics, taxonomy, biogeography,
and ecology of African amphibians for almost 30 years. With his group, comprising students
from around the world, he currently runs projects in Germany, Ecuador, Guinea, Ivory Coast,
Cameroon, and Mozambique. His special interest is on how species and ecological communities
react to environmental changes. He has authored or co-authored about 400 scientific and popular
publications, including several books.
102 October 2022 | Volume 16 | Number 2 | e318
Gongomin et al.
Appendix 1. Counts of Hyperolius nimbae individuals captured ina heavily degraded site (07°31.928’N, 008°25.401’W;
A425 m asl) at Yéalé from 2 August 2019 to 8 July 2020.
Appendix 2. Counts of Hyperolius chlorosteus individuals captured along forest streams at Mount Nimba Integrated
Nature Reserve (MNINR: 07°34.652’N, 008°24.966’W; 716 m asl) and Yéalé (07°31.932’N, 008°25.508’W; 387 m
asl) from 2 August 2019 to 8 July 2020.
SS |) 0") POF eS oS [a ole [ss lie
ee
Amphib. Reptile Conserv. 103 October 2022 | Volume 16 | Number 2 | e318
Amphibian & Reptile Conservation
16(2) [General Section]: 104-119 (e319).
Official journal website:
amphibian-reptile-conservation.org
Goliath Frog (Conraua goliath) abundance in relation to
frog age, habitat, and human activity
1*Nono LeGrand Gonwouo, ?Marvin Schafer, *Sedrick Junior Tsekané, 24Mareike Hirschfeld,
'F. Arnaud M. Tchassem, and 24Mark-Oliver Rodel
‘Laboratory of Zoology, Faculty of Science, University of Yaoundé I, P.O. Box 812, Yaoundé, CAMEROON *Museum fiir Naturkunde — Leibniz
Institute for Evolution and Biodiversity Science, InvalidenstraBe 43, D-10115 Berlin, GERMANY *Department of Biology and Animal Physiology,
University of Douala, P.O. Box 24157 Douala, CAMEROON *Frogs & Friends e.V., GroBbeerenstrape 84, 10963 Berlin, GERMANY
Abstract.—Habitat change and overexploitation are major factors driving species population declines
worldwide, and they often act in union. The Goliath Frog, Conraua goliath, is an iconic species that is known
to be extensively exploited by humans. However, Goliath Frog populations have not yet been assessed
quantitatively in relation to their proximity to human settlements, nor has the loss of terrestrial habitat adjacent
to the frogs’ riverine habitat been investigated. In this study, populations of the Goliath Frog were assessed
across its range in Cameroon during nocturnal, time-constrained, visual encounter surveys. Goliath Frogs
showed a patchy distribution along torrent rivers in three main habitat types: primary forest, secondary forest,
and agroforestry plantations. There were no significant differences in the encounter rates among the three
habitat types. However, we noted higher frog abundances, including larger sized adults, with increasing distance
from human settlements, an observation confirmed by local frog hunters. Our observations revealed strong
segregation in microhabitats with respect to age classes, as juvenile frogs were frequently found along river
beds with rock pools/rock crevices, while sub-adults were mostly encountered around exposed rocks at river
rapids, and adults were mostly recorded near cascades and waterfalls. The adults predominately perched on
rocks around waterfalls and rapids, with distances of about 3-5 m between them, suggesting both territoriality
and site fidelity. Adults were observed foraging at night, beyond 10 m from the river bank. During the day,
adults were seen basking on rocks along the river bank. The lower abundance and size of Goliath Frogs near
human settlements indicates the effects of hunting pressure, with terrestrial habitat showing less of an effect
on this species. Monitoring of the remaining Goliath Frog populations, raising local awareness on the effects
of hunting and habitat preservation, as well as law enforcement, are suggested as further efforts to conserve
the world’s largest frog species.
Keywords. Amphibia, Anura, Cameroon, conservation, exploitation, habitat choice, monitoring, threatened species
Citation: Gonwouo NL, Schafer M, Tsekané SJ, Hirschfeld M, Tchassem FAM, Rédel M-O. 2022. Goliath Frog (Conraua goliath) abundance in
relation to frog age, habitat, and human activity. Amphibian & Reptile Conservation 16(2) [General Section]: 104-119 (e319).
Copyright: © 2022 Gonwouo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Accepted: 29 August 2022; Published: 15 November 2022
Introduction
The world’s biodiversity crisis is almost exclusively
due to human activities, most notably the conversion
and destruction of natural habitats. However, the
overexploitation of many species, such as for food,
is an increasingly serious threat as well. Frogs are no
exception to this trend (Mohneke et al. 2010; Altherr et
al. 2022), and both of these threats may also affect the
world’s largest frog, Conraua goliath (Boulenger 1906).
This species is restricted to southwestern Cameroon and
northern Equatorial Guinea, where it occurs in lowland
to mid-altitude rainforests below 1,000 m asl (Lamotte
Correspondence. */gonwouo@gmail.com
Amphib. Reptile Conserv.
and Perret 1968; Sabater-Pi 1985; Wild et al. 2004;
Stuart et al. 2008; Channing and Rodel 2019). This frog
is associated with fast flowing rivers and larger streams
with rocky outcrops, rapids, and waterfalls (Perret 1957;
Amiet 1975; Sabater-Pi 1985; Gewalt 1996; Herrmann
et al. 2005). These natural habitats are becoming
progressively altered through various human activities,
such as conversion to farmland, construction of roads
and hydroelectric dams, and exploitation for artisanal
and commercial timber resources. The combination
of logging and conversion of the remaining forests
to agroforestry plantations has tremendous negative
consequences on biodiversity, including amphibians. The
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Gonwouo et al.
progressive fragmentation of original forest landscapes
leads to modified microclimates with obvious adverse
effects on amphibian communities (e.g., Ernst et al.
2006; Stuart et al. 2004, 2008; Ernst and Rodel 2008;
Hillers et al. 2008; Ofori-Boateng et al. 2013). Previous
studies suggested that fragmentation and destruction of
habitat has led to a reduction in Goliath Frog populations
at various Cameroonian sites (Amiet 2004; Herrmann et
al. 2005). If this is true, it is likely that these processes
would cause general population decline over the entire
range of the species. In addition, frog meat may be an
important (or at least a much valued) protein source
for many indigenous people throughout the Goliath
Frogs’ range (Gonwouo and Rodel 2008). Hence, the
increasing human population, expansion of settlements
and increased efficiency of hunting tools will intensify
the pressure on this species. This is especially evident
in the professionalized hunting methods (traps, hooks,
spears, throwing nets, etc.) that have been developed
specifically to collect Goliath Frogs (Amiet 2004;
Gonwouo and Rodel 2008; Schafer et al. 2019). The
hunt for subsidiary consumption, as well as for local
bush meat markets, might be one of the main factors
driving the population decline of Goliath Frogs. The
commercial harvesting of Hoplobatrachus occipitalis
has contributed to the population decline of this species
in northern Bénin (Mohneke et al. 2010). Based on its
rarity and much larger size (assuming a longer time
until frogs become mature), similar or even more severe
consequences may be assumed for the Goliath Frog.
As a result of these pressures, this species 1s currently
listed as Endangered by the IUCN and Class A under
Cameroonian law (IUCN Amphibian Specialist Group
2019a; NLG et al., unpub. data).
Previous studies on the Goliath Frog have focused
mostly on its distribution (Perret 1957, 1960; Sabater-
Pi 1962, 1967; Amiet and Perret 1969; Gewalt 1977),
taxonomy, and phylogeny (Lamotte and Perret 1968:
Neguiffo et al. 2019; Blackburn et al. 2020). Some
investigations have also investigated various aspects of
life-history, including larval development, parasites, and
reproduction (Lamotte et al. 1959; Perret 1957, 1960;
Sabater-P1 1985; Nguiffo et al. 2015). Parental care has
recently been documented in the species (Schafer et
al. 2019), and additional studies by the authors of this
paper are in progress to further improve our knowledge
of the life-history of this species. However, very little
is known concerning the population trends and habitat
preferences of this species, or the specific threats that this
species is facing. In the absence of research on the habitat
requirements and responses to the various threats facing
the Goliath Frog, the development and implementation
of appropriate conservation measures are difficult.
To remedy this general lack of knowledge, this study
examines the impact of land use and proximity to human
settlements on the relative abundance, demographics,
and body size of Goliath Frogs. The data presented in
Amphib. Reptile Conserv.
this paper are based on six years of investigations on the
Goliath Frogs in Cameroon, and allow us to examine
the correlations between this species and human-caused
forest alteration and to propose the directions and goals
of future research and conservation strategies.
Material and Methods
Study Area
Fieldwork was carried out from November 2014 to
December 2019 during both rainy and dry seasons (Table
1), although the dry seasons (November to February)
were emphasized as the rivers were more accessible.
Fieldwork focused on the areas around three main
localities in south-western Cameroon: Moungo, Sanaga
maritime, and Nkam division (Littoral region); Nyong-
Ekele (Central region); and Bipindi in Ocean division
(South region) (Fig. 1). In total, 13 rivers (Table 1) were
surveyed, including the Nkam and Sanaga rivers.
Investigations were carried out from near sea level
around Kribi (Ocean division), up to the foothills of Mount
Manengouba near Nkongsamba (Moungo division).
The latter locality hosts the northernmost population of
the Goliath Frog and is characterized by several large
rivers and streams. Overall, the landscapes of our sites
constituted mostly low to medium elevation habitats, with
the elevations of our frog observations ranging from 39 m
asl along Lobe River (Bifa, Ocean division) to about 677
m asl along Nkam River (Nkoungsou, Moungo division).
Other than the Moungo area, which is characterized by
a heterogeneous, mountainous landscape (Mts. Kupe,
Nlonako, Manengouba), the remaining sample localities
have a low-rise or flat relief, only rarely interrupted by
hills. The study areas comprised a mixture of several large
forest patches of Guinea-Congolian lowland rainforest
(both pristine and logged), agroforestry plantations,
and small-scale subsidiary agricultural sites. Especially
in the area around Yabassi (Nkam division), logging
companies commercially exploit timber for exportation,
despite the remoteness and difficulty in accessing the
area. The entire study region has a tropical climate, with
the wet season extending from March to October and the
dry season from November to February. Rainfall peaks
in August and September, and the driest period extends
from late December to the end of February. The annual
precipitation ranges from 2,000 to 3,000 mm (Amiet
1975).
Surveys and Data Acquisition
The visual encounter survey (VES) method (Heyer et
al. 1994; Rodel and Ernst 2004) was used in suitable
habitats to systematically survey for Goliath Frogs. The
VES consisted of counting all Goliath Frogs encountered
in every major habitat type, and provided an encounter
rate per person-hour. Three major habitat types were
November 2022 | Volume 16 | Number 2 | e319
Goliath Frog populations in Cameroon
Table 1. River sites investigated for Goliath Frogs in three surveyed habitat types in western Cameroon. The information provided
includes river name, total length of sampled trails, geographic position, and a short habitat description (including length of river
investigated and the total sampling effort per site in person-hours).
Locality
(river name, coordinates,
elevation [m asl])
Habitat characteristics (including approximate length surveyed for each
section and person-hours of effort for each site)
Section one: Composed of logged secondary forest (SF) with open to semi-
Poe PAD Scene closed canopy forest which covered about 70% of the surveyed trail, ~250 m.
2014
02°36'47.23”N,
10°01°05.51”E: 39 masl Section two: Small-scale cocoa plantation with few native trees interspersed in
the plantation and a relatively open canopy, ~150 m (9.77 person-hours).
Section one: River bank bordered by primary forest with a closed canopy of
native trees that were about 25-30 m high. Open understory including leaf
litter on floor. Steep flanks at some sites that were difficult to access, with no
rs signs of human activity, ~1,500 m
14 February e . MALY
2 ' - 2 a NY ce Section two: Selectively logged secondary forest along a path with constant
9°58’06.18”E; 231 m asl
human signs. Trees about 25 m high with relatively open to closed canopy.
Secondary growth trees observed where logging had been carried out, ~400 m
(13.74 person-hours).
Section one: Composed of logged forest along steep portions of the river
where farming activities are impossible. Many footpaths present and rampant
Ekomtolo wood extraction for local furniture and domestic fuel, ~300 m.
12 February
4°47°32.57°N, 2015 Section two: Composed of large- to small-scale cocoa plantations with
9°53’11.60”E; 332 m asl few native trees spaced all over the area and constantly managed by the
community. Chemicals used to sustain the crops are processed in the nearby
river with possible contamination, ~500 m (4.25 person-hours).
Forest composed of a mosaic of primary forest, secondary forest, and
agroforestry plantation interspersed all through the surveyed trail.
Section one: Mainly closed canopy of native trees, about 25—30 m tall, along
difficult-to-access terrain, no previous logging had occurred. Forest floor with
Dibombe ;
about 70% leaf litter cover, ~900 m.
15 February
9°4 Bs eee — 74 acl a Section two: Old selectively logged forest, easy access due to the many
i footpaths present, empty cartridges left behind by hunters, ~400 m.
Section three: Small-scale plantation, mainly composed of cocoa and banana
plants which covered the flat sections along the river on both flanks, ~300 m
(14.26 person-hours).
Sta MNna Mipein Section one: Primary forest on slopes along the river where movement and
St eee 7-12 July 2016 | tree exploitation is difficult, ~1,000 m.
10° a So Leet Section two: Included portions where access was easier with several human
° foot paths present, signs of forest exploitation, ~650 m (10.55 person-hours).
Section one: Composed of small patches of native large trees around difficult-
Sanaga (Tributary River) 13-15 July 2016 to-access points of the river, bordered by very large rocks, ~700 m.
4°03’23.19’N, Section two: Composed of recently logged forest patches, with several hunting
10°37? 12.88”E; 297 m asl paths. Frequent use of the forest to collect non-timber forest products, ~600 m
(14.55 person-hours).
Section one: Consisted of closed canopy trees of about 25 m in height on both
meinke sides of the river. Footpaths present within the forest seem to be regularly used
2-3 March 2017 | by fishermen and Goliath Frog hunters, ~900 m.
3 -4 2 me is NM Section two: Recently logged forest with open canopy and bushy understory.
10°04’56.75”E; 48 m asl
Regular use of this forest section evident, with many footpaths present, ~200
m (11.72 person-hours).
Amphib. Reptile Conserv. 106 November 2022 | Volume 16 | Number 2 | e319
Gonwouo et al.
Table 1 (continued). River sites investigated for Goliath Frogs in three surveyed habitat types in western Cameroon. The information
provided includes river name, total length of sampled trails, geographic position, and a short habitat description (including length
of river investigated and the total sampling effort per site in person-hours).
Locality
(river name, coordinates,
elevation [m asl])
Magatnba 6 April 2016
4°45'19.03"N,
9°52'16.68"E; 308 m asl
Habitat characteristics (including approximate length surveyed for each
section and person-hours of effort for each site)
Trail bordered by agroforestry plantations as well as subsistence plantations on
both banks. Fallow land present along river bordered by degraded forest with
very dense vegetation, edges with shrubs and only a few trees present, ~600 m
(6 person-hours).
Section one: Consisted of agroforestry plantations, mainly cash crops
Nkam 29 October —2
November 2018
5°08'17.43'N,
9°59'43.17"E; 677 m asl
including coffee, cocoa, and palm oil trees growing on the river bank, ~800 m.
Section two: Mainly composed of small relic forest patches on steep valleys
along the river, access was difficult. No possibility of farming at this site, but
forest patches appeared to have been logged with several foot paths found,
~350 m (4.96 person-hours).
Section one: Vegetation composed of a mosaic of secondary forest and
agroforestry plantations on both river banks. Secondary forest composed of
Mbo fallow land, more than 10 years old, and several cocoa plants and large palm
6 April 2016
4°49°39.16"N,
9°47 18.58”E; 465 m asl
trees could still be found.
Section two: Permanently cultivated plantation with young cocoa and palm
trees, intensively managed with signs of constant human presence, ~250 m
(14.97 person-hours).
Mpoula
27 February — 5
4°38'15"N, 9°43'07"E; 200 May 2018
m asl
Njuma 27 August —17
September 2019
4°20°53.1°N,
10°13’56.3”E; 304 m asl
Bisoue 27 August —17
September 2019
4°21°38.3°N,
10°12’30.4”E; 152 m asl
identified along the 13 rivers: primary or pristine forest
(PF; Fig. 2A), selectively logged or secondary forest (SF;
Fig. 2B), and agroforestry plantations (AP; Fig. 2C, also
see Table 1 and below for detailed descriptions of the
habitat types).
Transects along the rivers could comprise either a
single vegetation type, or a mosaic of different vegetation
types or segments (e.g., PF, SF, and AP) that could vary
considerably in short succession. This was especially
true when human settlements were nearby. To measure
the portion of a certain vegetation type in a single
transect, we passed the respective segment and measured
the covered distance with a GPS unit. The vegetation
type was identified on both sides of the river by assessing
the canopy cover (visual estimation to 25% accuracy),
estimated height (4+ 5 m), and measured diameter at
breast height (DBH) (+ 0.5 cm) of the trees, as well as
any obvious human impacts, such as selective logging,
hunting, or extraction of non-timber forest products (e.g.,
leaves, tree bark, fruits, resins, or roots).
Amphib. Reptile Conserv.
Surveyed trail composed of a mosaic of secondary forest (~200 m) and
agroforestry plantation (~300 m) on both sides of the river, constant human
activities noted along the trail (10.8 person-hours).
River bordered by primary forest (~1,200 m) on both sides with little or no
signs of human activity, though foot paths where present and have been used
by poachers and seasonally by Goliath Frog hunters (5.31 person-hours).
River bordered by primary forest (~ 400 m) on both sides with little or
no human impact. Access was difficult at some points due to the dense
undergrowth along old footpaths (15 person-hours).
Primary Forest (PF) consisted of closed canopy
forest with 75—-100% canopy cover. This forest type
was dominated by large, native trees of about 25—30
m in height, although the largest exceeded 50 cm in
DBH. No evidence of recent logging was present in PF.
Although hunting or fishing paths were regularly found
along the rivers (especially close to human settlements),
revealing some degree of natural resource exploitation,
this forest type was still considered mature and relatively
undisturbed. Primary Forest comprised seven segment
portions of the 13 rivers surveyed, and their lengths and
brief descriptions are provided in Table 1.
Selectively logged Secondary Forest (SF) included
all vegetation formations with a relatively closed canopy
(50-75% canopy cover) and medium to large trees (10-
25 m in height). Here, the tree composition included
both native and non-native tree species with DBH
usually exceeding 40 cm, including many secondary
growth trees. These forests had been previously logged
for commercial timber exportation, and/or by the local
November 2022 | Volume 16 | Number 2 | e319
Goliath Frog populations in Cameroon
10°0'0.000°E
5°0'0.000"N
Mpo Ekomtolo
Magamb#a ¢.
ene, Nkebe
Mpoul? ibomie
Littoral
4°0'0.000"N
2
[=]
o
=
Ss
So
°
om
pe obe
2°0'0.000"N
10°0'0.000"E
e kam
AS einke
11°0'0.000°E
5°0'0.000"N
goisoue
Njuma
4°0'0.000"N
3°0'0.000"N
“=polowa
Legend
© Study sites
Hl Rivers
—— Main roads
GB South and Littoral region
Cameroon
{__] Other borders
2°0'0,000"N
11°0'0,000°E
Fig. 1. Map of Cameroon indicating the locations of the study sites.
population for house construction or for local trade. Many
footpaths, as well as the remains of abandoned logs,
snare traps, and rifle cartridges, were found within these
forests, indicating ongoing and constant use for hunting
and timber exploitation. Secondary Forest comprised ten
segment portions of the 13 rivers surveyed.
Agroforestry Plantations (AP) included — all
plantations, ranging from small-scale subsidiary crops
and/or cash crops cultivated by the local people to
intensively farmed, large-scale monocultures created by
international commercial agro-companies. This habitat
type, especially when cultivated by local farmers, could
include native trees with more or less open canopies (<
50%), the largest stem diameters exceeded 40 cm, and they
were spaced all throughout the cropped species. Most of
the cultivated plants were introduced species, including
manioc (Manihot esculenta), papaya (Carica papaya),
pineapple (Ananas comosus), mango (Mangifera indica),
cocoa (Theobroma cacao), palm oil (Elaeis guineensis),
avocado (Persea americana), and bananas (Eumusa
spp.). Native large trees were found mostly in cocoa
plantations as shade-trees, whereas banana tended to be
cultivated in large monocultures. The latter is cultivated
at a commercial scale in the Njombe-Penja area for
exportation. Agroforestry Plantations comprised seven
Amphib. Reptile Conserv.
segment portions of the 13 rivers surveyed. To enhance
crop production, herbicide and pesticide mixtures are
prepared in nearby rivers and streams with likely runoff,
polluting the rivers.
Sampling took place between 0700 and 1200 h, and
included various microhabitats, such as waterfalls, rocky
rapids, rock pools, and riverbanks, as well as forest strips
up to 20 m from the rivers. Gaining access to the rivers
and their banks demanded careful clearance of trails, e.g.,
removing of some lianas or dead wood along a narrow
trail. Trails were set-up at least 24 h before surveying
the respective area. To maximize the probability of
documenting all individual frogs, teams of two or three
researchers walked along the rivers at a slow, steady
rate of 0.2 m per second, avoiding any jerky movements
that could disturb the frogs. Headlamps and handheld
flashlights were used to detect the frogs, particularly by
picking up eye-shine. All spatial data were recorded with
a Garmin GPS (60 cx; accuracy of 5-10 m). For every
frog, the perch site, date, time, posture, size, and distance
from the riverbed were recorded. Size categories were
classified as follows: adults (= 19 cm snout-vent length)
(Fig. 3A); subadults (approx. 10-18 cm) (Fig. 3B); and
juveniles (< 9 cm) (Fig. 3C).
Daytime habitat assessments preceded the nighttime
November 2022 | Volume 16 | Number 2 | e319
Gonwouo et al.
ee
>
ie
£
Fig. 2. Examples of the three different forest types investigated in this study: (A) primary forest (River Dibombe), (B) secondary
forest (River Nkam), and (C) agroforestry plantations (River Mpoula).
surveys, with notes taken on habitat features, such as
dominant vegetation, as well as notable, anthropogenic
influences on the sites. Notes on the microhabitats of
sun-basking frogs were made accordingly. Data for the
daytime searches are not generally comparable to the
nighttime searches, given that the frogs are mostly active
during the night. However, the locations of daytime frog
encounters regularly coincided with the presence of
similarly-sized individuals during the night.
Local Ecological Knowledge (LEK) was obtained
from local frog hunters around the surveyed areas who
could reliably identify Goliath Frogs and regularly hunt
them. This information was collected through informal
interviews and discussions, and it greatly contributed to
our assessments. To prevent any biasing toward certain
answers, we asked all of the respondents the following
six questions: Which are the rivers where Goliath Frogs
are present? How far are they from the village? What
was your biggest catch ever, and when was that? What
was your biggest catch in 2019? How often do you hunt
for the frogs? What is your perception about the Goliath
Frog population around the village?
Data Analysis
The sampling effort was recorded only for the nocturnal
surveys. Daytime searches were not time constrained as
they were mostly meant to identify nocturnal survey sites.
Amphib. Reptile Conserv.
Sampling effort is given in person-hours, 1.e., the number
of hours spent surveying multiplied by the number of
observers for any given river and habitat type (Table 2).
The relative abundance of frogs was calculated as the
number of individuals observed per time unit, divided
by the number of sightings through the total sampling
effort for each river or habitat type, and given as frogs per
person-hour. As the relative abundances of Goliath Frogs
were not normally distributed, Pearson’s Correlation
Coefficient was applied to compare the abundance of
frogs and age groups per habitat type.
In order to examine frog abundance in relation to
human presence, the GPS coordinates of the study sites
were used and a 10 km buffer around each point was
drawn in a geo-information system (QGIS Development
Team 2021). All streets and settlements within the
buffer zone were extracted from the Open Street Map
database (https://planet.openstreetmap.org), and the
total length of all roads (motorways, interregional
and regional highways, urban as well as agricultural
roads) was determined, as well as the number and type
of settlements. No recent, fine-scale census data are
available for the study area, thus the human population
within each buffer zone was estimated by assigning fixed
values to each of the different settlement types. Hamlets,
the smallest type of settlement, accounted for 200
people, villages for 1,500, towns for 25,000, and cities
for 100,000 inhabitants. Note that these values were
November 2022 | Volume 16 | Number 2 | e319
Goliath Frog populations in Cameroon
Ps ea NC ad
wee t
Fig. 3. The three different age sizes of Goliath Frogs considered in this study: (A) adult (= 19 cm), (B) subadult (10-18 cm), and
(C) juvenile (< 9 cm).
based on the open street maps criteria. Human population
density was calculated by dividing total population by
the area within the 10 km radius buffer zone (314 km/?).
The distance of each sampling site to the nearest road
and settlement boundary were determined. Subsequently,
the data were screened for any linear dependencies of the
GIS extracted values and the number of observed frogs
(iph) in a regression analysis. Distance measures were
log-transformed before the analysis.
To analyze the LEK data, a Welch-test comparing
the hunter’s perceived frog weights in different years
was performed. A linear regression model was used to
determine if there was a correlation between frog weight
measured by local hunters and distance to the nearest
settlement. All analyses were conducted using R v.4.0.0
(R Development Core Team 2014).
Results
Encounter Rates and Distances to Settlements and
Roads
A total of a 100 person-hours were spent surveying for
Goliath Frogs at 13 rivers across the entire range of the
species in southwestern Cameroon. During the study,
490 frogs were observed along 26.7 km of riverine
habitats, including 13.1 km in PF, 7.0 km in SF, and 6.6
km in AP. The number of person-hours spent on each
Amphib. Reptile Conserv.
habitat type varied, given the differences in river size and
habitat accessibility. The encounter rates of frogs varied
with respect to habitat types, rivers, and with grade of
anthropogenic influence. For the entire study period, the
average encounter rate was five frogs per person-hour (5
iph). Within the three habitat types, the highest mean iph
was 8.2 recorded in SF, followed by 7.1 in PF, and 4.6 in
AP. However, these values were not statistically different
(Fig. 4). The two individual study sites with the highest
encounter rates (17.0 iph) were both in SF, along the
Sanaga and Keinke rivers. At these sites, the forest had
been legally and commercially logged. These localities
are far from human settlements and the frogs seemed to
show lower flight-distances when approached compared
to the frogs at other sites (however, we did not collected
data to support this general impression). The lowest
encounter rates were along the Ekomtolo and Mpoula
Rivers (1.0 iph), and both localities are close to human
settlements. Although disturbed, the surveyed portion of
Mbo River, which is bordered by about 50% AP, revealed
very high encounter rates (8.4 iph).
Human densities and the levels of anthropogenic
disturbance varied considerably around the study sites.
Total road length within a 10 km radius buffer around
the sites ranged between 9 km and 168 km, with a mean
of 84.5 km. The number of settlements ranged from
1 to 20 within the buffers, with a mean value of 10.1.
The estimated human population densities ranged from
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Gonwouo et al.
Table 2. Encounter rates of Goliath Frogs (in person-hours of searching effort) during time-constrained visual encounter surveys in
the three different habitat types: PF, primary forest; SF, secondary forest; and AP, agroforestry plantation. Data are given for each of
three different age sizes: a, adult; s, subadult; and j, juvenile.
Habitat type PF
Age size a S j Dy
Lobe
Nkebe 2.07 133 0.93 4.33
Ekomtolo
Dibombe 3.50 2.33 1.33 7.17
Sanaga Ngo Mpem 240 1.05 1.05 4.50
Sanaga (Tributary River) 6.43 429 1.71 = 12.43
Keinke 3.67 5.67 1.33 10.67
Magamba
Nkam
Mbo
Mpoula
Njuma 163 1.25 0.00 2.88
Bisoue 3.38 450 0.00 7.88
Mean 3.29 2.92 0.91 7.12
1,000 to 99,200 inhabitants in the 314 km? of the buffer
zones (12.7—1,263.7 persons per km?), with a mean value
of 32,592.3 (415.2 persons per km’). Road length and
population density were negatively, but not significantly,
associated with higher frog numbers (Table 3). The
distances between study sites and the nearest settlement
ranged from 89 to 9,114 m (median = 2,741 m), and the
distances between study sites and the nearest road ranged
from 176 to 8,653 m (median = 701 m). While both
measures (after logarithmic transformation) indicated a
positive association between distance and frog numbers,
only the nearest settlement showed a robust and significant
linear dependency (Table 3, Fig. 5). In other words, more
frogs were found when the nearest settlement was farther
away. Only the Njuma River violated this rule, as it was
the most remote site but only provided a small number of
frogs (Table 3).
Age Categories and Microhabitats
Of the 490 Goliath Frog observations, 243 (49%) were
adults, 170 (35%) were subadults, and 77 (16%) were
juveniles. Of all the adults, 48% where from PF, 36%
from SF, and 16% from AP. The encounter rates of the
three age sizes varied among the rivers, as well as both
between and within the different habitat types. A Chi-
square test of the three age groups showed that there
was no difference in the population structures between
the three different habitat types (v7 = 3.48, df= 2, p =
0.48). The highest encounter rates among the three age
sizes were for adults (9.0 iph) recorded in SF; while the
lowest was in juveniles (1.0 iph) recorded in all three
habitats (PF, SF, and AP). The recorded encounter rates
Amphib. Reptile Conserv.
SF AP
a S j x a S j x
7.20 240 0.00 9.60 4.00 600 0.00 10.00
245- 225 050 5.50
100 0.00 0.00 1.00 180 080 0.20 2.80
3.00 1.88 413 9.00 200 250 0.00 4.50
2.77 2.08 1.62 6.46
9.00 650 1.50 17.00
9.00 7.50 0.00 16.50
0.89 0.78 0.33 2.00
429 257 0.00 686 2.63 150 0.00 4.13
420 1.20 1.20 660 240 420 1.80 8.40
2.17 O33 1.00 3.50 044 0.00 0.22 0.67
454 2.67 0.99 8.20 2.02 2.25 0.37 4.64
of the frogs, sorted by age sizes within the three surveyed
habitat types, are summarized in Table 4.
Goliath Frogs showed a patchy distribution across
the study sites and were mostly restricted to particular
microhabitats, which included moderate to fast flowing
rivers with cascading, turbulent rocky sections (Fig. 6),
or waterfalls with mostly sandy soils. The species was
recorded from Bifa, Babong, Ekomtolo, Magamba,
Manengotang, Nko-Olong, Ngo-Mpen, Nkongsou,
and Sole. The altitudinal range of the inhabited sites
spanned from 39 m asl at Lobe River around Bifa and
near the coast, to about 677 m asl at Nkam River. Goliath
Frogs were recorded in 75% of the surveyed rivers, but
only when these included suitable microhabitats. The
inhabited river sections surveyed varied from 50 m
to more than 300 m. The torrent, rocky sections were
inhabited while the in-between sections, slow moving,
meandering river parts with no rocks, revealed no frogs.
Goliath Frogs were completely absent from rivers
lacking fast flowing sections and rocks. For example,
the five rivers south of the newly constructed deep-sea
port at Kribi that were investigated all lacked the above-
mentioned microhabitats, and yielded no Goliath Frogs
despite being within the range of the species. Discussions
with local ethnic groups, including the Bagyli/Bakola
people who have lived in this forest for many generations,
confirmed that Goliath Frogs never occurred in this area.
Age dependent differences were noted in microhabitat
use. When Goliath Frogs came out at night to perch on
rocks, the adults used the areas around large cascading
waterfalls, while sub-adults were more often present on
rocks in the rapids, and juveniles inhabited rock pools and
crevices. Adult frogs were abundant around waterfalls
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Goliath Frog populations in Cameroon
15
10
Individuals per person-hour (ibh)
PF SF AP
Habitat type
Fig. 4. Number of individual Goliath Frogs recorded per person-
hour in each of the three surveyed habitat types: PF = primary
forest, SF = secondary forest; AP = agroforestry plantation.
Note that the encounter rates of frogs were not statistically
different between any of the three habitat types.
but maintained some distance from one another. The
closest distance between two adult frogs was 3 m,
observed at Dibombe River. A maximum of seven adult
individuals were observed at a single waterfall along
Nkebe River. On Mpoula River, adult frogs were seen
sitting on large branches within jumping distance of the
stream (~5 m in adult frogs), at more than 2 m above
the ground. At night, adult frogs that had fled from the
surveyors by diving into the stream returned to the same
perching rocks shortly (10 to 15 min) after disturbance,
indicating fidelity to particular perching sites. Adults
and subadults (7 = 24) were frequently observed at night
on low bushes and trees more than 10 m away from the
riverbed. During the daytime, our observations revealed
extensive sun-basking behavior, 1.e., more than 20 adults
were seen sun-basking throughout the study period.
Adults often leaped and dove into the rivers upon our
approach (flight distance 4 to 10 m). One individual was
observed basking on the same rock on three consecutive
days, along a relatively calm portion of Ekomtolo River.
When disturbed, this frog jumped into the river and
returned to its perch site after about 30 to 45 min.
Presence at Sites Impacted by Pollution and
Agricultural Activities
The data revealed that Goliath Frogs persist in forest
fragments, plantations, and rivers, even when surrounded
by human settlements. Observations from the localities
of Magamba and Manengotang indicate that small
populations can be present at about 200 m from human
settlements. Here, the habitat was patchy and comprised
a mosaic of small forest remnants and small subsidiary
plantations. The Goliath Frog occurrence at these places
Amphib. Reptile Conserv.
Distance to settlement
7
Individuals per person-hour
Fig. 5. Scatterplot of Goliath frog abundance (as individuals
per person-hour) and log transformed distance to the nearest
settlement. The red line is the trendline of the fitted linear
model and the blue dotted lines demarcate the 95% confidence
interval. Note that the top outlier point refers to Njuma River,
which was the most remote site sampled, however, it also
accounted for one of the lowest numbers of individuals.
Fig. 6. Typical forested and rocky-sandy riverbed characteristics
for Goliath Frog habitat (Dibombe River).
was also confirmed by Goliath Frog hunters, and frog
hunting at these sites was perpetual. We commonly
observed habitat pollution by the dumping of household
waste into the rivers and adjacent forests. Unfortunately,
there is no quantitative data regarding how long the
habitats had been impacted (by logging and/or pollution);
for how long and with what intensity the frogs had been/
are being hunted: or how large the populations had been
previously and how they had developed. Thus, there is no
way to estimate how long these populations may prevail
despite the small numbers of individuals and altered
habitats.
The vast majority of the local people (~70%)
around the study sites live on subsidiary and cash crop
agriculture. In the study area, many forests along large
rivers and streams have been transformed into cocoa and
palm oil plantations, with larger portions converted where
populations are high. To maintain these plantations and
to improve production, fertilizers, herbicides, fungicides,
and insecticides are used extensively. The preparation
of those chemicals generally happens along the nearby
rivers and streams, inevitably contaminating the water
(NLG, pers. obs.). The scale of these potential threats
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Gonwouo et al.
Table 3. Sample sites, numbers of frogs, and extracted values for number of roads, total length of roads, number of settlements,
derived population estimate within the 10-km buffer zone, as well as measured distances to nearest settlement and road. Correlation
coefficient and P-values from correlation analysis are given below each of the respective measures.
Total length of — Distance to
River IPH roads nearest road
Lobe 971 167.9 650.9
Keinke 172 86.6 2,741.1
Dibombe 14.26 78.2 3,508.5
Bisoue 15.00 23.8 5,624.6
Mpoula 10.80 131.7 2,464.6
Nkebe 13.74 31.8 3,634.7
Sanaga (N) 10.55 69.4 2,199.6
Sanaga (T) 14.55 82.5 4,175.9
Njuma 5.31 8.9 8,653.5
Magamba 6.00 80.5 358.8
Ekomtolo 4.25 94.6 175.8
Mbo 14.97 82.2 3,843.3
Nkam 4.96 160.1 229.9
R? -0.257 0.688
P 0.3972 0.0093
to the frogs varied through the study sites and time.
Along the river at Magamba for instance, large quantities
(estimated at around 70%) of the original forest were
transformed into plantations within our six-year survey
period. Nevertheless, the Goliath Frog populations
persisted at these sites.
Frog Size and Distance to Settlements
Frog size, estimated by the authors and the surveyed
hunters, was positively correlated with distance to
settlements, with smaller frogs living closer to the
settlements (Fig. 7). Discussions with 11 frog hunters
revealed that they have to move increasing distances of
300 to 4,000 m from the settlement in order to find large
frogs, and that the adult and subadult/juvenile Goliath
Frogs, which were once common around waterfalls and
rock pools, are now less abundant. Based on weight
estimates from the hunters, they agreed that the largest
Goliath Frog they ever encountered, estimated to weigh
about 5 kg, was caught before the year 2010. There was a
significant (Welch-test: t= 6.14, df= 15.87, p < 0.0001)
drop in the perceived frog weight when compared to the
largest frog caught in 2019 (Fig. 8).
Discussion
This study assessed Goliath Frog habitats and relative
abundance over large parts of the known range of this
species in Cameroon, in order to understand the influenc-
es of land use and vicinity to human settlements. Goliath
Frogs were found to occur within all of the three main
habitat types surveyed, 1.e., primary forest, secondary
Amphib. Reptile Conserv.
Distance to nearest Number of Population
settlement settlements estimate
701.26 5 1,000
2,941.09 6 9,000
525:02 6 9,000
6,126.63 1 1,500
505.07 10 85,500
2372 22 ci 10,500
2,236.13 5 31,000
5,603.30 19 28,500
9,113.55 1 1,500
149.07 7. 25,500
89.25 19 75,500
541.14 15 46,000
477.44 20 99,200
0.431 -0.304 -0.415
0.1410 0.3130 0.1590
forest, and agroforestry plantations. The frogs utilize a
combination of particular microhabitats that are stratified
by different age sizes. Torrent water and rocks seem to
be requirements for the presence of all ages. Based on
our data, Goliath Frogs seem to be able to deal with some
degree of habitat alteration, and the population decline is
mostly due to hunting.
Impacts of Anthropogenic Factors
Due to the lack of previous (quantitative) data, it is
difficult to reliably assess whether and to what extent the
Goliath Frog populations have changed. Therefore, we
had to base our assessment on indirect evidence, e.g., the
comparisons of frog occurrences in pristine versus altered
habitats, the severity of different threats, and interviews
with local frog hunters. One exception is the previously
published data on the abundance of Goliath Frogs along
the Sanaga River, described by Perret (1957, 1960) and
Amiet and Perret (1969). These populations still persist
today, despite the high degree of selective logging in the
area. However, this positive finding does not preclude
the fact that the species seems to be threatened by
human activities in general, and the situation for many
local populations is not very promising. We base this
conclusion on our observation that especially large adult
frogs are rare around human settlements and increase
progressively farther away, a basic finding confirmed
by the surveyed frog hunters. Two indirect measures of
anthropogenic impact, roads and population densities,
indicated a trend of increasing frog numbers with the
remoteness of habitats, although only frog abundance and
distance to settlement was robustly, positively correlated.
November 2022 | Volume 16 | Number 2 | e319
Goliath Frog populations in Cameroon
oO
aE 2) i)
Or KS
w)
aa EET o-
root S
=x
Cc -
a2)) te
oO
= fe)
2am
fap)
1?)
oO oO
Te) “
A GY
1000 2000 3000 4000
Distance to settlement [m]
Fig. 7. Scatterplot of frog weight and distance to the nearest
settlement. Note that the weight of the Goliath Frogs was
increasing with distance from human settlements.
This analysis has some limitations. First, there are
limitations in the dataset itself. For instance, we are
certain that not all small settlements and roads were
consistently recorded, and thus the human impact may
be generally larger. Our population estimates include
some errors and inaccuracies as well, e.g., the population
for the category ‘village’ in OpenStreetMap ranges
from 500—5,000. Clearly not every village will have a
population of about 1,500 inhabitants. Nonetheless, our
data generally indicated coherent patterns. The Goliath
Frog population of Lobe, for instance, is situated right
next to a vast banana plantation and gave the lowest
jo)
To)
“)
+
go
— wT
=
= 12
= 0s
jo)
ro)
i)
N
Before 2010 2019
Year of catch
Fig. 8. Changes in weight of Goliath Frogs from around 1990 to
2019, as estimated by the surveyed frog hunters.
frog population estimate. On the other hand, several
Goliath Frog populations were quite large despite being
in close proximity to major roads. Generally, the distance
to the nearest settlement was a better predictor for frog
abundance.
The impact of distance to the nearest settlement was
especially notable for populations that are exploited for
food and trade, and also comprise anthropogenic impact-
ed habitats. For instance, the Nkongsamba area has un-
dergone a drastic change in vegetation structure over the
past decades, as large-scale agro-industrial plantations
and an increasing number of subsistence plantations have
Table 4. Counts of the Goliath Frogs observed in the 13 rivers for the three habitat types (PF, primary forest; SF, secondary forest;
AP, agroforestry plantation) across its range in Cameroon. Count data are provided with respect to the three different age sizes: a,
adult; s, subadult; and j, juvenile.
Count data (numbers of observed individuals)
River PF
a S j x
Lobe
Nkebe 31 20 14 65
Ekomtolo
Dibombe 21 14 8 43
Sanaga Ngo Mpem 16 7 Zz 30
Sanaga (Tributary River) 15 10 4 29
Keinke 1] 17 4 32
Magamba
Nkam
Mbo
Mpoula
Njuma 13 10 23
Bisoue 9 12 21
Total 116 90 37 243
Amphib. Reptile Conserv.
SF AP Total
S j a S j x
2 8 3 5 13
11 2 22 87
3 3 4 1 14 M7
8 11 24 4 9 76
12 9 ip 28 58
18 13 34 63
6 5 11 43
8 a) 18 18
5 3 8 of 4 11 19
7d 11 4 14 25
13 21 4 2 6 27.
23
ZI
89 50 31 170 38 30 9 77 490
114 November 2022 | Volume 16 | Number 2 | e319
Gonwouo et al.
been established (NLG, pers. obs.). In this area, Goliath
Frogs are also intensively hunted for the food market.
This is the area where we recorded the lowest encounter
rates throughout the entire study period. Habitat conver-
sion and degradation usually went hand in hand with
hunting pressure, with both being more pronounced close
to settlements. Around the localities of the Ebo forest, an-
thropogenic pressure was almost absent, and here we en-
countered the highest numbers of frogs per survey effort.
Importance of Forest Habitats
In contrast to the human impact, vegetation type was
not a useful predictor, as Goliath Frogs were present in
all forest types from semi-open to close-canopy forests
(as long as cascading rocky river sections were pres-
ent). Goliath Frogs apparently need some forest, but not
necessarily pristine forest. They live in cold water and
regularly sun-bask, presumably to regulate body temper-
ature. Thus, the opening of forest habitats and resulting
raising of temperatures may not negatively impact them,
as long as the water temperature remains “low enough”
(although, unfortunately, the temperature preferences
of the species are unknown) and the habitat surround-
ing the rivers can still provide enough food and shelter.
Other African frog species with similar life-histories and
inhabiting forested, torrent rivers, e.g., Conraua alleni
and Odontobatrachus spp., also usually occur in cooler
streams in forest, but may persist in areas with little riv-
erine forest surrounded by savanna (Rodel 2003; Rodel
and Bangoura 2004).
In this survey, when cascading, turbulent water with
rocks and some forest patches was present, Goliath Frogs
were reliably recorded. Thus, Goliath Frogs may be able
to tolerate forest degradation to a surprising extent. This
is in line with predictions by Hirschfeld and Rodel (2017)
that large frogs in particular, with large clutch sizes and
aquatic larvae, may be more resilient to forest degrada-
tion than species with other trait combinations. We would
like to stress, however, that our observations should not
be interpreted as indicating that riverine vegetation 1s not
important for maintaining Goliath Frog populations.
Riverine forest may be important for Goliath Frogs
during their nocturnal foraging activity. It is likely that all
individuals observed along the river banks were adopting
a ‘sit and wait’ foraging strategy. A study on stomach
and intestinal contents revealed that the diet of C.
goliath consists of approximately 60% arthropods, 20%
crustaceans, 10% amphibians, and 10% indeterminate
food items, the latter comprising ingested stones as
well as pieces of wood and leaves (Sabater-Pi 1985).
The majority of the arthropods were terrestrial taxa.
The presence of leaves, wood, and stones also suggests
a mainly terrestrial foraging mode. If the quality of the
riparian forests impacts prey quality and quantity, this
would likely impact the Goliath Frog populations as well.
Our observations on one particular frog highlight the
Amphib. Reptile Conserv.
Goliath Frog’s use of riverine forest habitats. In prima-
ry forest along Nkebe River, a large adult was found in
the forest leaf litter at about 14 m from the river. When
disturbed, the frog covered this distance with three long
jumps back to the river (also see Herrmann and Edwards
2006). In about 1 m water depth, the frog could then be
spotted in the slow flowing, clear water. Further distur-
bance (with the torch beam) triggered the frog to bury
itself deep in the sandy and leaf-littered river bottom un-
til it could not be seen anymore, a behavior also known
from its smaller congener, C. crassipes (Knoepffler
1985). Goliath Frogs are less active during the day, and
when encountered, they were usually found sun-basking.
When disturbed, the behavior was the same as during the
night, with the frog seeking shelter in the water or be-
neath the rocks it was sitting on.
Use of Microhabitats by the Different Age Classes
Our observations revealed that Goliath Frogs partition
microhabitats by age-class. Therefore, a range of dif-
ferent riverine habitat features is likely crucial for sup-
porting the full complement of life stages of this species.
Large adults predominately perched on rocks around wa-
terfalls and rapids, with individual separated by a con-
siderable distance (minimum 3-5 m), thereby providing
evidence for territorialism and site fidelity, as already
suggested by Sabater-Pi (1985). In contrast, subadults
were rarely found around waterfalls. They appeared fre-
quently on exposed, mid-stream rocks in the vicinity of
cascades and waterfalls. Finally, metamorphosing and ju-
venile frogs most often used rook pools along the river-
beds where the current was slower. There they could find
refuge in rock crevices when disturbed (Fig. 3C). Such
sections also comprise the breeding sites of the species
(Sabater-Pi 1985; Schafer et al. 2019). The reason for this
microhabitat partitioning is unclear. It may be a linked to
thermoregulation, with small juveniles avoiding colder
water, and/or predation pressure, including cannibalism.
Habitat segregation has been reported from juvenile/sub-
adult and adult European water frogs, Pelophylax spp., in
order to escape cannibalism (Gunther 1990).
Based on daytime observations, Sabater-Pi (1985)
estimated the territory sizes of 20 to 40 m?’ for Goliath
Frogs along the Mbia River. Our observations suggest
that Goliath Frogs use small core areas or territories for
sun-basking and shelter (200 m7), and larger areas (>
1,000 m7) for foraging. However, quantitative research
on this issue 1s lacking and ideally should be based on
radio-tracked individuals (e.g., Spieler 1997).
One surprising finding of this study was that the Goli-
ath Frogs showed no apparent impact from the contami-
nation with agrochemicals from neighboring plantations
(at least to the extent that it is represented in our study
sites; although, unfortunately, the composition and quan-
tity of agrochemical run-off in the streams is unknown).
On the Mpoula River, a large banana plantation that is
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Goliath Frog populations in Cameroon
regularly sprayed by airplane occurs just upstream from
where the Goliath Frogs were observed. In most of the
study areas, small to medium-sized plantations along the
rivers are run by local farmers. They typically use small
spraying pumps and regularly process chemicals in the
rivers, and the Goliath Frogs could still be found at these
sites. Our observations, as well as the information from
the frog hunters, revealed that populations around human
settlements are smaller and adult frogs are rarer. As habi-
tat degradation seemed to be of little influence, the Goli-
ath Frogs might be mainly impacted by targeted hunting
for food (locally) and trade.
Conservation Needs of the Goliath Frog
In order to detect potential declines, populations should
be monitored on a regularly basis. However, no national
monitoring program for Goliath Frog populations has
been implemented thus far. Long-term data collection
from specific sites across the Goliath Frog range would
be essential for detecting changes in the distribution and
local abundances of this species. Standard guidelines and
techniques for monitoring amphibian populations and
habitats are well-established (e.g., Heyer et al. 1994).
Potential monitoring methods for Goliath Frogs should
include time-area constrained searches in order to estab-
lish baseline data against which population changes with
time could be judged. The data presented here may serve
as a baseline for future studies. Based on our findings,
regular surveys carried out at night by walking along
pre-defined river routes would probably be the most effi-
cient method. The Nkongsamba area is especially critical
for monitoring because of the particularly intensive frog
collection for food, and the severe habitat degradation
overall. The Campo-Ma’an National Park and the Ebo
Forest National Park should likewise be considered for
monitoring, as they consist of areas with limited human
impact. Monitoring in different parts of the species range
will allow comparisons of the population trends within
and outside protected areas. This will also potentially
allow differentiation between the different threats such
as collection, habitat degradation and pollution, climate
change, and disease. Given that most amphibian popula-
tions naturally fluctuate (Pechmann et al. 1991), it would
be ideal to start an initial monitoring program for at least
five years.
Several key aspects of Goliath Frog ecology remain
to be investigated in order to better understand the
biology of this species (1.e., larval and juvenile survival
rates, growth rates, age at maturity, and the longevity
of adults). Such information may ultimately help in
setting up a conservation action and management plan
for this species. In parallel, additional short-term surveys
(detecting as many populations as possible) and long-
term monitoring data (to follow population trends) are
needed to fully interpret the Goliath Frog’s occurrences
and threat status. This study has shown that conservation
Amphib. Reptile Conserv.
efforts for the Goliath Frog do not need to be prioritized
for terrestrial habitat loss, but that hunting is clearly a
prominent factor affecting the persistence of robust
populations.
Acknowledgements.—We are very grateful to the many
people and organizations who made this work possible.
We are particularly grateful to Frogs & Friends e.V.,
Germany. The Cameroonian Ministry of Forestry and
Wildlife (MINFOF) provided permission for the study.
Our thanks are also extended to several organizations
which commissioned part of the study (Rainbow Consult,
Sylvatrop Consult, and Diggi Wels), and permitted the
use of the data. We would also like to thank the local
communities for permission to access their land. The
people whose assistance in the field was invaluable
include: Ekane Pierre, Andre, Blaise, Motto, Alex from
the Nkongsamba region, Patrick, Olivier from Akom II
and Blaise from around Ngo-Pem and Moukol, Ottou,
and Nyanga boy and Black Joe from the Yabassi area. We
thank the reviewers, in particular Thomas Doherty-Bone,
for their constructive critiques on previous drafts of the
manuscript.
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Amphib. Reptile Conserv.
Nono LeGrand Gonwouo is a Conservation Biologist and Senior Lecturer at the University
of Yaoundé I Cameroon. He holds a Ph.D. on the biogeography and ecology of reptiles
from the same University and has long term experience studying the herpetofauna of central
and West Africa, particularly in the fields of biodiversity, taxonomy, and ecology. He has
combined research and community engagement to leverage conservation outcomes for highly
threatened herpetofauna in Cameroon. Nono is a member of the IUCN SSC for Amphibians,
Reptiles and Chameleon Specialist Groups. His recent research interest focuses on the
responses of biodiversity to environmental change, with particular interest in the distributions
and dynamics of endemic herpetofauna near their geographic range margins.
Marvin Schafer is a Ph.D candidate at Humboldt University Berlin, Germany working
within the group of M.-O. Rodel at the Natural History Museum in Berlin. Marvin has studied
biology and toxicology at the Master’s level, with a broad interest in ecology and physiology,
particularly of amphibians. For his Ph.D., he is researching chemical ecology in a group of
West African frogs. He has a keen interest in the natural history of Goliath Frogs, and was the
principal investigator on the recent paper on their nest building behavior.
Sedrick Junior Tsekané is currently enrolled as a Ph.D. student in the Department of Animal
Biology and Physiology, University of Douala, Cameroon, with research work focused on
the ecology of Goliath Frogs. Sedrick obtained a Master’s degree from the Laboratory of
Zoology, University of Yaoundé I, during which he studied certain aspects of the ecology
of Goliath frog tadpoles, and is co-author of a recent paper on the nest building behavior of
Goliath Frogs.
Mareike Hirschfeld is working as a scientist in the Collection Future department at the
Museum ftir Naturkunde Berlin, Germany. She studied Biology at the Universities of Marburg
and Wurzburg, Germany, and obtained her Ph.D. from the Humboldt University Berlin.
Mareike is interested in the ecology and taxonomy of West and Central African amphibians.
For her Doctoral thesis, she studied the amphibians of highland forests in Cameroon and
investigated their ability to cope with changes to their environment. Mareike is now leading
the science data management team at the Museum and is involved in institutional, national,
and international initiatives for opening up natural science collections to scientists and society
worldwide. As a Freelancer, Mareike supports the association Frogs and Friends and their
projects in Cameroon.
118 November 2022 | Volume 16 | Number 2 | e319
Amphib. Reptile Conserv.
Gonwouo et al.
Arnaud Marius Tchassem Fokoua recently obtained his Ph.D. on the ecology of
amphibians from the Laboratory of Zoology of the University of Yaoundé I, Cameroon.
Arnaud received his Bachelor’s degree at the same university, completing multiple research
projects in the domain of herpetology. His research focuses on the community ecology
and conservation of African amphibians, especially aiming to understand how altitude and
anthropogenic activities influence amphibian community composition.
Mark-Oliver Rédel works with his team at the Museum fiir Naturkunde, Berlin, Germany,
where he is the curator of herpetology. He has studied the systematics, taxonomy,
biogeography, and ecology of African amphibians for almost 30 years. With his group,
comprising students from around the world, he currently runs projects in Germany, Ecuador,
Guinea, Ivory Coast, Cameroon, and Mozambique. His special interest is on how species
and ecological communities react to environmental changes. He has authored or co-authored
about 400 scientific and popular publications, including several books.
119 November 2022 | Volume 16 | Number 2 | e319
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
16(2) [Taxonomic Section]: 120-132 (e320).
urn:Isid:zoobank.org:pub:7F752CB7-4667-46F5-A44E-E4D165D28CF4
Out of the Past: A new species of Tantilla of the calamarina
group (Squamata: Colubridae) from southeastern coastal
Guerrero, Mexico, with comments on relationships among
members of the group
‘Ricardo Palacios-Aguilar, *7Lydia Allison Fucsko, *Victor H. Jiménez-Arcos, *’Larry David Wilson,
and *Vicente Mata-Silva
'Museo de Zoologia “Alfonso L. Herrera” de la Facultad de Ciencias, Universidad Nacional Aut6noma de México, 3° Circuito Exterior s/n,
Coyoacan, CP 04510, MEXICO; Totlok A.C., C. P. 04350, Delegacién Coyoacdn, Ciudad de México, MEXICO *Department of Humanities and
Social Sciences, Swinburne University of Technology, Melbourne, Victoria, AUSTRALIA *Laboratorio de Herpetologia Vivario de la Facultad
de Estudios Superiores Iztacala, Universidad Nacional Auténoma de Mexico, Ay. de los Barrios 1, Tlanepantla, CP 54090, MEXICO “Centro
Zamorano de Biodiversidad, Escuela Agricola Panamericana Zamorano, Departamento de Francisco Morazan, HONDURAS; 1350 Pelican Court,
Homestead, Florida 33035-1031, USA *Department of Biological Sciences, The University of Texas at El Paso, El Paso, Texas 79968-0500, USA
Abstract.—A new species of Tantilla in the calamarina group from southeastern coastal Guerrero, Mexico is
described. This new species is part of a clade that contains T. calamarina, T. cascadae, T. ceboruca, T. coronadoi,
T. deppei, T. sertula, and T. vermiformis. All of these species are endemic to Mexico, except for T. vermiformis,
which is found along the Pacific coastal plain from El Salvador to northwestern Costa Rica. Members of this
group of Tantilla show varying adaptations to fossoriality, which might reflect their phylogenetic relationships.
Keywords. calamarina group, centipede snake, fossoriality, phylogenetics, Reptilia, taxonomy
Resumen.— Describimos una nueva especie de Tantilla del grupo calamarina de la costa sureste de Guerrero,
Mexico. Esta nueva especie forma parte de un clado que contiene a T. calamarina, T. cascadae, T. ceboruca, T.
coronadoi, T. deppei, T. sertula y T. vermiformis. Todas estas especies son endemicas de Mexico, excepto T.
vermiformis, que se encuentra a lo largo de la planicie costera del Pacifico desde El Salvador hasta el noroeste
de Costa Rica. Los miembros de este grupo de TJantilla muestran diversas adaptaciones a la fosorialidad, lo
que podria reflejar sus relaciones filogeneticas.
Palabras claves. Culebra ciempiés, fosorialidad, grupo calamarina, relaciones filogenéticas, Reptilia, taxonomia
Citation: Palacios-Aguilar R, Fucsko LA, Jiménez-Arcos VH, Wilson LD, Mata-Silva V. 2022. Out of the Past: A new species of Tantilla of the
calamarina group (Squamata: Colubridae) from southeastern coastal Guerrero, Mexico, with comments on relationships within members of the group.
Amphibian & Reptile Conservation 16(2) [Taxonomic Section]: 120-132 (e320).
Copyright: © 2022 Palacios-Aguilar et al. This is an open access article distributed under the terms of the Creative Commons Attribution License
[Attribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction
in any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced,
are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Accepted: 11 October 2022; Published: 12 November 2022
Introduction
A recent paper by Palacios-Aguilar et al. (2021) noted a
specimen of Zantilla from Guerrero that was collected
over acentury ago (BMNH 1906.6.1.241). This specimen,
a female clearly referable to the Tantilla calamarina
group (Wilson and Meyer 1981), was discussed by
Wilson and Mata-Silva (2014) and determined to be
either an atypical individual of Tantilla coronadoi or a
representative of an unnamed taxon. Palacios-Aguilar
et al. (2021) suspected the latter alternative because
the three hitherto known specimens of 7’ coronadoi are
consistent in key aspects of their scutellation, but they
also declined to name a new species based on specimen
BMNH 1906.6.1.241, which was collected in 1904 by
Hans Gadow and reported as Homalocranium miniatum
in his 1905 paper. According to Dixon et al. (2000), the
name H. miniatum is a synonym of 7: rubra.
Correspondence. ricardopalaciosaguilar@gmail.com (RPA), lydiafucsko@gmail.com (LAF), victorhja@iztacala.unam.mx (VHJA),
* bufodoc@aol.com (LDW), vmata@utep.edu (VMS)
Amphib. Reptile Conserv.
November 2022 | Volume 16 | Number 2 | e320
Palacios-Aguilar et al.
When the Palacios-Aguilar et al. (2021) paper
appeared, one author of this paper (LDW) contacted
the senior author and proposed reexamining the
BMNH specimen to determine whether its status could
be established more definitively, based on a modern
understanding of the content and relationships within the
Tantilla calamarina group. Consequently, the authors
of this paper decided to collaborate in an attempt to
determine on the status of this curious specimen, which
has been lying in anonymity since it was collected 118
years ago.
The first four words of the title of this paper (Out of
the Past) are used in reference to the period of time this
specimen, which now becomes the holotype of a new
species of Zantilla, has resided in the BMNH collection.
These words also refer to the period of time that has
elapsed since the person after whom this snake is being
named began her journey in 1956 to find freedom from
the tyranny in her homeland in her adopted land of
Australia. For aficionados of cinema, Out of the Past will
be recognized as the title of a well-regarded film noir, the
1947 work of French director Jacques Tourneur starring
Robert Mitchum, Jane Greer, and Kirk Douglas.
Materials and Methods
During the last five decades, author LDW has been
examining specimens of the genus Zantilla, resulting
in the publication of several taxonomic treatments and
species descriptions within this genus (e.g., Wilson and
Meyer 1981; Wilson 1999; Wilson and Campbell 2000;
Wilson and Mata-Silva 2014, 2015). While compiling
information for the first taxonomic study of the 7
calamarina species group (Wilson and Meyer 1981),
measurements and scale counts were obtained for the
specimen that now is the focus of this paper (BMNH
1906.6.1.241). Soon after that work started, the Senior
Curator of Reptiles at the Natural History Museum,
London, was contacted to obtain morphological data
on the specimen, as well as high quality photographs.
The photographs aided in making comparisons with the
representatives of the 7’ calamarina species group.
In addition to the aforementioned works on the genus
Tantilla, the comparisons in this paper benefitted from
examinations of more recent literature specifically
involving the calamarina species group (Canseco-
Marquez et al. 2007; Cisneros-Bernal et al. 2020;
Cruz-Saenz et al. 2015; Davalos-Martinez et al. 2021;
Palacios-Aguilar et al. 2021; Ramirez-Bautista et al.
2014; Rocha et al. 2016), as well from the examination of
comparative material housed at the Coleccién Nacional
de Anfibios y Reptiles (CNAR) and the Museo de
Zoologia “Alfonso L. Herrera,” Facultad de Ciencias
(MZFC), both at the Universidad Nacional Autonoma
de México. Scale counts and digital photographs of
specimens deposited in the herpetological collection of
the University of Texas at Arlington (UTA-R) were also
obtained. The measurements are indicated in millimeters,
and the ventral scales were counted following the
method proposed by Dowling (1951), with the segmental
counts referring to the sum of the ventrals + subcaudals,
excluding the cloacal scute.
Amphib. Reptile Conserv.
Results
After detailed comparisons of the BMNH specimen
with the pertinent published sources and specimens held
in scientific collections, we determined that BMNH
1906.6.1.241 does indeed represent a new species of the
genus Jantilla.
Tantilla carolina, new species
Figs. 1-2.
Suggested common name. Carolina’s Little Snake.
um:|sid:zoobank.org:act: B8520FC0-94E14A 6F-8312-F6D3EA3434EF
Holotype. BMNH 1906.6.1.241, an apparent subadult or
juvenile female from Tezonapan (= Tecoanapa), north of
Ayutla, Guerrero, Mexico, collected by Hans Gadow in
1904.
Diagnosis. Zantilla carolina is a member of the 7.
calamarina group (Table 1). This species differs from
Tantilla calamarina by the presence of more ventrals in
females (156 versus [hereinafter = vs.] 118-140), more
total segmental scales (194 vs. 146-179), a normally-
sized preocular scale in contact with the postnasal scale
(vs. a preocular with a tendency toward a decrease in size
to complete the loss of the scale), two postocular scales
(vs. one), seven supralabials (vs. usually six), a uniform
dorsal head color followed by two pale postparietal
spots (vs. a head pattern consisting of a spatulate dark
anterior extension of the middorsal dark stripe flanked by
Fig. 1. Dorsal (A), lateral (B), and ventral (C) views of the
head of the holotype of Zantilla carolina sp. nov. (BMNH
1906.6.1.241).
November 2022 | Volume 16 | Number 2 | e320
Anew Tantilla species in the calamarina group from Guerrero, Mexico
= — =t
) Se eee
Fig. 2. Dorsal view of the holotype of Zantilla carolina sp. nov. (BMNH 1906.6.1.241).
prominent pale narrow longitudinal markings confluent
with the pale postparietal spots), and a body pattern
involving a dark lateral stripe that does not extend to
the end of the body (vs. a dark brown lateral stripe on
rows 3 and 4 extending the length of the body). The new
species differs from Tantilla cascadae by the presence of
more ventrals in females (156 vs. 139-144), more total
segmental scales (194 vs. 176-192), seven supralabial
scales (vs. six), and the dorsum of the head without a
pattern but containing a pair of small pale postparietal
spots (vs. a spatulate dark anterior extension of the
middorsal dark stripe flanked by pale narrow longitudinal
markings confluent with pale postparietal spots, or
narrowly separated from the pale postparietal spots). The
new species differs from Tantilla ceboruca by lacking
a pattern and a pair of small pale postparietal scales
on the dorsum of the head (vs. a spatulate extension of
the middorsal dark stripe flanked by pale longitudinal
markings confluent with postparietal spots and extending
anteriorly along the sides of the parietal scales and
across the supraoculars and prefrontals to join on the
internasals), and a lateral portion of the head without
a pattern (vs. one having each supralabial with a white
border). The new species differs from Zantilla coronadoi
by the presence of fewer ventral scales (156 vs. 165—
178), fewer subcaudal scales (38 vs. 40-41), fewer total
segmental scales (194 vs. 205-219), the anterior and
posterior temporals 1n contact with one another (vs. those
two scales separated from one another by contact of the
7" supralabial and the parietal scale), and the dorsal
and lateral portions of the head lacking a pattern (vs. a
dorsal head pattern consisting of a spatulate dark anterior
extension of the middorsal dark stripe flanked by pale
anterior extensions of the dorsolateral ground color, and
a lateral head pattern consisting of supralabials with dark
upper and pale lower portions). The new species differs
from Tantilla deppei by the presence of fewer subcaudal
scales (38 vs. 43-50), fewer total segmental scales (194
vs. 196-214), and the dorsal and lateral portions of the
head lack a pattern and a pair of small pale postparietal
Amphib. Reptile Conserv.
spots (vs. a spatulate dark anterior extension of the
middorsal dark stripe flanked by pale anterior extensions
of a middorsally-divided pale nuchal band). The new
species differs from Tantilla sertula by the presence of
fewer ventrals in females (156 vs.161), more subcaudals
in females (38 vs. 30), more total segmental scales (194
vs. 191), and the dorsal and lateral portions of the head
lack a pattern (vs. a dorsal head pattern consisting of a
spatulate dark anterior extension of the middorsal dark
stripe flanked by prominent pale, narrow, longitudinal
markings confluent with pale postparietal spots). The
new species differs from Tantilla vermiformis by the
presence of more ventral scales in females (156 vs.
120-129), more subcaudal scales (38 vs. 19-24), more
total segmental scales (194 vs. 140-150), as well as by
the presence of a small pair of pale postparietal spots
confined to single scales (vs. a single pale spot crossing
both parietal scales).
Description of the holotype (Figs. 1-2). An apparent
subadult or juvenile female with 15 smooth dorsal scales
throughout the trunk, 156 ventrals, a divided cloacal
scute (= anal plate), 38 subcaudals, a total length of 112
mm, a tail length of 14 mm, and a tail/total length ratio
OF OI2S:
Nasal completely divided, posterior section in broad
contact with a single preocular on both sides of head; two
postoculars, approximately subequal in size; one anterior
and one posterior temporal, in contact with one another,
anterior temporal separating supralabials five, six, and
seven from parietal, posterior temporal shorter than
anterior temporal, approximately the shape of a dorsal
body scale, although somewhat larger; supralabials
7-7, the 1“ in contact with rostral, prenasal, postnasal,
and 2™ supralabial, the 2"? with postnasal, preocular,
and 3 supralabial, the 3 with preocular, orbit, and
4" supralabial, the 4" with orbit, lower postocular, and
5" supralabial, the 5" with lower postocular, anterior
temporal, and 6" supralabial, the 6" with 5" supralabial,
anterior temporal, and 7" supralabial, the 7 with the 6"
November 2022 | Volume 16 | Number 2 | e320
Palacios-Aguilar et al.
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November 2022 | Volume 16 | Number 2 | e320
123
Amphib. Reptile Conserv.
A new Tantilla species in the calamarina group from Guerrero, Mexico
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November 2022 | Volume 16 | Number 2 | e320
124
Amphib. Reptile Conserv.
Palacios-Aguilar et al.
supralabial, anterior and posterior temporals, and two
post-cephalic scales, with the 7" the largest; infralabials
6—6, with the 1* pair separated by contact of mental
and anterior chinshields, the first four in contact with
anterior chin shields, with the 4" largest; and anterior
chinshields larger than posterior pair.
In preservative, the dorsal and lateral portions of
the head are uniform dark brown, without a pattern
(Fig. 1). A pair of pale postparietal spots, pale yellow
in color, are present on the single scales located at the
juncture of the parietal and posterior temporal scales,
one each on either side of the head (Fig. 1). The dorsal
ground color in preservative is brown with a dark
brown middorsal stripe confined to the middorsal scale
row, which extends to the end of the tail, breaking up
into isolated dark spots, one per scale on the posterior
region of the body and tail (Fig. 2). The remainder of
the dorsum lacks a pattern. The venter is a uniform
(perhaps cream) color in preservative.
Distribution. Known only from the type locality
(Fig. 3). Tecoanapa is the seat of the municipality of
Tecoanapa in the Pacific lowlands of southeastern
Guerrero (coordinates 16°53’N, 99°24’W). Tecoanapa
is acity located on Mexico Highway 95, east-northeast
of Acapulco and south-southeast of Chilpancingo.
The town lies at an elevation of 431 m (http://
PueblosAmerica.com; accessed 30 March 2022).
Elevation (m):
MS 0-1,100
MM 1,101-2,200
(9) 2,201-3,300
GE 3,301-4,400
HS >4,400
100 200 300 400km
-108 -106 -104 -102 -100
The vegetation in the region consists of a mixture
of tropical deciduous forest (selva baja caducifolia),
oak forest (bosque de encino), and agricultural lands,
according to the available maps (CONABIO 1999).
Conservation assessment. The Environmental Vul-
nerability Score (EVS) for Tantilla carolina can be
calculated as 6 + 8 + 2 = 16, which places its score in
the middle of the high vulnerability category, as ex-
plained by Wilson et al. (2013).
Etymology. We are privileged to name this small
snake in honor of the Hungarian Freedom Fighter
Karolina Laszlo (Fig. 4), in recognition of her
dedication to the maintenance of human rights for
all peoples in the face of totalitarianism, beginning
with the Hungarian Revolution in 1956. As a young
woman, Karolina was forced to join the exodus of her
country people, in the company of her new husband,
a soldier, Ede Karoly Fucsk6, who bravely defied the
Hungarian dictatorship, communism, and the invading
Soviet army. Ede Karoly Udvarhely1 was adopted at
an early age, when his mother remarried and thus kept
the surname Fucsko. As the couple roamed through
several European countries, in search of a refuge from
the terror of oppressive political regimes, they escaped
to England before seeking asylum in Australia. Due
to unforeseen circumstances, however, the family of
Tantilla calamarina
Tantilla carolina 24
Tantilla cascadae
Tantilla ceboruca
Tantilla coronadoi
Tantilla deppei
Tantilla sertula
22
20
18
16
14
-98 -96 -94 -92
Fig. 3. Geographic distribution of the Zantilla calamarina group species in western Mexico. The black star represents
the type locality of Zantilla carolina sp. nov. described herein.
Amphib. Reptile Conserv.
125
November 2022 | Volume 16 | Number 2 | e320
A new Tantilla species in the calamarina group from Guerrero, Mexico
Key to the members of the Tantilla calamarina group
1. Anterior and posterior temporals separated by contact of 7" supralabial and parietal.................... T. coronadoi
Anterior and posterior temporals in contact, not separated by contact of 7" supralabial and parietal ................. 2
DPOStOC AMS ING Les soe Cie eee A he WE ee eh ON nia ee Ne OO BE Berg aptlensiaadte siecay aaaetden te T. calamarina
POSTOCUI ANSI Ont, elie Si, Re sett cn Sd sia AR Rt tie, tm tn Caley NEA ook 5 aide Mere Dace nie, San 8 ALND nash, # 2d 3
SsVentralsstewer than 30 ssubcaudalsitewer than-30).., 2.9.08 ods ele, ches, oA ale elie ads T. vermiformis
Ventrals;|30z0rmore<subcandals!S0:OraNOTe:, ac2.5 scree ne eens entesettr ll eed lege ee ES ete b eeelrnrerelalle 4 4
A MEA Sela a OG WOR... WE vee 2, OSS ER Eee SERA OE Bene pens en ln Od T. cascadae
NCHS SSO MOL ened. oon mre a ATs ee, Wenge, ete A 5 Wm ie WOE ce, ul i Wr OR Ores Amo 5, aw 5
SPB Eee thts Rae sit cl alee 0) @cas\cl ON Orc Mmee Ren cea he al tsa a OE leone ieee SLs Rn Ny Otte ae SRE le ey. Mlariedaen seme Roe ane, "ha 6
amie lreielles UISEA Se IMR, co: Rte ee ia BERT ec NTE ates 8 Al ce LR Pe A 8 ich Ne ae oR B Je fe
6. Dark lateral stripe on adjacent halves of rows 3 and 4.2.0... cece T. ceboruca
Darklateral:stripeon row S:OnOntOws:2 and gx soe he. wd feted et tet dS eee le Yen oy en eh leet Ay T. deppei
7. Dorsal head pattern consists of a spatulate dark anterior extension of the middorsal dark stripe occupying dorsum of
head, flanked by pale, narrow, longitudinal stripes broadly separated from pale postparietal spots occupying portions of
three dorsal scales immediately posterior to the posterolateral portion of each parietal scale.................. T. sertula
Dorsum of head without pattern, uniform brown in color; pale postparietal spots each confined to single postparietal scales
five later travelled back to Hungary, residing there
for several years before escaping again to Vienna,
Austria, then travelling to Italy, and from there they
journeyed to South Africa. There, they dared to oppose
the policy of apartheid but eventually, under duress,
had to flee as interracial tensions escalated into further
hostilities and reprisals. Finally, the family found
relative solace in the democratic land of Australia,
where life remained challenging in such a strangely
beautiful land. During this long trek to find a life of
freedom, Karolina and Ede were accompanied by their
three children, John Edward, Stephen Charles, and a co-
author of this paper, Lydia Allison Fucsko. Therefore,
in Karolina’s honor, we named this snake Jantilla
carolina sp. nov., with a reference to the meaning of
the name Carolina in Spanish as “the prettiest woman
of the town,” an apt descriptor for this truly lovely,
indomitable, and spirited lady whose humanitarian
efforts continue to inspire future generations.
a a ed einen eT
eg Na Dee ee
Fig. 4. (Left) The Hunga
Amphib. Reptile Conserv.
Le PM cl Ta ee! UR Risa Re Beary ns Bhan T. carolina sp. nov.
Discussion
Wilson and Meyer (1981: 2—3) established a case for
the recognition of the Zantilla calamarina group, which
they maintained consisted of four species, including 7°
calamarina, T. coronadoi, T: deppei, and a species they
described as new, T° cascadae. The justification for their
recognition of the calamarina group primarily was based
on a “similarity in head pattern.” Wilson and Meyer
(1981: 2) detailed that all four species they recognized
as part of this group “have the central portion of the
parietals covered with a spatulate anterior extension of
the middorsal dark stripe, which continues anteriorly to
cover the remainder of the head. On either side of this
central head mark is a postparietal pale spot that usually
grades posteriorly into the ground color of the dorsolateral
field [...] and, in its best-developed state, connects
~ = ote ust a ~ Ap A
rian Freedom Fighters, Karolina and Ede Karoly Fucsk6, in Hyde Park, London, England,
1958. (Right) Enduring photographs of Karolina and Ede Karoly Fucsko.
November 2022 | Volume 16 | Number 2 | e320
Palacios-Aguilar et al.
anteriorly with a narrow extension that proceeds along
the side of the parietal, over the supraocular and onto the
side of the prefrontals and internasals.” The members of
this group also exhibit a dark middorsal stripe occupying
some portion of the middorsal scale row and, in some
cases, a portion of the adjacent dorsal scale rows.
In subsequent years, another species of Zantilla, T:
vermiformis, was allocated to the calamarina group
(Wilson 1999), This allocation, however, was questioned
by Holm (2008: 98), who stated that “[his] results [lead
him] to not include 7! vermiformis in the T. calamarina
group as suggested by Wilson et al. (1999) and Wilson
and Campbell (2000). Similarities between these taxa
may be due to convergent adaptations for fossoriality and
the dark vertebral line is a shared primitive trait.” Other
hypotheses worth testing when sufficient molecular
material becomes available would include whether 7.
vermiformis is more closely related to the members of
the 7: melanocephala group (Wilson and Mena 1980) or
to some other member or members of the genus not yet
identified.
In 2000, Wilson and Campbell described Tantilla
sertula based on a single specimen from Pacific coastal
Guerrero, Mexico, and allocated this species to the
calamarina group. A second specimen of this species
was documented from the coastal plain of Guerrero
by Canseco-Marquez et al. (2007). Thereafter, Rocha
et al. (2016) reported a third specimen of this species
from the lower foothills of the Sierra Madre del Sur
of southern Oaxaca. Finally, Canseco-Marquez et al.
(2007) described Tantilla ceboruca from southern
Nayarit, Mexico. These authors also placed this species
in the calamarina group.
Thus, with the description of 7. ceboruca in 2007,
the calamarina group was considered to consist of
seven species, including, in order of year of description:
T. vermiformis (Hallowell 1861), 7) calamarina (Cope
1866), 7’ deppei (Bocourt 1883), 7: coronadoi (Hartweg
1944), T. cascadae (Wilson and Meyer 1981), 7.
sertula (Wilson and Campbell 2000), and 7? ceboruca
(Canseco-Marquez et al. 2007). With the description
of 7: carolina, the genus Tantilla currently is known to
contain 68 species (The Reptile Database, http://www.
reptile-database.org/; accessed 15 May 2022).
Most species in the calamarina group are distributed
in the western portion of Mexico, from northern Sinaloa
to south-central Oaxaca, except for Tantilla vermiformis,
which is found along the Pacific coastal plain of Central
America from El Salvador to northwestern Costa Rica
(Wilson and Mata-Silva 2015; Antunez-Fonseca et al.
2020a). The northernmost-occurring and most widely-
distributed species in the group 1s 7: calamarina, which is
known from northern Sinaloa to south-central Guerrero,
including the Tres Marias Islands (Isla Maria Madre)
lying off Nayarit; the elevational range for this species
is from near sea level to 1,677 m asl. In comparison,
the remaining species in the group are narrowly
distributed, as follows: 7. cascadae (1,430-1,858 m
asl from south-central Jalisco to central Michoacan); 7.
ceboruca (1,233-—2,094 m asl from southeastern Nayarit
to north-central Jalisco); 7’ coronadoi (650—1,524 m asl
in northeastern and central Guerrero); 7. deppei (1,524—
Amphib. Reptile Conserv.
2,438 m asl in northern Morelos, northern Guerrero, and
northwestern Oaxaca); 7? sertula (near sea level487
m asl from northwestern Guerrero to south-central
Oaxaca); and 7. vermiformis (40-520 m asl from El
Salvador to northwestern Costa Rica).
One of the most obvious features of the species
presently allocated to the calamarina group is that
they show varying adaptations to a fossorial existence.
Ramirez-Bautista et al. (2014) developed a so-called
“index of fossoriality” to quantify the degree of
fossorial adaptation among the seven members of this
group, as then comprised, based on features of cephalic
scutellation and segmental counts. These features
were documented in Table 1 of that paper, converted
to character states that were placed in Table 2 of that
paper, which then were collated to produce an index of
fossoriality. The reader should refer to that paper for a
more thorough explanation of the index of fossoriality.
These authors concluded their analysis of fossoriality
in the calamarina group by stating (pp. 803-804) that
“low indices [of fossoriality] are found in the more
generalized calamarina group species, such as 7! sertula
and 7: deppei..., intermediate values are found in the
more adapted species, such as 7: ceboruca, T: coronadoi,
T. cascadae, and T: vermiformis..., and high indices in
the most adapted species, 1.e., 7’ calamarina and G.
redimitus.”
Using the methodology employed by Ramirez-
Bautista et al. (2014), we determined the index of
fossoriality for Zantilla carolina as follows:
Preocular present—1
Preocular in contact with postnasal—1
Preocular fused with prefrontal and supraocular—1
Number of postoculars—1
5" supralabial separated from parietal—1
6" supralabial fused with anterior temporal—1
7" supralabial and parietal in contact—1
Number of supralabials—1
Supralabials entering orbit—1
Number of ventrals—1
Number of subcaudals—2
The sum of these 11 character-values for T. carolina is 12,
the same value as calculated for 7. sertula by Ramirez-
Bautista et al. (2014). This index of fossoriality is the
lowest among the members of the calamarina group,
in which the indices range from 12 to 24 (including
that for Geagras redimitus, which was included in the
calamarina group by Holm [2008]). This determination
indicates that 7. carolina and T: sertula are the two
members of the group that are the least adapted for a
fossorial existence. The indices of fossoriality for
the other species involved, in increasing value, are as
follows: T. deppei (13); T. ceboruca and T. coronadoi
(both 14); 7! cascadae (15); T: vermiformis (16); T.
calamarina (21); and G. redimitus (24).
As noted by Ramirez-Bautista et al. (2014), the
index of fossoriality is not intended to elucidate the
phylogenetic relationships within the calamarina group,
but it is tempting to hypothesize that this index perhaps
is reflective of the phylogenetic relationships that could
November 2022 | Volume 16 | Number 2 | e320
Anew Tantilla species in the calamarina group from Guerrero, Mexico
be substantiated by a molecular analysis, should such an
analysis ever become possible. The timeline for such an
analysis 1s difficult to predict, especially because most of
the species involved are known from only a handful of
preserved specimens (or only one).
If and when a molecular analysis of the phylogenetic
relationships of this group of snakes becomes possible,
five questions of principal interest to answer would be the
following: (1) Is Geagras redimitus closely related enough
to the members of the Zantilla calamarina group to be
subsumed into this group, as per the conclusion of Holm
(2008)? (2) Is Tantilla vermiformis closely related enough
to the unquestioned members of the calamarina group to be
included within it, or do its closest relationships lie elsewhere
in the genus Zantilla? (3) Is Tantilla carolina closely related
enough to the unquestioned members of the calamarina
group to be included within 1t? (4) What are the phylogenetic
relationships of the nine species involved to one another?
and (5) What are the relationships of these species to the
other members of the genus Zantilla?
In their treatment of the 7Zantilla clade, Wilson and Mata-
Silva (2015) noted that the genus Zantilla contained 61
species at that point. With the description of Zantilla carolina,
the genus now contains 68 species, and it remains the
second largest genus of snakes in the Western Hemisphere
after Atractus (currently containing 146 species, according
to The Reptile Database, http://www. reptile-database.org/;
accessed 9 April 2022). Only one other snake genus contains
more species than Zantilla, the Old-World genus Oligodon
(presently consisting of 88 species, according to The Reptile
Database, http://www.reptile-database.org/; accessed 9
April 2022). The seven species of Zantilla described since
the Wilson and Mata-Silva (2015) paper was published
are (listed alphabetically): 7’ berguidoi Batista et al. 2016;
T. excelsa McCranie and Smith 2017; 7’ gottei McCranie
and Smith 2017; 7 /ydia Antunez-Fonseca et al. 2020b; 7°
stenigrammi McCranie and Smith 2017; and 7 tiasmantoi
Koch and Venegas 2016. Six of these seven species are
allocated to the Yantilla taeniata group. The remaining
species (7? Hiasmantoi) was not placed in a species group by
the original authors, but its unusual pattern of dark banding
on a pale ground color might suggest that this species is
allied with another South American species that sometimes
is banded, 7’ semicincta (Wilson 1976).
In the last two decades, about 40 new species of snakes
have been described from Mexico, including four that are
known to occur on the Pacific Coastal Plains (PCP), where
the holotype of 7) carolina was obtained (1.¢., Zantilla
sertula Wilson and Campbell 2000; Thamnophis rossmani
Conant 2000; Coniophanes michoacanensis Flores-Villela
and Smith 2010; and Rhadinella dysmica Campillo et al.
2016). Surprisingly, this region has received less attention
when compared with the adjacent elevations of the Sierra
Madre del Sur, and few collections have been made in
this area (e.g., Holman 1964; Liner and Dundee 1969;
Saldafia de La Riva and Pérez Ramos 1987; Schatti and
Stutz 2016). Recent scattered reports have recorded several
species of snakes with hitherto restricted ranges that were
found hundreds of kilometers from their previously known
localities (Siria-Hernandez et al. 2006; Rocha et al. 2016;
Blancas-Hernandez et al. 2019; Arrazola-Bohorquez and
Palacios-Aguilar 2022), which apparently reinforces the
Amphib. Reptile Conserv.
proposal of Flores-Villela and Goyenechea (2001) that this
province serves both as a corridor for lowland species and
as a barrier for montane species of amphibians and reptiles.
Nonetheless, there are areas of the PCP where interesting
sets of microendemic species of reptiles are found (Palacios-
Aguilar et al. 2018), and overall, a high proportion of
endemic amphibians and reptiles occur in this province
(Johnson et al. 2017), which might suggest that it 1s not
as homogeneous as previously considered and that biotic
subprovinces may be present within it. Detailed, objective
biogeographic studies are necessary to test this hypothesis,
now that novel information on species previously known
from few localities or specimens is emerging.
Incomplete information and sampling biases affect what
we know about biodiversity. The biodiversity shortfalls such
as the Wallacean, the limited knowledge on the distribution
of species, and the Linnean, the proportion of undescribed
diversity, are two of the most important limiting factors
that beset our understanding and knowledge of the natural
world (Hortal et al. 2015). The effect that roads have on
the vertebrate fauna of southern Mexico has been reported
(Bojorquez-Tapia et al. 1994, 1995), and it is expected to
diminish progressively as collectors and researchers reach
previously inaccessible regions. In recent decades, it has
been reported that species extirpations and extinctions
have been augmented in an unprecedented way due to the
negative impact of human activities (Dirzo et al. 2014).
This highlights the importance of having accurate and
reliable sources of biological information, such as scientific
collections, that help us to diminish the effects of these
shortfalls and allow us to provide an accurate image of how
many, where, and which species exist in a particular region.
Also, one should note that not all taxa have the same rate of
species descriptions, and particularly in snakes, the shelf-life
that specimens have from their collection to their description
ranges from 0 to 146 years (mean 7.5 years, Guedes et al.
2020), inasmuch as the conduct of taxonomic treatments is
one of the factors that boosts species discovery. The new
species described herein has “awaited” being described for
118 years, which makes it a snake species with one of the
longest shelf lives, and thanks to the conduct of a taxonomic
treatment and the adequate housing of the individual in one
of the world’s largest scientific collections, it was possible to
identify it as a novel taxon. We can only imagine how many
more species in Mexico (and the world) probably are now
on a shelf awaiting discovery.
Acknowledgments.—We are indebted especially to Patrick
Campbell, who made it possible for us to obtain basic
morphological data on the BMNH specimen we designated
as the holotype of the new species of Zantilla described
herein. We also wish to thank Louis W. Porras for assistance
in securing the necessary literature for use in this paper, and
for his masterful review of our work. We also are grateful to
David Lazcano for his review, which greatly improved our
manuscript. We also thank Marisol Gomez for her invaluable
help in editing the figures. Luis F. Nieto Toscano, Gregory G.
Pandelis (UTA), Victor H. Reynoso (CNAR), Oscar Flores-
Villela, and Leticia M. Ochoa-Ochoa (MZFC) provided
access, associated data, photographs, and measurements
of the specimens under their care or those with which they
were working.
November 2022 | Volume 16 | Number 2 | e320
Palacios-Aguilar et al.
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Amphib. Reptile Conserv.
Palacios-Aguilar et al.
Ricardo Palacios-Aguilar is a Mexican biologist who earned his Bachelor’s degree at the Facultad
de Estudios Superiores Iztacala and his Master’s degree at the Museo de Zoologia “Alfonso L.
Herrera,” Facultad de Ciencias, both located at the Universidad Nacional Autonoma de México
(UNAM). Ricardo’s main interests are biogeography, evolution, and systematics using amphibians
and reptiles as a model, especially those of the Neotropics. Currently, he is a Professor at Facultad
de Ciencias, UNAM, where he teaches courses in biogeography and evolution.
Lydia Allison Fucsko, who resides in Melbourne, Australia, is an environmental activist and
amphibian conservationist. As a photographer with international publications, she has taken
countless amphibian photographs, including photo galleries of frogs mostly from southeastern
Australia. Lydia has a Bachelor of Humanities from La Trobe University (Bundoora, Victoria,
Australia) and a Diploma in Education from the University of Melbourne (Parkville, Victoria,
Australia). She has postgraduate diplomas in computer education and in vocational education and
training from the University of Melbourne (Parkville). Additionally, Lydia has a Master’s Degree
in Counseling from Monash University (Clayton, Victoria, Australia). She received her Ph.D. on
Environmental Education, in which she promoted habitat conservation, species perpetuation, and
global sustainable management, from Swinburne University of Technology (Hawthorn, Victoria,
Australia), while being mentored by the late Australian herpetologist and scholar Dr. Michael James
Tyler (Order of Australia recipient). Lydia is a sought-after educational consultant, with academic
interests that include: clinical psychology, focusing on psychopathology; neuroscience and empathy;
environmental education for sustainable development; sentient ecology; academic writing; and
creative writing, which includes poetry and creative non-fiction books for children and young
adults. She also is the senior author (with Boria Sax) of a chapter in the 2019 Springer Encyclopedia
of Sustainability in Higher Education entitled “Learning Activities for Environmental Education
for Sustainable Development.” Recently, Lydia has co-authored an obituary of Jaime D. Villa, a
study of the introduced Mesoamerican herpetofauna, a treatment of conservation prospects of the
Mesoamerican salamander fauna, papers on the herpetofauna of Veracruz and Querétaro, Mexico,
a review of the book Advances in Coralsnake Biology, and a study on the biological and cultural
diversity of Oaxaca, Mexico, among several other academic papers. In 2020, the species Tantilla
lydia, with the suggested common name of Lydia’s Little Snake, was named in her honor.
Victor H. Jiménez Arcos is an Associate Professor and the head of the Herpetology Lab, Facultad
de Estudios Superiores Iztacala, Universidad Nacional Autonoma de México. Through studies on
ecology and evolutionary biology, his laboratory focuses on understanding the evolution of the
phenotypic diversity of amphibians and reptiles, as well as the changes and losses of geographical
range associated with anthropogenic factors. He also works intensively with human communities
and the Mexican government agency in charge of Natural Protected Areas (CONANP) to achieve
the conservation of amphibian and reptile species in the short, medium, and long term.
Larry David Wilson is a herpetologist with lengthy experience in Mesoamerica. He was born
in Taylorville, Illinois, USA, and received his university education at the University of Illinois at
Champaign-Urbana (B.S. degree) and at Louisiana State University in Baton Rouge (M.S. and
Ph.D. degrees). He has authored or co-authored more than 465 peer-reviewed papers and books on
herpetology. Larry is the senior editor of Conservation of Mesoamerican Amphibians and Reptiles
and a co-author of seven of its chapters. His other books include The Snakes of Honduras, Middle
American Herpetology, The Amphibians of Honduras, Amphibians & Reptiles of the Bay Islands
and Cayos Cochinos, Honduras, The Amphibians and Reptiles of the Honduran Mosquitia, and
Guide to the Amphibians & Reptiles of Cusuco National Park, Honduras. To date, he has authored
or co-authored the descriptions of 75 currently recognized herpetofaunal species, and seven species
have been named in his honor, including the anuran Craugastor lauraster, the lizard Norops wilsoni,
and the snakes Oxybelis wilsoni, Myriopholis wilsoni, and Cerrophidion wilsoni, as well as the
oligochaete annelid Pheretima wilsoni and the coccidian parasite Caryospora wilsoni. In 2005,
he was designated a Distinguished Scholar in the Field of Herpetology at the Kendall Campus
of Miami-Dade College. Currently, Larry is a Co-chair of the Taxonomic Board for the website
Mesoamerican Herpetology.
131 November 2022 | Volume 16 | Number 2 | e320
Anew Tantilla species in the calamarina group from Guerrero, Mexico
Vicente Mata-Silva is a herpetologist originally from Rio Grande, Oaxaca, Mexico. His interests
include ecology, conservation, natural history, and biogeography of the herpetofaunas of Mexico,
Central America, and the southwestern United States. He received a B.S. degree from the Universidad
Nacional Autonoma de México (UNAM), and MLS. and Ph.D. degrees from the University of Texas
at El] Paso (UTEP). Vicente is an Assistant Professor of Biological Sciences at UTEP, in the Ecology
and Evolutionary Biology Program, and Co-Director of UTEP’s Indio Mountains Research Station,
located in the Chihuahuan Desert of Trans-Pecos, Texas, USA. To date, Vicente has authored or
co-authored over 100 peer-reviewed scientific publications. He also was the Distribution Notes
Section Editor for the journal Mesoamerican Herpetology, and is currently Associate Editor for the
journal Herpetological Review.
Appendix
Appendix I. In addition to published sources, the following comparative material was examined. All localities are in Mexico.
Tantilla calamarina. GUERRERO: Acapulco de Juarez, Viveros “El Huayacan,” La Poza (CNAR 29208—220, MZFC 13810-
815), Puerto Marquéz (CNAR 18729-735); Apaxtla de Castrejon, Tecolhuiztle (MZFC 2206); Arcelia, Campo Morado, Cafiada El
Limon (MZFC19793, 19798801), Campo Morado, Cafiada El Naranjo (MZFC 19795, 19797), Agua Zarca (MZFC 19794, 19796);
Eduardo Neri, San Miguel, Rancho del “Patillas” (MZFC 35822, 35826); Pilcaya, Parque Nacional Grutas de Cacahuamilpa (CNAR
28923924).
Tantilla ceboruca. JALISCO: Road between Copala and Ciudad Guzman, N of Nevado de Colima (UTA-R 58516).
Tantilla coronadoi. GUERRERO: Copalillo, 2.5 km NE Papalutla (MZFC 25507).
Tantilla deppii. OAXACA: 3.2 km SW of Yosocuno (MZFC 33820, 33822); San Pedro Nopala, Maguey Verde (MZFC 33747).
Amphib. Reptile Conserv. 132 November 2022 | Volume 16 | Number 2 | e320
Introductory page. Dryophytes eximius (Baird, 1854). The distribution of the Mountain Treefrog extends from south-central
Durango and the Sierra Madre Oriental in Tamaulipas southward to the Transverse Volcanic Range of Jalisco, Colima, Michoacan,
México, Morelos, Distrito Federal, Puebla, Hidalgo, and Veracruz, Mexico (Frost 2022). This individual was photographed in the
community of El Garbanzo, in the municipality of Irapuato. Wilson et al. (2013b) calculated its EVS as 10, placing it at the lower
limit of the medium vulnerability category. IUCN has considered its conservation status as Least Concern, but SEMARNAT has not
listed this species. Photo by Adrian Leyte-Manrique.
Amphib. Reptile Conserv. 133 November 2022 | Volume 16 | Number 2 | e321
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
16(2) [General Section]: 133-180 (e321).
The herpetofauna of Guanajuato, Mexico:
composition, distribution, and conservation status
‘Adrian Leyte-Manrique, ?Vicente Mata-Silva, 3Oscar Baez-Montes, ‘Lydia Allison Fucsko,
5Dominic L. DeSantis, Eli Garcia-Padilla, 7Arturo Rocha, *Jerry D. Johnson, ‘Louis W. Porras,
and ®Larry David Wilson
‘Laboratorio de Biologia, Investigacién y Posgrado, Instituto Tecnologico Superior de Salvatierra, Manuel Gomez Morin 300, Janicho, 38933,
Salvatierra, Guanajuato, MEXICO ?Department of Biological Sciences, The University of Texas at El Paso, El Paso, Texas 79968-0500, USA
>Departamento de Biotecnologia y Ambientales, Universidad Autonoma de Guadalajara, Av. Patria 1201, Lomas del Valle, 45129, Zapopan, Jalisco,
MEXICO *Department of Humanities and Social Sciences, Swinburne University of Technology, Melbourne, Victoria, AUSTRALIA °Department of
Biological and Environmental Sciences, Georgia College & State University, Milledgeville, Georgia 31061, USA °Oaxaca de Juarez, Oaxaca 68023,
MEXICO 17705 Wyatt Earp Avenue, Eagle Mountain, Utah 84005, USA *%Centro Zamorano de Biodiversidad, Escuela Agricola Panamericana
Zamorano, Departamento de Francisco Morazan, HONDURAS; 1350 Pelican Court, Homestead, Florida 33035-1031, USA
Abstract.—The herpetofauna of the Mexican state of Guanajuato currently consists of 24 anurans, three
salamanders, 71 squamates, and three turtles, for a total of 101 species. The members of the herpetofauna
are categorized among the three recognized physiographic regions of the Central Plateau, the Transmexican
Volcanic Belt, and the Sierra Madre Oriental. The total number of species in each of these regions ranges from
60 in the Central Plateau to 75 in the Sierra Madre Oriental. The numbers of species shared among these three
regions range from 44 between the Central Plateau and the Sierra Madre Oriental to 56 between the Central
Plateau and the Transmexican Volcanic Belt. A similarity dendrogram based on the Unweighted Pair Group
Method with Arithmetic Averages (UPGMA) demonstrates that of the three physiographic regions, the Central
Plateau (CP) and the Transmexican Volcanic Belt (TVB) cluster at the 0.84 level, and that the Sierra Madre
Oriental (SMO) clusters with the other two regions at the 0.65 level. This pattern was expected given that both
the CP and TVB are relatively large areas of similar size in the state that lie adjacent to one another; in contrast,
the SMO is the smallest region in the state and it is adjoined only to the CP region. The level of herpetofaunal
endemism in Guanajuato is relatively high, with 56 of the 101 species categorized as country endemics. The
distributional categorization of the entire herpetofauna includes 56 country endemics, 40 non-endemics, and
five non-natives. The 40 non-endemic species are placed into the following distributional categories: MXUS
(26), USCA (six), MXCA (four), MXSA (three), and USSA (one). The principal environmental threats to the
herpetofauna of Guanajuato are agriculture, industry, forestry, cattle production, and mining. We assessed the
conservation status of each native species by using the SEMARNAT, IUCN, and EVS systems, of which the EVS
system proved to be the most useful. We applied the Relative Herpetofaunal Priority method to determine the
rank order of the three regions, which indicates that the Transmexican Volcanic Belt is the region of greatest
conservation importance. Twenty-four natural protected areas have been designated in Guanajuato. Fourteen
of these areas lie within the Transmexican Volcanic Belt, which is fortunate from a conservation perspective. All
but four native species have been documented in these 24 areas. Finally, we provide a set of conclusions and
recommendations to help improve the future protection of the Guanajuato herpetofauna.
Keywords. Anurans, caudates, physiographic regions, protected areas, protection recommendations, squamates, turtles
Resumen.—La herpetofauna del estado mexicano de Guanajuato actualmente consiste de 24 anuros, tres
salamandras, 71 escamosos y tres tortugas, para un total de 101 especies. Los miembros de la herpetofauna
se clasifican en tres regiones fisiograficas reconocidas, que incluyen la Meseta Central, la Faja Volcanica
Transmexicana y la Sierra Madre Oriental. El numero total de especies en estas regiones consiste desde 60
en la Meseta Central hasta 75 en la Sierra Madre Oriental. El numero de especies compartidas entre estas tres
regiones va desde 44 entre el Altiplano Central y la Sierra Madre Oriental hasta 56 entre el Altiplano Central y
la Faja Volcanica Transmexicana. Un dendrograma de similitud basado en el Método de Grupos de Pares No
Ponderados con Promedios Aritméticos (UPGMA) demuestra que de las tres regiones fisiograficas, la Meseta
Central (CP) y la Faja Volcanica Transmexicana (TVB) se agrupan en el nivel .84 y que la Sierra Madre Oriental
(SMO) se agrupan con las otras dos regiones en el nivel .65. Se espera este patron dado que CP y TVB son
areas relativamente grandes de tamano similar en el estado y son adyacentes entre si; de lo contrario, la
Correspondence. aleyteman@gmail.com (ALM), vmata@utep.edu (VMS), biologo.oscar.baez@gmail.com (OBM),
lydiafucsko@gmail.com (LAF), dominic.desantis@gcsu.edu (DLD), eligarcia_18@hotmail.com (EGP), jjohnson@utep.edu (JDJ),
empub@msn.com (LWP), bufodoc@aol.com (LDW)
Amphib. Reptile Conserv. 134 November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
SMO es la region mas pequena del estado y esta unida solo a la region CP. El nivel de endemismo de la
herpetofauna en Guanajuato es relativamente alto, con 56 de las 101 especies categorizadas como endemicas
del pais. La categorizacion distribucional de toda la herpetofauna es la siguiente: 56 endemicas del pais, 40
no endemicas y cinco no nativas. Las 40 especies no endemicas se ubican en las siguientes categorias de
distribucion: MXUS (26), USCA (seis), MXCA (cuatro), MXSA (tres) y USSA (una). Las principales amenazas
ambientales son agricultura, industria, silvicultura, ganaderia y mineria. Evaluamos la conservacion de cada
especie nativa utilizando los sistemas de SEMARNAT, UICN y EVS, de los cuales el sistema EVS demostro
ser el mas utilitario. Se utilizo el metodo de Prioridad Relativa de la Herpetofauna para determinar el orden de
clasificacion de las tres regiones, y este metodo indico que la Faja Volcanica Transmexicana es la region de
mayor importancia para la conservacion. Todas menos cuatro especies nativas estan documentadas en estas
24 areas. Finalmente, brindamos un conjunto de conclusiones y recomendaciones destinadas a aumentar las
posibilidades para la futura proteccion de la herpetofauna guanajuatense.
Palabras Claves. Anuros, areas protegidas, caudados, escamosos, estatus de conservacion, recomendaciones de pro-
teccion, regiones fisiograficas, tortugas
Citation: Leyte-Manrique A, Mata-Silva V, Baez-Montes O, Fucsko LA, DeSantis DL, Garcia-Padilla E, Rocha A, Johnson JD, Porras LW, Wilson LD.
2022. The herpetofauna of Guanajuato, Mexico: composition, distribution, and conservation status. Amphibian & Reptile Conservation 16(2) [General
Section: 133-180 (e321).
Copyright: © 2022 Leyte-Manrique et al. This is an open access article distributed under the terms of the Creative Commons Attribution License
[Attribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction
in any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced,
are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Accepted: 10 October 2022; Published: 30 November 2022
“Tf we keep trashing our unique ecosystems, how much
longer with they be able to deal with wave after wave of
new challenges?”
Rick Shine (2018)
Introduction
The state of Guanajuato is located in central Mexico, at
the intersection of three major physiographic regions: the
Central Plateau, the Transmexican Volcanic Belt, and the
Sierra Madre Oriental. To the north, the state is bounded by
a sliver of Zacatecas and a large portion San Luis Potosi, to
the east by Querétaro, to the south by Michoacan, and to
the west by Jalisco. Guanajuato is the 22" largest state in
Mexico, with a surface area of 30,607 km/ (http://inegi.org.
mx/monografias/informacion/gto/; Accessed 18 February
2022). In 2020, the population of the state was 6,166,934,
which ranks sixth in the country, and the state’s population
density is 200 people/km?, which ranks fifth (http://inegi.
org.mx/monografias/informacion/gto/poblacion/default.
aspx; Accessed 25 May 2022).
Historically, Guanajuato is an important place with
regard to the Mexican herpetofauna, since this state is
considered the birthplace for the formal study of these
ectotherms by the father of Mexican herpetology,
Alfredo Duges, who conducted the first studies on the
diversity of vertebrates, including aspects of their natural
history (Reynoso et al. 2012; Leyte-Manrique et al. 2015;
Flores-Villela et al. 2018). Dugés recorded 56 species
in the state, including 12 amphibians and 44 reptiles.
However, although Guanajuato has been important in the
Mexican herpetological literature, there is no species list
representing the current composition of its herpetofauna.
Amphib. Reptile Conserv.
In this regard, the study of Mendoza-Quiyano et al.
(2001), carried out in Sierra de Santa Rosa, is viewed
as the watershed work for formally reestablishing the
investigation of the herpetofauna found in this state.
Important recent works include Guia de los Anfibios y
Reptiles de Charco Azul, Xichi, Guanajuato (Leyte-
Manrique and Dominguez-Laso 2014), which provides
a list of 18 species. Subsequently, two studies in 2018
assessed the herpetofauna at a larger scale. Baez-Montes
(2018) reported a total of 86 species (21 amphibians
and 65 reptiles) living in natural protected areas, and
Arciga-Hernandez et al. (2018) reported 108 species (27
amphibians and 81 reptiles). The latter study was based
mostly on records from natural protected areas, but it
includes species present in the surrounding states that are
also potentially found in Guanajuato. Furthermore, areas
outside of the natural protected areas in Guanajuato,
both considerably undisturbed and disturbed (such as
agro-ecosystems), have been studied during the last six
years (Cadena-Rico et al. 2020; Leyte-Manrique et al.
2015, 2016, 2019, 2021; Letye-Manrique 2022). The
work of Leyte-Manrique et al. (2015) focused on the
entire herpetofauna of the state, from both historical
and contemporaneous perspectives, and discusses the
findings in 10 published papers. Herein, we provide an
updated assessment of the herpetofauna of Guanajuato.
Materials and Methods
Our Taxonomic Position
In this contribution we follow the taxonomic position that
was explained in detail in previous works on other portions
of Mesoamerica (Johnson et al. 2015a,b; Mata-Silva et al.
November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
2015; Teran-Juarez et al. 2016; Woolrich-Pifia et al. 2016,
2017; Nevarez-de los Reyes et al. 2016; Cruz-Saenz et al.
2017; Gonzalez-Sanchez et al. 2017; Lazcano et al. 2019;
Ramirez-Bautista et al. 2020; Torres-Hernandez et al. 2021;
Cruz-Elizalde et al. 2022; Barragan-Vazquez et al. 2022).
Johnson (2015a) can be consulted for a statement of this
position, with special reference to the subspecies concept.
System for Determining Distributional Status
The system developed by Alvarado-Diaz et al. (2013) for
the herpetofauna of Michoacan was applied here to ascertain
the distributional status of members of the herpetofauna
of Guanajuato. Subsequently, Mata-Silva et al. (2015),
Johnson et al. (2015a), Teran-Juarez et al. (2016), Woolrich-
Pifia et al. (2016, 2017), Nevarez-de los Reyes et al. (2016),
Cruz-Saenz et al. (2017), Gonzalez-Sanchez et al. (2017),
Lazcano et al. (2019), Ramirez-Bautista et al. (2020),
Torres-Hernandez et al. (2021), Cruz-Elizalde et al. (2022),
and Barragan-Vazquez et al. (2022) utilized this system,
which consists of three categories in the present paper: CE
= endemic to Mexico; NE = not endemic to Mexico; and
NN = non-native in Mexico.
Systems for Determining Conservation Status
To assess the conservation status of the herpetofauna of
Guanajuato, this study employed the three systems (-.e.,
SEMARNAT, IUCN, and EVS) used by Alvarado-Diaz
et al. (2013), Mata-Silva et al. (2015), Johnson et al.
(2015a), Teran-Juarez et al. (2016), Woolrich-Pifia et al.
(2016, 2017), Nevarez-de los Reyes et al. (2016), Cruz-
Sanchez et al. (2017), Gonzalez-Sanchez et al. (2017),
Lazcano et al. (2019), Ramirez-Bautista et al. (2020),
Torres-Hernandez et al. (2021), Cruz-Elizalde et al.
(2022), and Barragan-Vazquez et al. (2022). Detailed
descriptions of these three systems appear in the earlier
papers in this series, and are not repeated here.
The Mexican Conservation Series
The Mexican Conservation Series (MCS) was initiated
in 2013, with a study on the herpetofauna of Michoacan
(Alvarado-Diaz et al. 2013), as part of a set of five
papers designated as the “Special Mexico Issue” of
Amphibian & Reptile Conservation. The basic format
of the entries in the MCS was established in this paper,
i.e., an examination of the composition, physiographic
distribution, and conservation status of the herpetofauna
of a given Mexican state or group of states. Two
years later, the MCS was resumed with a paper on the
herpetofauna of Oaxaca (Mata-Silva et al. 2015), and
that year Johnson et al. (2015a) presented a paper on
the herpetofauna of Chiapas. In the ensuing year, three
entries in the MCS were published, on Tamaulipas
(Teran-Juarez et al. 2016), Nayarit (Woolrich-Pifia et
Amphib. Reptile Conserv.
al. 2016), and Nuevo Leon (Nevarez-de los Reyes et al.
2016). Three more entries were published the following
year, on Jalisco (Cruz-Saenz et al. 2017), the Mexican
Yucatan Peninsula (Gonzalez-Sanchez et al. 2017), and
Puebla (Woolrich-Pifia et al. 2017). These entries were
followed by an article on Coahuila (Lazcano et al. 2019)
and another on Hidalgo (Ramirez-Bautista et al. 2020).
In the most recent two years, papers on Veracruz (Torres-
Hernandez et al. 2021), Querétaro (Cruz-Elizalde et
al. 2022), and Tabasco (Barragan-Vazquez et al. 2022)
were published. Thus, this paper on the herpetofauna of
Guanajuato is the 15" entry in the MCS series.
Physiography and Climate
Physiographic Regions
The state of Guanajuato contains a diversity of
landscapes, flora, and fauna, which is found within
the three physiographic regions recognized here: the
Sierra Madre Oriental, the Central Plateau, and the
Transmexican Volcanic Belt.
Sierra Madre Oriental (SMO). The Sierra Madre
Oriental is a mountain chain located in the eastern portion
of Mexico, outlining the Gulf coastal region, from
Chihuahua (Parras), Coahuila, San Luis Potosi, Nuevo
Leon, Hidalgo, Veracruz, Puebla, Tlaxcala, Querétaro,
and Guanajuato, to the Zongolica region in Veracruz,
at elevations above 1,500 m (Morrone 2001; Chavez-
Cabello et al. 2011). The SMO is characterized by the
presence of a set of minor mountain ranges with folded
sedimentary and marine strata (e.g., limestone, shale, and
sandstone), which were formed during the Cretaceous-
Jurassic periods (Oliva-Aguilar 2012). The SMO is
associated with the Gulf of Mexico and it is connected
with the TMB and the CP, so is considered a province
of Neotropical origin given its temperate and semi-warm
climates that support most of the montane cloud forests
in the country, primarily in the states of Hidalgo, Puebla,
and Veracruz (Morrone 2001; Rzedowski 2006; Cruz-
Elizalde et al. 2022). Innortheastern Guanajuato, the SMO
spans elevations ranging from 1,300 to 2,600 m, within
the municipalities of San Luis de La Paz, Victoria, Xichu,
and Atarjea, which are embedded in the Sierra Gorda
and border the states of San Luis Potosi and Querétaro
(Oliva-Aguilar 2012). The SMO is characterized by a
temperate climate in the southern portion of the Sierra
Gorda, which supports pine and oak forests. To the north,
in the municipalities of San Luis de La Paz, Xichu, and
Victoria, this region is characterized by a semi-warm
tropical climate and contains low tropical forest such
as in Xichu, which is influenced by the Gulf of Mexico
physiographic region, an area that contains the Rio Santa
Maria as one of the main tributaries (Rzedowski 2006;
INEGI 2009; Cruz-José et al. 2012; Oliva- Aguilar 2012).
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
No. 1. Anaxyrus compactilis (Wiegmann, 1833). The
distribution of the Plateau Toad is widely separated into
three populations: (1) the northern Sierra Madre of western
Chihuahua; (2) the eastern and western slopes of the Sierra
Madre in southern Durango and adjacent western Zacatecas;
and (3) south-central Zacatecas and the plateau of Jalisco and
Aguascalientes eastward to Tlaxcala and Puebla (Frost 2022).
This individual came from El Garbanzo, in the municipality
of Irapuato. Wilson et al. (2013b) ascertained its EVS as 14,
placing it at the lower limit of the high vulnerability category.
IUCN has judged its conservation status as Least Concern,
but SEMARNAT has not listed this species. Photo by Adrian
Leyte-Manrique.
No. 2. Anaxyrus punctatus (Baird and Girard, 1852).
The distribution of the Red-spotted Toad extends from
“southeastern California through southern Nevada and
southern Utah to southwestern and southeastern Colorado
(excluding high elevations) and southwestern Kansas
(USA), thence south to southern Baja California, Sinaloa,
Aguascalientes, Jalisco, Guanajuato, San Luis Potosi, Hidalgo,
and Tamaulipas (Mexico)” (Frost 2022). This individual came
from El Garbanzo, in the municipality of Irapuato. Wilson et
al. (2013b) calculated its EVS as 5, placing it in the lower
portion of the low vulnerability category. IUCN has considered
its conservation status as Least Concern, but SEMARNAT has
not listed this species. Photo by Maria del Carmen Mendoza-
Portilla.
No. 3. Jncilius occidentalis (Camerano, 1879). The Pine
Toad is a Mexican endemic species distributed from “the
mountains of northern Durango southward over much of the
Mexican Plateau and the Transvolcanic Belt” (Lemos-Espinal
and Dixon 2013: 39). This individual was encountered at El
Copal, in the municipality of Irapuato. Wilson et al. (2013b)
calculated its EVS as 11, placing it in the lower portion of
the medium vulnerability category. IUCN has considered its
conservation status as Least Concern, but SEMARNAT has
not listed this species. Photo by Adrian Leyte-Manrique.
Amphib. Reptile Conserv.
No. 4. Craugastor augusti (Duges, 1879). The distribution of
the Common Barking Frog extends from “Arizona to Texas in
the United States, and in Mexico from Sonora to Oaxaca, and
from Chihuahua, Coahuila, Nuevo Leon, and Tamaulipas to
Puebla” (Lemos-Espinal and Dixon 2013: 42). This juvenile
was found at Urirero, in the municipality of Salvatierra. Wilson
et al. (2013b) calculated its EVS as 8, placing it in the upper
portion of the low vulnerability category. IUCN has evaluated
its conservation status as Least Concern, but SEMARNAT has
not listed this species. Photo by Adrian Leyte-Manrique.
November 2022 | Volume 16 | Number 2 | e321
The herpetofauna o
Central Plateau (CP). The Central Plateau is located
in the north-central portion of Mexico, in a region
known as the Mexican Altiplano (= high plateau),
which is characterized by its semi-desert environment
with a Nearctic influence (Morrone 2001; Nieto-
Samaniego et al. 2005). The CP includes portions of the
states of Chihuahua, Coahuila, Durango, Guanajuato,
Hidalgo, Jalisco, Mich-oacan, Puebla, Querétaro, San
Luis Potosi, Tlaxcala, and Zacatecas (Cruz-Elizalde
et al. 2022). The elevation in this region ranges from
1,700 to 4,000 m. To the south, it is delimited by the
Rio Balsas depression, to the east by the Sierra Madre
Oriental, to the west by the Sierra Madre Occidental,
and to the north this region is influenced by the arid
areas of the Chihuahuan Desert. Its largest hydrological
basin is the Lerma-Santiago system (CONABIO
2008; Dominguez-Dominguez and Pérez-Ponce de
Leon 2009). This region comprises most of northern
Guanajuato, and is characterized by underground
aquifers and elevations above 2,000 m (e.g., the Sierra
de Guanajuato). In addition, the CP is composed of
wide plains interrupted by isolated volcanic mountains
and small mountain ranges (INEGI 2009; Cruz-José et
al. 2012), such as the Sierra Gorda with its intricate
topography of volcanic origin (Olivar-Aguilar 2012).
The municipalities located in the CP are the northern
portions of Leon, Guanajuato, Juventino Rosas,
Celaya, and Apaseo El Grande; the southern portions
of Xichu, Victoria, and San Luis de la Paz; as well
as Comonfort, Dolores Hidalgo, Doctor, Mora San
Miguel de Allende, San José Iturbide, Santa Catarina,
and Tierra Blanca (INEGI 2009). Geologically, this
region contains the oldest rocks in the state, which
are metamorphic rocks from the Triassic-Jurassic
period. Importantly, the plains and valleys seen in
this physiographic region today were formed during
the Quaternary (INEGI 2009). To the south, the CP is
delimited to by the Transmexican Volcanic Belt, and
to the east by the Sierra Madre Oriental (INEGI 2009;
Oliva-Aguilar 2012).
Transmexican Volcanic Belt (TMB). The
Transmexican Volcanic Belt is an arc of volcanic
mountain ranges (Pico de Orizaba is the highest peak, at
5,636 m asl) that extend across central-southern Mexico
f Guanajuato, Mexico
from Nayarit (Bahia de San Blas) and Jalisco (Bahia
Banderas) eastward in the direction of Veracruz to reach
the coast of the Gulf of Mexico; and this belt extends
for about 1,000 km from west to east, and from 80 to
230 km from north to south (GOmez-Tuena et al. 2005;
Ferrusquia-Villafranca 2007). Based on its geology and
tectonics, the TMB is divided into three regions: the
western portion includes the coastal area from the Gulf
of California to Nayarit and Jalisco; the central portion
contains the Taxco-San Miguel de Allende fault system;
and the eastern portion extends in the direction of the
Gulf of Mexico and has elevations ranging from 1,300
to 3,000 m (Gomez-Tuena et al. 2005).
The TMB covers approximately 45% of the state
of Guanajuato (portions in the central and southern
parts of the state), and is characterized by the presence
of volcanic mountains, calderas, and plains formed
by deposits, with El Bajio consisting of a mosaic of
landscapes that include alluvial plains, steep mountain
ranges, plains, hills, and lakes, including one of the
highest elevations of 3,110 m asl at Cerro de Los
Agustinos (Oliva-Aguilar 2012; CONABIO 2008).
The TMB crosses the southern part of the state from
the borders with Jalisco, Michoacan, and Querétaro;
the dominant climate in this physiographic region is
semi-arid, with temperatures ranging from 15 to 20 °C
(INEGI 2009). One of the main tributaries is the Rio
Lerma, which crosses this region from south to west,
in addition to other bodies of water, such as Laguna de
Yuriria (Walter and Brooks 2009). The municipalities
in the TMB are Huanimaro, Pénjamo, Cueramaro,
Abasolo, Pueblo Nuevo, Irapuato, Villagran, Romita,
Silao, Coroneo, Acambaro, Jerécuaro, Tarandacuao,
Santiago Maravatio, Salvatierra, Tarimoro, Apaseo El
Alto, Jaral del Progreso, Valle de Santiago, and those
that border the CP to the south including Apaseo El
Grande, Leon, Celaya, Juventino Rosas, and Salamanca.
Climate
Temperature. Table 1 shows the monthly minimum,
mean, and maximum temperatures for each of the three
recognized physiographic regions in Guanajuato based
on the data for numerous localities in each region (37
in the Central Plateau, 68 in the Transmexican Volcanic
Table 1. Monthly minimum, mean + SD (in parentheses), maximum, and annual temperature data (in °C) for the three physiographic
regions of Guanajuato, Mexico. Data were taken from the Network of Climatological Stations (CONAGUA 2021).
Physiographic
i Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Annual
region
Ceitral Plateau 10.1 11.8 13.9 16.3 17.1 16.6 16.1 16.5 15.6 13.8 12.5 11.3
(n= 37) (12.541.2) 13.941.2) (16.341.2) (18.64+1.2) (20.0+1.2) 19.5+1.2) (184+1.2) (18.3+1.2) (17.7#1.2) (16.2+41.2) 4.5+1.1) 13.041.1) 16.6
15.7 17.1 19.4 21.5 22.6 22.0 20.8 20.8 20.2 18.8 17.2 16.1
Transmexican 539 ‘ : 11.2 13.8 4.9 13.7 13.4 11.2 8.4 .
Volcanic Belt (14.541.5) (15.94£1.6) (18.141.6) (20.4£1.5) (22.041.5) (21.6+41.4) (20.3+41.3) (19.64£1.3) (196+4£1.3) (18.341.4) (16541.4) (15.041.5) 18.5
(n = 68) 17.1 18.2 20.7 23.0 24.5 23.6 22.2 21.6 21.6 20.3 18.8 17.8
Sierra Madre 15.9 17.3 20.8 23.2 24.7 24.1 22.9 22.7 21.4 19.4 17.6 15.6
Oriental (16.740.9) (18.4+1.2) (21.741.2) (24.1413) (25.741.3) (25.0+£1.2) (23.8+1.3) (23.741.5) (22.5+1.5) (20.741.5) (18.941.1) (17.0+41.5) 21.5
(n=3) 17.7 19.7 23.1 25.8 27.1 26.3 25.2 25.4 24.2 22.3 19.8 18.6
Amphib. Reptile Conserv.
138
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
a Gai 7 Or e
on ; i i toe a “ - ~'_* ‘ ,
No. 5. Craugastor occidentalis (Taylor, 1941). The distribution
of Taylor’s Barking Frog is from “western Michoacan,
Colima, and northeastern Jalisco west and north to southern
Zacatecas and southern Sinaloa, Mexico” (Frost 2022). This
individual was found at Area Natural Protegida Las Musas,
in the municipality of Manuel Doblado. Wilson et al. (2013b)
determined its EVS as 13, placing it at the upper limit of
the medium vulnerability category. IUCN has assessed its
conservation status as Data Deficient, but SEMARNAT has
not listed this species. Photo by Adrian Leyte-Manrique.
No. 7. Hypopachus variolosus (Cope, 1866). The distribution
of the Mexican Narrow-mouthed Toad is in southern Texas
(USA), southern Sonora and adjacent southwestern Chihuahua
(Mexico) southward in the lowlands and foothills (including
the Balsas Depression of southern Mexico) to northern Costa
Rica, at elevations mostly below 1,600 m, as well as on Isla
Maria Madre in the Tres Marias Archipelago of Nayarit,
Mexico (Frost 2022). This individual came from El Potrero
within Area Natural Protegida Las Musas, in the municipality
of Manuel Doblado. Wilson et al. (2013b) estimated its EVS
as 4, placing it in the lower portion of the low vulnerability
category. IUCN has judged its conservation status as Least
Concern, but SEMARNAT has not listed this species. Photo
by Adrian Leyte-Manrique.
Amphib. Reptile Conserv.
ll w ita Na oe
No. 6. Dryophytes arenicolor (Cope, 1866). The distribution
of the Canyon Treefrog is in the mountainous and plateau areas
of the USA (southern Utah and southern Colorado southward
through eastern Arizona, western and northern New Mexico
eastward to about Las Vegas, and the Trans-Pecos region of
Texas), southward in Mexico to Michoacan, Colima, México,
Guerrero, Hidalgo, and Oaxaca (Frost 2022). This individual
was photographed in El Ocotero, in the municipality of Xichu.
Wilson et al. (2013b) calculated its EVS as 7, placing it in
the middle portion of the low vulnerability category. IUCN
has evaluated its conservation status as Least Concern, but
SEMARNAT has not listed this species. Photo by Adrian
Leyte-Manrique.
2 tg 3 j 7 ‘
ates oS: eee xt Bete Lae
No. 8. Lithobates berlandieri (Baird, 1859). The distribution
of the Rio Grande Leopard Frog ranges from “central and
western Texas and southern New Mexico (USA) through
eastern Chihuahua to central Veracruz and Hidalgo, Mexico;
introduced into the lower Colorado River and lower Gila
River drainages of Sonora and Baja California del Norte,
Mexico, and California and Arizona, USA” (Frost 2022). This
individual was found in Xichu, in the municipality of the same
name. Wilson et al. (2013b) calculated its EVS as 7, placing it
in the middle portion of the low vulnerability category. IUCN
has considered its conservation status as Least Concern, and
SEMARNAT as a species of Special Protection (Pr). Photo by
Adrian Leyte-Manrique.
November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
Table 2. Monthly and annual precipitation data (in mm) for the physiographic regions of Guanajuato, Mexico. Data were taken from the
Network of Climatological Stations (CONAGUA 2021). The shaded area indicates the months of the rainy season. The monthly values are
given as minimum, mean + SD (in parentheses), and maximum.
eee re Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Annual
——reerom
Central Plat 4.6 3 : BS 51.6 44.9 2OF), 11.7
. ie 37) (14.5463) (10.843.8) (7.14+2.6) (14.844.4) (37.748.9) (87.5 + 26.3) (112.5 + 38.3) (95.5 428.9) (80.7+21.8) (36.4+10.6) (10.343.9) (75+43.3) 5153
42.2 17.6 11.5 27 551,7/ 158.8 213.2 154.5 127.8 TALI 21.2 19.1
Transmexican 4 1 0.6 3.6 12.8 61.1 99.7 82.2 54.7 17.8 3.5 232
Volcanic Belt (14.2445) (9543.1) (5.742.2) (9.7443) (29.8+47.0) (111.9+ 13.8)(158.2 + 21.9)(138.7 + 23.0)(107.2+ 17.4) (42.049.1) (9943.4) (6542.2) 642.9
(n= 68) 41.3 17.4 12.9 2531: 46.3 138.6 209.2 PED! 159.1 68.9 21.5 13.2
Sierra Madre 13.2 10.7 6.1 23.3 AY) S) 74.8 86 92.6 102.4 Bow 11.4 7.7
Oriental (15.2+2.0) (11.0+04) (7841.8) (274+43.9) (39.74 10.3) (94.04 17.1) (115.0 + 35.9) (102.5 + 10.4)(121.6 + 20.1) (54.64 20.8) (15.343.4) (9.2423) 613.4
(n= 3) 17.2 11.4 9.7 31 50.0 107.8 ISS 113.3 142.5 76.5 17.5 11.9
Belt, and three in the Sierra Madre Oriental). The mean
annual temperature is highest in the Sierra Madre Oriental
at 21.5 °C, followed by the Transmexican Volcanic Belt
at 18.5 °C, and is lowest in the Central Plateau at 16.6 °C.
In the Central Plateau the minimum monthly
temperatures range from 10.1 °C in January to 17.1 °C in
May, and the monthly maximum temperatures vary from
15.7 °C in January to 22.0 °C in June. In the Transmexican
Volcanic Belt, the minimum monthly temperatures range
from 5.9 °C in January to 14.9 °C in June, and the monthly
maximum temperatures from 17.1 °C in January to 24.5
°C in May. In the Sierra Madre Oriental, the minimum
monthly temperatures range from 15.6 °C in December to
24.7 °C in May, and the monthly maximum temperatures
from 17.7 °C in January to 27.1 °C in May.
The mean monthly temperatures in the Central Plateau
range from 12.5 °C in January to 20.0 °C in May; in the
Transmexican Volcan Belt these temperatures range from
14.5 °C in January to 22.0 °C in May; and in the Sierra
Madre Oriental they vary from 16.7 °C in January to 25.7
°C in May.
Precipitation. The precipitation regime typically seen in
tropical climates also occurs in Guanajuato. In general,
this regime is divided into a six-month wet season that
extends from May to October, and a dry season from
November to April (Table 2).
The mean monthly precipitation is highest in July in
the Central Plateau (51.6 mm) and the Transmexican
Volcanic Belt (99.7 mm), and in September in the Sierra
Madre Oriental (102.4 mm). Based on the mean monthly
figures during the rainy season, the percentages of the
annual precipitation are 76.4% in the Central Plateau,
86.0% in the Sierra Madre Oriental, and 91.4% in the
Transmexican Volcanic Belt. The annual rainfall 1s
lowest in the Central Plateau at 515.3 mm, followed by
the Sierra Madre Oriental at 613.4 mm, and highest is in
the Transmexican Volcanic Belt at 642.9 mm.
Composition of the Herpetofauna
Families
The species of amphibians and reptiles in Guanajuato
are arranged in 25 families, including seven families
Amphib. Reptile Conserv.
of anurans, two of salamanders, 14 of squamates, and
two of turtles (Table 3). No families of caecilians or
crocodylians are represented in the state. The total of 25
families comprises 45.5% of the 55 families represented
in Mexico (Ramirez-Bautista et al., In Press). Among
the nine families of amphibians, 56.7% (17) of the 30
species (Table 4) are in the families Bufonidae (five),
Hylidae (six), and Ranidae (six). Among the 16 families
of reptiles, 71.6% (53) of the 74 species (Table 4) are
in the families Phrynosomatidae (10), Colubridae (18),
Dipsadidae (11), Natricidae (nine), and Viperidae (five).
Genera
Fifty-four herpetofaunal genera are represented in
Guanajuato, including 11 genera of anurans, three of
salamanders, 38 of squamates, and two of turtles (Table
3). These 54 genera constitute 25.0% of the 216 known
from Mexico (Ramirez-Bautista et al., in press). Among
the amphibians (Table 4), the most speciose genera
are Eleutherodactylus (three), Dryophytes (three), and
Lithobates (six). Among the reptiles (Table 4), the most
speciose genera are Sceloporus (eight), Plestiodon
(three), Masticophis (three), Geophis (four), Rhadinaea
(three), Thamnophis (six), and Crotalus (five).
Species
The herpetofauna of Guanajuato consists of 101 species,
including 24 anurans, three salamanders, 71 squamates,
and three turtles (Table 3). Of these 101 species, 96 are
native to the state and five are non-native. Currently,
the numbers of native species in these groups are 255,
161, 920, and 53, respectively (Ramirez-Bautista et al.,
Table 3. Composition of the native and non-native herpetofauna
of Guanajuato, Mexico.
[subtotal [9a
Se OO
[tos set
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
200000 250000
2400000
A
Jalisco
2350000
2300000
2250000
Michoacan
0510 20 30 40 50Km
2200000
200000 250000
Fi
—
ge
In Press). The 96 native species in Guanajuato constitute
6.9% of the 1,395 native species in all of Mexico
(Ramirez-Bautista et al., In Press).
Patterns of Physiographic Distribution
We recognize three physiographic regions in Guanajuato
(Fig. 1), and the distribution of members of the
herpetofauna among these three regions is documented
in Table 4 and summarized in Table 5.
The numbers of species in the three physiographic
regions range from a low of 60 in the Central Plateau (CP)
to a high of 75 in the Sierra Madre Oriental (SMO). The
percentages of the entire state herpetofauna in each of the
three physiographic regions, 1n order of size, are (60/101)
59.4% (CP), (74/101) 73.3% (TVB), and (75/101) 74.3%
(SMO). The mean percentage of occupancy 1s 69.0%.
Among the amphibians and reptiles represented in
Guanajuato, the numbers of species are similar for the
two larger groups found in the Transmexican Volcanic
Belt (TVB) and the Sierra Madre Oriental (SMO), with
74 and 75 species, respectively. The numbers of species
in the four orders in these two regions are, respectively,
anurans (19 and 18), salamanders (two and three),
Amphib. Reptile Conserv.
300000
300000
. 1. Physiographic regions in the state of Guanajuato, Mexico.
350000 400000 450000
San Luis Potosi
Querétaro
Physiographic regions
= Central Plateau
|_| Transmexican Volcanic Belt
I) Sierra Madre Oriental
DO Water bodies
350000 400000 450000
squamates (50 and 51), and turtles (three and three).
The members of the Guanajuato herpetofauna occupy
from one to three of the three physiographic regions, as
follows: one (33; 32.7%); two (28; 27.7%); and three
(40; 39.6%). The average regional occupancy is 2.1,
indicating that each species inhabits about two-thirds of
the physiographic regions in the state.
A sizable portion of the herpetofauna occupies either
one or two regions (61 or 60.4% of the total of 101
species). As in most of the previous MCS studies, this
situation is of considerable conservation significance,
and we discuss it in detail in the section on conservation
status below.
The numbers of species inhabiting a single region
range from none in the Central Plateau (CP) to 22 in the
Sierra Madre Oriental (SMO). The intermediate number
of 10 is found in the Transmexican Volcanic Belt (TVB).
The 22 single-region species in the SMO are:
Incilius nebulifer
Rhinella horribilis
Rheohyla miotympanum*
Aquiloeurycea cephalica*
Abronia taeniata*
November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
Table 4. Distribution of the amphibians, squamates, and turtles of Guanajuato, Mexico, by physiographic region. Abbreviations are
as follows: CP = Central Plateau, TVB = Transmexican Volcanic Belt, and SMO = Sierra Madre Oriental. See text for descriptions
of these regions. * = species endemic to Mexico and ** = non-native species.
Sonnet
et SO | __resions occupied
De
PBufonidae(Sspecies) ————SSCSC~i SCSCidSSSC—S
[Rhine horribiis ———SSSSCSCi
[Craugastoridae @ species) Sd
| Crangastr occidemalis=® Od
[Eleutherodactylidae @epecies) |
Bleutherodactyhus angustdigitoran® |
THylidae (Gspecks)——SSCSCiS
[Drvophytes plicata® CdS
Rhealyla miooympamm™®
A
ST
[Microbylidae (Ispecis) ———SSCSC~i SCidSOC~id SSCS
Se
[tithobates bertandienh Cd dT Cd) Ud
cichobates catesbeiamis® ——SSCiSSSSCSCSC~‘iRSCSC‘ KCC
eS
tichobaves montenmae® dT dT Ud) Ud
EE SE
Lithobatesspectabits® ——=—SCSC~C~iSCSC‘ CdS
Seapiopoite pedi
ay
Co ae a Le!
[Ambystomatidae specie) |
ol.
—r
—
——a
AA
mi
NP WEN pe ]w
TPlethodontidae @ specie) SSC
Agulocuryoeacephalica® sd
CE
Tanguidae(@species) ——SSSCSC~iSSCidSSCSC—S
[Abroniataenita® Cd dT Cd
Ee SS
—-—
ee a ae a
[Dactyloidae Zspecis) ———SC—~i SSCidS SSCS
Norops nebulosus* — I
a
Ce
—-—
— |
dl
— |
Hemidactys renatus*® i
| Hemidactyis turciew** Si
Amphib. Reptile Conserv. 142 November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
Table 4 (continued). Distribution of the amphibians, squamates, and turtles of Guanajuato, Mexico, by physiographic region.
Abbreviations are as follows: CP = Central Plateau, TVB = Transmexican Volcanic Belt, and SMO = Sierra Madre Oriental. See
text for descriptions of these regions. * = species endemic to Mexico and ** = non-native species.
Physiographic region Number of
CP M regions occupied
eo)
Seeloparas aeneus* Sd
Sceloporas dugesif® ——SSSSCSCS~C~CSC‘“‘
| Sceloporus grammics SCS
Seeloporus sealaris® ——SSSCdS
Seeloparas spinosus® CdS
| Sceloporus torgaha® Od
[Seincidae Gspeciesy) SSCs SS
Plestiodon dugesi® Cd
Plestiodon ome* Cd
[Sphenomorphidae I specie) |
[Seincela sivicola® CdS
Teildae species) ———SSSCi
[Xantusfdae @epecies) ————SOSCi
‘Lepidophymagaigeae® Sd
Lepidophymaccewior® Od
[Boa imperator ———SSSC=*
+/+]+]+]+]+]+
+
Boa imperator
Colubridae (18 species) eo
Drymarchon melanurus
+
I
[Masticaphisschori ——SSCdS
| Onybelismicrophehatmas i
:
| Geophis dugesti® Cd
| Geophisarontals® Cd
| Geophispetersii® Cd
a
ceptodeira septenrionais Sid
Rhadinaca gaigeae® CdS
Amphib. Reptile Conserv. 143 November 2022 | Volume 16 | Number 2 | e321
=|
+ +] + + +] + + +/+ ]+]+]+ + +/+]+]+]+]4+]4+]+ - +|+ +/+ ]+ +/+] +1+/3
DN
The herpetofauna of Guanajuato, Mexico
Table 4 (continued). Distribution of the amphibians, squamates, and turtles of Guanajuato, Mexico, by physiographic region.
Abbreviations are as follows: CP = Central Plateau, TVB = Transmexican Volcanic Belt, and SMO = Sierra Madre Oriental. See
text for descriptions of these regions. * = species endemic to Mexico and ** = non-native species.
Physiographic region Number of
SMO regions occupied
“th 1
ine]
<
Taxa
Rhadinaea taeniata*
Elapidae (1 species)
Micrurus tener
Natricidae (9 species)
Adelophis copei*
Storeria dekayi
Storeria storerioides*
Thamnophis cyrtopsis
Thamnophis eques
Thamnophis melanogaster*
Thamnophis pulchrilatus*
Thamnophis scalaris*
Thamnophis scaliger*
Typhlopidae (1 species)
Virgotyphlops braminus**
Viperidae (5 species)
Crotalus aquilus*
Crotalus atrox
Crotalus molossus
Crotalus polystictus*
Crotalus scutulatus
Testudines (3 species)
Emydidae (1 species)
Trachemys scripta**
Kinosternidae (2 species)
Kinosternon hirtipes
Kinosternon integrum*
—
By}+]+ + +] + + - +/+]/+]+]+]+]+ + +
ws
Total (101 species) 4 5
Norops sericeus Craugastor occidentalis*
Holbrookia maculata Smilisca fodiens
Sceloporus variabilis Lithobates catesbeianus**
Plestiodon tetragrammus Gerrhonotus liocephalus
Scincella silvicola* Hemidactylus frenatus**
Lepidophyma gaigeae* Hemidactylus turcicus**
Lepidophyma occulor* Plestiodon dugesii*
Boa imperator Geophis dugesii*
Masticophis schotti Geophis petersii*
Pantherophis emoryi Adelophis copei*
Tantilla rubra
Geophis latifrontalis* Five of the 10 single-region TVB species are country
Leptodeira septentrionalis endemics (50.0%), two are non-endemics (20.0%), and
Rhadinaea gaigeae* the three indicated by double-asterisks are non-natives
Rhadinaea taeniata* (30.0%).
Storeria dekayi In summary, of the 32 single-region species, 15 are non-
Crotalus atrox endemics (46.9%), 14 are country endemics (43.8%), and
three are non-natives (9.4%). Of the three physiographic
As the single asterisks indicate country endemics, 13 regions, the SMO _ has considerable conservation
of the 22 SMO single-region species are non-endemics __ significance (but see section on Relative Herpetofaunal
(59.1%) and nine are country endemics (40.9%). Priority), inasmuch as it contains the highest numbers of
The 10 single-region species in the TVB are: species (75 of 101, or 74.3%), country endemics (37 of 56,
or 66.1%), and single-region species (22 of 32, or 68.8%).
Amphib. Reptile Conserv. 144 November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
No. 9. Lithobates neovolcanicus (Hillis and Frost, 1985). The
distribution of the Transverse Volcanic Leopard Frog is in pine-
oak forest and mesquite-grassland at elevations from 1,500 to
2,500 m along the southern edge of the Mexican Plateau in the
states of Guanajuato, Jalisco, Colima, Zacatecas, Michoacan,
México, and Hidalgo, Mexico (Frost 2022). This individual
came from San Nicolas de los Agustinos, in the municipality
of Salvatierra. Wilson et al. (2013b) calculated its EVS as
13, placing it at the upper limit of the medium vulnerability
category. IUCN has judged its conservation status as Near
Threatened, but SEMARNAT has not listed this species.
Photo by Adrian Leyte-Manrique.
No. 10. Spea multiplicata (Cope, 1863). The distribution of the
Mexican Spade-foot Toad is in southeastern Utah and southern
Colorado through western Oklahoma, Arizona, New Mexico,
and West Texas, in the USA, southward to the southern edge
of the Mexican Plateau as far as Nayarit, Guerrero, Oaxaca,
Hidalgo, and Tlaxcala, Mexico, at elevations from sea level to
2,743 m (Frost 2022). This individual came from La Torrecilla
within Area Natural Protegida Las Musas, in the municipality
of Manuel Doblado. Wilson et al. (2013b) reported its
EVS as 6, placing it in the middle of the low vulnerability
category. IUCN has not evaluated its conservation status,
and SEMARNAT has not listed this species. Photo by Adrian
Leyte-Manrique.
No. 11. Ambystoma velasci (Dugés, 1888). The Plateau
Tiger Salamander is a Mexican endemic occurring from
“northwestern Chihuahua south along the eastern slope of
the Sierra Madre Occidental and southern Nuevo Leon to
Hidalgo in the Sierra Madre Oriental, west to Zacatecas, and
south into the Transverse Volcanic range of central Mexico”
(Frost 2022). This individual was photographed in pine-oak
forest within the Reserva de la Bidsfera Sierra Gorda in the
community of El Ocotero, in the municipality of Xichu.
Wilson et al. (2013b) calculated its EVS as 10, placing it at
the lower limit of the medium vulnerability category. IUCN
has considered its conservation status as Least Concern, and
SEMARNAT as a species of Special Protection (Pr). Photo by
Adrian Leyte-Manrique.
Amphib. Reptile Conserv.
No. 12. Isthmura bellii (Gray, 1850). Bell’s Salamander is
a Mexican endemic occurring from “southern Tamaulipas,
Tlaxcala, Hidalgo and the Sierra Madre del Sur of Guerrero,
Mexico, and west and north to southern Nayarit and southern
Zacatecas” (Frost 2022). This individual was found in the
Sierra de los Agustinos, in the municipality of Guanajuato.
Wilson et al. (2013b) established its EVS as 12, placing it
in the upper portion of the medium vulnerability category.
IUCN has judged its conservation status as Vulnerable, and
SEMARNAT lists this species as Threatened (A). Photo by
José Carlos Arenas-Monroy.
November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
Table 5. Summary of the distributional occurrence of herpetofaunal families in Guanajuato, Mexico, by physiographic province.
See Table 4 for an explanation of the abbreviations.
Distributional occurrence
Family
]
Xantusiidae
Subtotal
C—O
Colubridae
Dipsadidae
Elapidae
Natricidae
Typhlopidae
Viperidae
Subtotal
Subtotal
Sum Total 101
A Coefficient of Biogeographic Resemblance
(CBR) matrix was constructed using the Duellman
(1990) algorithm to assess the herpetofaunal similarity
relationships among the three physiographic regions
in Guanajuato (Table 6). These data were then used to
produce a UPGMA dendrogram (Fig. 10; Sokal and
Michener 1958). The SMO harbors the greatest amount
of species richness (75 species), and the CP has the least
(60 species). The average species richness value for
the three regions is 69.7. The lowest number of shared
species (44) 1s between the CP and the SMO, which is
interesting inasmuch as these two regions of the state
abut one another. The highest number of shared species
(56) is between the CP and the TVB, two regions that
also contact one another.
Distribution Status Categorizations
The system employed by Alvarado-Diaz et al. (2013)
and the remainder of the MCS entries (see above) was
used to analyze the distributional status of members of
Amphib. Reptile Conserv.
74
the Guanajuato herpetofauna. The three categories that
apply to the Guanajuato herpetofauna are non-endemic,
country endemic, and non-native. No state endemic
Table 6. Pair-wise comparison matrix of Coefficient of
Biogeographic Resemblance (CBR) data for the herpetofaunal
relationships between the three physiographic regions in
Guanajuato, Mexico. Underlined values = number of species
in each region; upper triangular matrix values = species in
common between two regions; and lower triangular matrix
values = CBR values. The formula for this algorithm is CBR
= 2C/N, + N, (Duellman 1990), where C is the number of
species in common to both regions, N, is the number of
species in the first region, and N, is the number of species in
the second region. See Fig. 10 for the UPGMA dendrogram
produced from the CBR data.
Central Transmexican | Sierra Madre
Plateau Volcanic Belt Oriental
Transmexican 48
Sierra Madre
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
species are known to occur in Guanajuato. The basic data
are given in Table 7 and summarized in Table 8.
The numbers of species in each of these three
categories, in descending order of size, are as follows:
country endemics, 56 (55.4%); non-endemics, 40
(39.6%); and non-natives, five (5.0%). In this fashion,
the Guanajuato herpetofauna resembles those of many of
the other states dealt with in the MCS, 1.e., the largest
number of species occupies the country endemic category,
as was found in Michoacan (Alvarado-Diaz et al. 2013),
Nayarit (Woolrich-Pifia et al. 2016), Jalisco (Cruz Saenz
et al. 2017), Puebla (Woolrich-Pifia et al. 2017), Hidalgo
(Ramirez-Bautista et al. 2020), and Querétaro (Cruz-
Elizalde et al. 2022). In other states, the number of non-
endemic species exceeds that of the country endemic
species: Oaxaca (Mata-Silva et al. 2015); Chiapas
(Johnson et al. 2015a); Tamaulipas (Teran-Juarez et al.
2016); Nuevo Leon (Nevarez-de los Reyes et al. 2016):
the Mexican Yucatan Peninsula (Gonzalez-Sanchez et al.
Fig. 2. Water pool in low deciduous forest in the community of
La Torrecilla, Manuel Doblado, Las Musas Natural Protected
Area, Transmexican Volcanic Belt. Photo by Ma. del Carmen
Mendoza-Portilla.
Fig. 4. Cerro de Tetillas. Low deciduous forest near Janicho,
Salvatierra, south of Guanajuato. This area is an agricultural
region in the Transmexican Volcanic Belt. Photo by Adrian
Leyte-Manrique.
Amphib. Reptile Conserv.
2017), Coahuila (Lazcano et al. 2019), Veracruz (Torres-
Hernandez et al. 2021), and Tabasco (Barragan- Vazquez
et al. 2022).
As noted above, in some instances in the MCS the
number of country endemics is higher than the number of
non-endemic species, whereas in other cases the reverse
is true. Therefore, the ratios of country endemics to non-
endemic species vary extensively. The ratios in which the
number of country endemics is higher than the number
of non-endemics range from 0.53 in the case of Jalisco to
0.88 in Hidalgo. The ratios in which the number of non-
endemics exceeds the number of country endemics range
from 1.12 in the case of Oaxaca (Mata-Silva et al. 2015)
to 127.0 in the Yucatan Peninsula (Gonzalez-Sanchez et
al. 2017). In general, the nature of this ratio depends on
how close the state in question is to either the United
States or Central America. This ratio also depends upon
the size of these two aspects of a given herpetofauna
as to whether the ratio will be more or less than one.
Fig. 3. Panoramic view of Cerro de “El Veinte.” The vegetation
consists of low deciduous forest, with agricultural crops in the
background. Town of Cuchicuato, Irapuato, Guanajuato, in the
Transmexican Volcanic Belt. Photo by Adrian Leyte-Manrique.
Fig. 5. A mountain range at Vergel de Bernalejo, in the
municipality of San Luis de la Paz, Guanajuato in the Sierra
Madre Oriental physiographic region. Photo by Oscar Bdez-
Montes.
November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
Table 7. Distributional and conservation status measures for members of the herpetofauna of Guanajuato, Mexico. Distributional
status: CE = endemic to country of Mexico; NE = not endemic to state or country; and NN = non-native. The numbers suffixed to
the NE category signify the distributional categories developed by Wilson et al. (2017) and implemented in the taxonomic list at
the Mesoamerican Herpetology website (http://mesoamericanherpetology.com), as follows: 3 (species distributed only in Mexico
and the United States); 6 (species ranging from Mexico to South America); 7 (species ranging from the United States to Central
America); and 8 (species ranging from the United States to South America). Environmental Vulnerability Score categories (taken
from Wilson et al. 2013a,b): low (L) vulnerability species (EVS of 3—9); medium (M) vulnerability species (EVS of 10-13);
and high (H) vulnerability species (EVS of 14-20). IUCN categorization: CR = Critically Endangered; EN = Endangered; VU =
Vulnerable; NT = Near Threatened; LC = Least Concern; DD = Data Deficient; NE = Not Evaluated. SEMARNAT Status: A =
Threatened; P = Endangered; Pr = Special Protection; and NS = No Status. See Alvarado-Diaz et al. (2013), Johnson et al. (2015a),
and Mata-Silva et al. (2015) for explanations of the EVS, IUCN, and SEMARNAT rating systems.
Distributional Environmental Vulnerability IUCN SEMARNAT
Species
—"— Category (score) categorization status
| Anaxyrus compactilis* = H(4) Lo ter ™ he NS
a —— Te L(5) ss a
Incilius nebulifer L (6)
Incilius occidentalis* M (11)
Rhinella horribilis L (3)
tr
+
| Craugastoraugusti | NES TB) NS
| Craugastor occidentalis* | CET M3) DNS
| Eleutherodactylus angustidigitorum* | CE |) VP
Eleutherodactylus verrucipes* H (16)
Dryophytes arenicolor L(7)
Dryophytes eximius* M (10)
ZIZ
{Z| Z
RALA|AIM
ro
—
Z
Nn
Z
a
nin
Dryophytes plicata* M (11) nd ak |
Rheohyla miotympanum* L (9)
Smilisca baudinii L (3)
ZIiZ
Nin
>
| Smiliscafodiens | NER L (8) Pp CC CNS
Hypopachus variolosus a ae L(@4 ee oe
Z
Nn
N
Cithobates Berlandier? | NBs) tr
| Lithobates catesbeianus | NNO
| Hemidactylus frenatus** NNO
| Hemidactylusturcicus®* | NNO
Holbrookia maculata | NES M (10) a ce
Phrynosoma orbiculare* Ce: a M (12) _ a Ce es
M (13)
Nin
Sceloporus dugesii* M (13)
LQ) [Ai 07 (i 7 cee]
H (14)
Z
rg
—
IL
M (12) a a ee
Sceloporus spinosus* M (12)
Z
| Sceloporus torquatus* TCE M (11) a a
Sceloporus variabilis [ee L (5) PC
Z
ry | 'Z
|Z) Z
ALA|AInAIN
[| Plestiodondugesii* | CE TS)
| Plestiodontynxe® CEM)
Amphib. Reptile Conserv. 148 November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
Table 7 (continued). Distributional and conservation status measures for members of the herpetofauna of Guanajuato, Mexico.
Distributional status: CE = endemic to country of Mexico; NE = not endemic to state or country; and NN = non-native. The
numbers suffixed to the NE category signify the distributional categories developed by Wilson et al. (2017) and implemented in the
taxonomic list at the Mesoamerican Herpetology website (http://mesoamericanherpetology.com), as follows: 3 (species distributed
only in Mexico and the United States); 6 (species ranging from Mexico to South America); 7 (species ranging from the United States
to Central America); and 8 (species ranging from the United States to South America). Environmental Vulnerability Score categories
(taken from Wilson et al. 2013a,b): low (L) vulnerability species (EVS of 3—9); medium (M) vulnerability species (EVS of 10-13);
and high (H) vulnerability species (EVS of 14-20). IUCN categorization: CR = Critically Endangered; EN = Endangered; VU =
Vulnerable; NT = Near Threatened; LC = Least Concern; DD = Data Deficient; NE = Not Evaluated. SEMARNAT Status: A =
Threatened; P = Endangered; Pr = Special Protection; and NS = No Status. See Alvarado-Diaz et al. (2013), Johnson et al. (201 5a),
and Mata-Silva et al. (2015) for explanations of the EVS, IUCN, and SEMARNAT rating systems.
A,
Tantilla rubra
Diadophis punctatus
Geophis dugesii*
Thamnophis scaliger*
Trimorphodon tau*
Kinosternon integrum*
7
Tantilla bocourti*
Amphib. Reptile Conserv.
Distributional
status
Environmental Vulnerability
Category (score)
M (13)
M (11)
L(6)
H (15)
M (11)
H (14)
L (8)
L(6)
M (13)
M (11)
M (13)
H (14)
M (13)
H(15)
L (6)
L(9)
L(5)
M (13)
L(4)
M (13)
H(14)
H (15)
L(9)
L(6)
H (15)
L (8)
M (12)
M (10)
M (13)
M (11)
H (15)
L(7)
M (11)
L(7)
L (8)
H(15)
H (15)
H (14)
H(15)
CE
CE
NE6
GE
CE
GE
NE3
NE6
NE3
NE3
NE3
CE
CE
CE
NE7
E
NE4
FE
NE3
E
E
E
NE4
NE3
E
NE8
CE
CE
E
C
C
C
C
C
c
Cc
YE3
es
YE7
es]
es
N
YE3
C
‘3
E
E
E
E
NN
E
C
6
c H (16)
L(9)
L (8)
H (16)
M (11)
es
ies)
YE3
YE3
CE
M (10)
M (11)
149 November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
Fig. 6. Small seasonal wetlands used to store water in the Central
Plateau at San Jose del Llano, in the municipality of San Felipe,
Guanajuato. Photo by Yadira Fabiola Estrada-Sillas.
Fig. 8. An agricultural landscape with patches of native
vegetation and isolated hills at Chicamito, in the municipality
of Valle de Santiago, Guanajuato, Transmexican Volcanic Belt.
Photo by Oscar Bdaez-Montes.
So, we would expect that the herpetofaunas of states
more or less equidistant from both the USA and Central
America (Guatemala and/or Belize) would have ratios
closer to one. As noted in Torres-Hernandez et al. (2021):
“In the case of the three MCS states that border the USA,
the ratios are 3.22 (100/31 in Coahuila; Lazcano et al.
2019), 2.44 (95/39 in Nuevo Leon; Navarez-de los Reyes
et al. 2016), and 2.32 (130/56 in Tamaulipas; Teran-
Juarez et al. 2016). In the case of the states or the region
sharing a border with Central America, the ratios are
8.38 (268/32 in Chiapas; Johnson et al. 2015a) and 127.0
(127/1 in the Yucatan Peninsula; Gonzalez-Sanchez et al.
2017). The extremely high ratio for the Yucatan Peninsula
is due, at least in part, to this region lying adjacent to its
southern portion lying in northern Guatemala.”
The five non-native species reported as occurring in
Guanajuato are Lithobates catesbeianus, Hemidactylus
frenatus, H. turcicus, Virgotyphlops braminus, and
Trachemys scripta. Two of these species (H. frenatus
and V. braminus) are the most widespread of the non-
native species recorded in the previous 14 MCS entries,
inasmuch as they have been reported in 14 and 15 states,
respectively.
Amphib. Reptile Conserv.
Fig. 7. Xeric scrub along the Central Plateau, in the
municipality of San Felipe, Guanajuato. Photo by Oscar
Badez-Montes.
Fig. 9. A water pool and pine-oak vegetation at Charco Azul,
Xichu, Guanajuato, in the Sierra Gorda-Guanajuato Biosphere
Reserve, located in the Sierra Madre Oriental. Photo by Adrian
Leyte-Manrique.
Fig. 10. UPGMA generated dendrogram illustrating the simi-
larity relationships of species richness among the herpetofaunal
components in the three physiographic regions of Guanajuato
(based on the data in Table 6; Sokal and Michener 1958). Simi-
larity values were calculated using the Coefficient of Biogeo-
graphic Resemblance (CBR) of Duellman (1990).
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
Alligator Lizard is a Mexican endemic inhabiting the
mountains of the Transmexican Volcanic Belt and the Sierra
Madre Occidental in the states of México, Distrito Federal,
Querétaro, Hidalgo, Jalisco, Puebla, Michoacan, Morelos, and
Tlaxcala; additional isolated populations have been recorded
in Oaxaca and Veracruz (Ramirez-Bautista et al. 2014). This
individual was found in Sierra del Tigre, in the municipality
of Mazamitla. Wilson et al. (2013a) determined its EVS as 14,
placing it at the lower limit of the high vulnerability category.
IUCN has judged its conservation status as Least Concern, and
SEMARNAT as a species of Special Protection (Pr). Photo by
Adrian Leyte-Manrique.
<<
- % . we,
> - ao \ \
) P ‘™E
7 i Fie!
No. 14. Norops nebulosus (Wiegmann, 1834). The Clouded
Anole is a Mexican endemic distributed from “Sinaloa to
the Isthmus of Tehuantepec on the Pacific coast, extending
to the states of Morelos, Puebla, and Durango” (translation
ours; Santiago-Pérez et al. 2012: 136). This individual was
encountered at Cuchicuato, in the municipality of Irapuato.
Wilson et al. (2013a) determined its EVS as 13, placing it at
the upper limit of the medium vulnerability category. IUCN
has assessed its conservation status as Least Concern, but
SEMARNAT has not listed this species. Photo by Adrian
Leyte-Manrique.
No. 15. Sceloporus spinosus (Wiegmann, 1828). The
Eastern Spiny Lizard is a widespread endemic species found
over much of central Mexico, at elevations from 1,500 to
2,300 m asl (Florez and Gerez 1994). This individual was
photographed in Temascatio, in the municipality of Irapuato.
Wilson et al. (2013a) ascertained its EVS as 12, placing it
in the upper portion of the medium vulnerability category.
IUCN has assessed its conservation status as Least Concern,
but SEMARNAT has not listed this species. Photo by Adrian
Leyte-Manrique.
Amphib. Reptile Conserv.
No. 16. Plestiodon lynxe (Wiegmann, 1834). The Oak Forest
Skink is a Mexican endemic distributed in southern San Luis
Potosi, Guanajuato, Querétaro, Hidalgo, and the mountains
of western Veracruz, with isolated populations occurring in
southern Durango, southwestern Zacatecas, southeastern
Nayarit, and Jalisco (Webb 1968; Ponce-Campos and Romero-
Contreras 2006; Canseco-Marquez et al. 2007; Lemos-Espinal
and Dixon 2013). This individual was encountered at Puente
de Camotlan, in the municipality of La Yesca. Wilson et al.
(2013a) determined its EVS as 10, placing it at the lower limit
of the medium vulnerability category. IUCN has judged its
conservation status as Least Concern, and SEMARNAT as
a species of Special Protection (Pr). Photo by Adrian Leyte-
Manrique.
November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
Table 8. Summary of the distributional status of herpetofaunal families in Guanajuato, Mexico.
. . Distributional status
Family Number of species : - :
Non-endemic (NE) Country Endemic (CE) Non-native (NN)
mM, —_-|___. e
a A
a A
a il
a a
en eS [TC]
a CC
Fambystomatiee fT
a A CC
San | |
a aes 7 S| cc: Sa! | i] | T/
Panis
a A
A
nC
(a (SS (=
a
a a a a | Se
Ca a a ( (
FT
aS TS ST (= a (=
Le
re CA
a SC a [ (
Ce CC
a a
a a CC
a ( (
femdides ee
a A CC
a A Se (| [NY
sumo PCC C*~dC“(‘(SCséSCS!!OOUOUCUCdYOOC~<C(SCSC*‘(’
Wilson et al. (2017) originated a system for
Series (see above). The herpetofauna of San Luis Potosi
categorizing the distribution of the non-endemic species
in the Mexican herpetofauna. The categorizations of the
40 non-endemic species in Guanajuato (Table 9) indicate
that the largest number of these 40 species (26, or 65.0%)
are MXUS species, 1.e., those that occur in both Mexico
and the United States. The next highest number (six, or
15.0%) are USCA species, 1.e., species that range from
the United States through Mexico to some point in
Central America. The remaining eight species are MXCA
species (four, or 10.0%), MXSA species (three, or 7.5%),
or USSA species (one, or 2.5%).
Comparisons to the Herpetofaunas of Adjacent States
As noted above, Guanajuato is a state in central Mexico
bordered by San Luis Potosi, Querétaro, Michoacan,
Jalisco, anda small portion of Zacatecas. The herpetofaunas
of three of these five states (Querétaro, Michoacan, and
Jalisco) have been dealt with in the Mexican Conservation
Amphib. Reptile Conserv.
has been studied by Lemos-Espinal and Dixon (2013) and
Lemos-Espinal et al. (2018). We have not dealt with the
herpetofauna of Zacatecas, as the amount of the border
shared between these states is very small compared to the
length of the border in either state, and because this state
has not been dealt with tn either the MCS or the series of
Lemos-Espinal et al.
In order to compare the herpetofaunas of the
four neighboring states (San Luis Potosi, Querétaro,
Michoacan, and Jalisco) to that of Guanajuato, a table
was constructed (Table 10) that indicates the numbers of
Species in the various herpetofaunal groups for the five
states, along with the numbers of endemic species, non-
endemic species, and non-native species, as well as the
respective proportions of endemic species in each state.
The numbers of herpetofaunal species per state range
from a low of 101 in Guanajuato to a high of 223 in
Jalisco. The numbers of non-endemic species range from
a low of 40 in Guanajuato to a high of 105 in San Luis
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
Table 9. Summary of the distributional categories of the herpetofaunal families in Guanajuato, Mexico, that contain non-endemic
species. The categorizations are as follows: MXUS = species distributed only in Mexico and the United States (except for a few
perhaps found in Canada); MXCA = species found only in Mexico and Central America; MXSA = species ranging from Mexico to
South America; USCA = species ranging from the United States to Central America (except for a few perhaps found in the Antilles);
and USSA = species ranging from the United States to South America.
Number of non- -
endemic species MXUS species | MX
(3)
2
Family
Hylidae
Microhylidae
Ranidae
Scaphiopodidae
Anguidae
Dactyloidae
Phrynosomatidae
Scincidae
Teiidae
Subtotal
Boidae
Colubridae
Dipsadidae
Elapidae
Natricidae
Viperidae
Subtotals
Potosi. The numbers of non-native species range from
a low of three in Michoacan and Querétaro to a high of
five in Guanajuato. The numbers of endemic species
range from a low of 56 in Guanajuato to a high of 144
in Jalisco. Finally, the percentages of endemism range
from a low of 40.1 in San Luis Potosi to a high of 66.0
in Michoacan. The average proportion of endemism in
these five states is 55.8. Interestingly, the herpetofauna of
Guanajuato is the smallest of those in the five states, but
the percentage of endemism (55.4) is very close to that of
the average for the five states (55.8).
Principal Environmental Threats
The state of Guanajuato is located in a_ highly
commercialized region of Mexico, and this geographic
entity connects the central portion of the country with
Distributional status
CA species
(4)
the northern states. Guanajuato also encompasses an
agro-industrial belt, beginning in the southern portion
in Celaya, extending toward the northwest to the city
of Leon, and toward the north to connect with the state
of Aguascalientes, which represent the direction to the
United States. Consequently, this area of Guanajuato
also has a large number of people, constituting
approximately 70% of the population. Unfortunately,
because of these characteristics, significant impacts are
seen on the flora and fauna of this area. Included among
these organisms are the amphibians and reptiles, many
of which tend to be more vulnerable to human-related
activities. The effects of these factors can be noticed
on the diversity and distribution of the herpetofauna
across the state. For example, ongoing human activities
in the last three decades have reduced significantly the
original vegetation to isolated patches within a matrix
Table 10. Comparison of the numbers of endemic, non-endemic, and non-native species, and the percentage of endemism for
Guanajuato, Mexico, and the states that surround it.
223 144
215 142
130
a a a a
[0 OP C~isSC“‘CSéSC*'”
a A a a a (a aS
182
Amphib. Reptile Conserv.
November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
Fig. 11. Agricultural activity takes place all over the state,
but particularly in the south-central region. This image shows
agroecosystems with secondary vegetation and remnants
of low tropical forest in the vicinity of Urirero, Salvatierra,
where seasonal crops are grown with the use of fertilizers and
pesticides. Photo by Adrian Leyte-Manrique.
of cornfields, industrial parks, and continuous housing
developments, particularly in the south-central portion of
the state. However, Guanajuato 1s diverse with respect to
all the sources that threaten its herpetofauna. Although
the south-central region is presumably the most impacted,
forestry and livestock activities have been intensive and
continuous in the northern and northwestern portions
of the state. In the southwest, however, agriculture is
the most important factor, particularly the agave fields
that involve considerable amounts of land that used to
contain the native vegetation. Additionally, the pollution
of streams, reservoirs, and the Lerma River (including
its tributaries) are affecting populations of aquatic and
semi-aquatic herpetofauna. Given the current situation,
the herpetofauna of Guanajuato is represented by
populations that are subjected to conditions impacted by
five key human activities.
Agriculture. This activity takes place in approximately
70 to 80% of the state. In particular, fields are present
in the south-central region, where the main crops
traditionally have been corn, sorghum, and wheat, as well
as legumes and other vegetables. Over the last five years,
barley also has become an important crop, due to beer
production by large companies such as Heineken (INEGI
2021). Traditional agricultural systems (seasonal) also
are involved, but in smaller proportions, since these
products are primarily produced for local consumption
when compared to systems with intense irrigation. The
latter systems have involved significant loss of the native
vegetational cover (low tropical deciduous forest and
scrub) and therefore, the loss of important shelter, feeding,
and reproduction sites for amphibians and reptiles (Leyte-
Manrique 2021). For instance, the distributions of frog
species such as Lithobates neovolcanicus, Dryophytes
eximius, and D. arenicolor, and the toads Anaxyrus
Amphib. Reptile Conserv.
154
Fig. 12. This image taken in San Nicolas de los Agustinos,
Municipio de Salvatierra, shows solid wastes which are a
byproduct of industrial activities. A worn-out tire, empty
bottles, and used cans of insecticides and fertilizers can be
observed in the Lerma River in the southeastern portion of the
state. Photo by Adrian Leyte-Manrique.
Fig. 13. Forestry activities inevitably result in the loss of
vegetation cover. This image from El Varal, Guanajuato, shows
patches of pine-oak forest. Trees are removed for construction
and the production of charcoal. Currently, a reforestation
program is being implemented at this site. Photo by Adrian
Leyte-Manrique.
compactilis, A. punctatus, and Incilius occidentalis
have decreased considerably, as indicated by fewer
observations of these species in the past six years,
especially in the south-central region of the state (Leyte-
Manrique 2021). The pollution of reproduction sites
for amphibians is associated with agricultural activity,
due to the excessive use of chemicals in insecticides,
herbicides, and fertilizers. Additionally, increasing
ambient temperatures are reducing viable habitats
(Corral et al. 2007; Guanajuato Produce 2022) due to the
higher evaporation rates of seasonal ponds. With regards
to reptiles, negative cultural perceptions have resulted in
the indiscriminate killing of harmless species, such as
the snakes Pituophis deppei, Masticophis mentovarius,
and Drymarchon melanurus, locally known as Cencuate,
Chirrionera, and Limpia Campos, respectively. Other
snake species that also are affected include Conopsis
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
No. 17. Conopsis nasus (Gunther, 1858). The Long-nosed
Spotted Earthsnake ranges from the Sierra Madre Occidental
of southern Chihuahua southward and eastward through much
of the Mexican Plateau, occurring in the states of Chihuahua,
Durango, Sinaloa, Zacatecas, Aguascalientes, San Luis Potosi,
Jalisco, Michoacan, Guanajuato, Querétaro, Estado de México,
Morelos, Distrito Federal, Hidalgo, and Puebla (Heimes
2016). This individual came from Guayabo de Santa Rita, in
the municipality of Manuel Doblado. Wilson et al. (2013a)
ascertained its EVS as 11, placing it in the lower portion of
the medium vulnerability category. IUCN has assessed its
conservation status as Least Concern, but SEMARNAT has
not evaluated this species. Photo by Adrian Leyte-Manrique.
No. 18. Drymarchon melanurus (Dumeéril, Bibron, and
Dumeril, 1854). The Black-tailed Cribo is distributed “from
south-central Texas, USA, on the Atlantic versant and from
southern Sonora, Mexico, on the Pacific versant to northern
Venezuela and northwestern Peru...It also occurs on the Islas
Tres Marias, Nayarit, Mexico, and on the Islas de la Bahia
and Isla del Tigre, Honduras” (McCranie 2011: 114). This
individual was found in Area Natural Protegida Las Musas,
in the municipality of Manuel Doblado. Wilson et al. (2013a)
determined its EVS as 6, placing it in the middle of the low
vulnerability category. IUCN has established its conservation
status as Least Concern, but SEMARNAT has not listed this
species. Photo by Adrian Leyte-Manrique.
No. 19. Lampropeltis polyzona (Cope, 1861). The Mexican
Milksnake “ranges on the Pacific side from southern Sonora
south to Guerrero, and across the southern part of the
Mexican Plateau eastward to Veracruz and northern Oaxaca”
(Heimes 2016: 89). This individual came from Janicho, in the
municipality of Salvatierra. Mata-Silva et al. (2015) judged
its EVS as 11, placing it in the lower portion of the medium
vulnerability category. IUCN and SEMARNAT have not
evaluated this species. Photo by Adrian Leyte-Manrique.
Amphib. Reptile Conserv.
Fig. 20. Masticophis mentovarius (Dumeéril, Bibron, and
Dumeril, 1854). The Neotropical Whipsnake is distributed on
the Pacific versant from Sonora and on the Atlantic versant
from Tamaulipas south to Colombia and Venezuela. Its vertical
distribution extends from near sea level to around 2,100 m
(Johnson 1977, 1982 cited in Heimes 2016). This individual
came from El Copal, in the municipality of Irapuato. Wilson
et al. (2013a) ascertained its EVS as 6, placing it in the
middle portion of the low vulnerability category. IUCN
has not evaluated its conservation status, but SEMARNAT
has assessed it as Threatened (A). Photo by Adrian Leyte-
Manrique.
November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
south-central, and western portions of the state toward the Sierra Gorda. Cows can trample tadpoles (e.g., of Anaxyrus compactilis)
living in the pools formed in these areas, consequently increasing the mortality rate of this amphibian developmental stage. (a)
Cows feeding on grass, (b) an individual of A. compactilis. Photo by Adrian Leyte-Manrique.
lineata, C. nasus, Trimorphodon tau, and Lampropeltis
polyzona, with the last species usually being mistaken for
the venomous coralsnake Micrurus tener. With respect
to turtles, the pollution of bodies of water, uncontrolled
collection of individuals, and the presence of highly
traveled roads contribute to the continuous decimation
of local populations of Kinosternon (Leyte-Manrique
2021b).
Industrial activity. At the national level, Guanajuato
is well known for its industrial sector. This includes
vehicle assembly and the production of vehicle parts by
companies such as Honda in the south (municipality of
Celaya), Mazda in Silao, Toyota in Apaseo EI Alto, and
Volkswagen near the capital in the Celaya-Leon belt.
Another large-scale activity is the production of agro-
industrial chemicals, such as fertilizers, insecticides, and
herbicides, particularly in the south-central region of the
state. Likewise, the textile and fur industries are major
activities taking place in the northwestern portion, in the
municipality of Leon. Not surprisingly, all of these large-
scale activities contribute significantly to the pollution of
water bodies. Guanajuato contains 29 reservoirs that are
important for fish farming and agriculture (Walter and
Brooks 2009). One of the most important water sources
is Laguna Yuriria, a natural protected area considered
as a RAMSAR site due to its high bird diversity and
abundance of amphibians and reptiles, such as Lithobates
montezumae (POEGG 2005). All of the waste generated
by these industrial businesses is discarded in these
water sources in liquid and solid forms in both dams
and rivers, particularly the Rio Lerma, which transects
the southeastern and northwestern regions of the
state and runs through the industrial belt and the most
populated region of the state. The flora and fauna present
in reservoirs such as La Purisima have been affected
Amphib. Reptile Conserv.
significantly by the vehicle-related industries, but also by
intense water extraction to satisfy the needs of nearby
cities such as Guanajuato and Irapuato. Furthermore,
nearby farming activities and recreational events, such as
nautical regattas, also have an impact on these sites. All
of these processes affect amphibians more directly, since
species such as Lithobates montezumae, L. megapoda,
and L. neovolcanicus, require water for accomplishing
their reproductive cycles and their presence in La
Purisima appears to be less evident (Leyte-Manrique
et al. 2015). Conversely, it is encouraging to have a
natural protected area such as Cuenca La Esperanza that
provides protection to the herpetofauna present in the
central portion of the state where reptiles, particularly
snakes, seem to be more abundant (Instituto de Ecologia
del Estado de Guanajuato 1998).
Forestry. The exploitation of forests is regulated in the
north, and this activity also takes place inside natural
protected areas such as Cuenca La Esperanza, Sierra de
Lobos, Sierra de los Agustinos, Sierra de Pénjamo, and
Reserva de la Biosfera Sierra Gorda-Guanajuato (Ortiz-
Mantilla et al. 2022). The exploitation of trees such as
conifers and oaks is important in the state INANPEG
2020). Although the extraction of lumber is regulated
in the cold forests of the state, this is not the case for
unprotected areas with low tropical deciduous forest. The
latter forests experience illegal exploitation associated
with the production of wood and charcoal, and the removal
of vegetation for increasing housing development,
as well as livestock and agricultural activities. For
instance, the natural protected area Cerro de Arandas,
in the municipality of Irapuato, has a low diversity of
amphibians and reptiles likely due to the loss of native
vegetation, even though this area has a management
program. The herpetofauna of this area is forced to adapt
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
’ #*
de ere
la Biosfera Sierra Gorda-Guanajuato) in the municipality of Xichu. In general, the productivity in the city of Guanajuato is low, and
only remnants of minerals were being extracted by 2013 in the Sierra Gorda. The pollution resulting from this activity, however, is
evident in the air, soil, and water. (a) the mining area in the east, (b) an individual of Lithobates berlandieri found dead in a stream
within the mining area, and tadpoles in a pool. Photo by Adrian Leyte-Manrique.
to the surrounding agroecosystems, especially during the
dry season. Amphibians such as Dryophytes arenicolor
and D. eximius, the snakes Conopsis nasus, Masticophis
mentovarius, and Senticolis triaspis, and the turtle K.
integrum have been recorded in agricultural areas near
the city of Irapuato (Leyte-Manrique et al. 2021).
Livestock. This activity is more common in_ the
northwestern and southwestern parts of the state, such
as in the Sierra Gorda and the municipality of Manuel
Doblado, where production 1s mostly at the regional and
state levels. Observations indicate that the most visible
impact of this activity is on populations of frogs and toads
that use seasonal water sources for reproduction. At these
sites, horses and cows can step on the eggs and tadpoles of
these amphibians, and the toads Anaxyrus compactilis and
Spea multiplicata are the species most commonly affected
(Leyte-Manrique 2018). The same situation is expected to
exist in other parts of the state that remain unstudied.
Mining. This activity is of great significance in the
Amphib. Reptile Conserv.
municipalities of Guanajuato and Xichu, in the northern
portion of the state. One consequence of mining is
the loss of native arboreal vegetation. Additionally, a
high concentration of residues, such as lead and silver,
eventually reach streams and ponds and affect a variety
of aquatic organisms, including fish, amphibians, and
freshwater turtles. Although the actual effect of this
process on amphibians has not been examined, we
assume that it 1s impacting the health and survival of the
eggs and larval stages (Leyte-Manrique and Dominguez-
Laso 2014; A. Leyte-Manrique, pers. obs.). Additionally,
it is noteworthy that the impacts of mining on the
populations of salamanders have been poorly studied, as
we are aware of few salamander records from regions
that are well known for their mining activity, such as
Guanajuato and Xichu. Species such as /sthmura bellii,
Aquiloeurycea cephalica, and Ambystoma velasci have
been reported from these areas. Regarding A. velasci,
there is information on its ecology and reproduction in
Xichu, and it was determined that one of the main factors
affecting its survival is the pollution of their aquatic
November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
habitats by phosphates and other chemicals used in
agriculture. Additionally, these organisms are unlawfully
collected and sold on the black market (Leyte-Manrique
et al. 2016; De la Cruz-Beltran et al. 2018).
Conservation Status
This study employed the three systems of conservation
assessment that were used in all the entries in the Mexican
Conservation series (see above), 1.e., the systems of
SEMARNAT (2010), the IUCN Red List (http://www.
iucnredlist.org), and the EVS (Wilson et al. 2013a, b).
The assessments from these three systems were updated
as necessary.
The SEMARNAT System
Torres-Hernandez et al. (2021: 117) stated that “the
SEMARNAT system for assessing conservation status
was developed and implemented by the Secretaria del
Medio Ambiente y Recursos Naturales of the federal
government of Mexico (SEMARNAT 2010),” and the
status ratings for the native herpetofaunal species in
Guanajuato are provided in Table 7 and summarized in
Table 11. Three categories of assessment are established
in the SEMARNAT system, including Endangered (P),
Threatened (A), and Under Special Protection (Pr); and
those species that are not assessed are allocated to a “No
Status” (NS) category (Tables 7 and 11).
As in previous MCS entries, one frequently asked
question is why so few species in any given state
herpetofauna have been assessed using this system.
Perhaps the personnel at SEMARNAT favor listing
Species endemic to Mexico and not those that also
are shared with either the USA or countries in Central
America (i1.e., the non-endemics). If so, then it might
be possible to ascertain an answer to this question by
comparing the SEMARNAT assignments in the endemic
and non-endemic categories. In an effort to determine
whether such a bias might exist, these comparisons are
shown in Table 12. The data in Table 12 demonstrate
that of the 96 total native species in Guanajuato, only
44 species (45.8%) have been assessed to date, with
16 placed in the Threatened (A) category and 28 in the
Table 11. SEMARNAT categorizations for herpetofaunal species in Guanajuato, Mexico, arranged by families. Non-native species
are excluded.
Number of
species
Hylidae
Microhylidae
Elapidae
Natricidae
Viperidae
Amphib. Reptile Conserv.
Endangered (P)
Threatened (A)
i
—=|—_
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
Bm . eS i
MW 4 aOR NS a zs
No. 21. Pituophis deppei (Dumeéril, 1853). The Mexican
Bullsnake occurs in the states of Aguascalientes, Chihuahua,
Coahuila, Durango, Guanajuato, Hidalgo, Jalisco, México,
Michoacan, Nuevo Leon, Oaxaca, Puebla, San Luis Potosi,
Querétaro, Tlaxcala, Veracruz, Zacatecas, and Ciudad de
México (Ramirez-Bautista et al. 2014). This individual was
encountered in the municipality of Mineral El Chico. Wilson
et al. (2013a) calculated its EVS as 14, placing it at the lower
limit of the high vulnerability category. IUCN has determined
its conservation status as Least Concern, and SEMARNAT as
Threatened (A). Photo by Adrian Leyte-Manrique.
No. 22. Salvadora bairdi (Jan, 1860). Baird’s Patch-nosed
Snake occurs throughout much of the Sierra Madre Occidental
and the Mexican Plateau, ranging from southwestern
Chihuahua and adjacent eastern Sonora to the Transverse
Volcanic Cordillera as far south as southeastern Puebla (Valle
de Tehuacan) and northwestern Oaxaca (Heimes 2016).
This individual came from Campamento las Palomas, in the
municipality of Guanajuato. Wilson et al. (2013a) estimated
its EVS as 15, placing it in the lower portion of the high
vulnerability category. IUCN has assessed its conservation
status as Least Concern, and SEMARNAT as a species of
Special Protection (Pr). Photo by Adrian Leyte-Manrique.
No. 23. Trimorphodon tau (Cope, 1869). The Mexican Lyre
Snake is widely distributed along the coastal slopes and
foothills of the Sierra Madre Oriental, the Sierra Madre
Occidental, and the Sierra Madre del Sur, and across the
Mexican Plateau and the Mesa de Oaxaca (Heimes 2016). This
individual was photographed in the vicinity of Aldama, in the
municipality of Guanajuato. Wilson et al. (2013a) determined
its EVS as 13, placing it at the upper limit of the medium
vulnerability category. IUCN evaluated its conservation status
as Least Concern, but SEMARNAT has not listed this species.
Photo by Samuel Cadena-Rico.
Amphib. Reptile Conserv.
No. 24. Thamnophis melanogaster (Peters, 1864). The
Black-bellied Gartersnake is a Mexican endemic occurring
from “southwestern Chihuahua and adjacent Sonora south-
southeastward to the Valley of Mexico, western Querétaro, and
southern San Luis Potosi” (Lemos-Espinal and Dixon 2013).
This individual came from San Nicolas de los Agustinos, in the
municipality of Salvatierra. Wilson et al. (2013a) calculated
its EVS as 15, placing it in the lower portion of the high
vulnerability category. IUCN has evaluated its conservation
status as Endangered, and SEMARNAT as Threatened (A).
Photo by Adrian Leyte-Manrique.
November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
Table 12. Comparison of SEMARNAT and distributional categorizations for the Guanajuato herpetofauna. Non-native species are
excluded.
a. SEMARNAT category
Distributional category
SO
a OC
Special Protection (Pr) category. No species are placed in
the Endangered (P) category. The data indicate that of the
16 species allocated to the Threatened (A) category, four
(25.0%) are non-endemic species and 12 (75.0%) are
country endemics (Table 12). Of the 28 species placed
in the Special Protection (Pr) category, nine (32.1%) are
non-endemics and 19 (67.9%) are country endemics.
Apparently, some favor has been given to the assessment
of country endemic species. Conversely, however, since
52 (54.2%) of the 96 species that could be allocated using
the SEMARNAT categories have not been assessed, the
conservation assessment of the Guanajuato herpetofauna
using this system is seriously deficient and of little value
in our effort to determine the conservation status of the
herpetofauna of this state.
The IUCN System
The IUCN system of conservation assessment 1s applied
primarily to vertebrate animals and flowering plants,
leaving the conservation status of the major swath of
organisms, including prokaryotes, algae, fungi, and
invertebrates largely unassessed. This system has been
applied to amphibians and reptiles to some degree, and it
Table 13. IUCN Red List categorizations for herpetofaunal families in Guanajuato, Mexico. Non-native species are excluded.
The shaded columns to the left are the “threat categories,”
and those to the right the categories for which too little information on
conservation status exists to allow the taxa to be placed in any other IUCN category, or they have not been evaluated.
Family Mumber.of Critically
species Endangered
Endangered
|Bufonidae |S
| Craugastoridae | 2
| Eleutherodactylidae | 3
| Hylidae |
| Microhylidae [| 1
| Ranidae |S
| Scaphiopodidae ||
| Subtotal | 23
| Ambystomatidae [| 1
| Plethodontidae | 2
| Subtotal | 3
| Total | 6
| Anguidae | 4
| Dactyloidae | 2
| Phrynosomatidae | 10
|Scincidae | 3
| Sphenomorphidae | 1
| Teiidae
| Xantusiidae | 2
| Subtotal | 23
|Boidae |
| Colubridae | 8
| Dipsadidae |
|Elapidae |
| Natricidae |
| Viperidae |S
| Subtotal | 45
| Kinosternidae | 2
[Subtotal |
| Total 70
|Sumtotal | 96
| Category total | 96
Amphib. Reptile Conserv.
Near
Vulnerable Threatened | Concern
IUCN Red List categorization
Least
Data Not
Deficient | Evaluated
om
Ge
ie)
sr] um
—
7
a
=
7
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
Table 14. Environmental Vulnerability Scores (EVS) for the herpetofaunal species in Guanajuato, Mexico, arranged by family. The
shaded area on the left encompasses low vulnerability scores, and the one on the right indicates the high vulnerability scores. Non-
native species are excluded.
Famil Number of Environmental Vulnerability Score (EVS)
i species emcee 10 | 11 | 12 | 13 | 14 | as | a6 | 17 |
|Bufonidae | OS |||
| Craugastoridae | 2 SSS Tt
| Eleutherodactylidae | 3 Ft
TOL lll le EEL
| Microhylidae | |) |||
|Ranidae |S ||] | 2
| Scaphiopodidae | 1 || | rr
ES ee ee rere
| Ambystomatidae | ot J
| Plethodontidae | 2 Ft |
OE lll | — ETE
[Total | eee 2 | 3 | 2 | 3 a
[Anguidaee | 4A |||)
Dales EE)!
m i] i | 3 | 2
‘scinciae |; |
| Sphenomorphidae | ot | CT CT CT CT CT CT tt ECE CT
fTeidae | ee || | rr
| Xantusiidae | 2 || |) rr
STE = ee ere
[Bode |) ee |||
|Coubride || ll |; || | ee
|Dipsadidee || ETO | ||] | fe
Epic = | | |||
[Naricidae | DT]! | |
[Vipridee |S |! | | er
[Subtotal = |S NA 2 | s | 1 | 7) eee
| Kinostenidac | 2 | |! | |
[Subtotal | 2 |! | ||
[Total =| 0 ee 5 | 8 | 6 | 1 eee
| Sumtotal | 96 STAN 7 | 1 | 8 | 15 OSA
| Category total | 96 TS
Table 15. Comparison of Environmental Vulnerability Scores (EVS) and IUCN categorizations for the members of the herpetofauna
of Guanajuato, Mexico. Non-native species are excluded. The shaded area at the top encompasses the low vulnerability category
scores, and the shaded area at the bottom indicates the high vulnerability category scores.
IUCN category
Critically Near Least Data Not Total
== —_ bath ane | —
eS
Amphib. Reptile Conserv. 161 November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
No. 25. Crotalus aquilus (Klauber, 1952). The Dusky
Rattlesnake is found “from the region of Lake Chapala, Jalisco,
eastward through Michoacan, Guanajuato, Querétaro, central
San Luis Potosi, and southeastward through northern Hidalgo
and northwestern Veracruz” (Lemos-Espinal and Dixon 2013:
249). This individual was encountered in Cuenca Baja del
Rio Temascatio, in the municipality of Irapuato. Wilson et al.
(2013a) ascertained its EVS as 16, placing it in the middle
portion of the high vulnerability category. IUCN has assessed
this species as Least Concern, and SEMARNAT as in the
Special Protection (Pr) category. Photo by Mara Fernanda
Rodriguez-Gutiérrez.
consists of six categories (Table 13), including three so-
called “threat categories” of Critically Endangered (CR),
Endangered (EN), and Vulnerable (VU). Two categories
of so-called “lesser risk,” 1.e., Near Threatened (NT)
and Least Concern (LC), also are involved. A sixth
category, called Data Deficient (DD) is established, and
it is assigned to species which lack sufficient information
for placement into another category. Finally, another
category of Not Evaluated (NE) is used here for species
that the IUCN has not evaluated thus far. Two other
categories exist for species thought to be either Extinct
(EX) or Extinct in the Wild (EW), but these are seldom
applicable to herpetofaunal species.
The data for allocating the species that comprise
the Guanajuato herpetofauna are shown in Table 7 and
summarized in Table 13. The data in Table 13 demonstrate
that only 10 species are allocated to two of the three
“threat categories.” A single species (Zhamnophis
melanogaster*) is placed in the Endangered (EN)
category, and nine species are in the Vulnerable (VU)
category (Eleutherodactylus angustidigitorum*, E.
verrucipes*, Lithobates megapoda*, Isthmura bellii*,
Abronia taeniata*, Plestiodon dugesii*, Lepidophyma
gaigeae*, Adelophis copei*, and Thamnophis scaliger* ).
These 10 species are all country endemics. No species are
allocated to the Critically Endangered (CR) category. Of
the 74 species placed in the “lesser risk” categories, three
country endemics (Rheohyla miotympanum* , Lithobates
neovolcanicus*, and Aquiloeurycea cephalica*) are
considered as Near Threatened (NT), and 71 species are
classified as Least Concern (LC). The five Data Deficient
(DD) species are Craugastor occidentalis*, Geophis
Amphib. Reptile Conserv.
No. 26. Crotalus molossus (Baird and Girard, 1853). The
Black-tailed Rattlesnake occurs from northwestern Arizona
and southwestern New Mexico on the west, southward along
the Pacific Coastal Plain, Sierra Madre Occidental, and
Mexican Plateau to Michoacan, and from Coahuila and Nuevo
Leon on the east, southward along the Sierra Madre Oriental
and Mexican Plateau to northwestern Oaxaca (Anderson and
Greenbaum 2012). This individual came from El Garbanzo, in
the municipality of Irapuato. Wilson et al. (2013a) calculated
its EVS as 8, placing it in the upper portion of the low
vulnerability category. IUCN has determined its conservation
status as Least Concern, and SEMARNAT as a species of
Special Protection (Pr). Photo by Adrian Leyte-Manrique.
No. 27. Kinosternon integrum (Le Conte, 1854). The Mexican
Mud Turtle is endemic to Mexico, and it is distributed from
central Sonora to Oaxaca, as well as from southwestern
Tamaulipas and the central and southern portions of the
Mexican Plateau (Lemos-Espinal and Dixon 2013). This
individual was found at Presa La Galera, in the municipality
of Abasolo. Wilson et al. (2013a) determined its EVS as 11,
placing it in the lower portion of the medium vulnerability
category. IUCN has assessed its conservation status as Least
Concern, and SEMARNAT has placed it in the Special
Protection (Pr) category. Photo by Adrian Leyte-Manrique.
latifrontalis*, G. petersii*, Hypsiglena tanzeri*, and
Rhadinaea gaigeae*. As with the EN and VU species, all
of these five species are country endemics.
Seven species have not been evaluated by the
IUCN, as follows: Rhinella horribilis, Norops sericeus,
Boa _ imperator, Lampropeltis polyzona*, Oxybelis
microphthalmus, Hypsiglena jani, and Leptodeira
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
Table 16. Environmental Vulnerability Scores (EVS) for members of the herpetofauna of Guanajuato, Mexico, that are allocated to
the IUCN Data Deficient category. * = country endemic.
Environmental Vulnerability Score (EVS)
Taxon Geographic Ecological Reproductive mode/Degree Total
distribution distribution of ee score
5
Craugastor occidentalis*
Geophis latifrontalis*
Hypsiglena tanzeri*
— al i Tol
a
septentrionalis. Only one of these seven species is a
country endemic, and the others are relatively widespread
non-endemic species (two are NE3 species, and one each
are NE4, NE6, NE7, and NE8 species).
The 71 species allocated to the LC category comprise
74.0% of the 96 native species in Guanajuato. Thirty-seven
of these 71 species (52.1%) are country endemics and the
remaining 34 (47.9%) are non-endemics. Given that almost
three-quarters of the herpetofauna has been judged as
Least Concern by using the IUCN system of conservation
assessment, it might seem that the herpetofauna of
Guanajuato is in reasonably good shape from a conservation
perspective. However, since such a status has not been the
case in the other MCS studies, this assumption is subjected
to further analysis using the EVS system.
The EVS System
Initially, the Environmental Vulnerability Score (EVS)
system of conservation assessment was developed to
examine the herpetofauna of Honduras (Wilson and
McCranie 2003), inasmuch as the population status
of species in this herpetofauna was not sufficiently
understood for assessment using the IUCN system.
Since that time, the EVS has been applied to all of the
Mexican and Central American herpetofaunas (Wilson et
al. 2013a,b; Johnson et al. 2015a), as well as all 14 of
the previously-published Mexican Conservation Series
(MCS) studies (see above). In addition, this system
is becoming increasingly applied in studies by other
workers on the Mexican herpetofauna, especially by J
Lemos-Espinal and his co-authors.
In this study, we calculated the EVS values for the 96
native species of the Guanajuato herpetofauna, and they
are shown in Table 7 and summarized in Table 14. The
EVS values range from 3 to 17, three fewer than the total
theoretical range of values (3-20). The most frequent
values (1.e., those associated with 10 or more species) are
11 (11 species), 13 (15), and 14 (10). Note that these three
values apply to 36 of the 96 native species in Guanajuato.
The lowest score of 3 was determined only for two anuran
species (Rhinella horribilis and Smilisca baudinii). The
highest value of 17 was applied to only a single anuran
species (Eleutherodactylus angustidigitorum* ).
As with all the previous MCS studies, the EVS values
were grouped into the categories of low (3-9), medium
(10-13), and high (14-17) vulnerability. Based on this
categorization, the resulting figures increase from low
vulnerability (31 species) through medium (41), and
then decrease to high vulnerability (24). In both of these
states, the native herpetofaunas consist essentially of non-
endemic and country endemic species, with the exception
being that Querétaro harbors a single state endemic, 1.e.,
Sceloporus exsul. In the Querétaro herpetofauna, there
are 60 non-endemics and 67 country endemics, while the
respective figures in Guanajuato are 40 and 56.
In an effort to assess how the IUCN ratings relate
to those for the EVS, the categorizations of these two
systems are compared in Table 15. Only 10 of the 24 high
vulnerability species (41.7%) are allocated to the IUCN
“threat categories.” At the other extreme, 31 of the low
vulnerability species (by EVS) account for only 43.7%
of the 71 LC species (by IUCN). Thus, as generally seen
in the other MCS studies, there is little correspondence
between the conservation evaluations provided by the
IUCN and the EVS categorizations.
Table 17. Environmental Vulnerability Scores (EVS) for members of the herpetofauna of Guanajuato, Mexico, that are currently
Not Evaluated (NE) by the IUCN. Non-native taxa are excluded. * = country endemic.
Taxon
Environmental Vulnerability Score (EVS)
Geographic Ecological Reproductive mode/Degree Total
distribution distribution of — —.
Rhinlla horribils a
a a a a a a
[Lanpropelispobeona® «| 1 ~+i| 3 Od) OS CCdSCtSCC*'
a CT
En a (OY
A (
Amphib. Reptile Conserv. 163 November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
Table 18. Environmental Vulnerability Scores (EVS) for members of the herpetofauna of Guanajuato, Mexico, that are assigned
to the IUCN Least Concern (LC) category. Non-native taxa are excluded. * = country endemic.
distribution distribution of persecution score
| Anaxyrus compactilis* | 8
| Anaxyruspunctatus | 8
| Inciliusnebulifer | 4
| Inciliusoccidentalis* |
| Craugastoraugusti dE 8
| Eleutherodactylus gutilatus | 2S
| Dryophytesarenicolor | CT A
| Dryophyteseximius* Tt
| Dryophytesplicata* |
| Smiliscabaudinii Et 8
| Smiliscafodiens CE CE ST
| Hypopachusvariolosus |
| Lithobates berlandieri_— | AT
| Lithobates montezumae* | ST
| Lithobates spectabilis* |
| Speamultiplicata CL 4
| Ambystomavelasci* | 4
| Barisiaimbricata* |
| Gerrhonotus infernalis | 5
| Noropsnebulosus* | 5
| Holbrookia maculata |
| Phrynosoma orbiculare* |
| Sceloporusaeneus* |
| Sceloporusdugesii* |
| Sceloporus grammicus |
| Sceloporusminor* ES
| Sceloporus scalaris* |
| Sceloporus serrifer |
| Sceloporustorquaus* |
| Sceloporusvariabilis |
| Plestiodonlynxe* LO
| Plestiodon tetragrammus |
| Scincellasilvicola* |
| Aspidoscelis gularis |
| Lepidophymaoceulor®* |
| Conopsislineata* |
| Conopsisnasus* EY
| Leptophis diplotropis* |
| Masticophis flagellum |
| Masticophis mentovarius |
| Masticophis schotti_— |
| Pantherophisemoryi |
| Pituophisdeppei* | 5
5
| Salvadorabairdi* LS
ae ON Meee CAN Meee BCA fee ee ee Be Beam ie ee)
—e ee ee ee ee
as
Nn Tapa pro
Amphib. Reptile Conserv. 164 November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
Table 18 (continued). Environmental Vulnerability Scores (EVS) for members of the herpetofauna of Guanajuato, Mexico, that
are assigned to the IUCN Least Concern (LC) category. Non-native taxa are excluded. * = country endemic.
Environmental Vulnerability Score (EVS)
Taxon Geographic
distribution distribution of persecution
| Micrurustener |
| Storeriadekayi
| Storeria storerioides* |S
| Thamnophiscyrtopsis |
| Thamnophis pulchrilaus* |S
| Thamnophisscalaris* |S
| Crotalusaguilus* LS
| Crotalusatrox, |
| Crotalus motossus
| Crotalus polystictus* |S
| Crotalus scuulatus |
| Kinosternonhirtipes |
| Kinosternonintegrum® TS
As shown in previous MCS studies, the principal
reason for the poor correspondence between the two
systems of conservation evaluation is the large number
of species allocated to the IUCN LC, DD, and NE
categories. In the case of the Guanajuato herpetofauna,
this applies to 83 of the 96 total native species (86.5%).
Of these 83 species, five are allocated to the DD
category (Table 16); one is an anuran and four are
snakes. All five species are country endemics, and their
EVS values range from 12 to 15. Leaving these five
species in the DD category consigns them to a status of
being ignored. In our opinion, the two species with EVS
values of 12 (Rhadinaea gaigeae*) and 13 (Craugastor
occidentalis*) should be placed in the NT category.
The species with an EVS of 14 (Geophis latifrontalis* )
should be allocated to the VU category, and the two
species with an EVS of 15 (Geophis petersii* and
Hypsiglena tanzeri*) should be relegated to the EN
category.
Seven species remain unassessed by the IUCN (Table
17). These species include one anuran, one lizard, and
five snakes. Only one of these species (Lampropeltis
polyzona*) is a country endemic, and the remaining are
non-endemics. Their EVS values range from three to
11. The six species with an EVS from 3 to 10 can be
allocated to the LC category and the remaining species
(Oxybelis microphthalmus), with an EVS of 11, should
be placed in the NT category.
ATEN
Ecological Reproductive mode/Degree
3
5
3
1
4
5
3
The highest number of species in the Guanajuato
herpetofauna (71) is allocated to the LC category (Table
18). Comprising this group of 71 species are 16 anurans,
one salamander, 19 lizards, 33 snakes, and two turtles. Of
these species, 37 are country endemics and 34 are non-
endemics. Their EVS values range from 3-16, just one
less than the entire range for the Guanajuato herpetofauna
(3-17). Thirty-two of these species have EVS scores
from 3 to 10, and in our opinion, they can be retained
in the Least Concern category. Twenty-seven species
have EVS values ranging from 11 to 13, and thus they
could be placed in the NT category. Seven species have
an EVS of 14 and could be allocated to the VU category.
The three species with an EVS of 15 (Barisia imbricata* ,
Salvadora bairdi*, and Thamnophis pulchrilatus*) and
the two species with an EVS of 16 (Crotalus aquilus* and
C. polystictus*) should be allocated to the EN category.
Relative Herpetofaunal Priority
The concept of Relative Herpetofaunal Priority (RHP)
was developed by Johnson et al. (2015a) in the MCS
paper on the state of Chiapas. This method involves a
simple means of ascertaining the relative conservation
importance of the herpetofauna of any geographical
entity (e.g., a physiographic region, a municipality, or
a state), and consists of two parts: (1) determining the
proportion of country endemic species (and in some
Table 19. Number of herpetofaunal species in three distributional status categories among the three physiographic regions of
Guanajuato, Mexico. Rank is based on the number of country endemics.
i J : Distributional category
Physiographic region ; : : Total Rank order
Country endemic
Cental Plateau
3
lee a ae aa eee
Transmexican
Sierra Madre Oriental
Amphib. Reptile Conserv. 165 November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
Table 20. Number of herpetofaunal species in the three EVS categories among the three physiographic regions in Guanajuato,
Mexico. Rank order is determined by the relative number of high EVS species. Non-native species are excluded.
EVS category
Physiographic province Total Rank order
: ee ee ee ee
| CentralPlateau ssid Plateau
Transmexican Voleanic Bek Se
Sierra Madre Oriental
cases, state endemic species) relative to the entire regional
herpetofauna; and (2) calculating the absolute number of
high EVS category species in each regional herpetofauna.
The pertinent data for these two approaches are presented
in Tables 19 and 20.
Based on the number of country endemic species in
each of the three physiographic regions and the rank each
region occupies (Table 19), this measure indicates that
the most important region is, interestingly enough, the
Transmexican Volcanic Belt with 43 country endemic
species. In most cases, the Sierra Madre Oriental occupies
the first rank in the states that encompass a portion of this
biodiverse range, including Puebla (Woolrich-Pifia et al.
2017), Hidalgo (Ramirez-Bautista et al. 2020), Veracruz
(Torres-Hernandez et al. 2021), and Querétaro (Cruz-
Elizalde et al. 2022). In the case of Guanajuato, the likely
reason for this shift in rank for the Sierra Madre Oriental
is that the Transmexican Volcanic Belt segment is several
times larger than the Sierra Madre Oriental segment.
Based on the relative numbers of high vulnerability
species (Table 20), the first rank is occupied by the
Transmexican Volcanic Belt, with 18 high vulnerability
species out of a total of 69 native species (26.1%). The
second rank is occupied by the Sierra Madre Oriental,
with 15 high vulnerability species out of a total of 74
native species (20.3%). Finally, the third rank is held by
the Central Plateau, with 14 high vulnerability species
out of a total of 59 native species (23.7%).
The rankings based on the country endemic species
numbers are the same as for the high vulnerability species
numbers, 1.e., first rank 1s the Transmexican Volcanic
Belt; second rank is the Sierra Madre Oriental; and third
rank is the Central Plateau. Thus, the Transmexican
Volcanic Belt is the most important physiographic
region because it contains the second highest number
of native species (70), the highest number of country
endemic species (43), and the highest number of high
vulnerability species (18). As noted above, this result
was a bit surprising, although the Sierra Madre Oriental
herpetofauna, which was often was the most important in
several other MCS studies, occupies the smallest amount
of area in Guanajuato.
The 43 country endemic species in the TVB include 10
anurans, two salamanders, 30 squamates, and one turtle.
The TVB also harbors 18 high vulnerability species (with
their EVS scores in parentheses):
Anaxyrus compactilis* (14)
Eleutherodactylus angustidigitorum* (17)
Amphib. Reptile Conserv.
Lithobates megapoda* (14)
Barisia imbricata* (14)
Plestiodon dugesii* (16)
Lampropeltis mexicana* (15)
Leptophis diplotropis* (14)
Pituophis deppei* (14)
Salvadora bairdi* (15)
Geophis petersi* (15)
Hypsiglena tanzeri* (15)
Adelophis copei* (15)
Thamnophis melanogaster* (15)
Thamnophis pulchrilatus* (15)
Thamnophis scalaris* (14)
Thamnophis scaliger* (15)
Crotalus aquilus* (16)
Crotalus polystictus* (16)
These 18 species include three anurans, two lizards, and
13 snakes. All of these species are country endemics and
they have EVS values ranging from 14 to 17.
The Sierra Madre Oriental (rank two) contains 15
high vulnerability species:
Eleutherodactylus angustidigitorum* (17)
Eleutherodactylus verrucipes* (16)
Aquiloeurycea cephalica* (14)
Abronia taeniata* (15)
Barisia imbricata* (14)
Sceloporus minor* (14)
Lepidophyma occulor* (14)
Lampropeltis mexicana*™ (15)
Pituophis deppei* (14)
Salvadora bairdi* (15)
Geophis latifrontalis* (14)
Hypsiglena tanzeri* (15)
Thamnophis pulchrilatus* (15)
Thamnophis scalaris* (14)
Crotalus aquilus* (16)
These 15 species include two anurans, one salamander,
four lizards, and eight snakes. All 15 species are country
endemics and are assigned EVS values from 14 to 17.
Finally, the Central Plateau (rank three) harbors 14
high vulnerability species:
Anaxyrus compactilis* (14)
Eleutherodactylus verrucipes* (16)
Lithobates megapoda* (14)
Barisia imbricata* (14)
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
Sceloporus minor* (14)
Leptophis diplotropis* (14)
Pituophis deppei* (14)
Salvadora bairdi* (15)
Hypsiglena tanzeri* (15)
Thamnophis melanogaster* (15)
Thamnophis scalaris*
Thamnophis scaliger* (15)
Crotalus aquilus* (16)
Crotalus polystictus* (16)
These 14 species include three anurans, two lizards, and
nine snakes. All 14 species are country endemics and
have EVS values ranging from 14 to 16.
Of the 101 species that comprise the Guanajuato
herpetofauna (96 of which have calculable EVS), 24
are high vulnerability species and the proportions of
these species in the three physiographic regions are as
follows: TVB (75.0%), SMO (62.5%), and CP (58.3%).
These data will be of considerable value in developing
management plans for the protected areas in Guanajuato,
as discussed in the next section.
Protected Areas in Guanajuato
Protected Areas and Worldview
Most humans appear to be afflicted with a social disease
termed anthropocentrism, for which the symptoms
arise from denying the reality of natural law. Briefly
stated, life on Earth is entirely dependent on the
functional interaction of the three abiotic spheres, L.e.,
the atmosphere, hydrosphere, and lithosphere. This
relationship dates back to the origin of life on this planet,
approximately 3.5 billion years ago. Since modern-day
humans are socialized to support worldviews at odds with
this reality, such a belief system has been the source of all
current environmental problems. The most widespread
worldviews adopted by humans are contrasted by
Wilson and Lazcano (2019: 26), who promulgated the
categorical ethical position that “what is good 1s defined
in terms of what is right.” Thus, these authors would
argue that what is bad is defined in terms of what 1s
wrong. Further, they argue, “What is right is that which
enhances the survival of life on Earth” and “that which
is wrong is that which compromises it.” Their position,
therefore, is that “with the right to enjoy life comes
the responsibility to not endanger the lives of others”
(Wilson and Lazcano 2019: 26).
Clearly, based on varying experiences, this view of
life is not shared by most people. As noted by Miller
(2006: 431), environmental worldviews are based on
“how people think the world works, what they believe
their environmental role in the world should be, and
what they believe is right and wrong environmental
behavior.” Miller (2006: 432) identified three principal
environmental worldviews: the Planetary Management
Amphib. Reptile Conserv.
Worldview, Stewardship Worldview, and Environmental
Wisdom Worldview. The worldview adopted by the
authors of this paper is characterized by the following
ethical positions: (1) “we are a part of and totally
dependent on nature and nature exists for all species”;
(2) “resources are limited, should not be wasted, and
are not all for us”; (3) “we should encourage earth-
sustaining forms of economic growth and discourage
earth-degrading forms”; and (4) “our success depends
on learning how nature sustains itself and integrating
such lessons from nature into the ways we think.”
Miller (2006: 431) also stated that “many people in
today’s industrial consumer societies have a planetary
management worldview.” This worldview, which clearly
is at odds with our own, is based on the following ideas:
(1) “we are apart from the rest of nature and can manage
nature to meet our increasing needs and wants”; (2)
“because of our ingenuity and technology we will not run
out of resources”; (3) “the potential for economic growth
is essentially unlimited”; and (4) “our success depends
on how well we manage the earth’s life-support systems
mostly for our benefit.”
The dangers associated with the Planetary
Management Worldview are becoming more evident
with the passing of time. Judging by the news of the day,
climate change is becoming an issue that is more difficult
to ignore than in the past. The latest (sixth) report of the
Intergovernmental Panel on Climate Change (IPCC)
appeared in March 2022 (Portner and Roberts, Climate
Change 2022: Impacts, Adaptation and Vulnerability).
This highly complicated and detailed report is not
likely to become casual reading for the average person,
but it probably should allow for an understanding and
internalization of the bottom-line assessment offered
by Robinson Meyer in a piece in The Atlantic entitled
There's no scenario in which 2050 is ‘normal.’ Meyer
concluded that, “We have been backed into a corner [by
our inaction]. The scale of [climate] change headed our
way is unimaginable. And it is also inevitable.”
However, the latest IPCC report is not all “doom and
gloom.” The report also outlines the changes in the human
way of “doing business” that have to occur to mitigate the
“inevitable” effects of climate change, but these changes
will have to be implemented over a distressingly short
period of time. On 28 February 2022, Antonio Guterres,
the Secretary-General of the United Nations wrote that,
“Nearly half of humanity is living in the danger zone
now. Many ecosystems are at the point of no return—now.
Unchecked carbon pollution is forcing the world’s most
vulnerable on a frog march to destruction—now. The facts
are undeniable. This abdication of leadership is criminal.
The world’s biggest polluters are guilty of arson of our
only home... Today’s report underscore[s] two core truths.
First, coal and other fossil fuels are choking humanity.
(Second,) investments in adaptation work... Delay means
death” (https://media.un.org/en/asset/k 1 x/k1 xcijyxjhp;
accessed 16 November 2022).
November 2022 | Volume 16 | Number 2 | e321
Mexico
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November 2022 | Volume 16 | Number 2 | e321
168
The herpetofauna of Guanajuato
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Amphib. Reptile Conserv.
Park guards;
Administrative services; R
Table 21 (continued). Characteristics of the Natural Protected Areas in Guanajuato, Mexico. Abbreviations for Facilities available are as follows: A
Leyte-Manrique et al.
The consideration of these dire warnings
forces on us a somewhat altered viewpoint on
the importance of protected areas in responding
effectively to the problem of biodiversity
decline. In one of the most recent entries in the
Mexican Conservation Series, Cruz-Elizalde
et al. (2022: 183) wrote the following: “Since
humans apparently are not predisposed to deal
with the threats posed to planetary biodiversity
(Wilson and Lazcano 2019), 1e., to change
the ways of thinking to promote the control
of human population growth, conservation
biologists generally propose the establishment
of protected areas to ensure the safety of
populations of organisms within those areas.”
Whereas the authors of this paper are fully
in support of establishing, maintaining, and
expanding the limits of such areas, under the
best of circumstances this process is intended
to hold at bay the encroachment of humanity
on the remaining natural areas. So even if this
effort is successful, these areas are cloaked
by the same atmosphere that harbors the
burgeoning populations of our own species.
The damage to the atmosphere originating
from human population centers obviously is
not confined to these areas, but ultimately will
impact the so-called protected areas. Again,
this realization is not to be construed as an
argument against setting up protected areas, but
these steps alone will not guarantee protection
from the ravages of humanity for an entire
group of organisms, for perpetuity.
Management
plan available
Yes (not
updated)
Yes (not
updated)
Yes (not
updated)
Yes (not
updated)
Yes (not
updated)
Yes (not
updated)
Yes (not
updated)
Herpetofaunal
survey
completed
Partially
Partially
Partially
Partially
Partially
Partially
Partially
Partially
Occupied by
landowners
Personnel
Facilities
available
Area
demarcated
region(s)
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Transmexican
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Transmexican
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Eastern Sierra
Madre Oriental
15 Sep
Transmexican
Volcanic Belt
se Central Plateau Yes
ne
State/Federal
pe
General Features of the Protected Areas
in Guanajuato
Given this background, an analysis of the
current level of protection offered by the
areas that have been set aside in Guanajuato
is presented here, beginning with the basic
characteristics of these areas in Table 21.
Twenty-four protected areas have been
established in Guanajuato, and they fall
into six categories: (1) sustainable use (11
areas); (2) ecological park (four areas); (3)
ecological preservation area (five areas);
(4) natural monument (one area); (5)
conservation reserve (two areas); and (6)
biosphere reserve (one area). These 24 areas
were established from 1997 to 2013, and
range in size from 15.0 to 236,882.8 ha.
Most of these areas are administered at the
state level, except for one at both the state
and federal levels.
It is of major importance that 14 of the
24 areas are located within the Transmexican
Municipalities
Tierra Blanca, San
José Iturbide
Atarjea, San Luis de
la Paz, Santa Catarina,
Victoria, Xichu
Facilities for visitors.
[a | eo |e oa
Valle de Santiago
6 Jun
000 13,862.0
2 Feb
3007 236,882.8
21 Nov
1997 8,928.5
Ecological
Preservation
Ecological
Preservation
Ecological
Preservation
Area
Ecological
Preservation
Area
Monument
Conservation
Conservation
Biosphere
Reserve
System of pathways; and V
Laguna de
Yuriria y
su zona de
influencia
Cerro del
Cubilete
Cuenca de la
Soledad
Presa de
Neutla y
su zona de
influencia
Region
Volcanica
Siete
Luminarias
Cuenca de la
Esperanza
Pinal de
Zamorano
Sierra Gorda
de Guanajuato
S
Amphib. Reptile Conserv. 169 November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
Table 22. Distribution of herpetofaunal species in the Natural Protected Areas of Guanajuato, Mexico, based on herpetofaunal surveys.
Abbreviations are as follows: * = species endemic to Mexico and ** = non-native species. The numbers of the Natural Protected Areas
signify the following: 1 = Sierra de Lobos; 2 = Cuenca Alta del Rio Temascatio; 3 = Pefia Alta; 4 = Las Musas; 5 = Cerros el Culiacan
y La Gavia; 6 = Sierra de los Agustinos; 7 = Cerro de los Amoles; 8 = Cerro de Arandas; 9 = Presa La Purisima y su zona de influencia;
10 = Sierra de Pénjamo; 11 = Cerro de Palenque; 12 = Megaparque de la Ciudad de Dolores, Hidalgo; 13 = Las Fuentes; 14 = Parque
Metropolitano; 15 = Lago Crater La Joya; 16 = Presa de Silva y areas aledafias; 17 = Laguna de Yuriria y su zona de influencia; 18 =
Cerro del Cubilete; 19 = Cuenca de la Soledad; 20 = Presa de Neutla y su zona de influencia; 21 = Regién Volcanica Siete Luminarias; 22 =
Cuenca de la Esperanza; 23 = Pinal de Zamorano; and 24 = Sierra Gorda de Guanajuato. Note. *Dryophytes plicata (-) is found in the state
and is part of the herpetofauna of Guanajuato, but at the moment has not been recorded in any of the natural protected areas. This species
has been recorded the municipalities of Acambaro, Salvatierra, Sa José Iturbide, and Tierra Blanca.
Natural Protected Areas
Taxon
PERE [sp [a] s [fis] ire] o [apes [ [pee
AMPHIBIA (26 species)
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Amphib. Reptile Conserv. 170 November 2022 | Volume 16 | Number 2 | e321
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Leyte-Manrique et al.
Table 22 (continued). Distribution of herpetofaunal species in the Natural Protected Areas of Guanajuato, Mexico, based on herpetofaunal
surveys. Abbreviations are as follows: * = species endemic to Mexico and ** = non-native species. The numbers of the Natural Protected
Areas signify the following: 1 = Sierra de Lobos; 2 = Cuenca Alta del Rio Temascatio; 3 = Pefia Alta; 4 = Las Musas; 5 = Cerros el Culiacan
y La Gavia; 6 = Sierra de los Agustinos; 7 = Cerro de los Amoles; 8 = Cerro de Arandas; 9 = Presa La Purisima y su zona de influencia;
10 = Sierra de Pénjamo; 11 = Cerro de Palenque; 12 = Megaparque de la Ciudad de Dolores, Hidalgo; 13 = Las Fuentes; 14 = Parque
Metropolitano; 15 = Lago Crater La Joya; 16 = Presa de Silva y areas aledafias; 17 = Laguna de Yuriria y su zona de influencia; 18 =
Cerro del Cubilete; 19 = Cuenca de la Soledad; 20 = Presa de Neutla y su zona de influencia; 21 = Regién Volcanica Siete Luminarias; 22 =
Cuenca de la Esperanza; 23 = Pinal de Zamorano; and 24 = Sierra Gorda de Guanajuato. Note. *Dryophytes plicata (-) is found in the state
and is part of the herpetofauna of Guanajuato, but at the moment has not been recorded in any of the natural protected areas. This species
has been recorded the municipalities of Acambaro, Salvatierra, Sa José Iturbide, and Tierra Blanca.
;
= 16 [17 [18 [19 [20 [2 [22 [23 [28
Sphenomorphidae (1)
GERBERA Bee ne eee Sa eae eee
Scincella selvicola* al
Amphib. Reptile Conserv. 171 November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
Table 22 (continued). Distribution of herpetofaunal species in the Natural Protected Areas of Guanajuato, Mexico, based on herpetofaunal
surveys. Abbreviations are as follows: * = species endemic to Mexico and ** = non-native species. The numbers of the Natural Protected
Areas signify the following: 1 = Sierra de Lobos; 2 = Cuenca Alta del Rio Temascatio; 3 = Pefia Alta; 4 = Las Musas; 5 = Cerros el Culiacan
y La Gavia; 6 = Sierra de los Agustinos; 7 = Cerro de los Amoles; 8 = Cerro de Arandas; 9 = Presa La Purisima y su zona de influencia;
10 = Sierra de Pénjamo; 11 = Cerro de Palenque; 12 = Megaparque de la Ciudad de Dolores, Hidalgo; 13 = Las Fuentes; 14 = Parque
Metropolitano; 15 = Lago Crater La Joya; 16 = Presa de Silva y areas aledafias; 17 = Laguna de Yuriria y su zona de influencia; 18 =
Cerro del Cubilete; 19 = Cuenca de la Soledad; 20 = Presa de Neutla y su zona de influencia; 21 = Regién Volcanica Siete Luminarias; 22 =
Cuenca de la Esperanza; 23 = Pinal de Zamorano; and 24 = Sierra Gorda de Guanajuato. Note. *Dryophytes plicata (-) is found in the state
and is part of the herpetofauna of Guanajuato, but at the moment has not been recorded in any of the natural protected areas. This species
has been recorded the municipalities of Acambaro, Salvatierra, Sa José Iturbide, and Tierra Blanca.
Natural Protected Areas
sr [2 [3 [47s [6] 7 [8 [> [io] [ia fas [is |as [as] 7 [a8 [19 [20] 2a [22 [23 [20
Salvadora bairdi*
Senticolis triaspis
Tantilla bocourti*
Tantilla rubra
Trimorphodon tau
Dipsadidae (10)
Diadophis punctatus
Geophis dugesii*
Geophis latifrontalis*
Geophis petersii*
Hypsiglena jani
Hypsiglena tanzeri*
Rhadinaea gaigeae*
Rhadinaea hesperia*
Rhadinaea teaniata*
Elapidae (1)
Micrurus tener
Natricidae (8)
Storeria dekayi
Storeria storerioides*
Thamnophis cyrtopisis
Thamnophis eques
Thamnophis melanogaster*
Thamnophis pulchrilatus*
Thamnophis scalaris*
Thamnophis scaliger*
Typhlopidae (1)
Virgotyphlops braminus**
Viperidae (5)
Crotalus aquilus*
Crotalus atrox
Crotalus molossus
Crotalus polystictus*
Crotalus scutulatus
Testudines (3)
Kinosternidae (2)
Kinosternon hirtipes
Kinosternon integrum*
Emydidae (1)
Trachemys scripta**
Leptodeira septentrionalis
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172 November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
Table 23. Summary of the distributional status of the herpetofaunal species in the protected areas in Guanajuato, Mexico. Total =
total number of species recorded in all of the listed protected areas.
Distributional status
Non-endemic Country :
(NE) Endemie(CEy. jo oo maave NN)
a OS
BS
a
[Presa La Purisimay suzonadeinfuenca [| _17—Ss«dT SO Sd] CT COS
a TC
eS
Mewaparque de la Ciudad de Dolons Hidalgo [1 | -—-+| 1 ~~~*<| SSS
a CC A
a
or a
ee
EC Cr
[Presa de Newtlay suzonadeinfuencia =| —a7SCidT = Sf dT CT OCS
NC A
a OC
a 7
Pe TC
Number of
Protected area :
species
Volcanic Belt, the physiographic region of greatest
importance in Guanajuato, since the TVB contains a
herpetofauna almost equivalent to that of the Sierra
Madre Oriental, the largest number of country endemic
species, and the greatest number of high vulnerability
species.
In all 24 cases, the areas are demarcated. Only two of
the 24 areas encompass the full range of services; while
almost one-half of the areas provide either park guards, a
system of pathways, and facilities for visitors (five areas)
or administrative services, a system of pathways, and
facilities for visitors (six areas). Unfortunately, personnel
are present year-round in only seven of the 24 areas.
Similarly, only two of the 24 areas are not occupied to
some degree by private landowners.
Most herpetofaunal surveys in the protected areas only
have been partially completed, and although management
plans are available for most areas, they have not been
updated. Currently, plans are available for 20 areas, but
not for the other four areas.
Effectiveness of the Protected Areas in Guanajuato
In order to determine the effectiveness of the 24 protected
areas in Guanajuato, the available herpetofaunal records
have been assembled for each of these areas and the results
Amphib. Reptile Conserv.
are shown in Table 22, and summarized in Table 23.
Of the 101 species documented for the herpetofauna
of Guanajuato, 97 (96.0%) have been recorded in the 24
protected areas in the state (Table 23). Thus, all but four
species have been recorded for the compendium of the 24
protected areas. This favorable situation is far better than
has been reported in some other Mexican Conservation
Series entries.
The four species recorded for the state that have not
been reported from one or more of the protected areas
are: the hylid frog Dryophytes plicatus, the gekkonid
lizard Hemidactylus turcicus, the dipsadid snake
Geophis sartorii, and the natricid snake Adelophis copei.
Fortunately, three of these four species are native to
Guanajuato, while H. turcicus is a non-native species and
thus not desirable within the natural protected areas.
The numbers of protected areas (of a total of 24)
inhabited by the 97 species range from one to 19. The
sizes of the herpetofaunas of these 24 areas range from
one for the Megaparque de la Ciudad de Dolores, Hidalgo
to 69 for the Sierra Gorda de Guanajuato (mean, 24.8).
However, additional work is necessary to fully document
the herpetofauna of these natural protected areas.
In most cases, the number of country endemic species
in each area exceeds that of the non-endemic species (16
of 24 areas, or 66.7%). In the other eight cases, either the
November 2022 | Volume 16 | Number 2 | e321
The herpetofauna of Guanajuato, Mexico
numbers of these groups of species are the same (four
of 24 areas, or 16.7%) or the number of non-endemic
species is higher than the number of country endemic
species (four of 24 areas, or 16.7%).
All 40 of the non-endemic species and 53 of the 56
country endemic species (94.6%) have been recorded
in the compendium of the 24 protected areas. Although
their presence in the protected areas is not desirable,
four-fifths (9 species, or 80.0%) of the non-native
species have been recorded in one or more of the 24
areas. The most widely distributed non-native species
is Virgotyphlops braminus, which has been reported
in five of the 24 areas. Not surprisingly, this fossorial
snake is one of the two most widely distributed non-
native species in Mexico (Cruz-Elizalde et al. 2022).
What is surprising is that the other non-native species,
Hemidactylus frenatus (Cruz-Elizalde et al. 2022), has
been reported from only one of the 24 areas.
Conclusions and Recommendations
Conclusions
A. Presently, the herpetofauna of Guanajuato consists of
101 species, including 24 anurans, three salamanders,
71 squamates (25 lizards and 46 snakes), and three
turtles.
B. The numbers of herpetofaunal species recorded from
the three physiographic regions in Guanajuato range
from 60 in the Central Plateau to 75 in the Sierra
Madre Oriental.
C.The numbers of species shared among the
physiographic regions range from 44 between the
Central Plateau and the Sierra Madre Oriental to 56
between the Central Plateau and the Transmexican
Volcanic Belt. The Coefficient of Biogeographic
Resemblance values range from a low of 0.65 between
the Central Plateau and the Sierra Madre Oriental to
0.84 between the Central Plateau and the Transmexican
Volcanic Belt. The UPGMA dendrogram demonstrates
that the Central Plateau (CP) and the Transmexican
Volcanic Belt (TVB) cluster with one another at the
0.84 level and that the Sierra Madre Oriental (SM)
region clusters with the other two regions at the 0.65
level. This clustering pattern is consistent with the fact
that the CP and TVB regions are similarly large in size
within the state (Fig. 10) and are located adjacent to
one another, and that the SMO is the smallest region
in the state and is adjacent only to the CP region.
.The level of endemism in the Guanajuato
herpetofauna is relatively high. Of the 101 species
comprising the entire state herpetofauna, 56 (55.4%)
are country endemics including 12 anurans (50.0%
of 24 species), three salamanders (100% of three
species), 15 lizards (60.0% of 25 species), 25 snakes
(54.3% of 46 species), and one turtle (33.3% of three
turtles). Thirty-nine percent of the state endemics in
Amphib. Reptile Conserv.
174
Guanajuato are squamates of the genera Abronia (one
species), Barisia (one), Norops (one), Phrynosoma
(one), Sce/oporus (six), Plestiodon (two), Scincella
(one), Lepidophyma_ (two), Conopsis (two),
Lampropeltis (two), Leptophis (one), Pituophis (one),
Pseudoficimia (one), Salvadora (one), Tantilla (one),
Geophis (three), Hypsiglena (one), Rhadinaea (three),
Adelophis (one), Storeria (one), Thamnophis (four),
and Crotalus (two).
. The distributional status of the 101 members of the
Guanajuato herpetofauna is as follows (in order of
decreasing species numbers): country endemics (56,
55.4%); non-endemics (40, 39.6%); and non-natives
(5, 5.0%).
. The 40 non-endemic species are placed in the
following distributional categories: MXUS (26,
65.0%); USCA (six, 15.0%); MXCA (four, 10.0%);
MXSA (three, 7.5%); and USSA (one, 2.5%).
G. The principal environmental threats to the
herpetofauna of Guanajuato are agriculture, industry,
forestry, cattle production, and mining.
H. The conservation status of the herpetofauna of
Guanajuato was assessed using the SEMARNAT,
IUCN, and EVS systems. As with all previous MCS
studies, the SEMARNAT system was found to be of
minimal utility, inasmuch as only 44 of 96 species have
been evaluated using this system. Of these 44 species,
16 are allocated to the Threatened (A) category and
28 to the Special Protection (Pr) category. The use of
the SEMARNAT system does not appear to be biased
toward evaluating endemic species as opposed to non-
endemic species; although it has not been applied to a
sufficient segment of the Guanajuato herpetofauna to
be of much use.
Application of the IUCN conservation system by
category and the proportions of the 96 native species
in Guanajuato are as follows: EN (one species, 1.0%);
VU (nine, 9.4%); NT (three, 3.1%); LC (71, 74.0%):
DD (five, 5.2%); and NE (seven, 7.3%).
Application of the EVS system of conservation
assessment to the 96 native Guanajuato species
indicates that the categorical values increase from
low scores (31 species, 32.3%) to medium scores (41
species, 42.7%), and then decreases to high scores (24
species, 25.0%).
.A comparison of the IUCN and EVS conservation
status categorizations indicates that 41.7% of the 24
high vulnerability species (by EVS) are allocated to
one of the two IUCN “threat categories” (EN or VU),
and that 83.9% of the 31 low vulnerability species are
placed in the LC category. As in all previous MCS
studies, the correlation between the results of applying
the IUCN and EVS systems 1s relatively poor.
. An examination of the 83 native species (86.5% of all
96) placed into the IUCN DD, NE, and LC categories
demonstrates that many of these species have been
evaluated improperly when compared to their
November 2022 | Volume 16 | Number 2 | e321
Leyte-Manrique et al.
respective EVS values, so we indicated how these
species might be reassessed in the IUCN system to
better reflect their prospects for survival in perpetuity.
M.The RHP measure was utilized to ascertain the
conservation significance of the three regional
herpetofaunas in Guanajuato. This analysis
demonstrates that the most significant regional
herpetofauna is that of the Transmexican Volcanic
Belt, as it contains a herpetofauna only slightly smaller
than that of the Sierra Madre Oriental, the largest
number of country endemic species (43, 76.8% of 56
species), and the greatest number of high vulnerability
species (18, 26.1% of 69 species).
N. Twenty-four protected areas are established in
Guanajuato, most at the state level. Fourteen of these
areas are in the Transmexican Volcanic Belt, two
of which overlap onto the Central Plateau, and the
Transmexican Volcanic Belt is the most important
herpetofaunal region in the state. Unfortunately,
landowners occupy most areas, most herpetofaunal
surveys have only been partially completed, and
management plans are generally available but seldom
updated.
O. Collectively, the unusually high number of protected
areas are shown to harbor 97.0% of the species
recorded for the state of Guanajuato, which is a highly
desirable situation. Even so, much work remains to
be done to fully document the herpetofauna in these
protected areas.
P. The 97 species recorded in the state’s protected areas
includes all 38 of the non-endemic species and 55 of
the 56 country endemic species. In addition, although
not desirable in these areas, four of the five non-
native species also have been recorded. The most
widely distributed of these non-native species is
Virgotyphlops braminus.
Recommendations
A. This survey demonstrated that 97 of the 101 species
that comprise the herpetofauna of Guanajuato have
been recorded in the 24 protected areas established in
the state thus far. This is a highly desirable state of
affairs, and can be used as a starting point in securing
a future for the herpetofauna of this rather highly
urbanized state.
B. Evidently, however, the degree of completeness of the
herpetofaunal surveys varies from one protected area
to another. Thus, our most basic recommendation is
to provide additional studies in each of these areas,
especially those that are now the least studied.
C. Once reasonably complete herpetofaunal surveys
are available for each of the 24 natural protected
areas, monitoring programs can be established to
continually assess the health of populations of the
constituent species. Additionally, efforts should be
made to determine whether the two native species
Amphib. Reptile Conserv.
(Dryophytes plicatus and Adelophis copei) that have
not been recorded from any of the 24 areas can be
found, so they can be included in ongoing monitoring
programs.
D. These steps should be taken with urgency, given that
the small state Guanajuato is the 6" most populous
and the 5" most densely populated in the country.
“How to serve both humanity and the rest of life is the
great challenge of the modern era.”
Edward O. Wilson (2014)
Acknowledgments.—We are thankful to the following
people for providing some of the images used in this
paper: José Carlos Arenas-Monroy; Samuel Cadena-
Rico: Yadira Fabiola Estrada-Sillas; Maria del Carmen
Mendoza-Portilla, and Mara Fernanda Rodriguez-
Gutiérrez.
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Adrian Leyte-Manrique is a Biologist originally from Mexico City. He holds a Ph.D. in
Biodiversity and Conservation from the Biological Research Center of the Autonomous University
of the State of Hidalgo, Mexico. His interests are focused on the diversity, ecology, and conservation
of amphibians and reptiles in conserved and anthropized environments. Adrian has been an author
and co-author of several works dealing with the amphibians and reptiles of the states of Yucatan,
Hidalgo, and Guanajuato, including book chapters, books, notes, and articles in refereed and indexed
journals. He has been the director for 14 theses and a member of the thesis committees for 12 more
at the Doctoral level, as well as the director for a Master’s thesis. He currently works as a full-
time A-degree Research Professor, and directs residencies and theses on various topics. He teaches
courses on ecology, entomology, research workshops, and sustainable development at the Instituto
Tecnoldgico Superior de Salvatierra, Guanajuato, Mexico.
Amphib. Reptile Conserv.
Vicente Mata-Silva is a Herpetologist originally from Rio Grande, Oaxaca, Mexico. His interests
include the ecology, conservation, natural history, and biogeography of the herpetofaunas of
Mexico, Central America, and the southwestern United States. Vicente received a B.S. degree from
the Universidad Nacional Autonoma de México (UNAM), and MS. and Ph.D. degrees from the
University of Texas at El Paso (UTEP). Vicente is an Assistant Professor of Biological Sciences
at UTEP, in the Ecology and Evolutionary Biology Program, and Co-Director of UTEP’s Indio
Mountains Research Station, located in the Chihuahuan Desert of Trans-Pecos, Texas, USA. To
date, Vicente has authored or co-authored over 100 peer-reviewed scientific publications. He was
the Distribution Notes Section Editor for the journal Mesoamerican Herpetology, and is currently
Associate Editor for the journal Herpetological Review.
Oscar Baéez-Montes received his B.S. and M.S. degrees from the Universidad de Guadalajara
in Mexico. His interests include the ecology and conservation of terrestrial vertebrates and their
relationships to human communities. Oscar has worked with diverse groups of fauna in areas of
conservation importance, such as priority terrestrial regions, Ramsar sites, and natural protected
areas in the Mexican Plateau and Western Mexico. He is currently a part-time professor at the
Universidad Autonoma de Guadalajara in Mexico. He has three children, Ian, Max, and Regina, and
a loving wife Faby (also a Biologist) who accompanies him during his fieldwork.
November 2022 | Volume 16 | Number 2 | e321
Amphib. Reptile Conserv.
Leyte-Manrique et al.
Lydia Allison Fucsko, who resides in Melbourne, Australia, is an environmental activist and
amphibian conservationist. As a photographer with international publications, she has taken countless
amphibian photographs, including photo galleries of frogs mostly from southeastern Australia. Lydia
has a Bachelor of Humanities from La Trobe University (Bundoora, Victoria, Australia), a Diploma
in Education from the University of Melbourne (Parkville, Victoria, Australia), and postgraduate
diplomas in computer education and in vocational education and training from the University of
Melbourne (Parkville). Additionally, Lydia has a Master’s degree in Counseling from Monash
University (Clayton, Victoria, Australia). She received her Ph.D. in Environmental Education,
which promoted habitat conservation, species perpetuation, and global sustainable management,
from Swinburne University of Technology (Hawthorn, Victoria, Australia), while being mentored by
the late Australian herpetologist and scholar Michael James Tyler (Order of Australia recipient). As
a sought-after educational consultant, Lydia has academic interests that include: clinical psychology,
focusing on psychopathology; neuroscience and empathy; environmental education for sustainable
development; sentient ecology; academic writing; and creative writing, which includes poetry and
creative non-fiction books for children and young adults. Lydia is the senior author (with Boria
Sax) of a chapter in the 2019 Springer Encyclopedia of Sustainability in Higher Education entitled
“Learning activities for environmental education for sustainable development.” Recently, she has
co-authored an obituary of Jaime D. Villa, a study of the introduced Mesoamerican herpetofauna,
a treatment of the conservation prospects of the Mesoamerican salamander fauna, papers on the
herpetofauna of Veracruz and Querétaro, Mexico, a review of the books Advances in Coralsnake
Biology and Lizards of Mexico, Part 1, and a study on the biological and cultural diversity of
Oaxaca, Mexico, among several other academic papers. In 2020, the species Zantilla lydia, with the
suggested common name of Lydia’s Little Snake, was named in her honor.
Dominic L. DeSantis is an Assistant Professor of Biology at Georgia College and State University,
Milledgeville, Georgia, USA, in the Department of Biological and Environmental Sciences.
Dominic’s research interests broadly include the behavioral ecology, conservation biology, and
natural history of herpetofauna. In addition to ongoing collaborative projects associated with the
Mesoamerican Research Group, much of Dominic’s current research focuses on using novel animal-
borne sensor technologies to study the behavior of snakes in the field. While completing his Ph.D.
at the University of Texas at El Paso, Dominic accompanied Vicente Mata-Silva, Eli Garcia-Padilla,
and Larry David Wilson on survey and collecting expeditions to Oaxaca in 2015, 2016, and 2017,
and is a co-author on numerous natural history publications produced from those visits, including
an invited book chapter on the conservation outlook for herpetofauna in the Sierra Madre del Sur
of Oaxaca.
Eli Garcia-Padilla is a Social Biologist and Professional Photographer with more than 12 years
of experience in the formal study and photo documentation of the biological and cultural diversity
of Mexico. He has published one book, entitled Mexican Biodiversity: the Snake, the Jaguar and
the Quetzal, and more than 100 formal contributions on knowledge, the communication of science
and the conservation of Mesoamerican biodiversity. Since 2006, Eli has been exploring Oaxaca
and Chiapas, which are the most biodiverse and multicultural states in Mexico. In 2017, he began
to enter the mythical region of Los Chimalapas in the Isthmus of Tehuantepec, which is the most
biologically rich region in all of Mexico, under a community social conservation scheme. Eli has
published his photographic work in prestigious magazines such as National Geographic in Spanish
and Cuartoscuro. In 2020, he co-founded the Mesoamerican Biodiversity initiative with the aim of
creating a community around the dissemination of the most important wealth of Mexico, which is
its biodiversity and its culture. His writings are published regularly in Oaxaca Media, the Jornada
Ecologica and the Ojarasca Supplement of La Jornada.
Arturo Rocha is a Ph.D. student in the Ecology and Evolutionary Biology program at the
University of Texas at El Paso. His interests include the study of the biogeography, physiology, and
ecology of amphibians and reptiles in the southwestern United States and Mexico. A graduate of
the University of Texas at El Paso, his thesis centered on the spatial ecology of the Trans-Pecos Rat
Snake (Bogertophis subocularis) in the northern Chihuahuan Desert. To date, he has authored or
co-authored over 20 peer-reviewed scientific publications.
179 November 2022 | Volume 16 | Number 2 | e321
Amphib. Reptile Conserv.
The herpetofauna of Guanajuato, Mexico
_ Jerry D. Johnson is Professor of Biological Sciences at The University of Texas at El Paso, and
has extensive experience studying the herpetofauna of Mesoamerica, especially southern Mexico.
Jerry is the Director of the 40,000-acre Indio Mountains Research Station, was a co-editor on
Conservation of Mesoamerican Amphibians and Reptiles and co-author of four of its chapters. He
is also the senior author of the recent paper “A conservation reassessment of the Central American
herpetofauna based on the EVS measure” and is the Mesoamerica/Caribbean editor for the
Geographic Distribution section of Herpetological Review. Jerry has authored or co-authored over
142 peer-reviewed papers, including two 2010 articles, “Geographic distribution and conservation
of the herpetofauna of southeastern Mexico” and “Distributional patterns of the herpetofauna of
Mesoamerica, a Biodiversity Hotspot.” One species, Zantilla johnsoni, has been named in his honor.
Presently, Jerry is Co-chair of the Taxonomic Board for the journal Mesoamerican Herpetology.
Louis W. Porras graduated with a degree in Biology in 1971 from what today is known as Miami-
Dade College in Florida, USA. Over his career, he has authored or co-authored over 60 academic
publications, including the descriptions of two new species, and two taxa have been named in
his honor. Louis developed an interest in herpetology at an early age in his native Costa Rica.
His passion for the field led him to travel to many remote areas, including sites throughout the
Bahamas, the United States, Mesoamerica, and parts of South America. In 1968, he worked at the
Houston Zoological Gardens, and from 1982 to 1984 at Utah’s Hogle Zoo. In 1976, he attended
the inaugural meeting of the International Herpetological Symposium (IHS), and later served the
group as Vice-President and President. In 1993, along with Gordon W. Schuett, he helped launch
the journal Herpetological Natural History, and for the 20" anniversary of IHS, in recognition of his
contributions, three former Presidents dedicated the book Advances in Herpetoculture in his honor.
Louis’ career in publishing began in 1995, when he helped publish Fauna magazine as a member
of Canyonlands Publishing Group. In 2002, he founded Eagle Mountain Publishing, LC, which
has published such herpetological titles as Biology of the Vipers (2002), Biology of the Boas and
Pythons (2007), Amphibians, Reptiles, and Turtles in Kansas (2010), Conservation of Mesoamerican
Amphibians and Reptiles (2010), and Amphibians and Reptiles of San Luis Potosi (2013). From 2014
to 2018 Louis was the Publisher and Managing Editor of the journal Mesoamerican Herpetology,
and recently he was the Publisher and Co-editor of the book Advances in Coralsnake Biology: with
an Emphasis on South America.
Larry David Wilson is a herpetologist with lengthy experience in Mesoamerica. He was born
in Taylorville, Illinois, USA, and received his university education at the University of Illinois at
Champaign-Urbana (B.S. degree) and at Louisiana State University in Baton Rouge (M.S. and
Ph.D. degrees). He has authored or co-authored more than 470 peer-reviewed papers and books on
herpetology. Larry is the senior editor of Conservation of Mesoamerican Amphibians and Reptiles
(2010) and the co-author of seven of its chapters. His other books include The Snakes of Honduras
(1985), Middle American Herpetology (1988), The Amphibians of Honduras (2002), Amphibians &
Reptiles of the Bay Islands and Cayos Cochinos, Honduras (2005), The Amphibians and Reptiles
of the Honduran Mosquitia (2006), and Guide to the Amphibians & Reptiles of Cusuco National
Park, Honduras (2008). He is also the co-author of 14 previous entries in the Mexican Conservation
Series dealing with the herpetofauna of the states of Michoacan, Oaxaca, Chiapas, Tamaulipas,
Nayarit, Nuevo Leon, Jalisco, Puebla, Coahuila, Hidalgo, Veracruz, Querétaro, and Tabasco, as
well as the tri-state Mexican Yucatan Peninsula. In addition, he is a co-author of several significant
publications on the development and extensive application of the EVS measure and on conservation
issues related to the Mexican herpetofauna at the national level. To date, he has authored or co-
authored the descriptions of 76 currently-recognized herpetofaunal species, and seven species have
been named in his honor, including the anuran Craugastor lauraster, the lizard Norops wilsoni,
and the snakes Oxybelis wilsoni, Myriopholis wilsoni, and Cerrophidion wilsoni, as well as the
oligochaete annelid Pheretima wilsoni, and the coccidian parasite Caryospora wilsoni. In 2005,
he was designated a Distinguished Scholar in the Field of Herpetology at the Kendall Campus of
Miami-Dade College by the then-campus president Dr. Wasim Shomar. Currently, Larry is a Co-
chair of the Taxonomic Board for the website Mesoamerican Herpetology.
180 November 2022 | Volume 16 | Number 2 | e321
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
16(2) [General Section]: 181-214 (e322).
Contributions to the herpetofauna of the Angolan Okavango-
Cuando-Zambezi River drainages. Part 2: Lizards (Sauria),
chelonians, and crocodiles
12.3.*Werner Conradie, 2**°Chad Keates, *°’Luke Verburgt, **°°Ninda L. Baptista,
3.1 James Harvey, *?Timoteo Julio, and *Gotz Neef
'Port Elizabeth Museum, Beach Road, Humewood, Port Elizabeth 6013, SOUTH AFRICA *Department of Nature Conservation Management,
Natural Resource Science and Management Cluster, Faculty of Science, George Campus, Nelson Mandela University, George, SOUTH AFRICA
3National Geographic Okavango Wilderness Project, Wild Bird Trust, SOUTH AFRICA *Department of Zoology and Entomology, Rhodes University,
Grahamstown, SOUTH AFRICA °*South African Institute for Aquatic Biodiversity (SAIAB), Makhanda, SOUTH AFRICA °Enviro-Insight CC, Unit &
Oppidraai Office Park, Pretoria 0050, SOUTH AFRICA ‘Department of Zoology and Entomology, University of Pretoria, Pretoria, 0001, SOUTH
AFRICA *8CIBIO/InBio, Centro de Investigacao em Biodiversidade e Recursos Genéticos, Laboratorio Associado, Universidade do Porto, Campus
Agrario de Vairdo, Rua Padre Armando Quintas, 4485-661 Vairdo, PORTUGAL °Faculdade de Ciéncias, Universidade do Porto, Porto, PORTUGAL
'\BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Campus de Vairdo, 4485-661 Vairdo, PORTUGAL ''Harvey Ecological,
41 Devonshire Avenue, Howick, 3290, SOUTH AFRICA 'Fundagdo Kissama, Rua 60 Casa 560, Lar do Patriota, Luanda, ANGOLA
Abstract.—This work is the second report of the results obtained from a series of rapid biodiversity surveys
of the upper Cuito, Cubango, Cuando, Zambezi, and Kwanza River basins in Angola, which were conducted
between 2015 and 2019 in conjunction with the National Geographic Okavango Wilderness Project. The
herpetofauna of this region are poorly documented and the results of these surveys help to address the
knowledge gap regarding the conservation importance of this region. Here, an updated checklist is provided
for the current and historical records of lizards, chelonians, and crocodiles from the southeastern region of
Angola. A total of 369 new records were documented comprising 40 species, bringing the total number of
recognized lizard, chelonian, and crocodile species in this region to 58. These surveys documented four new
country records (i.e., Lygodactylus chobiensis, Agama armata, Pachydactylus wahlbergii, and Ichnotropis cf.
grandiceps) and increased the total number of reptile species known to occur in Angola (excluding snakes)
from approximately 157 to 161. Finally, updated distribution maps for the whole country are provided for all of
the species encountered in this study.
Key words. Africa, Cuanavale, Cuito, headwaters, Okavango Delta, reptile
Resumo.—Este trabalho é€ a segunda parte dos resultados de uma série de levantamentos rapidos de
biodiversidade realizados nas bacias dos rios Cuito, Cubango, Cuando, Zambeze e Kwanza em Angola, entre 2015
e 2019, em conjunto com o National Geographic Okavango Wilderness Project. A herpetofauna desta regiao esta
pouco documentada, e os resultados destes levantamentos ajudarao a colmatar a lacuna de conhecimento sobre
a importancia da sua conservagao. Aqui apresentamos uma lista atualizada de registos historicos e recentes
dos lagartos, quelonios e crocodilos do sudeste de Angola. Ao todo, foram documentado 369 novos registros,
relativos a 40 especies, elevando o numero total de espécies desses trés grupos na regiao para 58. Nestes
levantamentos foram registadas em Angola pela primeira vez quatro as espécies de lagartos (Lygodactylus
chobiensis, Agama armata, Pachydactylus wahlbergii, Ilchnotropis cf. grandiceps), aumentando o numero total
de especies conhecidas de répteis (excluindo cobras) de Angola de 157 para 161. Por fim, apresentamos mapas
de ocorréncia/distribuigao atualizados das espécies encontradas neste estudo para todo o pais.
Palavras-chave. Africa, Cuanavale, Cuito, Delta do Okavango, nascentes, réptil
Citation: Conradie W, Keates C, Verburgt L, Baptista NL, Harvey J, Julio T, Neef G. 2022. Contributions to the herpetofauna of the Angolan Okavango-
Cuando-Zambezi River drainages. Part 2: Lizards (Sauria), chelonians, and crocodiles. Amphibian & Reptile Conservation 16(2) [General Section]:
181-214 (e322).
Copyright: © 2022 Conradie et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Accepted: 18 November 2022; Published: 8 December 2022
Correspondence. *werner@bayworld.co.za
Amphib. Reptile Conserv. 181 December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
Introduction
A surge of studies on the Angolan herpetofauna has
occurred in the last decade, including numerous new
species descriptions. This is especially true for lizards
(Order Sauria), with 28 species newly described during
this period (Conradie et al. 2012, 2022; Stanley et al.
2016; Branch et al. 2019a, 2021; Marques et al. 2019a,b,
2020, 2022a,b; Ceriaco et al. 2020a,b,c; Lobon-Rovira et
al. 2021, 2022a; Parrinha et al. 2021; Wagner et al. 2021),
and many more descriptions in preparation (e.g., Bates
et al., pers. comm.). In addition, the taxonomic revisions
in those studies have further refined the number of lizard
species occurring in Angola, and they are the result of
numerous collaborative biodiversity surveys which have
also added many new country records (Marques et al.
2020; Lobon-Rovira et al. 2022b).
The most recent synthesis of Angolan reptiles,
excluding snakes (Conradie et al. 2021), set the national
total at 145 species (Marques et al. 2018; Branch et
al. 2019b). Considering the new additions mentioned
above and the results of taxonomic revisions since 2018,
this elevates the total number of recognized species of
lizards, chelonians, and crocodiles for Angola to 157
(excluding cases of unconfirmed subspecies status). The
currently known Angolan lizard richness is nearly half
that of South Africa (157 versus 286 species), a country
almost equivalent in size and biome diversity (Branch et
al. 2019b). This is higher than in neighboring countries to
the east and north (Botswana ~74, Democratic Republic
of the Congo [DRC] ~105, and Zambia ~81), and
slightly lower than countries to the south (Namibia ~178)
(Pietersen et al. 2021; Uetz et al. 2022; W. Conradie,
unpub. data).
Branch et al. (2019b) predicted that at least 75 new
lizard species will be added to the growing national list,
and if the current rate of ~4 species per year is maintained,
this estimate will be exceeded in less than two decades.
This will make Angola one of the most herpetofauna-rich
countries in mainland Africa.
This paper is the second installment in a series of
articles which document the herpetofauna of the poorly
studied southeastern Angolan region. The first provided
a synthesis of the snakes of this region (Conradie et
al. 2021), while the present paper focuses on lizards,
chelonians and crocodiles, and a third paper on the
amphibians is in preparation. The overarching aim of this
project is to document and quantify the herpetofaunal
diversity and richness of southeastern Angola, and
improve our knowledge of the conservation importance
of this area in both regional and national contexts.
Methods
See Conradie et al. (2021) for details on the number
of surveys conducted, as well as a description of the
study area, sampling techniques, and species mapping
Amphib. Reptile Conserv.
procedure. The specific methods pertaining to this paper
are provided here.
Species Identification and Morphology
Upon completion of the fieldwork component of this
study, preliminary species identifications were made
using relevant field guides or published identification
keys (FitzSimons 1943; Branch 1998; Pietersen et al.
2021) and through comparisons with material housed in
the Port Elizabeth Museum (PEM). Nomenclature was
based on the online Reptile Database (Uetz et al. 2022)
and was updated as needed. Common names follow
Marques et al. (2018) and Pietersen et al. (2021).
Snout-vent length (SVL, measured from the tip of
the snout to the posterior end of the cloacal scale or
vent opening) and tail length (TL, measured from the
cloacal opening to the tip of the tail) were measured
to the nearest 0.1 mm using a digital calliper. For the
sake of brevity, in presenting these measurements, the
SVL is presented first, followed by an addition sign
(+) and then the TL is given. The following basic scale
counts were also documented using a Nikon SMZ1270
binocular stereo microscope: number of scale rows at
midbody; number of transverse scale rows dorsally
(along the vertebral line, from the nuchal [excluded
from count] to base of the tail; except for Lacertidae and
Agamidae, where this was counted from the shoulder
to the base of the tail); number of transverse scale rows
ventrally (along the midline, from the mental [excluded
from count] to the cloacal plate [excluded]; except for
Lacertidae and Agamidae, where they were counted from
the shoulder to the groin); number of longitudinal rows
of ventral scales or enlarged ventral plates in Lacertidae
and Gerrhosauridae; number of subdigital lamellae under
4‘ toe; number of supraciliaries; number of supralabials
(in Lacertidae, but in Scincidae only those anterior to the
subocular were counted); number of infralabials; number
of femoral or precloacal pores (including number of
rows, as observed in agamids); and maximum number of
keels per scale. Where scale or pore counts are presented
from both sides of the body they are separated by a slash
(/) with the right counts given first, then the left counts.
For amphisbaenids, the following additional scale counts
were recorded: number of body annuli (counted dorsally
from behind the head shields to anterior to the precloacal
shield) and number of caudal annuli (counted ventrally
from the posterior cloacal cap to the last annulus). Each
scale count is presented as a range with the average in
parentheses.
Results
The surveys yielded a total of 283 individual lizard, 12
chelonian, and 74 crocodile records from approximately
321 unique localities in southeastern Angola, primarily
around the source lakes of the Cuito, Cuanavale, Cuando
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
and Quembo rivers. Herpetofauna trap arrays (see
Conradie et al. 2021) were deployed for a total of 240
trap nights and resulted in the capture of 68 specimens
comprising 12 species (Table 1). A total of 30 lizard
species (comprising eight families and 17 genera), four
chelonians (two families and two genera), and one
crocodile were recorded during this study (Table 2). Five
additional species (Acanthocercus margaritae, Afroedura
wulfhaackei, Ichnotropis bivitatta, | Hemidactylus
mabouia, and Trachylepis sulcata ansorgii) are reported
here. Although they were not collected from the defined
core study area, these species are expected to occur
within this area. Updated Angolan species distribution
maps are provided for each of the 40 species discussed in
this paper (Maps 1—40). The mapping exercise included
collating 1,665 unique records: 626 historical records
from Marques et al. (2018), 261 additional literature
records, 171 virtual museum records, and 507 additional
records mostly from our surveys or unpublished records
in the Port Elizabeth Museum and Ditsong National
Museum of Natural History (formerly Transvaal Museum,
TM) collections. This mapping exercise increased the
number of Angolan records for the 40 species of lizards,
chelonians, and crocodiles by 65.6%.
Fig. 1. Adult female Acanthocercus cf. cyanocephalus (PEM
R23560) from Quembo River source. Photo by Werner
Conradie.
Fig. 2. Adult male Acanthocercus cf. cyanocephalus (PEM
R27387) from Luvu River camp. Photo by Chad Keates.
Amphib. Reptile Conserv.
What follows is a checklist of all lizard, chelonian, and
crocodile species found during these surveys. The account
for each species includes a list of material examined, brief
descriptions of newly collected material, and comments
on habitat/natural history and taxonomy. Detailed
morphological data and natural history notes, mostly for the
adult material, can be found in Supplementary Table 1 at:
https://doi.org/10.6084/m9 figshare.21670706.v1. The
new distributional data used to compile the distribution
maps can be found in Supplementary Table 2 at:
https://doi.org/10.6084/m9 figshare.21670676. Abbrev-
lations: asl, above sea level; DOR, dead on road; ‘t’
after measurements refers to truncated, and ‘r’ refers to
regenerated.
Reptilia
Squamata
Sauria
Agamidae
Acanthocercus cf. cyanocephalus (Falk, 1925)
Angolan or Western Tree Agama (Figs. 1-2, Map 1)
Material (9 specimens): PEM R23267, Cuanavale
River source, -13.09330° 18.89396°, 1,367 m asl; PEM
R23318, Cuito River source, -12.68935° 18.36012°,
1,435 m asl; PEM R23480, Cuando River source,
-13.00164° 19.12960°, 1,372 m asl; PEM R23503,
Sombanana village, -12.31082° 18.62392°, 1,403 m
asl; PEM R23517, near Cuito River source, -12.68563°
18.36686°, 1,460 m asl; PEM R23529, INBAC: WC-
4588, drive back from Quembo River source, -13.10543°
19.01698°, 1,555 m asl; PEM R23560, old hunters camp
near Quembo River source, -13.13167° 19.09639°, 1,290
m asl; PEM R27387, Luvu River camp, -13.71200°
21.83538°, 1,082 m asl. Description: The absence of
an enlarged occipital scale and its arboreal habits allow
the distinction between sympatric congeners and Agama
f
Elevation (m)
5
Oo
Oo
12 14 16 18 20 22 24
Map 1. Distribution of Acanthocercus cf. cyanocephalus in
Angola. Historical records are indicated by white dots while
all new records are indicated by black dots. Axis values are
in degrees (°). Purple polygon — Okavango River basin, blue
polygon — Cuando River basin, brown polygon — Zambezi
River basin.
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
Table 1. Herpetofauna drift fence funnel trap array sites for the 2016-2019 surveys, with coordinates presented in the WGS84
datum, elevation, brief habitat description, number of days installed (expressed as “trap nights”), and number of captures. R = river.
- : P Elevation : Bir Trap
Trap site Latitude Longitude (m asl) Habitat description Dates nights Captures
Cuito R. 1 -12.688693 | 18,360164 eae | Marenmal Vegetation at 15-25 Feb 2016
source lake
Cuito R. 2 -12.688956 18.361870 1,438 Miombo woodland 15-25 Feb 2016
Cuito R. 3 -12.686020 | 18.364500 {Ai Notes ule ane slope 16-25 Feb 2016
with scattered shrubs
Cuanavale R. 1 -13.088937 | 18.892570 (a6) | Yaremalerassy 27 Feb-15 Mar 2016
vegetation at source lake
Cuanavale R. 2 -13.092677 | 18.895518 4357 _| Motemal erassy 27 Feb-15 Mar 2016
vegetation at source lake
Degraded/secondary
Cuanavale R. 3 -13.092813 18.894921 1,361 miombo woodland and 28 Feb-15 Mar 2016
grass
Cuanavale R. 4 -13.050780 | 18.897450 1396: | DANS Dash with 30 Feb-15 Mar 2016
scattered grass
Quembo R. 1 -13.135917 19.044167 1,369 | Marginal grassy 27 Oct-11 Nov 2016
vegetation at source lake
Quembo R. 2 -13.135444 19.043972 1,375 Miombo woodland 27 Oct-11 Nov 2016
Quembo R. 3 -13.130725 19.037245 1,443 Miombo woodland 29 Oct-11 Nov 2016
Quembo R. 4 -13.135863 | 19.047088 i363 | Mateial grassy 27 Oct-11 Nov 2016
vegetation at source lake
Cuando R. 1 -13.003929 | 19.128079 (550 =| ateipal sassy 12-23 Nov 2016
vegetation at source lake
4
2
2
4
2
Cuando R. 2 -13.004259 | 19.127187 1,350 | Marginal grassy 12-23 Nov 2016
vegetation at source lake
Cuando R. 3 -13.003337 | 19.135640 1,360 13-23 Nov 2016
Degraded/secondary
Cuando R. 4 -13.001637 19.129598 1,374 miombo woodland and 13-23 Nov 2016
grass
21
LungwebunguR.2 | -12.581990 | 18.665616 1,208 | Miombo woodland 21-25 Apr 2018
LungwebuneuR.3 | -12.580561 | 18.664190 1,302 21-25 Apr 2018
21
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
10
Lungwebungu R. 1 -12.580126 18.667396 1,298 Miombo woodland —25 Apr 2018
1
3
LungwebunguR.4 | -12.578694 | 18.664674 1,305 ~25 Apr 2018
3
3
Lower Quembo R.1 | -13.52801 19.28147 ose | Matemal casey: 23-29 Nov 2019
vegetation next to river
23
3
1
5
4
Lower Quembo R. 2 -13.52816 19.28067 1,240 Miombo woodland —29 Nov 2019
Lower Quembo R.3 | -13.52778 19.27455 1,256 23-29 Nov 2019
Lower Quembo R.4 | -13.25658 19.27810 ode. | Cicteultivated lands: 23-29 Nov 2019
fallow fields
Degraded/secondary
Luanguinga R. 1 -13.70885 21.26234 1,116 miombo woodland and 1—2 Dec 2019
grass
Lake Hundo 1 -14.99158 2163096 1,100 4-6 Dec 2019
Lake Hundo 2 -14.97279 21.62890 1,102 Miombo woodland 4—6 Dec 2019
Lake Hundo 3 -14.97002 21.63139 iige. | Deeded) secondaby 4-6 Dec 2019
miombo and grass
Table 2. Species of lizards, chelonians, and crocodiles recorded in the three Angolan Okavango-Cuando-Zambezi River basins.
? = not recorded from the core study area, but expected to occur based on nearby records.
3
2
0
0)
8
8
7
5
3
3
2
2
1
1
0
0
4
4
4
4
7
7
7
7
1
2 ]
2
2
. Okavango River Cuando Zambezi River
Species ; ; . : Source of records
Basin River Basin Basin
Agamidae
Acanthocercus cf. cyanocephalus (Falk, 1925) x x x This study; Managas 1963; Laurent 1964
Acanthocercus margaritae Wagner, Butler, x Monard 1937
Ceriaco, and Bauer, 2021
Amphib. Reptile Conserv. 184 December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
Table 2 (continued). Species of lizards, chelonians, and crocodiles recorded in the three Angolan Okavango-Cuando-Zambezi
River basins. ? = not recorded from the core study area, but expected to occur based on nearby records.
Species
Agama aculeata Merrem, 1820
Agama armata Peters, 1855
Agama schacki Mertens, 1938
Amphisbaenidae
Dalophia angolensis Gans, 1976
Dalophia ellenbergeri (Angel, 1920)
Dalophia pistillum (Boettger, 1895)
Monopeltis anchietae (Bocage, 1873)
Monopeltis infuscata Broadley, 1997
Zygaspis nigra Broadley and Gans, 1969
Zygaspis quadrifrons (Peters, 1862)
Chamaeleonidae
Chamaeleo dilepis Leach, 1819
Chamaeleo gracilis Hallowell, 1844
Gekkonidae
Afroedura wulfhaackei Branch, Schmitz,
Loboén-Rovira, Baptista, Antonio, and
Conradie, 2021
Chondrodactylus laevigatus (Fischer, 1888)
Hemidactylus mabouia (Moreau De Jonnés,
1818)
Hemidactylus nzingae Ceriaco, Agarwal,
Marques, and Bauer, 2020
Lygodactylus angolensis Bocage, 1896
Lygodactylus nyaneka Marques, Ceriaco,
Buehler, Bandeira, Janota, and Bauer, 2020
Lygodactylus chobiensis FitzSimons, 1932
Lygodactylus tchokwe Marques, Ceriaco,
Buehler, Bandeira, Janota, and Bauer, 2020
Pachydactylus cf. punctatus Peters, 1855
Pachydactylus wahlbergii (Peters, 1869)
Gerrhosauridae
Gerrhosaurus auritus Boettger, 1887
Gerrhosaurus cf. nigrolineatus Hallowell,
1857
Tetradactylus ellenbergeri (Angel, 1922)
Lacertidae
Ichnotropis bivittata Bocage, 1866
Ichnotropis capensis (Smith, 1838)
Ichnotropis cf. grandiceps Broadley, 1967
Heliobolus lugubris (Smith, 1838)
Amphib. Reptile Conserv.
Okavango River
Basin
Cuando
River Basin
185
Zambezi River
Basin
x
x
Source of records
Monard 1937; Managas 1963; Laurent 1964
This study; Conradie et al. 2016 (as A.
aculeata)
This study
Monard 1937; Laurent 1964; Gans 1976
This study; Branch and McCartney 1992 (as
D. pistillum)
Monard 1937
Monard 1930, 1937
Broadley et al. 1976
This study; Broadley and Gans 1969, 1975
Monard 1931; Conradie et al. 2016
This study; Mertens 1937; Monard 1937;
Managas 1963; Laurent 1964; Conradie et al.
2016.
Laurent 1964
Conradie et al. 2016
Ceriaco et al. 2020a
This study
This study; Conradie et al. 2016 (as L.
bradfieldi)
This study
Marques et al. 2020
This study
This study
This study
This study; Monard 1937; Conradie et al. 2016
This study; Laurent 1964; Conradie et al. 2016
Monard 1937; Managas 1973
This study; Branch and McCartney 1993;
Conradie et al. 2016
This study
Conradie et al. 2016
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
Table 2 (continued). Species of lizards, chelonians, and crocodiles recorded in the three Angolan Okavango-Cuando-Zambezi
River basins. ? = not recorded from the core study area, but expected to occur based on nearby records.
Species
Meroles squamulosus (Peters, 1854)
Nucras scalaris Laurent, 1964
Scincidae
Acontias jappi Broadley, 1968
Acontias kgalagadi Lamb, Biswas, and Bauer,
2010
Eumecia anchietae Bocage, 1870
Lubuya ivensii (Bocage, 1879)
Mochlus sundevallii (Smith, 1849)
Panaspis maculicollis Jacobsen and Broadley, 2000
Panaspis wahlbergii (Smith, 1849)
Panaspis sp.
Sepsina angolensis Bocage, 1866
Trachylepis albopunctata (Bocage 1867)
Trachylepis bayonii (Bocage, 1872)
Trachylepis chimbana (Boulenger, 1887)
Trachylepis damarana (Peters, 1870)
Trachylepis punctulata (Bocage, 1872)
Trachylepis spilogaster (Peters, 1882)
Trachylepis sulcata ansorgii (Peters, 1882)
Trachylepis wahlbergii (Peters, 1869)
Typhlacontias rohani Angel, 1923
Varanidae
Varanus albigularis (Daudin, 1802)
Varanus niloticus (Linnaeus, 1766)
Crocodylidae
Crocodylus niloticus Laurent, 1768
Order: Testudines
Pelomedusidae
Pelomedusa subrufa (Bonnaterre, 1789)
Pelusios bechuanicus FitzSimons, 1932
Pelusios nanus Laurent, 1956
Pelusios rhodesianus Hewitt, 1827
Testudinidae
Kinixys belliana Gray, 1863
Stigmochelys pardalis (Bell, 1828)
Species totals: 58
Amphib. Reptile Conserv.
Okavango River
Basin
x
x
~
~
x
44
Cuando
River Basin
x KKK
186
Zambezi River
Basin
x
~~ x
~*~
32
Source of records
This study; Conradie et al. 2016
Baptista et al. 2020
Broadley 1968
Conradie and Bourquin 2013; Conradie et al.
2016
This study; Monard 1931, 1937
This study; Managas 1963; Conradie et al.
2016
Conradie et al. 2016
Conradie et al. 2016
Ceriaco et al. 2020
This study
This study; Monard 1931, 1937; Branch and
Haagner 1992
This study; Laurent 1964; Conradie et al. 2016
This study; Monard 1937
Laurent 1964
This study; Conradie et al. 2016 (as 7. varia),
Weinell and Bauer 2018
This study
This study; Conradie et al. 2016
This study; Conradie et al. 2016
This study; Angel 1921; Monard 1931;
Conradie et al. 2016
Monard 1937
This study; Monard 1937; Managas 1963;
Conradie et al. 2016
This study; Monard 1937; Branch and
Haagner 1992; Conradie et al. 2016
Monard 1931, 1937; Conradie et al. 2016
This study; Laurent 1964; Conradie et al. 2016
This study; Monard 1937; Laurent 1964
This study; Monard 1937; Laurent 1964
This study; Monard 1937; Laurent 1964;
Conradie et al. 2016; Kindler et al. 2016
Conradie et al. 2016
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
spp. Large agamid with blue head, chest, and shoulders,
mostly in males; 122-148 (133) dorsal scale rows at
midbody; 68—74 (71) transverse ventral scales; 78-95
(87) transvers dorsal scales; 11-13 supralabials; 11-15
infralabials; 22-26 (24) subdigital lamellae under 4"
toe; 17-35 precloacal pores in 2—3 rows. Largest female:
174.0 + 192.0 mm (PEM R23560); largest male: 137.0 +
162.0 mm (PEM R27387). The new material presented
here represents the largest recorded sizes of both male
and female for the species (Pietersen et al. 2021; Wagner
et al. 2021). Habitat and natural history notes:
Juveniles were collected in February from the bases of
large trees in miombo woodland, while gravid females
were collected in October. Adult specimens were found
very close to holes in trees, into which they retreated
when approached. Comments: Wagner et al. (2018)
initially assigned all Angolan Acanthocercus material
to A. cyanocephalus, and although they provided a
detailed account of Falk’s work in Angola, they assigned
a specimen from northern Zambia as the neotype, and
only examined three Angolan specimens from a single
locality. Numerous records of Acanthocercus are known
across the entire extent of Angola, and recent studies
(Marques et al. 2018; Butler et al. 2019) allude to the
fact that cryptic species are present in Angola. Follow-
up studies (Wagner et al. 2021; Marques et al. 2022b)
focused primarily on Namibian and Angolan material
and further subdivided this group into three species: A.
margaritae, ranging from northern Namibia northwards
into central and western Angola, A. ceriacoi from north-
western Angola, and A. cyanocephalus from eastern
Angola. While these studies made use of integrative
taxonomy, they only used a single gene (a fragment of
the 16S rDNA) and a small morphological dataset to
support their results. The genetic differences among
the Acanthocercus atricollis group, which includes A.
atricollis, A. branchi, A. ceriacoi, A. cyanocephalus, A.
margaritae, A. gregorii, and A. ugandaensis, are very
small (< 5%) and additional phylogenetic work is needed
to support the current taxonomy. Based on geographic
proximity, we tentatively assign our material collected
from the eastern side of our study area to A. cyanocephalus,
pending the results of further phylogenetic work.
Acanthocercus margaritae Wagner, Butler, Ceriaco, and
Bauer, 2021
Margarita’s Tree Agama (Map 2)
Material (1 specimen): PEM R20011, Huambo HALO
training site, -12.73722° 15.81825°, 1,670 m asl.
Description: Juvenile male specimen, measuring 55.9 +
72.0 mm; 120 scale rows at midbody; 76 transvers ventral
scales; 76 transverse dorsal scales; 12/13 supralabials;
11/12 infralabials; 24 subdigital lamellae under 4" toe;
18 precloacal pores in two rows. Habitat and natural
history notes: This specimen was found basking in the
early morning on the shade cloth erected around the
ablution blocks of the compound. Comments: Most
Amphib. Reptile Conserv.
historical material from central and western Angola has
been reassigned to this recently described species, A.
margaritae (Wagner et al. 2021). Since our record is from
the known distribution of A. margaritae, we tentatively
assign it to this species, pending further phylogenetic
results. This species was not recorded from within the
core study area, but based on historical records (Monard
1937), it is expected to occur in the western side of the
study area.
Agama armata Peters, 1855
Peter’s Ground Agama (Figs. 3—4, Map 3)
Material (12 specimens): PEM R23252, Cacundu
falls, -13.77390° 18.75520°, 1,281 m asl; PEM R23310,
between Cuchi River to Menongue, -14.67986°
17.17512°, 1,391 m asl; PEM R23319, Cuito River
source lake, -12.68935° 18.36012°, 1,435 m asl; PEM
R23356, Cuito River source lake, grasslands, -12.67756°
18.35589°, 1,495 m asl; PEM R23380, Kuvango River
old hydro plant site, -14.38754° 16.30166°, 1,438 m
asl; PEM R23391, camp near Malova Village, Mipanha
River, -14.09140° 16.41476°, 1,569 m asl; PEM R23407,
Lungwebungu River bridge crossing, -12.58346°
18.66598°, 1,304 m asl; PEM R23520, grassland west
of Cuanavale River source, -13.01347° 18.81669°, 1,538
m asl; PEM R23994 (iNaturalist 12154222), Aquaculture
farm outside Cuito town, -12.439722° 16.89833°, 1,691
m asl; PEM R27388, Luvu River camp, -13.71200°
21.83538°, 1,082 m asl; INBAC: WC-5169, Huambo
HALO training site, -12.73726° 15.81828°, 1,665 m asl;
INBAC: WC-4574, Lungwebungu River bridge crossing,
-12.58347° 18.66598°, 1,294 m asl. Description: In
juveniles, the ventral scales are more keeled and the
ventrum has small, black-edged white circular blotches
that seem to fade or disappear with age. The gular region
is spotted in both juveniles and adults, although more
defined in juveniles. Dorsal scales strongly keeled with
nine rows of enlarged scales arranged in longitudinal
rows; 89-97 (93) scale rows at midbody; 71-81 (76)
transverse ventral scale rows; 45-62 (54) transverse
dorsal scale rows; 11—14 supralabials; 10—13 infralabials;
f
Elevation (m)
5
So
oOo
Map 2. Distribution of Acanthocercus margaritae in Angola.
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
f
Ya
">
=> > - >
“3 -
‘ee Pee
Fig. 3. Adult male Agama armata (PEM R23252) from
Cacundu Falls. Photo by Werner Conradie.
Fig. 4. Gravid female Agama armata (PEM R27388) from
Luvu River camp. Photo by Chad Keates.
15-18 (16) subdigital lamellae under 4" toe; 10-12
precloacal pores ina single row. Largest female: 88.5 +95.0
mm (INBAC: WC-4574); largest male: 85.9 + 113.0 mm
(PEM R23380, new maximum size). Habitat and natural
history notes: Juveniles were collected in February, while
gravid females were collected in October. Comments:
Species identification was based on the gular pattern
(spotted versus striped in A. aculeata) as documented by
Jacobsen (1992). Re-examination of a specimen recorded
as A. aculeata from north of Cachingues in Conradie et
al. (2016) also conforms to this species. Although some
historical Angolan material was referred to A. armata (see
Bocage 1895; Boulenger 1905), Marques et al. (2018)
regarded all material from Angola as A. aculeata, and
mention that A. armata is ‘extralimital’ and restricted to
southeastern South Africa. In contrast, A. armata has been
regularly documented from adjacent Zambia (Broadley
1971; Pietersen et al. 2017, 2021; Bittencourt-Silva
2019). All available historical Angolan material under the
names A. aculeata and A. armata, especially those from
eastern Angola (Manacas 1963; Laurent 1964), needs to
be re-examined to establish the true identification and full
extent of the ranges of these two species in Angola. It is
noteworthy that members of the Agama aculeata-armata
group are genetically similar, which may necessitate
the synonymy of these species in the future (Leaché et
Amphib. Reptile Conserv.
Elevation (m)
3
So
Oo
12 14 16 18 20 22 24
Map 3. Distribution of Agama armata in Angola.
al. 2014). If the specific status of these two species is
confirmed, then both might be present in Angola, with
A. aculeata restricted to the more arid western regions of
Angola and A. armata to the more mesic eastern regions.
Agama schacki Mertens, 1938
Schack’s Rock Agama (Fig. 5, Map 4)
Material (16 specimens): PEM R23367, en route
to Cuito, east of Huambo, -12.73615° 15.97442°,
1,777 m asl; PEM R23381—7, INBAC: WC-5208-9,
campsite near old Cuvango Mission on Cubango River,
-13.32887° 16.41167°, 1,520 m asl; PEM R23395—
400, INBAC: WC-5162, Cubango River near source,
-12.66256° 16.09324°, 1,764 m asl. Description: Large,
rupicolous agama. Male with orange head and tail; 84—
101 (92) scale rows at midbody; 80—94 (88) transverse
ventral scale rows; 71-80 (74) transverse dorsal scale
rows; 9-11 supralabials; 9-12 infralabials; 21-24 (22)
subdigital lamellae under 4 toe; 11-13 precloacal pores
in a single row. Largest female: 102.3 + 142.0 mm (PEM
R23383); largest male: 118.0 + 95t mm (PEM R23387
had the longest intact tail which measured 173 mm [1.5 x
SVL]). Habitat and natural history notes: Individuals
were associated with large rocky outcrops, especially
along the upper Cubango River. Comment: Based on the
higher midbody scale counts, we can confidently assign
our material to the A. schacki group (Mertens 1938).
Ignoring the erroneous records of Monard (1937) from
Cuando Cubango Province, our material represents the
most easterly records for this species. The status of the
Angolan Rock Agamas was briefly discussed by Ceriaco
et al. (2014). Preliminary phylogenetic results indicate
that.A. schacki should be treated as a full species, and that
more cryptic species are present in the larger Angolan
Rock Agama group (Marques et al. 2018; Butler 2020).
We follow these studies and treat A. schacki as a distinct
species from A. planiceps, restricting the latter to the
arid regions of the Namibe Province, and we treat all
other records as A. aff. schacki until the taxonomic
status of the cryptic species are addressed. Butler
(2020) lacked genetic material from central Angola,
and our material may potentially represent either of the
two inland clades identified in that study. Since efforts
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
Fig. 5. Adult male Agama schacki (PEM R23367) from near
source of the Cubango River. Photo by Werner Conradie.
to separate the species in the Agama planiceps complex
are still ongoing, we produced a map for the entire
species complex (Map 4).
Amphisbaenidae
Dalophia ellenbergeri (Angel, 1920)
Ellenberger’s Worm Lizard (Fig. 6, Map 5)
Material (4 specimens): PEM R23408, Lungwebungu
River camp bridge crossing, -12.58346° 18.66598°,
1,304 m asl; PEM R23492, Cuanavale River source lake,
-13.09442° 18.89372°, 1,396 m asl; PEM R24002, 5 km
west of Cuemba, -12.14751° 18.11650°, 1,329 m asl;
PEM R27392, Quembo River bridge camp, -13.52745°
19.2806°, 1,241 m asl. Description: All specimens
exhibit the diagnostic ‘herringbone’ scale arrangement
on the dorsal side of the tail; 16—21 dorsal segments per
body annulus; 12—14 ventral segments per body annulus;
309-319 body annuli; 29-43 caudal annuli; caudal
autonomy site at the 8" caudal annulus; 3—4 supralabials;
3 infralabials. Largest specimen: 336.0 + 76.0 mm
(PEM R27392). Habitat and natural history notes: All
specimens were excavated from sandy soils, except for
one individual that was found on the surface after heavy
rain and another which was found taking refuge under
a tree log. Comments: Angola has one of the richest
Fig. 6. Adult Dalophia ellenbergeri (PEM R23408) from
Lungwebungu River. Photo by Werner Conradie.
Amphib. Reptile Conserv.
Elevation (m)
oS
i=)
Oo
Map 4. Distribution of Agama planiceps complex in Angola.
assemblages of amphisbaenians in Africa, represented
by three genera and 11 species (Marques et al. 2018).
The taxonomy of Angolan amphisbaenians has a turbid
history, and many of the species have not been evaluated
in a phylogenetic framework. The only phylogenetic
study on African amphisbaenians incorporated only one
Angolan sample (Measey and Tolley 2013). Dalophia
ellenbergeri was first reported from Angola by Branch and
McCartney (1992) under the name D. pistillum and later
re-identified as D. ellenbergeri (Broadley 1997). This is
only the second time this species has been recorded from
Angola and it is now documented from four additional
localities. Elsewhere it 1s only recorded from western
Zambia (Broadley 1971; Pietersen et al. 2021).
Zygaspis nigra Broadley and Gans, 1969
Black Round-headed Worm Lizard (Fig. 7, Map 6)
Material (3 specimens): PEM R23564—5, Samanunga
village, -12.93250° 18.81476°, 1,363 m asl; PEM
R23984, Lungwebungu River crossing, -12.58020°
18.66773°, 1,298 m asl. Additional records: Quembo
River source, -13.13586° 19.04709°, 1,368 m asl
(stomach contents of Xenocalamus mechowii — PEM
R23463). Description: Male (PEM R23564) with four
precloacal pores; hemipenis bifurcated and extending
to 6-7" caudal annuli. Female (PEM R23564) with
Elevation (m)
5
Oo
oO
Map 5. Distribution of Dalophia ellenbergeri in Angola.
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
ny
whi mies K. il *~)
7]
“omy mr
sg a
Fig. 7. Adult Zygaspis nigra (PEM R23564) from Samanunga
village. Photo by Werner Conradie.
truncated tail at 7 annulus. Adults have distinct black
bars, while juveniles are much lighter in color; 16-17
dorsal segments per body annulus; 12 ventral segments
per body annulus; 189-194 body annuli; 42-43 caudal
annuli, caudal autonomy site at 7" caudal annulus; 3
supralabials; 3 infralabials. Largest female: 216.0 + 8t
mm (PEM R23565); largest male: 232.0 + 41.0 mm
(PEM R23564). Habitat and natural history notes:
One female contained three elongated eggs (20 x 5 mm).
Two specimens were excavated by local farmers while
preparing agricultural fields. Comments: Only two
species of Zygaspis are known from scattered records
in southern and eastern Angola (Marques et al. 2018;
Baptista et al. 2019; Butler et al. 2019). Zygaspis nigra
was originally described from western Zambia, with
only a few records from eastern Angola and the Zambezi
Region in northeastern Namibia (Broadley and Gans
1969; Pietersen et al. 2021). Historically this species
is only known from three localities in eastern Angola
(Marques et al. 2018), so these new records double the
number of known localities from Angola.
Chamaeleonidae
Chamaeleo dilepis Leach, 1819 complex
Flap-necked Chameleon (Fig. 8, Map 7)
Fig. 8. Adult female Chamaeleo dilepis (not collected) from
lower Quembo River. Photo by Werner Conradie.
Amphib. Reptile Conserv.
Elevation (m)
r=)
Oo
So
12 14 16 18 20 22 24
Map 6. Distribution of Zygaspis nigra in Angola.
Material (5 specimens): PEM R23322, Cuito River
source lake, -12.68935° 18.36012°, 1,435 m asl; PEM
R27391, Luvu River camp, -13.71200° 21.83538°,
1,082 m asl; PEM R27389-90, INBAC: WC-6789,
Lungwebungu River camp, -12.58439° 18.66748°,
1,297 m asl. Additional observations: Quembo River,
walk back from small waterfall, -13.52987° 19.28340°,
1,242 m asl; Quembo River right side tributary (Micongo
River) past village, -13.51877° 19.28486°, 1,248 m
asl; Camp at side tributary (Luandai River) of the
Luanguinga River, -13.70885° 21.26234°, 1,116 m asl;
Cuelei River west of Menongue, -14.70511° 17.38014°,
1,392 m asl; Chitembo, -12.78792° 16.75706°, 1,693
m asl. Description: All specimens presented a small,
reduced occipital flap. Largest female: 97.1 + 84.0 mm
(PEM R27391); largest male: 88.5 + 95.0 mm (PEM
R23322). Habitat and natural history notes: All adult
specimens were encountered sleeping at night in larger
trees up to a height of 2 m, while hatchlings were found
very low on scrub below 30 cm height. A gravid female
(photographed and released) was found at the Cuito River
source in February. Comment: Although the casques
and occipital lobes of our material seem very reduced
(a feature diagnostic of C. gracilis), the tail is long and
the dorsal keel is formed by a single row of enlarged
tubercles (double in C. anchietae), conforming to typical
Elevation (m)
Map 7. Distribution of Chamaeleo dilepis in Angola.
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
Fig. 9. Adult female Afroedura wulfhaackei (PEM R22490)
from 1 km west of Candumbo on road to Boas Aguas. Photo
by Luke Verburgt.
C. dilepis features (Tilbury 2010, 2018). Chameleons are
very poorly represented in Angola, with only two genera
and five species recorded (Marques et al. 2018). Of these,
C. dilepis is the most common and widespread (Marques
et al. 2018), although only a few records are known from
the southeast (Conradie et al. 2016). The new records
presented here fill the sampling gap in the distribution
of this species in Angola. Numerous subspecies and
variations have been described in this group over
the years (Uetz et al. 2022), but a recent large-scale
phylogenetic study (Main et al. 2022) identified only
three species-level lineages that do not fully agree with
previously identified subspecies. Of these lineages, two
occur in Angola, but due to the lack of topotypic material
and the fact that the recognized lineages are incongruent
with previously described subspecies, further studies are
recommended for this taxon. We therefore refer to our
collected material by the binominal name.
Gekkonidae
Afroedura wulfhaackei Branch, Schmitz, Lobon-Rovira,
Baptista, Antonio, and Conradie, 2021
Angolan Flat Gecko (Fig. 9, Map 8)
Material (3 specimens): PEM R22490-1, PEM
R24200, Candumbo Rocks Memorial, -12.73614°
15.97442°, 1,777 m asl. Description: 77-79 dorsal
midbody scale rows; 8—9 supralabials; 8 infralabials;:
7-8 enlarged scales under 4" toe; 4 ventral verticils and
5 dorsal verticils per tail whorl. Largest female: 54.4 +
Ot mm (PEM R 22491). Habitat and natural history
notes: Found under exfoliating rocks among larger rock
boulders. Comment: These represent the most inland
records of this recently described species (Branch et al.
2021). Although this species was not documented from
within the defined core study area of this project, suitable
habitat is found along the northern and western edge of
the study area.
Hemidactylus mabouia (Moreau de Jonnes, 1818)
Common Tropical House Gecko (Map 9)
Amphib. Reptile Conserv.
i 2000
Elevation (m)
=)
So
Oo
Map 8. Distribution of Afroedura wulfhaackei in Angola.
Material (3 specimens): PEM R24001, Cuemba town,
-12.14786° 18.09100°, 1,351 m asl; PEM R23558,
Munhango village, -12.16445° 18.5548°, 1,435 m
asl; PEM R23377, Kwanza River bridge, -11.99348°
17.66965°, 1,727 m asl. Description: Subcaudal
scales enlarged and elongated; 88-89 dorsal midbody
scale rows; 16-17 longitudinal rows of enlarged
keeled tubercles; 34 ventral midbody scale rows; 10
supralabials; 9-10 infralabials; 6—7 divided scansors
under 4" toe; 14/15 precloacal pores in a single row.
Largest female: 52.6 + 61.0 mm (PEM R23558); largest
male: 53.5 + 62.0 mm (PEM R24001). Habitat and
natural history notes: All specimens were found on or
near anthropogenic structures. Comment: The species
is present across most of Angola, but has not yet been
recorded from extreme southeastern Angola (Marques et
al. 2018; Ceriaco et al. 2020a; Lobon-Rovira et al. 2021).
Due to its high human-assisted dispersal capacity and
adaptation to anthropogenic structures (Agarwal et al.
2021), this species is expected to spread to larger towns
and settlements in southeastern Angola. A recent large-
scale phylogenetic study revealed at least 20 species-
level lineages, with most Angolan material corresponding
to the H. mabouia sensu stricto lineage (Agarwal et al.
2021).
Elevation (m)
3
[=]
Oo
Map 9. Distribution of Hemidactylus mabouia in Angola.
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
Fig. 10. Adult male Hemidactylus nzingae (PEM R23991) from
Cuquema River. Photo by Werner Conradie.
Hemidactylus nzingae Ceriaco, Agarwal, Marques, and
Bauer, 2020
Queen Nzinga’s Tropical Gecko (Fig. 10, Map 10)
Material (2 specimens): PEM R23990 (iNaturalist
12128372), Rio Cuquema, downstream, -12.47021°
16.82334°, 1,644 m asl; PEM R23991, Rio Cuquema,
upstream, -12.46902° 16.82415°, 1,640 msl.
Description: 58-66 dorsal midbody scale rows; 16
longitudinal rows of enlarged keeled tubercles; 25
ventral midbody scale rows; 9-10 supralabials; 8—9
infralabials; 7 divided scansors under 4" toe; 3/3
precloacal pores in a single row. Largest male: 40.2 +
37.9 mm (PEM R23991). Habitat and natural history
notes: Specimens were found actively running on the
ground during the day. Comment: This species was
only recently described and seems to be common in
miombo woodland on the Angolan plateau (Ceriaco et
al. 2020a; Lobon-Rovira et al. 2021). In a follow-up
study, ‘unpatterned’ specimens that occur sympatrically
with H. nzingae were described as a new species, H.
hannahsabinae (Ceriaco et al. 2020b). The addition
of more material, with some from this study including
these ‘unpatterned’ specimens, showed that the latter
taxon is a junior synonym of H. nzingae (Lobon-Rovira
et al. 2021).
Fig. 11. Adult female Lygodactylus angolensis (PEM R23995)
from south of Cuito town. Photo by Alex Rebelo.
Amphib. Reptile Conserv.
Elevation (m)
S
Oo
o
Map 10. Distribution of Hemidactylus nzingae in Angola.
Lygodactylus angolensis Bocage, 1896
Angolan Dwarf Day Gecko (Fig. 11, Map 11)
Material (3 specimens): PEM R23311, drive back from
Cuchi to Menongue, -14.67986° 17.17512°, 1,391 m asl;
PEM R23343, 10 km west of Cuemba village, -12.03481°
18.04869°, 1,437 m asl; PEM R23995 (iNaturalist
12123557), south of Cuito town, -12.43930° 16.99143°,
1,624 m asl. Description: Mental divided by a pair of
lateral clefts; 81-87 (84) dorsal midbody scale rows;
21-22 ventral midbody scale rows; 7—8 supralabials; 7—8
infralabials; 2—3 scales touching nostril; 4 divided scansors
under 4" toe; 9 precloacal pores in a V-shape. Largest
female: 29.8 + 34.0 mm (PEM R23995); largest male: 30.1
+ 34.6 mm (PEM R23311). Habitat and natural history
notes: Found on tree trunks during the day in miombo
woodland. Comment: Assigned to L. angolensis based on
the high number of precloacal pores (9) and the number of
scales touching the nostril (~3; Marques et al. 2020). One
specimen (PEM R23312) was found tn sympatry with L.
nyaneka and constitutes the southernmost Angolan record
and the first from Cuando Cubango Province.
Lygodactylus chobiensis FitzSimons, 1932
Okavango Dwarf Gecko (Fig. 12, Map 12)
Material (1 specimen): PEM R27402, Luvu River camp,
-13.71200° 21.83538°, 1,082 masl. Description: Mental
Elevation (m)
ra)
Lo)
3
12 14 16 18 20 22 24
Map 11. Distribution of Lygodactylus angolensis in Angola.
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
Fig. 12. Adult female Lygodactylus chobiensis from Luvu
River. Photo by Chad Keates.
not divided by lateral clefts, two faint dark V-shaped
chevrons on throat; 74 dorsal midbody scale rows;
22 ventral midbody scale rows; 6/6 supralabials; 6/6
infralabials; 4 scales touching nostril; 5 divided scansors
under 4" toe. Largest female: 25.5 + 26.2 mm (PEM
R27402). Habitat and natural history notes: Found
sleeping in a tree at night. Comment: This represents the
first documented record for Angola, although this species
has been predicted to occur in eastern and southeastern
Angola (Marques et al. 2018).
Lygodactylus nyaneka Marques, Ceriaco, Buehler,
Bandeira, Janota, and Bauer, 2020
Nyaneka Dwarf Gecko (Fig. 13, Map 13)
Material (2 specimens): PEM R23312, drive back from
Cuchi to Menongue, -14.67986° 17.17512°, 1,391 m
asl; PEM R23540, Longa River, -14.55956° 18.41389°,
1,320 m asl. Description: Mental divided by a pair of
lateral clefts; 83 and 93 dorsal midbody scale rows; 16
and 22 ventral midbody scale rows; 7—8 supralabials;
7-8 infralabials; 3-4 scales touching nostril; 4 divided
scansors under 4" toe; 6 precloacal pores in a V-shape.
Largest female: 32.4 + 30.3 mm (PEM R23540); largest
male: 35.2 + 17.4t mm (PEM R23312). Habitat and
natural history notes: Found in miombo woodland.
Comment: We tentatively assign our new material,
Fig. 13. Adult male Lygodactylus nyaneka (PEM R23312) from
west of Menongue. Photo by Werner Conradie.
Amphib. Reptile Conserv.
Elevation (m)
3
oO
Oo
Map 12. Distribution of Lygodactylus chobiensis in Angola.
including the material reported as L. bradfieldi by
Conradie et al. (2016), to this species based on shared
morphological characters (number of scales touching the
nostril and low number of precloacal pores, Marques et
al. 2020) until further phylogenetic studies are conducted.
Pachydactylus cf. punctatus Peters, 1854 complex
Speckled Thick-toed Gecko (Fig. 14, Map 14)
Material (2 specimens): PEM R23262, Cuchi River
gorge, -14.59000° 16.90758°, 1,350 masl; PEM R23537,
Cuchi River gorge, -14.58983° 16.90744°, 1,364 m asl.
Description: Specimens are light brown above with
fine white speckles; 74 and 76 midbody scale rows; 6—7
supralabials; 8—6 infralabials; 4 undivided scansors under
4" toe. Largest female 33.8 + 32.7 mm (PEM R23262);
largest male: 34.7 + 25.8t mm (PEM R23537). Habitat
and natural history notes: Specimens were found active
at night on rock surfaces adjacent to Cuchi River gorge.
Comment: The taxonomic status of this species complex
is currently under revision and it may represent multiple
cryptic lineages (H. M. Heinz, unpub. data).
Pachydactylus wahlbergii (Peters, 1869)
Kalahari Ground Gecko (Fig. 15, Map 15)
Material: PEM R25083, Cuando River, CUD2018
AC Camp 22, -15.82175° 21.58647°, 1,050 m asl.
Elevation (m)
3
i=]
i=)
Map 13. Distribution of Lygodactylus nyaneka in Angola.
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
Cpe Sgn’ Te og et : £ ‘Wa. Ley. ‘- ea 2) one ae
Gop Ts rena acca megs at pee
Fig. 14. Adult female Pachydactylus cf. punctatus (PEM
R23262) from Cuchi River gorge. Photo by Werner Conradie.
Description: 72 midbody scale rows; 7/8 supralabials;
6/6 infralabials; 2 undivided scansors under 4" toe.
Largest male: 25.5 + 26.2 mm (PEM R25083). Habitat
and natural history notes: Found beneath a tent
pitched on the sandy bank adjacent to the Cuando River.
Comment: Although Haacke (1976) recorded this
species from the border between Angola and Namibia,
no official records have been documented from Angola.
This therefore represents the first confirmed record for
Angola. This new record is unsurprising, given the recent
record of this species in western Zambia (Pietersen et al.
2017).
Gerrhosauridae
Gerrhosaurus auritus Boettger, 1887
Kalahari Plated Lizard (Fig. 16, Map 16)
Material (7 specimens): PEM R23273, Cuanavale River
source, -13.09330° 18.89396°, 1,367 masl; PEM R23313,
drive to Quemba village on grasslands, -12.14597°
18.39728°, 1,402 masl; PEM R23324, Cuito River source
lake, -12.68935° 18.36012°, 1,435 m asl; PEM R23481,
Cuando River source, trap 4, -13.00164° 19.1296°, 1,372
m asl; PEM R23557, DOR en route from Munhango to
Cuanavale River source, -12.56364° 18.66669°, 1,317 m
Fig. 15. Adult male Pachydactylus wahlbergii (PEM R25083)
from middle Cuando River. Photo by Gétz Neef.
Amphib. Reptile Conserv.
Elevation (m)
3
Oo
Oo
Map 14. Distribution of Pachydactylus punctatus complex in
Angola.
asl; PEM R23974 (iNaturalist 12410724), Lungwebungu
River, ad hoc, -12.58619° 18.66538°, 1,300 m asl;
PEM R23975 (iNaturalist 12410714), Lungwebungu
River new campsite, -12.58445° 18.66538°, 1,308 m
asl. Description: No dorsolateral yellow stripe; flanks
with scattered orange scales; tympanic shield very
broad and crescentic; weak to moderately keeled lateral
scales; scales on soles of feet keeled; 26—28 (26) dorsal
midbody scale rows; 8 enlarged ventral plates; 50-52
(51) transverse ventral scale rows; 3 supralabials; 3-4
infralabials; 4—5 supraciliaries; 16-18 (17) subdigital
lamellae under 4" toe; 13-17 (15) femoral pores per
thigh. Largest female: 156.0 + 254.0 mm (PEM R23557);
largest male: 143.5 + 249.0 mm (PEM R23273). Habitat
and natural history notes: Found active during the day
in close proximity to their burrows in miombo woodland
or grasslands, to which they retreated when disturbed.
Comment: Although a historical record exists from
Lunda Sul Province (Monard 1937), these are the first
modern records of this species for Angola. The species
has also been recorded from adjacent western Zambia
(Pietersen et al. 2017).
Gerrhosaurus cf. nigrolineatus Hallowell, 1857 complex
Black-lined Plated Lizard (Fig. 17, Map 17)
Elevation (m)
r=)
°o
Oo
Map 15. Distribution of Pachydactylus wahlbergii in Angola.
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
ae
1g EE Pe PE te
Fig. 16. Adult male Gerrhosaurus auritus (PEM R23273) from
Cuanavale River source. Photo by Werner Conradie.
ig
Material (10 specimens): PEM R23260, R23302,
Cuchi River gorge, -14.5900° 16.90758°, 1,350 m asl;
PEM R23324—5, Cuito River source lake, -12.68935°
18.36012°, 1,435 m asl; PEM R23447, Cuando River
source, trap 3, -13.00334° 19.13564°, 1,364 m asl;
PEM R23534, EN280 west of Menongue, -14.68908°
17.41242°, 1,454 m asl; PEM R23541, Longa River,
-14.55942° 18.41431°, 1,321 m asl; PEM R23544—5,
Quembo River source camp, -13.14557° 19.04571°,
1,423 m asl; PEM R23973, Lungwebungu River, ad
hoc, -12.58619° 18.66538°, 1,300 m asl; PEM R23988,
Lungwebungu River, ad hoc, -12.56806° 18.66639°,
1,294 m asl. Description: Distinct dorsolateral yellow
stripe and bright orange flanks with yellow spots;
tympanic shield narrow; weak to moderately keeled
lateral scales; scales on soles of feet smooth; 23—24 (24)
dorsal midbody scale rows; 8 enlarged ventral plates;
49-51 (50) transverse ventral scale rows; 3 supralabials;
3 infralabials; 4 supraciliaries; 15—18 subdigital lamellae
under 4" toe; 15-20 (16) precloacal pores per thigh.
Largest female: 150.9 + 233.0 mm (PEM R23544),;
largest male: 139.0 + 277.0 mm (PEM R23325). Habitat
and natural history notes: Found sympatrically with
G. auritus at certain localities, e.g., Cuito River source
and Lungwebungu River bridge site. Gerrhosaurus cf.
Fig. 17. Adult male Gerrhosaurus cf. nigrolineatus (PEM
R23325) complex from Cuito River source. Photo by Werner
Conradie.
Amphib. Reptile Conserv. 195
Elevation (m)
Map 16. Distribution of Gerrhosaurus auritus in Angola.
nigrolineatus utilizes the same habitats as G. auritus and
exhibits similar behavior. Comment: A species with a
wide distribution in Africa and in Angola (Marques et al.
2018). Eastern African populations of G. nigrolineatus
were re-assigned to G. intermedius by Bates et al.
(2013), and the status of the Angolan north-central and
western populations of G. multilineatus, as well as their
relationships within the G. nigrolineatus complex in
Angola, are under investigation (M. Bates, pers. comm. ).
Tetradactylus ellenbergeri (Angel, 1922)
Ellenberger’s Long-tailed Seps (Fig. 18, Map 18)
Material (4 specimens): PEM R23375 (neonate), outlet
of Cuito River source lake, -12.70453° 18.35445°, 1,429
m asl; PEM R23424, Cuando River source, -13.00345°
19.12751°, 1,343 m asl; PEM R23976 (posterior half
of body and tail only), Lungwebungu River campsite,
-12.58319° 18.66573°, 1,284 m asl; PEM R24275,
Cuanavale River source lake, -13.09442° 18.89372°,
1,397 m asl. Description: Dorsal scales ridged with a
central keel; 12—14 dorsal midbody scale rows; 6 enlarged
longitudinal ventral plates; 63 transverse ventral scale
rows; 63 transverse dorsal scale rows; 4 supralabials; 3
infralabials; 3 supraciliaries; no front limbs; hind limbs
monodactyle (< 2 mm). Largest specimen: 62.5 + 160.0
Elevation (m)
Map 17. Distribution of Gerrhosaurus nigrolineatus complex
in Angola.
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
Fig. 18. Adult female 7etradactylus ellenbergeri (PEM R23424)
from Cuando River source. Photo by Werner Conradie.
mm (PEM R24275). Habitat and natural history notes:
All specimens were found near waterbodies. One female
specimen (PEM R23424) was captured by a Cattle Egret
(Bubulcus ibis) that released the specimen upon being
startled. The specimen contained two eggs (8.4 x 3.5 mm)
in November. One neonate (PEM R23375) was collected
at the outlet of the Cuito River source lake in February.
Comment: These new records fill the gap between the
most southeastern Luassinga River record (Conradie et
al. 2016) and the northeastern Angolan records (Monard
1937; Laurent 1964), and they are the first records for
the Cuando River basin. The taxonomy of this species
in Angola has been complicated by the naming of 7
lundensis Monard, 1937 and 7) fitzsimonsi simplex
Laurent, 1950. Laurent (1964) synonymized these two
species with 7’ boulengeri, which he in turn separated
from T: ellenbergeri based on the lower number of dorsal
scale rows (12 versus 14). Broadley (1971) rejected this,
as he found specimens in eastern Zambia whose dorsal
scale rows varied from 12—14 (the outer scale rows being
much smaller). Most of our specimens had 12 dorsal scale
rows, except for two specimens from the Cuando River
(PEM R23424) and the Luassingua River (Conradie et al.
Fig. 19. Adult female /chnotropis bivittata (PEM R23530) from
west of Cuito town on the Aludungo road. Photo by Werner
Conradie.
Amphib. Reptile Conserv.
Elevation (m)
Map 18. Distribution of Tetradactylus ellenbergeri in Angola.
2016), which each had 14 dorsal scale rows (outer scale
rows half the size of adjacent rows).
Lacertidae
Ichnotropis bivittata Bocage, 1866
Angolan Rough-scaled Lizard (Fig. 19, Map 19)
Material (1 specimen): PEM R23530, west of Cuito
town on Aludungo road, -12.32784° 16.90673°, 1,742 m
asl. Description: 35 midbody scale rows; 10 longitudinal
rows of enlarged ventral plates; 31 transverse ventral
scale rows; 4/4 supralabials; 6/6 infralabials; 4/4
supraciliaries; 19 subdigital lamellae under 4" toe; 10/10
femoral pores per thigh. Largest female: 59.9 + 98.0 mm
(PEM R23530). Comment: Collected outside of the core
study area, but it contributes to the distributional data for
both the species and the region. Laurent (1964) described
I. b. pallida from Huila based on duller coloration and
minor differences in head scalation. Recently, Butler et al.
(2019) and Bandeira (2019) erroneously referred material
from Bicuar National Park to /. b. pallida, but these are
actually subadult non-breeding /. capensis (see Baptista
et al. 2019 and the following species account). Bandeira
m)
Elevation (
3
3S
oO
Map 19. Distribution of [chnotropis bivittata in Angola.
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
ae, i
|. eel ere re :
i ae Me
Ss eo ee
= ao ‘
Yo “~ s =
rt
ine
Fe *
a
‘)
ein
Fig. 20. Adult male /chnotropis capensis from Lungwebungu
River camp. Photo by Werner Conradie.
in eee sear ha
: \. pes a
Fig. 22. Juvenile /chnotropis capensis (iNaturalist 12228725)
from east of Cuemba. Photo by Alex Rebelo.
(2019) found that material from the type locality of 1. 5.
pallida (KTHO09-075 and AMB 10722) shows very little
genetic difference from typical /. bivittata (JV V 2970 and
CAS 258409), and thus should remain in the synonymy
of the latter until more material becomes available for a
detailed phylogenetic study.
Ichnotropis capensis (Smith, 1838)
Cape Rough-scaled Lizard (Figs. 20-22, Map 20)
Material (66 specimens): PEM R23274—8, Cuanavale
River source, -13.0933° 18.89396°, 1,367 m asl; PEM
R23253-4, Cacundu falls, -13.7739° 18.7552°, 1,281
m asl; PEM R23298, grasslands W of Cuanavale to
Samanunga village, -13.07508° 18.88481°, 1,366 m
asl; PEM R23326-8, INBAC: (no number); Cuito River
source lake, -12.68935° 18.36012°, 1,435 m asl; PEM
R23351-—3, Kulua River source, 6 km SE of Cuito River
source, -12.736749° 18.3931022°, 1,446 m asl; PEM
R23370, INBAC: (no number), Cuanavale River source,
-14.85472° 19.28639°, 1,203 m asl; PEM R23409-10,
Lungwebungu River camp bridge crossing, -12.58346°
18.66598°, 1,304 m asl; PEM R23414—-9, Cuando
River source, -13.00345° 19.12751°, 1,343 m asl;
PEM R23440, INBAC: (no number x2), Cuando River
source trap 1, -13.00393° 19.12808°, 1,351 m asl; PEM
R23453, INBAC: WC-4584 (plus | additional specimen),
Amphib. Reptile Conserv.
wr a Re ag .
Fig. 21. Adult female /chnotropis capensis from Sombanana
village. Photo by Werner Conradie.
Elevation (m)
00
—
12 14 16 18 20 22 24
Map 20. Distribution of Ichnotropis capensis in Angola.
Quembo River trap 4, -13.13586° 19.04709°, 1,368 m
asl; PEM R23489, Quembo River trap 2, -13.13544°
19.04397°, 1,375 m asl; PEM R23493—-5, Cuanavale
River source lake camp side, -13.09442° 18.89372°,
1,396 m asl; PEM R23502, Sombanana village,
-12.31082° 18.62392°, 1,403 m asl; PEM R23505-7,
source lake north of Lungwebungu River crossing,
-12.41024° 18.63483°, 1,414 m asl; PEM R23508-9,
amphitheatre at Cuanavale River source, -13.05048°
18.89623°, 1,415 masl; PEM R23521-2, grassland drive
west of Cuanavale River source, -13.01347° 18.81669°,
1,538 m asl; PEM R23531, Sombanana village, Dala
River, -12.3071° 18.6235°, 1,407 m asl; PEM R23539,
Longa River, -14.55956° 18.41419°, 1,321 m asl; PEM
R23546-8, Quembo River source camp, -13.14557°
19.04571°, 1,423 m asl; PEM R23977, Lungwebungu
River near trap 2, ad hoc, -12.58200° 18.66562°, 1,208
m asl; PEM R23986, Lungwebungu River trap 1,
-12.580126° 18.667396°, 1,298 m asl; PEM R23996-7,
INBAC: WC-4544 (plus 2 additional specimens), Lake
Tchanssengwe, -12.41402° 18.64418°, 1,393 m asl;
PEM R27393, INBAC: WC-6796, Cuanavale River
source lake, -13.09052° 18.89394°, 1,357 m asl; PEM
R27394—401, INBAC: WC-6796, Quembo River bridge
camp, -13.52745° 19.2806°, 1,241 m asl. Description:
35—46 (40) midbody scale rows; 8-10 (9) longitudinal
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
Fig. 23. Adult male /chnotropis cf. grandiceps from Cuando
River source. Photo by Werner Conradie.
s S
ey ed
sir
from Cuanavale River source. Photo by Werner Conradie.
rows of enlarged ventral plates; 26-31 (27) transverse
ventral scale rows; 4—5 supralabials; 6—7 infralabials; 4/4
supraciliaries; 19-26 (22) subdigital lamellae under 4"
toe; 9-13 (10) femoral pores per thigh. Largest female:
63.1 + 117.0 mm (PEM R23531); largest male: 67.7 +
160.0 mm (PEM R23410, new maximum size record).
Habitat and natural history notes: In February 2016
and April 2018, only juveniles and subadult specimens
were observed, while in October 2016 and November
2019 only adult specimens were observed. Comment:
Based on general coloration and morphology, we assign
these specimens to the widespread /. capensis. The
large series of material (adults, subadults, and juveniles)
allowed us to assess the color variability within this
species, and in doing so we could confirm that previous
material assigned to Ichnotropis sp. by Conradie et
al. (2016) and /. b. pallida by Butler et al. (2019) and
Bandeira (2019) is referrable to subadult [ capensis.
The status of I. c. overlaeti remains unresolved, although
Marques et al. (2018) suggest that it might be a valid
species based on its geographical separation from the
nominotypical form that occurs further south. These new
records and unpublished PEM records from Saurimo
in Lunda Sul Province breach the distributional gap,
potentially forming a link between the southern and
northwestern Zambian and DRC records (Haagner et al.
2000; Pietersen et al. 2021).
Amphib. Reptile Conserv.
ae Te ae
pol coat ha - ‘¢
. rps x ANGE ye
Fig. 24. Adult female Jchnotropis cf. grandiceps from
grasslands west of Cuanavale River source to Samanunga
village. Photo by Werner Conradie.
-§
Elevation (m)
S
oO
oOo
Map 21. Distribution of Ichnotropis cf. grandiceps in Angola.
Ichnotropis cf. grandiceps Broadley, 1967
Caprivi Rough-scaled Lizard (Figs. 23-25, Map 21)
Material (17 specimens): PEM R23279-80; INBAC
(no number), Cuanavale River source, -13.0933°
18.89396°, 1,367 masl; PEM R23299—300, Grassland W
of Cuanavale River to Samanunga village, -13.07508°
18.88481°, 1,366 m asl; PEM R23303-9, 4 km
upstream from Cuanavale River source, -13.05084°
18.89726°, 1,380 m asl; PEM R23361-2, drive to
Cuanavale River camp from Samanunga village,
-13.03803° 18.82977°, 1,605 m asl; PEM R23420-1,
Cuando River source, -13.00345° 19.12751°, 1,343
m asl; PEM R23482, Cuando River source Trap 4,
-13.00164° 19.1296°, 1,372 m asl. Description: 41—49
(44) midbody scale rows; 9-10 (10) longitudinal ventral
scale rows; 30—37 (34) transverse ventral scale rows;
4—5 supralabials; 6—7 infralabials; 5—6 supraciliaries;
19-26 (22) subdigital lamellae under 4" toe; 10-13 (12)
femoral pores per thigh. Largest female: 78.2 + 126.0
mm (PEM R23362); largest male: 73.5 + 95t mm (PEM
R23420, longest tail measured 117 mm [2x SVL]).
Habitat and natural history notes: Juveniles were
only observed in February 2016 on sandy areas around
the source of the Cuanavale River, while two adults
were found on the elevated grassland ridges. In October
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
Elevation (m)
5
S
o
Map 22. Distribution of Meroles squamulosus in Angola.
2016, only adult specimens were found in sympatry
with adult 7. capensis. Comment: Described from the
Zambezi Region in northeastern Namibia based on only
three specimens (Broadley 1967), and further known
only from four additional specimens collected from
northeastern Namibia (Haacke 1970) and one specimen
from western Zambia (Pietersen et al. 2017). The newly
collected material conforms in part (broad head, large
overall size, dorsal coloration, and higher midbody scale
counts) with the original description. These therefore
represent the first records from Angola and the largest
series of specimens for this species ever collected. The
species displays a substantial amount of ontogenetic
variation (coloration and size), which originally led to
the belief that the juveniles and adults of /. grandiceps
represented separate species (W. Conradie, pers. obs.).
Since this is the first genetic material available for this
species, a phylogenetic study is underway (W. Conradie,
in prep.).
Meroles squamulosus (Peters, 1854)
Common Rough-scaled Lizard (Map 22)
Material (1 specimen): PEM R24291, EN140 road
between Caiundo and Katwitwi, -16.38169° 17.7337°,
Baloo aie | ua oe og) . ie : Pex?
Fig. 26. Subadult male Eumecia anchietae (PEM R23983)
from Lungwebungu River campsite. Photo by Werner
Conradie.
Amphib. Reptile Conserv.
1,143 m asl. Description: 53 midbody scale rows; 8
longitudinal and 36 transverse ventral scale rows; 7/7
supralabials; 7/7 infralabials; 4/4 supraciliaries; 17
subdigital lamellae under 4" toe; 14 femoral pores per
thigh. Largest male: 60.8 + 88.0 mm (PEM R24291).
Habitat and natural history notes: Found active during
the day in Zambezian Baikiaea woodland. Comment:
This species is only known from a handful of records in
southern Angola (Monard 1937; Conradie et al. 2016),
although it is more widespread further south and east
(Branch 1998; Pietersen et al. 2021).
Scincidae
Eumecia anchietae Bocage, 1870
Anchieta’s Serpentiform Skink (Fig. 26, Map 23)
Material (1 specimen): PEM R23983 (iNaturalist
12410715), Lungwebungu River campsite, ad hoc,
-12.58027° 18.66278°, 1,302 m asl. Description: Dorsal
scales with two keels per scale; tail 1.3 times the SVL;
22 midbody scale rows; 107 transverse ventral scale
rows; 3/4 supralabials; 4/4 infralabials; 4 supraciliaries
(1 semi-divided); 2 toes on front limbs and 3 on hind
limbs. Size (male): 127.0 + 157.0 mm (PEM R23983).
Habitat and natural history notes: Found dead on
road. Stomach contained unidentified grasshopper,
caterpillar, and small beetles. Comment: Laurent (1964)
described E. a. major from northern Angola, based on the
first supraciliary being fused with the second. Monard
(1937) documented the same difference for material from
Lunda. The new specimen reported here conforms to the
description of E. a. major and was collected in close
proximity to the material documented by Laurent (1964).
The status of this subspecies needs to be determined
using phylogenetic analyses.
Lubuya ivensii (Bocage, 1879)
Iven’s Water Skink (Fig. 27, Map 24)
Material (2 specimens): PEM R23422, Cuando
River source, -13.00345° 19.12751°, 1,343 m asl;
Elevation (m)
=)
So
Oo
Map 23. Distribution of Eumecia anchietae in Angola.
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
- -ii
<=
Fig. 27. Juvenile Lubuya ivensii (PEM R23422) from Cuando
River source. Photo by Werner Conradie.
PEM R24276, Cuando River, Camp 19, -14.79365°
20.20482°, 1,121 m asl. Description: Dorsal scales with
three keels each; tail twice SVL; 29 midbody scale rows;
64—66 transverse ventral scale rows; 62-64 transverse
ventral scale rows; 6—7 supralabials; 6 infralabials:
3-4 supraciliaries; 16-19 subdigital lamellae under
4 toe. Largest specimen: 113.0 + 216.0 mm (PEM
R24276). Habitat and natural history notes: One of
the specimens was caught basking on top of dense grass
within a grassy wetland. Comment: Monard (1937)
reported that the material from northeastern Angola has
an extra lateral white line, but took no taxonomic action.
Subsequently, Laurent (1964) described northeastern
material as Mabuya ivensi septemlineata. Branch and
Haagner (1993), while reporting on a large collection of
specimens from northwestern Zambia and adjacent DRC,
found no evidence to support the continued recognition
of M. i. septemlineata. The two new records reported
here and the record in Conradie et al. (2016) represent the
most southern records of this species and the first from
the Okavango and Cuando River basins.
Panaspis sp.
Snake-eyed Skink (Fig. 28, Map 25)
Material (14 specimens): PEM R23317, Protea stop
en route to Cuito River source, -12.3004° 18.6207°,
Fig. 28. Adult unsexed Panaspis sp. (PEM R23347) from en
route to the Cuito River source. Photo by Werner Conradie.
Amphib. Reptile Conserv.
-14
Elevation (m)
=
oO
So
-16
-18
Map 24. Distribution of Lubuya ivensii in Angola.
1,425 m asl; PEM R23347, road from Cuanavale River
to Cuito River sources, -12.81739° 18.63236°, 1,446
m asl; PEM R23411, Lungwebungu River camp bridge
crossing, -12.58346° 18.66598°, 1,304 m asl; PEM
R23469, Quembo River source, trap 1, -13.13592°
19.04417°, 1,369 m asl; PEM R23524, Quembo River
source, -13.11264° 19.01789°, 1,539 m asl; PEM
R23980, Lungwebungu River trap 3, -12.58056°
18.66419°, 1,302 m asl; PEM R23998 (iNaturalist
12261402), Lake Tchanssengwe, -12.41402° 18.64418°,
1,393 m asl; PEM R27407, Quembo River bridge camp,
-13.527455° 19.2806°, 1,241 m asl; PEM R27403-46,
INBAC: WC-6984, lower Quembo River bridge camp
trap 2, -13.52816° 19.28067°, 1,240 m asl. Description:
No white spots on lateral sides of neck; no dorsolateral
white stripes; 25—29 (27) midbody scale rows; 55-61
(57) transverse ventral scale rows; 54—61 (58) transverse
dorsal scale rows; 4 supralabials; 7 infralabials; 5—6
supraciliaries; 12-14 (13) subdigital lamellae under 4"
toe. Largest female: 41.4 + 56.0 mm (PEM R3524);
largest male: 39.2 + 56.0 mm (PEM R23411). Habitat
and natural history notes: Found among leaf litter
in closed canopy miombo woodland. Comment: The
snake-eyed skinks of Angola were recently reviewed
(Ceriaco et al. 2020c) with the recognition of five
species occurring in Angola: P. cabindae, P. breviceps,
f
Elevation (m)
Map 25. Distribution of Panaspis sp. in Angola.
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
s
ae “
ma - ‘ ; | : Wis
ree tas © wer i As WR ae
Fig. 29. Adult unsexed Sepsina angolensis (PEM R23498)
from Cuanavale River source. Photo by Werner Conradie.
P. wahlbergii, P. maculicollis, and the newly described
P. mocamedensis. Our specimens lack the typical white
neck spots diagnostic of the P. maculicollis group and the
diagnostic black-edged white dorsolateral stripe of the P.
wahilbergii group. The taxonomic status of this material
is pending the outcome of future phylogenetic studies.
Sepsina angolensis (Bocage, 1866)
Angola Reduced-limb Skink (Fig. 29, Map 26)
Material (20 specimens): PEM R23264, Cuchi River
gorge, -14.59° 16.90758°, 1,350 m asl; PEM R23316,
Cuanavale River, trap 4 active search, -13.05071°
18.89843°, 1,419 m asl; PEM R23332-3, Cuito River
source lake, -12.68935° 18.36012°, 1,435 m asl; PEM
R23460, Quembo River source, trap 5, -13.13586°
19.04709°, 1,368 m asl; PEM R23498-9, INBAC:
WC4571, Cuanavale source lake, -13.08934° 18.89485°,
1,396 m asl; PEM R23515, Quembo River source, trap
3, -13.13072° 19.03724°, 1,443 m asl; PEM R23972,
Lungwebungu River campsite, ad hoc, -12.58862°
18.66827°, 1,309 m asl; PEM R23978 (iNaturalist
12373403), Lungwebungu River, trap 2, -12.58199°
18.66562°, 1,208 m asl; PEM R27412, Quembo River
bridge camp, -13.52816° 19.28067°, 1,240 m asl; PEM
R27413,INBAC: WC-6792, Quembo River bridge camp,
trap 3, -13.52778° 19.27455°, 1,256 m asl; PEM R27414,
Quembo River bridge camp, -13.52745° 19.2806°, 1,241
m asl; PEM R27415, left side tributary (Condinde River)
at Cuando River bridge, -13.60076° 19.52675°, 1,219 m
asl; PEM R27416, Camp at side tributary (Luandai River)
of the Luanguinga River, -13.708854° 21.262343°,
1,116 m asl; PEM R27417, lower Quembo River bridge
camp, trap 4, -13.52658° 19.27810°, 1,248 m asl; PEM
R27418-9, Luvu River camp, -13.71200° 21.83538°,
1,082 m asl. Description: Smooth dorsal scales; 24—25
(24) midbody scale rows; 90-98 (95) transverse ventral
scale rows; 89-97 (93) transverse dorsal scale rows; 5—6
supralabials; 6—7 infralabials; 5 supraciliaries; reduced
limbs with three clawed toes per limb. Largest female:
84.6 + 56.0 mm (PEM R27413); largest male: 71.0 +
54.0 mm (PEM R23515). Habitat and natural history
Amphib. Reptile Conserv.
Elevation (m)
Map 26. Distribution of Sepsina angolensis in Angola.
notes: Tracks of these fossorial species can be seen in
the early mornings on sandy soil. Most specimens were
either caught in traps or by raking through leaf litter. Some
specimens were collected under tree logs. Comment:
This species 1s known from Angola, Namibia, Zambia,
and DRC (Branch 1998; Marques et al. 2018; Pietersen
et al. 2021). These records fill the gap within the known
distribution in Angola and western Zambia (Broadley
1971; Pietersen et al. 2021).
Trachylepis albopunctata (Bocage, 1867)
White-spotted Variable Skink (Fig. 30, Map 27)
Material (15 specimens): PEM R23256-8, south
of Menongue en route to Cuebe River, -14.96288°
17.69089°, 1,300 m asl; PEM R23265, INBAC (no
number), Cuchi River gorge, -14.59° 16.90758°, 1,350
m asl; PEM R23344—5, 10 km west of Cuemba village,
-12.03481° 18.04869°, 1,437 m asl; PEM R23355, Stop
2: road to Cuito River source, -12.2823° 18.6291°,
1,487 m asl; PEM R23379, Kuvango River hydro plant
site, -14.38775° 16.29365°, 1,429 m asl; PEM R23389,
INBAC: WC-5207, Cubango River campsite 2 near
mission, -13.32887° 16.41167°, 1,520 m asl; PEM
R23390, Cubango River, campsite 1 below rapids, west
of Fundo village, -13.04483° 16.3752°, 1,557 m asl;
PEM R23479, Quembo River source trap 4, -13.13586°
19.04709°, 1,369 m asl; PEM R23543, EN140 North
of Menongue, -13.84775° 17.25308°, 1,503 m asl.
Description: Dorsal scales with three keels each;
30-35 (33) midbody scale rows; 44-47 (45) transverse
ventral scale rows; 47—55 (51) transverse dorsal scale
rows; 4—6 (5) supralabials; 6—7 (6) infralabials; 4—7 (5)
supraciliaries; 19-21 (20) subdigital lamellae under 4"
toe. Largest specimen: 55.6 + 92.0 mm (PEM R23265).
Habitat and natural history notes: Diurnal species
found active in miombo woodland. Comment: Part
of the larger Trachylepis varia group (Weinell and
Bauer 2018; Weinell et al. 2019). Two species of this
group occur in Angola: 7? damarana, known only from
southeastern Angola, and 7. albopunctata, from the
central and coastal regions of Angola. The two species
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
ah cl
Fig. 30. Adult unsexed Trachylepis albopunctata (PEM
R23256) from south of Menongue. Photo by Werner Conradie.
can be separated by head scalation and coloration. In 7.
albopunctata, the parietals are mostly in contact anterior
of the interparietal (13 out of 19 specimens examined),
mostly five supralabials (average 4.6, 1 = 22) that are dark-
edged anteriorly, and a mostly uniform dark brown dorsum
with less white speckling compared to 7’ damarana.
Trachylepis bayonii (Bocage, 1872)
Bayao’s Skink (Fig. 31, Map 28)
Material (21 specimens): PEM R23336—-8, Cuito
River source lake, -12.68935° 18.36012°, 1,435 m asl;
PEM R23354, Kulua River source lake, 6 km SE of
Cuito River source, -12.736749° 18.3931022°, 1,446
m asl; PEM R23378, Kwanza River bridge, -11.99348°
17.66965°, 1,273 m asl; PEM R23477, Quembo River
trap 2, -13.13544° 19.04397°, 1,369 m asl; PEM
R23478, Quembo River trap 3, -13.13072° 19.03724°,
1,369 m asl; PEM R23501, Quembo River source lake,
-13.14104° 19.05426°, 1,399 m asl; PEM R23514,
Cuito River source lake, -12.68866° 18.36025°, 1,426
m asl; PEM R23516, Kulua River source, -12.73723°
18.3934°, 1,444 m asl; PEM R23553—-5, INBAC:
WC-4674, Quembo River source camp, -13.14104°
19.05426°, 1,371 m asl; PEM R23971 (iNaturalist
%
Fig. 31. Adult unsexed Trachylepis bayonii from Cuito River
source. Photo by Werner Conradie.
Amphib. Reptile Conserv. 202
Elevation (m)
Map 27. Distribution of Trachylepis albopunctata in Angola.
12347684), Rio Comba, -12.62442° 18.65159°, 1,299
m asl; PEM R23987, Lungwebungu River trap 1,
-12.58012° 18.66740°, 1,298 m asl; PEM R27420,
Lungwebungu River camp, at bridge, -12.58391°
18.66545°, 1,295 m asl; PEM R27421, Lungwebungu
River camp, -12.58439° 18.66748°, 1,297 m asl; PEM
R27422, Quembo River bridge camp, trap 1, -13.52801°
19.28147°, 1,236 m asl; PEM R27423—4, Quembo
River right side tributary (Micongo River) past village,
-13.51877° 19.284866°, 1,248 m asl. Description:
Dorsal scales with five keels each; scales under toes
spinose; 30-35 (32) midbody scale rows; 45-56 (52)
transverse ventral scale rows; 40—53 (49) transverse
dorsal scale rows; 4—6 supralabials; 6—8 infralabials; 3—4
supraciliaries; 15-17 (16) subdigital lamellae under 4"
toe. Largest specimen: 76.2 + 152 mm (PEM R27424).
Habitat and natural history notes: Lateral sides of
body and tail orange in breeding males. Comment:
Two subspecies are currently recognized: 7: b. bayonii
and 7! b. huilensis. Weinell et al. (2019) showed that 7.
b. huilensis requires full species recognition. Our new
material is tentatively assigned to T. b. bayonii, based
on distribution and unpublished barcoding results (W.
Conradie, unpub. data).
Elevation (m)
“14
-16
-18
Map 28. Distribution of Trachylepis bayonii in Angola.
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
Fig. 32. Adult male Trachylepis damarana (PEM R27434)
from Quembo River bridge camp. Photo by Chad Keates.
Trachylepis damarana (Peters, 1870)
Damara Variable Skink (Fig. 32, Map 29)
Material (14 specimens): PEM R23266, en route to
Cuanavale River source, -12.72368° 18.6228°, 1,355
m asl; PEM R27425-6, PEM R27430, camp at side
tributary (Luandai River) of the Luanguinga River,
-13.708854° 21.262343°, 1,116 m asl; PEM R27427,
R27431, Lake Hundo, -14.974308° 21.629657°, 1,100
m asl; PEM R27428-9, R27432-3, INBAC: WC-6769,
Quembo River bridge camp, -13.527455° 19.2806°,
1,241 masl; PEM R27434, PEM R27436, Quembo River
bridge camp, trap 3, -13.527782° 19.274545°, 1,256 m
asl; PEM R27435, left side tributary (Condinde River)
at Cuando River bridge, -13.60076° 19.52675°, 1,219
m asl; PEM R27437, Luvu River camp, -13.712001°
21.835381°, 1,082 m asl. Description: Dorsal scales
with three keels each; 30—35 (33) midbody scale rows;
40-46 (43) transverse ventral scale rows; 50-59 (53)
transverse dorsal scale rows; 4-5 (4) supralabials:
6-7 (6) infralabials; 4—6 (5) supraciliaries; 20—23 (22)
subdigital lamellae under 4" toe. Largest specimen:
59.6 + Ot mm (PEM R27425, longest tail 89.8 mm
[1.7 x SVL]). Habitat and natural history notes:
Lateral sides of body and tail orange in breeding males
(Fig. 32). All specimens were found in degraded/
secondary miombo woodland. Comment: See 7
hae =
Fig. 33. Adult unsexed Trachylepis cf. Behe from ouene
River source. Photo by Werner Conradie.
Amphib. Reptile Conserv.
Elevation (m)
S
S
oO
12 14 16 18 20 22 24
Map 29. Distribution of Trachylepis damarana in Angola.
albopunctata species account for details on taxonomy
and identification.
Trachylepis cf. punctulata (Bocage, 1872)
Speckled Sand Skink (Fig. 33, Map 30)
Material (18 specimens): PEM R23255, Cacundu
falls, -13.7739° 18.7552°, 1,281 m asl; PEM R23371,
Cuanavale River source, -14.85472° 19.28639°: PEM
R23372, Cuanavale River, -13.99475° 19.14919°; PEM
R23425—6, Cuando River source, -13.00345° 19.12751°,
1,343 m asl; PEM R23461—2, Quembo River, trap 4,
-13.13586° 19.04709°, 1,368 m asl; PEM R23504,
Sombanana village river, -12.3071° 18.6235°, 1,408
m asl; PEM R23550—2, Quembo River source camp,
-13.14557° 19.04571°; PEM R23981-2, Lungwebungu
River trap 3, -12.58056° 18.66419°, 1,302 m asl;
PEM R27438—-40, WC-6769, Quembo River bridge
camp, -13.52746° 19.28060°, 1,241 m asl; WC-6942,
Lake Hundo, -14.974308° 21.629657°, 1,100 m asl.
Description: Dorsal scales with five keels each; scales
under toes spinose; 3 1-35 (33) midbody scale rows; 45—55
(51) transverse ventral scale rows; 40—SO (45) transverse
dorsal scale rows; 5—6 supralabials; 6 infralabials; 4—5
supraciliaries; 16-22 (19) subdigital lamellae under 4"
toe. Largest specimen: 46.0 + 45 mm (PEM R 23255).
Habitat and natural history notes: A small skink that
f
Elevation (m)
rS
3
Oo
Map 30. Distribution of Trachylepis punctulata in Angola.
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
me C “Ss ee : E : ya ®
as . , ied, a — : : a — eA =
ti 4 a es tie Rs See: » Re
eS a TS aes 0A oer tae 7 ow :
Fig. 34. Adult female Trachylepis cf. spilogaster (PEM
R23334) from Cuito River source. Photo by Werner Conradie.
was often found moving around on the sandier regions,
in close proximity to water sources. Comment: Most of
the Angolan distribution is centred around the arid south-
western regions of the country (Marques et al. 2018). Our
records are the first from eastern Angola, forming a link
with the records from western Zambia and the Zambezi
Region of Namibia (Broadley 1971, 1975; Pietersen et
al. 2017, 2021). The taxonomic status of this Kalahari
Basin population requires further investigation.
Trachylepis cf. spilogaster (Peters, 1882)
Kalahari Tree Skink (Fig. 34, Map 31)
Material (7 specimens): PEM R23334—5, Cuito River
source lake, -12.68935° 18.36012°, 1,435 m asl; PEM
R23528, Quembo River source, -13.10699° 19.01785°,
1,545 m asl; PEM R23358—60, DOR en route to village,
-13.05967° 18.83239°, 1,567 m asl; PEM R27441, DOR
en route between Cuanavale River source and Tempué,
-13.33954° 18.85122°, 1,386 m asl; INBAC: WC-
6813, Quembo River, walk back from small waterfall,
-13.52988° 19.28340°, 1,242 m asl. Description: Dorsal
scales with five keels each; scales under toes spinose;
35-38 (37) midbody scale rows; 54-59 (57) transverse
ventral scale rows; 47-48 (48) transverse dorsal scale
rows; 5—6 supralabials; 6 infralabials; 4—6 supraciliaries;
Fig. 35. Adult female Zrachylepis sulcata ansorgii (PEM
R23368) from en route between Huambo and Cuito. Photo by
Luke Verburet.
Amphib. Reptile Conserv.
Elevation (m)
5
(=)
°
Map 31. Distribution of Trachylepis cf. spilogaster in Angola.
19-20 (20) subdigital lamellae under 4" toe. Largest
specimen: 81.4 + 125 mm (PEM R23334). Habitat and
natural history notes: This species was often observed
on the ground at the base of trees but quickly ascended
the tree trunks in miombo woodland when disturbed.
Comment: The status of 7rachylepis cf. spilogaster is
discussed by Conradie et al. (2016). Broadley (2000)
reported that specimens from northwestern Botswana do
not have the characteristic ventral black markings. The
new material from the source lakes and material reported
by Conradie et al. (2016) either lack ventral markings,
or have markings restricted to the gular region. The
taxonomic status of this population is currently under
review (L. M. P. Ceriaco et al., pers. comm. ).
Trachylepis sulcata ansorgii (Boulenger, 1907)
Western Rock Skink (Fig. 35, Map 32)
Material (1 specimen): PEM R23368, en route to Cuito,
east of Huambo, -12.73615° 15.97442°, 1,777 m asl.
Description: Dorsal scales with five keels each; scales
under toes smooth; 39 midbody scale rows; 53 transverse
ventral scale rows; 49 transverse dorsal scale rows;
5/5 supralabials; 7/7 infralabials; 5/5 supraciliaries; 23
subdigital lamellae under 4" toe. Size: 80.6 + Ot mm.
Habitat and natural history notes: Rupicolous skink
Elevation (m)
3
oO
oO
12 14 16 18 20 22 24
Map 32. Distribution of Trachylepis sulcata in Angola.
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
Fig. 36. Adult male Trachylepis wahlbergii from Cuito
Photo by Werner Conradie.
found in sympatry with Agama planiceps and Afroedura
wulfhaackei. Comment: Both Butler et al. (2019) and
Weinell et al. (2019) showed that 7: s. ansorgii deserves
full species recognition. As this species group is still
under taxonomic revision, we mapped it at the species
level. Not collected within the core study area, but this
record contributes to the overall distribution of this
species and the region and this species is expected to
occur along the western edge of the study area.
Trachylepis wahlbergii (Peters, 1869)
Wahlberg’s Striped Skink (Fig. 36, Map 33)
Material (33 specimens): PEM R23259, en route to
Cuanavale River source, -12.63683° 18.65984°, 1,316 m
asl; PEM R23289-95, Cuanavale River source, -13.0933°
18.89396°, 1,356 m asl; PEM R23339-41, Cuito River
source lake, -12.68935° 18.36012°, 1,435 m asl; PEM
R23363-6, HALO Cuito, -12.39584° 16.96067°, 1,700
m asl; PEM R23376, outlet of Cuito River source lake,
-12.70453° 18.35445°, 1,429 m asl; PEM R23393,
Huambo HALO training camp, -12.73726° 15.81828°,
1,667 m asl; PEM R23401, INBAC: WC-5181, Cubango
River source site, -12.66051° 16.08998°, 1,777 m
asl; PEM R23412, Lungwebungu River camp bridge
crossing, -12.58346° 18.66598°, 1,304 m asl; PEM
R23427, INBAC (2 x no number), Cuando River source,
Fig. 37. Adult unsexed 7yphlacontias rohani (PEM R27445)
from Cuanavale River source. Photo by Werner Conradie.
Amphib. Reptile Conserv.
town.
Elevation (m)
r=)
i=]
oO
Map 33. Distribution of Trachylepis wahlbergii in Angola.
-13.00345° 19.12751°, 1,343 m asl; PEM R23484—
5, INBAC: WC-4776, Cuando River source trap 4,
-13.00164° 19.1296°, 1,372 m asl; PEM R23513, Cuito
River source lake, -12.68866° 18.36025°, 1,426 m asl;
PEM R23559, Munhango village, -12.16067° 18.55042°,
1,428 m asl; PEM R27442, Quembo River bridge camp,
-13.527455° 19.2806°, 1,241 m asl; PEM R27443,
INBAC (no number), Luio River camp floodplains,
-13.197108° 20.221937°, 1,181 m asl; PEM R27444,
INBAC: WC-6919, Lake Hundo, trap 1, -14.99158°
21.63096°, 1,100 m asl. Description: Dorsal scales with
3-5 keels each; 38-42 (38) midbody scale rows; 51-63
(58) transverse ventral scale rows; 44—52 (49) transverse
dorsal scale rows; 5—6 supralabials; 5—8 infralabials; 4—7
supraciliaries; 18-22 (19) subdigital lamellae under 4"
toe. Largest female: 88.2 + 105.0 mm (PEM R23364);
largest male 86.0 + 104 mm (PEM R23485). Habitat
and natural history notes: Specimens were mostly
encountered running on sand and retreating to holes
when approached. No specimens were encountered on
trees. Comment: This species has a wide distribution
in southern Africa (Branch 1998; Pietersen et al. 2021)
and Angola (Marques et al. 2018). The taxonomy of
the Trachylepis striata species complex, to which this
species belongs, is still unresolved and requires further
investigation (Weinell et al. 2019; Stephens et al. 2021).
imi
Elevation (m)
S
oO
oO
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
Fig. 38. Adult unsexed Varanus niloticus from en route between
the Munhango and Cuanavale River sources. Photo by Werner
Conradie.
Typhlacontias rohani Angel, 1923
Rohan’s Blind Legless Skink (Fig. 37, Map 34)
Material (5 specimens): PEM R23342, Cuito River
source lake, -12.68935° 18.36012°, 1,435 m asl; PEM
R23497, Cuanavale River source lake, camp side,
-13.09442° 18.89372°, 1,396 m asl; PEM R24279,
Cuando River, Camp 21, -14.94935° 20.34483°, 1,115 masl;
PEM R27445, Cuanavale River source lake, -13.090523°
18.89394°, 1,357 masl; PEM R27446, en route from Cuando
River to Cangamba. Description: Dorsal scales smooth; 18
midbody scale rows; 117—129 (123) transverse dorsal scale
rows; 4 supralabials; 4 infralabials; 2 supraciliaries. Largest
specimen: 76 + 39.8 mm (PEM R27445). Habitat and
natural history notes: All specimens were found while
raking through leaf litter in sandy soil. Comments: This
fossorial legless skink is known from southeastern Angola,
northeastern Namibia, western Zimbabwe, northern
Botswana, and western Zambia (Haacke 1997; Marques
et al. 2018; Pietersen et al. 2021). Although described
from southeastern Angola (Angel 1923), very few records
exist for the country (Monard 1937; Conradie et al. 2016).
These new records are the northernmost for Angola. Most
of the genus is restricted to the western coastal regions
of Namibia and Angola, with only two species occurring
in the Kalahari Basin, 1.e., 7’ rohani and T: gracillis. The
former 1s widespread while the latter is restricted to western
Zambia. The two species occur tn sympatry at Kalabo in
western Zambia (Haacke 1997). Future studies should
utilize an integrative systematic approach to elucidate the
species boundaries and taxonomic structuring within the
whole genus.
Varanidae
Varanus niloticus (Linnaeus, 1766)
Water Monitor (Fig. 38, Map 35)
Observations: Cuando River -13.09320° 19.36016°,
-13.10063° 19.37254°, -13.12122° 19.39664°, -13.17326°
19.42046°, -13.18493° 19.43374°, -13.19005° 19.44007°,
-13.19016° 19.44147°, -13.20209° 19.46860°, -13.21743°
19.45877°, -13.31917° 19.49327°, -13.32957° 19.49497°,
-13.35510° 19.50343°, -13.35558° 19.50442°, -13.67297°
Amphib. Reptile Conserv.
Elevation (m)
3
i=)
i=)
12 14 16 18 20 22 24
Map 35. Distribution of Varanus niloticus in Angola.
19.56172°, -13.79270° 19.61024°, -13.85453° 19.629620°,
-13.90348° 19.65057°, -13.92381° 19.65753°, -14.03595°
19.69015°, -14.27281° 18.85794° (Naturalist 1727927),
-14.346620° 19.87581°, -14.92236° 20.31874°: Quembo
River -13.17842° 19.13734°, -13.25178° 19.17143°,
-13.25356° 19.17294°, -13.29163° 19.18123°, -13.33984°
19.20500°, -13.43206° 19.23945°, -13.48539° 19.24675°,
-13.56702° =19.305067°, = -13.56871° —-19.30585°,
-13.67061° 19.35595°, -13.67866° 19.35836°, -13.77110°
19.37386°, -13.79160° 19.38176°, -13.80572° 19.38648°,
-13.81202° 19.38591°, -13.88262° 19.39604°, -13.93431°
19.42397°, -13.93599° 19.42577°, -13.99462° 19.43543°,
-14.55758° 19.70635°, -14.67219° 19.83275°, -14.68235°
19.84010°, -14.68799° 19.85021°, -14.74537° 19.90861°,
-14.76761° 19.93762°, -14.77509° 19.95381°, -14.92917°
20.15534°, -14.95729° 20.21396°, -14.95792° 20.36728°,
-14.96685° 20.29766°, -14.96740° 20.46661°, -14.97001°
20.56494°, -14.97947° 20.23928°, -14.97965° 20.43558°,
-14.98357° 20.45164°, -15.12585° 21.03947°, -15.18248°
21.08478°, -15.34301° 21.25209°, -15.42151° 21.34750°,
-15.42435° 21.34192°, -15.49507° 21.38893°, -15.53690°
21.40043°, -15.58262° 21.43537°, -15.92187° 21.70659°,
-15.96243° 21.79459°, -16.34916° 22.06133°, -16.37759°
22.069423°, -16.38589° =. 22.08581°, = -16.39687°
22.097313°; Lungwebungu River -12.55000° 19.37939°,
-12.50378° 19.44091°, -12.43436° 19.47018°, -12.38381°
19.54014°, -12.38389° 19.77781°, -12.40754° 19.80887°,
-12.42778° 19.84023°, -12.43711° 19.85936°, -12.77029°
20.98921°, -12.80185° 21.03409°, -12.81192° 21.04544°,
-12.85937° 21.14091°, -12.93685° 21.24336°, -12.95462°
21.26790°, -12.98417° 21.28638°, -13.24428° 21.59976°.
Comment: This species was mostly encountered on
the banks of rivers or basking on overhanging fig trees.
However, one individual was captured very far from any
known water source, presumably during a migration event
between water sources.
Crocodylia
Crocodylidae
Crocodylus niloticus Laurenti, 1768
Nile Crocodile (Fig. 39, Map 36)
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
Fig. 39. Juvenile Crocodylus niloticus from Quembo River
bridge camp. Photo by Chad Keates.
Observations: Cuito River source lake, -12.68935°
18.36012°; Cuchi River gorge, -14.59000° 16.90758°,
1,350 m asl; Kulua River source, lake 6 km SE of Cuito
source, -12.736749° 18.3931022°, 1,446 m asl; Cuanavale
River source lake, -13.09052° 18.89394°; Quembo River
source lake, -13.13586° 19.04709°; Quembo River
bridge site, -13.52801° 19.28147°; Lake Tchanssengwe,
-12.41402° 18.64418°, 1,393 m asl; Cuando River
-13.32009° 19.49338°, -13.79438° 19.60793°, -13.88734°
19.64641°, -14.29429° 19.81956°, -14.602330° 20.13131°,
Quembo River -13.43374° 19.24170°, -13.53046°
19.28822°, -13.96865° 19.42061°, -13.99376° 19.43288°,
-14.027810° 19.44206°, -14.09658° 19.46397°, -14.11456°
19.46687°, -14.15561° 19.48322°, -14.15577° 19.48615°,
-14.22304° 19.50668°, -14.27701° 19.54167°, -14.34465°
19.57520°, -14.38198° 19.60944°, -14.39925° 19.61876°,
-14.41994° 19.63391°, -14.51911° 19.69112°, -14.61351°
19.76039°, -14.67203° 19.83250°, -14.73636° 19.90068°,
-14.94193° 20.16986°, -14.96962° 20.55838°, -14.97661°
20.53455°, -14.97668° 20.50791°, -14.97877° 20.38383°,
-14.9834° 20.51638°, -15.05622° 20.95461°, -15.12544°
21.03706°, -15.26815° 21.23438°, -16.31355° 22.0369°,
-16.31651° 22.0363°; Lungwebungu River -12.51823°
18.54648°, -12.57812° 18.67840°, -12.63833° 18.82899°,
-12.64124° 18.86644°, -12.67050° 18.96596°, -12.68586°
19.06160°, -12.66937° 19.17765°, -12.66345° 19.21794°,
ae
alee
ae a ph d™
Fig. 40. Subadult female Pelusios bechuanicus (PEM R27408)
from Lake Hundo. Photo by Werner Conradie.
Amphib. Reptile Conserv.
Elevation (m)
3
oO
oO
Map 36. Distribution of Crocodylus niloticus in Angola.
-12.65688° 19.25919°, -12.60808° 19.29928°, -12.57965°
19.34484°, -12.52636° 19.40970°, -12.45915° 19.47460°,
-12.45031° 19.47158°, -12.41964° 19.48228°, -12.38694°
19.77156°, -12.45968° 19.90906°, -12.45414° 20.005371°,
-12.45218° 20.01162°, -12.48533° 20.09848°, -12.50573°
20.11481°, -12.70198° 20.47726°, -12.72187° 20.56667°,
-12.75665° 20.94848°, -12.78606° 21.02360°, -12.88576°
21.18927°, -12.93852° 21.24419°, -13.25902° 21.61123°,
-13.28100° 21.62614°, -13.31189° 21.71873°. Comment:
No evidence was found that this species was breeding in
the upper reaches of the rivers.
Testudines
Pelomedusidae
Pelusios bechuanicus FitzSimons, 1932
Okavango Mud Terrapin (Fig. 40, Map 37)
Material (2 specimens): PEM R27408-9, Lake Hundo,
-14.97431° 21.62966°, 1,100 m asl. Description:
Specimen with large carapace (235 mm; PEM R27409)
collected on the edge of a lake and a sub-adult female
(123 mm; PEM R27408) collected from the lake itself.
Head black with yellow blotches; plastron and carapace
uniform black; front limbs black with yellow markings;
interlimb skin pale white. Habitat and natural history
notes: The specimen caught alive was captured with a
-14
Elevation (m)
3
i)
Oo
-16
-18
Map 37. Distribution of Pelusios bechuanicus in Angola.
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
ee
Fig. 41. Adult female Pelusios nanus (PEM R23423) from
Cuando River source. Photo by Werner Conradie.
net while collecting fish in the deeper waters of the lake.
Comment: This is only the 4" record of this species for
Angola (see Conradie et al. 2016; Marques et al. 2018).
Elsewhere this species is restricted to the Okavango and
Zambezi River systems (Pietersen et al. 2021).
Pelusios nanus Laurent, 1956
African Dwarf Mud Terrapin (Fig. 41, Map 38)
Material (2 specimens): PEM R23423, Cuando River
source, -13.00345° 19.12751°, 1,343 m asl; PEM
R27410 (shell), Quembo River bridge camp, -13.52745°
19.2806°, 1,241 m asl. Description: Carapace lengths
91.6 mm (PEM R27410) and 88.4 mm (PEM R23423),
respectively. Carapace very smooth and _ rounded,
uniform dark brown with black edges to scutes; plastron
beige with lateral and anterior edges dark brown to
black; head brown with yellow vermiculation; limbs
dark brown; skin of neck and limbs light yellow. Habitat
and natural history notes: The live specimen was
caught in shallow water covered by grass at the source
of the Cuando River. Comment: The new records close
the distributional gap between the central and eastern
Angolan records (Marques et al. 2018) and are the first
from the Cuando River basin.
Fig. 42. Subadult female Pelusios rhodesianus (PEM R23329)
from Cuito River source. Photo by Werner Conradie.
Amphib. Reptile Conserv.
-14
Elevation (m)
ra
°o
o
-16
-18
Map 38. Distribution of Pe/usios nanus in Angola.
Pelusios rhodesianus Hewitt, 1927
Variable Mud Terrapin (Fig. 42, Map 39)
Material (4 specimens): PEM R23329, Cuito River
source lake, -12.68935° 18.36012°, 1,435 m asl; PEM
R23490 (shell), Quembo River source, -13.13959°
19.04890°, 1,375 m asl; PEM R23562, en route to
the Cuando and Quembo confluence; PEM R27411,
Luvu River camp, -13.71200° 21.83538°, 1,082 m asl;
uncatalogued individual from middle Cubango River.
Description: Most specimens were juveniles, but one
adult carapace measured 177 mm (PEM R23490). The
carapace and plastron of the shell were uniform dark
brown to black. Juveniles had dark brown carapaces, but
the plastrons varied from uniform black to beige with
darker centers; head and limbs uniform brown; interlimb
skin white to yellowish. The adult carapace was elongate
and smooth with a weak vertebral keel anteriorly,
while all the juveniles’ carapaces were rounded with a
pronounced vertebral crest. Habitat and natural history
notes: Juvenile specimens were caught with a net while
collecting fish in the deeper waters of the lake and rivers.
Comment: The new records fill the gap in the known
distribution between central Angola and the Okavango
Delta (Rhodin et al. 2021).
Elevation (m)
ra)
[=]
Oo
Map 39. Distribution of Pel/usios rhodesianus in Angola.
December 2022 | Volume 16 | Number 2 | e322
Conradie et al.
Fig. 43. Adult female Kinixys belliana from Samanunga village.
Photo by Werner Conradie.
Testudinidae
Kinixys belliana Gray, 1831
Bell’s Hinge-back Tortoise (Fig. 43, Map 40)
Observations: Camp at side tributary (Luandai River)
of the Luanguinga River, -13.70885° 21.26234°, 1,116m
asl; Samanunga village, approx. -12.93169° 18.81458°;
between Tempué and Cuanavale, approx. -13.07438°
18.9075°. Habitat and natural history notes: All
specimens were collected or encountered in miombo
woodland. Comment: According to the revision of the
Kinixys genus by Kindler et al. (2012), eastern Angolan
material should be assigned to Kinixys belliana.
Discussion
The findings of this study contribute to our growing
knowledge of the Angolan herpetofauna, increasing the
number of documented lizard, chelonian, and crocodile
species in the country from 157 to approximately 161.
This number is expected to increase even more in the
coming years as more remote regions are surveyed and
taxonomic revisions that are currently underway are
completed. Southeastern Angola has been regarded as one
of the most poorly studied regions in Angola (Marques et
al. 2018). Due to a series of biodiversity surveys in the
region since 2012 (Conradie et al. 2016, 2021; this study)
our knowledge of the region has grown, resulting in a
more robust understanding of the herpetofaunal diversity
of southeastern Angola. However, most of the records
originate from the more easily accessible areas, while
most of southeastern Angola remains unexplored due to its
remoteness and lack of road infrastructure. Consequently,
the region is likely to harbor additional species that were
not detected during the surveys in this study and will
require further explorative surveys in the near future.
At a regional level, the results of this survey raise the
number of lizard, chelonian, and crocodile species known
from the Angolan Okavango-Cuando River system to 52,
an increase of 14 species from a previously compiled
checklist for the region (Conradie et al. 2016). When the
Amphib. Reptile Conserv.
Elevation (im)
S
o
oO
Map 40. Distribution of Kinixys belliana in Angola.
Zambezi River system is included, the number of species
recorded for southeastern Angola increases to 58.
Since a previous compilation of historical records for
Angola (Marques et al. 2018), citizen science activity
has escalated dramatically, and numerous additional
biodiversity expeditions in Angola have increased the
number of herpetological records from Angola. This
new information has led to an increase of ~60% in the
new unique occurrence records for Angola, and allowed
us to update the distribution maps for the 40 species
documented during this study. Many of these new records
fill the gaps between the central Angolan and western
Zambian records (e.g., Chamaeleo dilepis, Ichnotropis
capensis, and Sepsina angolensis), demonstrating that
these species have more continuous distributions than
previous data had suggested.
The results of this study confirm the presence of three
species that were previously only predicted (Conradie et
al. 2016; Marques et al. 2018) to occur in the region (-.e.,
Pachydactylus wahlbergii, Lygodactylus chobiensis, and
Ichnotropis cf. grandiceps). Our records of these three
species also represent the first confirmed country records.
The presence of Agama armata from eastern Angola was
confirmed with records from Huambo region (Map 3),
indicating that this species might be much more widely
distributed in Angola than previously considered. One
recommendation is that all available historical material
assigned to either A. aculeata or A. armata should be
re-examined to document the presence of both species
and their respective ranges in Angola. These surveys
further provided the first modern record of Gerrhosaurus
auritus for eastern Angola and have shown that it occurs
sympatrically with Gerrhosaurus nigrolineatus, noting
that the taxonomy of the latter group 1s still unresolved
(Bates et al. 2013). New records were also documented
for several rare species (e.g., Dalophia ellenbergeri,
Zygaspis nigra, and Pelusios bechuanicus), which are
only known from a handful of records within Angola.
Given the robust sampling regime afforded by this
study (e.g., 240 trapping nights) additional surveys in
southeastern Angola are unlikely to yield many more
December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
species for the Angolan Okavango-Cuando-Zambezi
River drainages. At least two additional species
(Typhlacontias gracilis and Trachylepis maculilabris)
are expected (Auerbach 1987; Branch 1998; Broadley
1971; Pietersen et al. 2017, 2021). However, ongoing
phylogenetic studies on the newly collected material may
lead to the description of additional undescribed species,
such as in the genus Panaspis.
Acknowledgments.—We thank the Wild Bird
Trust, which administers the National Geographic
Okavango Wilderness Project (2016-2019 National
Geographic Society grant). Material was collected and
exported under the following export permits issued
by the Angolan Ministry of Environment Institute of
Biodiversity (MINAMB): 31/GGPCC/2016, 89/INBAC.
MINAMB/2017, 002/GGPTBOK/18, = 151/INBAC/
MINAMB/2019. Ethical clearance for the study was
obtained from the Port Elizabeth (Bayworld) ethics
committee (Ethical Clearance nos. 2013 and 2017-2). The
project was endorsed and supported by the Governors of
Cuando Cubango, Bié, and Moxico provinces. Various
colleagues are thanked for collecting herpetological
material during their fieldwork, including Alex Rebelo,
Roger Bills, Paul Skelton, Maans Booysens, and Kerllen
Costa. WC thanks the Eastern Cape Province Department
of Sport, Recreation, Arts, and Culture (DSRAC) and
Port Elizabeth Museum for granting special leave to
take part in these surveys. We thank Enviro-Insight for
constructing and donating the drift fences required for
the trapping exercise. NLB is currently supported by
FCT contract SFRH/PD/BD/140810/2018. We thank
the anonymous reviewer for their insightful edits and
comments.
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Amphib. Reptile Conserv.
Conradie et al.
Werner Conradie has a Masters in Environmental Science (M.Env.Sc.) and 18 years of experience
working with the southern African herpetofauna. His main research interests focus on the taxonomy,
conservation, and ecology of amphibians and reptiles. Werner has published numerous principal and
collaborative scientific papers, and has served on a number of conservation and scientific panels,
including the Southern African Reptile and Amphibian Relisting Committees. He has undertaken
research expeditions to many African countries, including Angola, Botswana, Lesotho, Malawi,
Mozambique, Namibia, South Africa, Zambia, and Zimbabwe. Werner is currently the Curator of
Herpetology at the Port Elizabeth Museum (Bayworld), South Africa.
Chad Keates is currently a Post-doctoral Fellow at the Port Elizabeth Museum, funded by WC
research funds through Nelson Mandela University (Port Elizabeth, South Africa). Having recently
completed his Ph.D. in Zoology, Chad’s research focuses on the African herpetofauna and its
evolutionary and ecological structuring. In Chad’s short professional career, he has published several
principal and collaborative peer-reviewed scientific papers and book chapters. As a strong advocate
for reptile and amphibian awareness, Chad regularly conducts walks, talks, and presentations and
he has produced numerous popular scientific outputs on the subject. He has undertaken numerous
expeditions in various African countries, such as Angola, Zambia, and South Africa, with a variety
of both professional and scientific organizations.
Luke Verburgt is a consulting herpetologist in South Africa with over 19 years of herpetofauna
survey experience across 23 African countries (Angola, Botswana, Cameroon, Democratic Republic
of Congo, Ghana, Ivory Coast, Kenya, Lesotho, Liberia, Namibia, Madagascar, Malawi, Mall,
Morocco, Mozambique, Republic of Guinea, Sao Tomé and Principe, Sierra Leone, South Africa,
Swaziland, Tanzania, Uganda, and Zimbabwe). He is a co-owner of Enviro-Insight (Pretoria, South
Africa), holds an M.Sc. in Zoology from the University of Pretoria and is a registered scientific
professional with the South African Council for Natural Scientific Professions (SACNASP). Luke
has published more than 30 scientific articles, which include the descriptions of several new African
herpetofauna species, and he is a co-author of the book Snakes and other Reptiles of Zambia and
Malawi (Struik Random House Publishers, Cape Town, South Africa). He is also an extraordinary
lecturer in the Department of Zoology & Entomology at the University of Pretoria.
Ninda Baptista is an Angolan biologist with an M.Sc. degree in Conservation Biology from the
University of Lisbon (Portugal). She is currently pursuing a Ph.D. in Biodiversity, Genetics, and
Evolution at the University of Porto (Portugal) that addresses the diversity of Angolan amphibians.
Over the last 13 years, she has worked on research, in-situ conservation projects, and environmental
consulting in Angola, including priority areas for conservation along the Angolan escarpment
and highlands. She has conducted herpetological surveys throughout the country and created a
herpetological collection (Coleccaéo Herpetol6gica do Lubango) that is currently deposited in
Instituto Superior de Ciéncias da Educacao da Huila (SCED — Huila) in Angola. Ninda is an author
of various scientific papers and book chapters on Angolan herpetology and ornithology. She also
works on scientific outreach, producing magazine articles, books for children and posters about the
country’s biodiversity in collaboration with Fundacao Kissama (Luanda, Angola).
James Harvey lives in South A frica and works as an independent herpetologist, ecological researcher,
and consultant. He holds degrees in Zoology, Hydrology, and Environmental Management, and has
performed herpetological fieldwork widely, primarily within Africa, in such places as South Africa,
Botswana, Zimbabwe, Angola, Malawi, Kenya, Mali, Democratic Republic of Congo, Madagascar,
and Vietnam. His interests are diverse but center on the taxonomy, ecology, and conservation of
herpetofauna and other biodiversity. James has contributed to conservation assessments, workshops,
and Red Data publications for reptiles, amphibians, mammals, and plants for the southern and
eastern African regions. James regularly attends herpetological conferences, and has published
several scientific papers and contributed to a number of herpetological publications as an author.
213 December 2022 | Volume 16 | Number 2 | e322
Lizards, Chelonians, and Crocodiles of the Okavango Delta headwater area in Angola
Amphib. Reptile Conserv.
Tim6teo Julio is an Angolan with a degree in Biology. He is a researcher with five years of experience
with the Angolan herpetofauna, where his research is directed towards the study of the conservation
and ecology of reptiles and amphibians. He has worked on surveying snake bite incidents in Angola,
in the region of Luanda, and served as a co-author of scientific articles published on work done in
southern and eastern Angola. He has carried out some work with the herpetological collections of
the Kissama Foundation and Holisticos (Colec¢ao herpetologica da Funda¢ao Kissama e Holisticos)
in Luanda and as a collaborator with the Amphibian Survival Alliance in Angola.
Gotz Neef is a Namibian-born Biologist who joined the National Geographic Okavango Wilderness
Project in 2015 as the Research Manager. Since then, he has coordinated all the research, data, and
sample collection efforts for the project. During the expeditions, he works closely with the various
specialists and research assistants who undertake the sampling, trapping, and data recording.
214 December 2022 | Volume 16 | Number 2 | e322
Official journal website:
amphibian-reptile-conservation.org
Amphibian & Reptile Conservation
16(2) [General Section]: 215—236 (e323).
The herpetofauna of Xuan Nha Nature Reserve, Vietnam
12.*Anh Van Pham, **Truong Quang Nguyen, **Cuong The Pham, 2Nenh Ba Sung, ***Minh Duc Le,
g g
‘Tao Thien Nguyen, and ®*Thomas Ziegler
'Faculty of Environmental Sciences, University of Science, Vietnam National University, Hanoi, 334 Nguyen Trai Road, Hanoi 11400, VIETNAM
>Tay Bac University, Quyet Tam Ward, Son La City, Son La Province 34000, VIETNAM ?Institute of Ecology and Biological Resources, Vietnam
Academy of Science and Technology, 18 Hoang Quoc Viet Road, Cau Giay, Hanoi 10072, VIETNAM *Graduate University of Science and Technology,
Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet Road, Hanoi 10072, VIETNAM °*Central Institute for Natural Resources and
Environmental Studies, Vietnam National University, Hanoi, 19 Le Thanh Tong, Hanoi 11400, VIETNAM °Department of Herpetology, American
Museum of Natural History, Central Park West at 79" Street, New York, New York 10024, USA ‘Institute of Genome Research, Vietnam Academy of
Science and Technology, 18 Hoang Quoc Viet Road, Hanoi 10072, VIETNAM *AG Zoologischer Garten K6In, Riehler StraBe 173, D-50735 Koéln,
GERMANY “Institute of Zoology, University of Cologne, Ziilpicher Street 47b, D-50674 Cologne, GERMANY
Abstract.—This article presents the results of a herpetofaunal inventory of Xuan Nha Nature Reserve, Vietnam
conducted between April 2016 and May 2021, comprising 41 species of amphibians and 66 species of reptiles,
and 82 of the 107 species were recorded directly in this study. One species, Hemiphyllodactylus bonkowskii,
represents a new record for Son La Province and 20 species of amphibians and reptiles are new records
for the Xuan Nha Nature Reserve, comprising 10 species of frogs (Boulenophrys palpebralespinosa, B. cf.
parva, Leptobrachella eos, L. ventripunctata, Nanohyla marmorata, Kurixalus bisacculus, Rhacophorus orlovi,
R. rhodopus, Zhangixalus feae, and Z. pachyproctus), two species of lizards (Hemidactylus garnotii and
Sphenomorphus indicus), and eight species of snakes (Boiga cyanea, Dendrelaphis pictus, Elaphe taeniura,
Gonyosoma frenatum, Oligodon fasciolatus, Hebius chapaensis, Rhabdophis nigrocinctus, and Pareas
hamptoni). Remarkably, Gonyosoma coeruleum, a recently described species from southern China, is recorded
for the first time in Vietnam based on a single specimen from Son La Province. The herpetofauna of Xuan Nha
Nature Reserve contains a high number of species of conservation concern, including 12 species listed in the
Governmental Decree No. 84/2021/ND-CP, 19 species listed in the Vietnam Red Data Book, 18 species listed in
the IUCN Red List, and 12 species listed in CITES Appendices. In addition, data on the distribution and natural
history of the amphibian and reptile species in Xuan Nha Nature Reserve are provided.
Keywords. Amphibians, biodiversity, distribution, natural history, new records, reptiles
Citation: Pham AV, Nguyen TQ, Pham CT, Sung NB, Le MD, Nguyen TT, Ziegler T. 2022. The herpetofauna of Xuan Nha Nature Reserve, Vietnam.
Amphibian & Reptile Conservation 16(2) [General Section]: 215—236 (e323).
Copyright: © 2022 Pham et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution
4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Accepted: 6 November 2022; Published: 31 December 2022
Introduction Reserve (NR). Additional new records of reptiles and
amphibians from this nature reserve were documented by
Son La Province is located in northwestern Vietnam,
bordering Lao PDR in the southwest, and it is covered
by 599,000 hectares of natural forest (The People’s
Committee of Son La Province 2019). Xuan Nha is one
of the five nature reserves in Son La Province, located
in Moc Chau and Van Ho districts. This nature reserve
was established in November 2002 with an area of
18,268 hectares (The People’s Committee of Son La
Province 2019). The landscape of the nature reserve is
characterized by steep and mountainous topography with
elevations ranging from 400 to 1,800 m asl.
In terms of the herpetofaunal diversity, Nguyen et al.
(2010) provided the first list which included 27 amphibian
species and 50 reptile species from Xuan Nha Nature
Correspondence. *phamanh@hus.edu.vn
Amphib. Reptile Conserv.
Nguyen et al. (2017) and Pham et al. (2018, 2020). Most
recently, a new species and subspecies of salamander
was described from Xuan Nha NR, namely Zylototriton
pasmansi obsti Bernardes, Le, Nguyen, Pham, Pham,
Nguyen, and Ziegler, 2020 (Bernardes et al. 2020). As a
result of our ongoing research in the past five years, this
article provides an updated list of amphibians and reptiles
from Xuan Nha NR, with new data on their distributions
and natural history.
Material and Methods
Four field surveys were conducted at eight sites in Xuan
Nha NR, Son La Province, Vietnam over a total of 51
December 2022 | Volume 16 | Number 2 | e323
Herpetofauna of Xuan Nha Nature Reserve, Vietnam
103°36’ 104°00°
104°24° 104°48” 15°12"
<4 |
o ~ -
av
pe CAMBODIA %
= 3
1 a I >
< -
on
IP
00°
21°
36°
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ai"
12°
20°
48°
3
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aw f
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Fig. 1. Survey sites in Xuan Nha Nature Reserve, Son La Province, Viet Nam: 1. Hin Pen Village, Chieng Son Commune; 2. Cong
Troi Village, Chieng Son Commune; 3. Kho Hong Village, Chieng Xuan Commune; 4. Lay Village, Tan Xuan Commune; 5. Nga
Village, Tan Xuan Commune; 6. Muong An Village, Xuan Nha Commune; 7. Sao Do Village, Van Ho Commune; and 8. So Linh
Village, Van Ho Commune.
days. The sites and dates are: Van Ho District: from
24 to 27 June 2016 in Kho Hong Village, Chieng Xuan
Commune, from 28 June to 2 July 2016 in Muong An
Village, Xuan Nha Commune, and from 3 to 6 July 2016
in Sao Do Village, Van Ho Commune, by A.V. Pham
and N.B. Sung; from 15 to 20 October 2020 in Kho
Hong Village, Chieng Xuan Commune by A.V. Pham,
C.V. Hoang, T.Q. Phan, and N.B. Sung; from 20 to 24
April in Sao Do Village, from 25 to 27 April in So Linh
Village, Van Ho Commune; from 28 to 30 April 2021 in
Muong An Village, Xuan Nha Commune; from 1 April
to 3 May 2021 in Lay Village, from 4 to 7 May 2021
in Nga Village, Tan Xuan Commune by A.V. Pham,
T. Vaxenh, T.A. Sung, C.A. Sung, and L.A. Sun; Moc
Chau District: from 15 to 18 June 2017 and from 12 to
14 October 2020 in Hin Pen Village, and from 19 to 24
June 2017 in Cong Troi Village, Chieng Son Commune
by A.V. Pham and N.B. Sung (Fig. 1 and Table 1).
The typical habitats at the study sites were undisturbed
evergreen forest, disturbed secondary forest, and
agricultural areas (Fig. 2). The geographic coordinates
(WGS84) were recorded by using a Garmin GPSMAP
62s. Specimens were collected by hand between 0800
and 2300 h. After taking photographs in life, animals
were identified to the species level, measured, sexed,
and released at the site. For voucher specimens, a few
individuals were anaesthetized and euthanized in a
closed vessel with a piece of cotton wool containing
Table 1. Information for the survey sites in Xuan Nha Nature Reserve, Vietnam.
Z
°
Site
Forest near Hin Pen Village, Chieng Son Commune
Forest near Cong Troi Village, Chieng Son Commune
Forest near Lay Village, Tan Xuan Commune
Forest near Nga Village, Tan Xuan Commune
Forest near Muong An Village, Xuan Nha Commune
Forest near Sao Do Village, Van Ho Commune
OND Nn BW NY
Forest near So Linh Village, Van Ho Commune
Amphib. Reptile Conserv.
Forest near Kho Hong Village, Chieng Xuan Commune
Latitude Longitude Elevation (m)
20°44.115’°N 104°34.113°E 940
20°45.418°N 104°37.156°E 1,144
20°43.185’N 104°40.267°E 739
20°38.015’N 104°40.175°E 850
20°37.416’N 104°47.039°E 412
20°44.012’N 104°47.022’E 576
20°49.002’N 104°46.132’E 626
20°46.550’N 104°55.415°E 677
December 2022 | Volume 16 | Number 2 | e323
Pham et al.
if Ps) Ve
secondary forest.
ethyl acetate (Simmon 2002), fixed in 80% ethanol, and
then transferred to 70% ethanol for permanent storage.
Some road-killed specimens were also collected for
morphological examination. These specimens were
subsequently deposited in the collection of the Tay Bac
University (TBU), Son La Province, Vietnam.
Taxonomic identifications referred to the descriptions
in Bain et al. (2003), Boulenger (1893), Bourret (1942),
Fei et al. (2012), Hecht et al. (2013), Inger et al. (1999),
Smith (1935, 1943), and Taylor (1962). Species names
followed Frost (2021) for amphibians and Uetz et al.
(2021) for reptiles.
Conservation status levels of amphibian and reptile
species followed the Convention on International Trade
in Endangered Species of Wild Fauna and Flora (CITES),
the Red List of International Union for Conservation of
Nature and Natural Resources (IUCN), Vietnam Red
Data Book (Dang et al. 2007), and The Governmental
Decree No. 84/2021/ND-CP, dated on 22 September
2021 by the Government of Vietnam on the management
of endangered wild flora and fauna.
Results
A total of 107 species belonging to 75 genera and 26
families were recorded from Xuan Nha NR, comprising
41 species of amphibians (24 genera, seven families) and
66 species of reptiles (51 genera, 19 families) (Table 2).
Remarkably, one species of lizard is reported for the first
time from Son La Province and 20 additional species
are documented for the first time from Xuan Nha NR,
Amphib. Reptile Conserv.
Fig. 2. Habitat types in Xuan Nha Nature Reserve, Vietnam: (A, Al, A2) Evergreen forest, (B) Agricultural areas, and (C) Disturb
<4
ed
comprising 10 species of anurans, two species of lizards,
and eight species of snakes. Based on a single snake
specimen from Son La Province of Vietnam, we also
report the first record of Gonyosoma coeruleum outside
of its type locality in Yunnan Province, China.
Amphibia
Anura
Bufonidae
Duttaphrynus melanostictus (Schneider, 1799) (Fig. 3A):
Individuals were observed at night on the ground in
meadowlands, croplands, gardens, and road edges
near residential areas.
Megophryidae
Boulenophrys palpebralespinosa (Bourret, 1937) (Fig.
3B): Two specimens were found at night on leaves,
20-50 cm above the ground, near a stream in evergreen
forest. This is a new record for Xuan Nha NR.
Boulenophrys cf. parva (Boulenger, 1893) (Fig. 3C):
One specimen was found at night on the ground, near
a stream in evergreen forest. Boulenophrys parva
seems to be restricted in Myanmar and records of
this species in northern Vietnam should be assigned
to other named and unnamed species (Manhony et al.
2020).
Leptobrachella eos (Ohler, Wollenberg, Grosjean,
Hendrix, Vences, Ziegler, and Dubois, 2011) (Fig.
3D): One specimen was found at night on the ground
December 2022 | Volume 16 | Number 2 | e323
Herpetofauna of Xuan Nha Nature Reserve, Vietnam
Table 2. List of amphibian and reptile species recorded from Xuan Nha NR, Vietnam. New record types: ***= new record for Vietnam;
** = new record for Son La Province; * = new record for Xuan Nha NR. Site: Descriptions of the sites numbered from 1 to 8 are provided
in Table 1. Habitat codes: 1 = Evergreen forest, 2 = Disturbed secondary forest, and 3 = Agricultural areas. Red Data Book refers to Red
Data Book of Vietnam (Dang et al. 2007), and IUCN refers to The IUCN Red List of Threatened Species (UCN 2021) with the following
conservation status codes: CR = Critically Endangered, EN = Endangered, VU = Vulnerable, NT = Lower Risk/Near Threatened. CITES
refers to CITES appendices (2021): I, Il = Appendix I and II. Decree No. 84 refers to The Governmental Decree No. 84/2021/ND-CP,
dated on 22 September 2021 (The Government of Vietnam 2021), with the following codes: IB = Group IB (Prohibited exploitation and
use for commercial purpose); IIB = Group IIB (limited exploitation and use for commercial purpose). Record evidence: The types of
observations made for each species in the field surveys of this study. Previous record codes indicate literature references: 1 = Nguyen et
al. (2010), 2 = Nguyen et al. (2017), 3 = Pham et al. (2018), 4 = Bernardes et al. (2020), 5 = Pham et al. (2020), and 6 = Pham et al. (2022).
2 : Red Data Decree | Record evidence Previous
ANURA
Bufonidae Gray, 1825
ps feces | one Les TE LP ft
Megophryidae Bonaparte, 1850
Pcs
p> femmes | ¢ Lo LT LT snes
Leptobrachella eos (Ohler,
Wollenberg, Grosjean, Hendrix,
Vences, Ziegler, and Dubois, ‘ : ppecimen
2011)*
Leptobrachella namdongensis
Hoang, Nguyen, Luu, Nguyen, Specimens (4)
and Jiang, 2019
Leptobrachella ventripunctata
Ea (Fe, Ye, and Li, 1990) oe ee
Ayaan i masatakasatoi
Xenophrys maosonensis
(Bourret, 1937)
Microhylidae Giinther, 1858 (1843)
Kaloula pulchra Gray, 1831
Microhyla berdmorei (Blyth,
1856)
Microhyla butleri Boulenger,
1900
Microhyla heymonsi Vogt, 1911 | 3, 4,5, 7, 8
Microhyla mukhlesuri Hasan,
Islam, Kuramoto, Kurabayashi,
and Sumida, 2014
Microhyla pulchra (Hallowell, 1,4,5,7,8 Specimens (2)
1861) Photos
Nanohyla marmorata (Bain and
Neuyen, 2004)* Specimens (2)
Dicroglossidae Anderson, 1871
Fejervarya limnocharis
(Gravenhost, 1829) pes fart fff mmm fo
Amphib. Reptile Conserv. 218 December 2022 | Volume 16 | Number 2 | e323
Specimen (1)
Photos
Specimens (2)
Photos
Specimen (1)
Photos
—
ies)
N
ve
vy
Pham et al.
Table 2 (continued). List of amphibian and reptile species recorded from Xuan Nha NR, Vietnam. New record types: ***= new record
for Vietnam; ** = new record for Son La Province; * = new record for Xuan Nha NR. Site: Descriptions of the sites numbered from 1 to 8
are provided in Table 1. Habitat codes: 1 = Evergreen forest, 2 = Disturbed secondary forest, and 3 = Agricultural areas. Red Data Book
refers to Red Data Book of Vietnam (Dang et al. 2007), and IUCN refers to The IUCN Red List of Threatened Species (IUCN 2021) with the
following conservation status codes: CR = Critically Endangered, EN = Endangered, VU = Vulnerable, NT = Lower Risk/Near Threatened.
CITES refers to CITES appendices (2021): I, Il = Appendix IJ and II. Decree No. 84 refers to The Governmental Decree No. 84/202 1/ND-
CP, dated on 22 September 2021 (The Government of Vietnam 2021), with the following codes: IB = Group IB (Prohibited exploitation
and use for commercial purpose); IIB = Group IIB (limited exploitation and use for commercial purpose). Record evidence: The types of
observations made for each species in the field surveys of this study. Previous record codes indicate literature references: 1 = Nguyen et
al. (2010), 2 = Nguyen et al. (2017), 3 = Pham et al. (2018), 4 = Bernardes et al. (2020), 5 = Pham et al. (2020), and 6 = Pham et al. (2022).
Bis, a Decree Record evidence Previous
Name Site
Hoplobatrachus rugulosus 1,3, 5-7
(Wiegmann, 1834)
Limnonectes bannaensis Ye, Fei,
Xie, and Jiang, 2007
Occidozyga lima (Gravenhorst,
1829)
Occidozyga martensii (Peters,
1867)
Quasipaa verrucospinosa
(Bourret, 1937)
Ranidae Batsch, 1796
1, 3, 4, 6, 8
Amolops cremnobatus Inger and
Kottelat, 1998
N
N
Specimen (1)
Photos
Hylarana macrodactyla
Gunther, 1858
N
Hylarana taipehensis (Van
Denburgh, 1909)
N
Nidirana chapaensis (Bourret,
1937)
N
Odorrana chloronota (Gunther,
1876)
N
Oo
Odorrana nasica (Boulenger,
1903)
Odorrana tiannanensis (Yang
and Li, 1980)
N
Specimens (2)
Specimen (1)
Specimen (1)
Specimen (1)
Photos
Rhacophoridae Hoffman, 1932 (1858)
Kurixalus bisacculus (Taylor, Specimen (1)
1962)* Photos
34 Polypedates megacephalus 1-8 13 Specimens (2) 1
Hallowell, 1861 Photos
Raorchestes parvulus Specimens (2)
(Boulenger, 1893) Photos
serait kio Ohler and
Rhacophorus orlovi Ziegler and Specimens (3)
Kohler, 2001* Photos
Amphib. Reptile Conserv. 219 December 2022 | Volume 16 | Number 2 | e323
Rana johnsi Smith, 1921
Sylvirana guentheri (Boulenger,
1882)
eS)
j=)
eS) N
1, 3, 4, 6,7
Sylvirana maosonensis (Bourret,
1937)
oS)
—
Sylvirana nigrovittata (Blyth,
1856)
—
eS)
v
Herpetofauna of Xuan Nha Nature Reserve, Vietnam
Table 2 (continued). List of amphibian and reptile species recorded from Xuan Nha NR, Vietnam. New record types: ***= new record
for Vietnam; ** = new record for Son La Province; * = new record for Xuan Nha NR. Site: Descriptions of the sites numbered from 1 to 8
are provided in Table 1. Habitat codes: 1 = Evergreen forest, 2 = Disturbed secondary forest, and 3 = Agricultural areas. Red Data Book
refers to Red Data Book of Vietnam (Dang et al. 2007), and IUCN refers to The IUCN Red List of Threatened Species (IUCN 2021) with the
following conservation status codes: CR = Critically Endangered, EN = Endangered, VU = Vulnerable, NT = Lower Risk/Near Threatened.
CITES refers to CITES appendices (2021): I, Il =Appendix I and II. Decree No. 84 refers to The Governmental Decree No. 84/202 1/ND-
CP, dated on 22 September 2021 (The Government of Vietnam 2021), with the following codes: IB = Group IB (Prohibited exploitation
and use for commercial purpose); IIB = Group IIB (limited exploitation and use for commercial purpose). Record evidence: The types of
observations made for each species in the field surveys of this study. Previous record codes indicate literature references: 1 = Nguyen et
al. (2010), 2 = Nguyen et al. (2017), 3 = Pham et al. (2018), 4 = Bernardes et al. (2020), 5 = Pham et al. (2020), and 6 = Pham et al. (2022).
‘ , Red Data Decree | Record evidence Previous
Rhacophorus rhodopus Liu and
Hu, 1960* eee
Zhangixalus feae (Boulenger,
1893)* 3 1 EN Photos
Zhangixalus pachyproctus Yu,
Hui, Hou, Wu, Rao, and Yang, 3,3 1 Photos
2019*
CAUDATA
Salamandridae Goldfuss, 1820
Tylototriton pasmansi obsti
Bernardes, Le, Nguyen, Pham,
Pham, Nguyen, and Ziegler, ee i H np ENGIOS 4
2020
SQUAMATA
Agamidae
Acanthosaura lepidogaster
(Cuvier, 1829) uae foe fff mos fo
Calotes versicolor (Daudin, Specimen (1)
i See ee Ee
Draco maculatus (Gray, 1845) i fi
46 Physignathus cocincinus Cuvier, VU VU
1829
Gekkonidae
EN
Cyrtodactylus otai Nguyen, Le,
47 Pham, Ngo, Hoang, Pham, and
Nguyen, Do, Ngo, Pham, Pham,
Le, and Ziegler, 2020**
1
one fa) aaa L
Photos
Ziegler, 2015
48 Gekko palmatus Boulenger, Specimen (1)
1907 Photos
Hemidactylus frenatus Duméril
5] Hemidactylus garnotii Duméril Specimen (1)
and Bibron, 1836*
Amphib. Reptile Conserv. 220 December 2022 | Volume 16 | Number 2 | e323
Pham et al.
Table 2 (continued). List of amphibian and reptile species recorded from Xuan Nha NR, Vietnam. New record types: ***= new record
for Vietnam; ** = new record for Son La Province; * = new record for Xuan Nha NR. Site: Descriptions of the sites numbered from 1 to 8
are provided in Table 1. Habitat codes: 1 = Evergreen forest, 2 = Disturbed secondary forest, and 3 = Agricultural areas. Red Data Book
refers to Red Data Book of Vietnam (Dang et al. 2007), and IUCN refers to The IUCN Red List of Threatened Species (IUCN 2021) with the
following conservation status codes: CR = Critically Endangered, EN = Endangered, VU = Vulnerable, NT = Lower Risk/Near Threatened.
CITES refers to CITES appendices (2021): I, Il = Appendix I and II. Decree No. 84 refers to The Governmental Decree No. 84/202 1/ND-
CP, dated on 22 September 2021 (The Government of Vietnam 2021), with the following codes: IB = Group IB (Prohibited exploitation
and use for commercial purpose); IIB = Group IIB (limited exploitation and use for commercial purpose). Record evidence: The types of
observations made for each species in the field surveys of this study. Previous record codes indicate literature references: 1 = Nguyen et
al. (2010), 2 = Nguyen et al. (2017), 3 = Pham et al. (2018), 4 = Bernardes et al. (2020), 5 = Pham et al. (2020), and 6 = Pham et al. (2022).
, } ie ae cent Record evidence Previous
Lacertidae
Scincidae
5A Eutropis chapaensis (Bourret, 1
1937)
Eutropis longicaudatus
(Hallowe, 1857) pests | | mm
56 Eutropis multifasciatus (Kuhl, 45,7 3 Phdes 1
1820)
Sphenomorphus indicus (Gray,
1853)* 1 Specimen (1)
Ti ee ore baviensis
Varanidae
Varanus salvator (Laurenti,
1768) Pf tm] fe fm] ft
Typhlopidae
sors] Te TT TTT see
Pythonidae
Python molurus (Linnaeus,
1758) — { fete te fet
Xenopeltidae
62 Xenopeltis unicolor Reinwardt, 1.6 3 Specimen (1) 1
1827 ‘ Photos
Colubridae
Boiga cyanea (Dumeéril, Bibron,
and Duméril, 1854)* . : ebeomen gl)
Boiga multomaculata (Boie,
Ea Ege ps fet ft ff fmm
Calamaria pavimentata
Dumeéeril, Bibron, and Duméril, 1 2 Specimen (1) 1
1854
eee) ee eae
Amphib. Reptile Conserv. 221 December 2022 | Volume 16 | Number 2 | e323
Herpetofauna of Xuan Nha Nature Reserve, Vietnam
Table 2 (continued). List of amphibian and reptile species recorded from Xuan Nha NR, Vietnam. New record types: ***= new record
for Vietnam; ** = new record for Son La Province; * = new record for Xuan Nha NR. Site: Descriptions of the sites numbered from 1 to 8
are provided in Table 1. Habitat codes: 1 = Evergreen forest, 2 = Disturbed secondary forest, and 3 = Agricultural areas. Red Data Book
refers to Red Data Book of Vietnam (Dang et al. 2007), and IUCN refers to The IUCN Red List of Threatened Species (IUCN 2021) with the
following conservation status codes: CR = Critically Endangered, EN = Endangered, VU = Vulnerable, NT = Lower Risk/Near Threatened.
CITES refers to CITES appendices (2021): I, Il = Appendix I and II. Decree No. 84 refers to The Governmental Decree No. 84/202 1/ND-
CP, dated on 22 September 2021 (The Government of Vietnam 2021), with the following codes: IB = Group IB (Prohibited exploitation
and use for commercial purpose); IIB = Group IIB (limited exploitation and use for commercial purpose). Record evidence: The types of
observations made for each species in the field surveys of this study. Previous record codes indicate literature references: 1 = Nguyen et
al. (2010), 2 = Nguyen et al. (2017), 3 = Pham et al. (2018), 4 = Bernardes et al. (2020), 5 = Pham et al. (2020), and 6 = Pham et al. (2022).
Red Data Decree | Record evidence Previous
Dendrelaphis pictus (Gmelin, Specimens (2)
1789)* Photos
Elaphe moellendorffi (Boettger, V Photos
1886)
Elaphe taeniura (Cope, 1861)*
Specimen (1)
Specimen (1)
N
Euprepiophis mandarinus
0.
70
71
i (Cantor, 1842)
Coat |e
Fakes
Lie
Gonyosoma coeruleum Liu,
Hou, Lwin, Wang, and Rao, 5
2021***
Gonyosoma frenatum (Gray,
1853)*
er | es
ee | oe
1
1
1
Specimen (1) 5
1
1
1
Specimen (1)
Photos
Photos 1
Lycodon meridionalis (Bourret,
1935)
Oligodon fasciolatus (Gunther,
1864)*
Oreocryptophis porphyraceus
(Cantor, 1839)
Ptyas korros (Schlegel, 1837)
Ptyas mucosa (Linnaeus, 1758)
Elapidae
VU
—
Wo
i i
8
U
2 es
74
15 Lycodon futsingensis (Pope
1928)
76
77 6
78
79 oo pare NT
0.
II IIB
8] Bungarus fasciatus (Schneider,
1801)
89 Bungarus wanghaotingi Pope, 1.6 5 Phidies 1
1928
BA Ophiophagus hannah (Cantor, CR VU Ul IB 1
1836)
Sinomicrurus macclellandi :
(Reinhardt 1844) pe ttt TT inne
ook
2
2 VU
1 VU
2
1
1
2
2
2
: EN
EN
2 EN
y
7
7
cS,
5
Homalopsidae
Hypsiscopus plumbea (Boie, 1
1827)
Pseudaspididae
Psammodynastes pulverulentus
(Boie, 1827) Pt fet | ff fmm
Amphib. Reptile Conserv. 222 December 2022 | Volume 16 | Number 2 | e323
Pham et al.
Table 2 (continued). List of amphibian and reptile species recorded from Xuan Nha NR, Vietnam. New record types: ***= new record
for Vietnam; ** = new record for Son La Province; * = new record for Xuan Nha NR. Site: Descriptions of the sites numbered from 1 to 8
are provided in Table 1. Habitat codes: 1 = Evergreen forest, 2 = Disturbed secondary forest, and 3 = Agricultural areas. Red Data Book
refers to Red Data Book of Vietnam (Dang et al. 2007), and IUCN refers to The IUCN Red List of Threatened Species (IUCN 2021) with the
following conservation status codes: CR = Critically Endangered, EN = Endangered, VU = Vulnerable, NT = Lower Risk/Near Threatened.
CITES refers to CITES appendices (2021): I, Il = Appendix I and II. Decree No. 84 refers to The Governmental Decree No. 84/202 1/ND-
CP, dated on 22 September 2021 (The Government of Vietnam 2021), with the following codes: IB = Group IB (Prohibited exploitation
and use for commercial purpose); IIB = Group IIB (limited exploitation and use for commercial purpose). Record evidence: The types of
observations made for each species in the field surveys of this study. Previous record codes indicate literature references: 1 = Nguyen et
al. (2010), 2 = Nguyen et al. (2017), 3 = Pham et al. (2018), 4 = Bernardes et al. (2020), 5 = Pham et al. (2020), and 6 = Pham et al. (2022).
‘ : Red Data Decree | Record evidence Previous
Natricidae
88 Amphiesma stolatum (Linnaeus, 1
1758)
Fowlea flavipunctatus (Hallwell, 1
1861)
Hebius chapaensis (Bourret,
Ea weal Raa eaargae L
9] Rhabdophis chrysargos 1
(Schlegel, 1837)
Rhabdophis nigrocinctus (Blyth,
1856)* 1 Specimen (1)
93 Rhabdophis helleri (Schmidt, 1,2,6,7 23 Photos 1
L923)
Trimerodytes percarinatus
(Boulenger, 1899) pete TE Pm
Pareidae
Pareas hamptoni (Boulenger, .
° | 1905)" ee a ee ariasien =
Viperidae
Ovophis monticola (Gunther, :
este Pa a pad
Trimeresurus albolabris Gray, Specimen (1)
Trimeresurus stejnegeri 1
Schmidt, 1925
TESTUDINES
Platystermidae
Platysternon megacephalum 4 1 EN CR I IB PHBE 1
Gray, 1831
Geoemydidae
100 Cuora galbinifrons Bourret, EN CR Ul IB 1
1939
102 Geoemyda spengleri (Gmelin, EN Il IB 1
1789)
Sacalia quadriocellata
(Siebenrock, 1903) | Ee pf
Amphib. Reptile Conserv. 223 December 2022 | Volume 16 | Number 2 | e323
Herpetofauna of Xuan Nha Nature Reserve, Vietnam
Table 2 (continued). List of amphibian and reptile species recorded from Xuan Nha NR, Vietnam. New record types: ***= new record
for Vietnam; ** = new record for Son La Province; * = new record for Xuan Nha NR. Site: Descriptions of the sites numbered from 1 to 8
are provided in Table 1. Habitat codes: 1 = Evergreen forest, 2 = Disturbed secondary forest, and 3 = Agricultural areas. Red Data Book
refers to Red Data Book of Vietnam (Dang et al. 2007), and IUCN refers to The IUCN Red List of Threatened Species (IUCN 2021) with the
following conservation status codes: CR = Critically Endangered, EN = Endangered, VU = Vulnerable, NT = Lower Risk/Near Threatened.
CITES refers to CITES appendices (2021): I, Il = Appendix I and II. Decree No. 84 refers to The Governmental Decree No. 84/202 1/ND-
CP, dated on 22 September 2021 (The Government of Vietnam 2021), with the following codes: IB = Group IB (Prohibited exploitation
and use for commercial purpose); IIB = Group IIB (limited exploitation and use for commercial purpose). Record evidence: The types of
observations made for each species in the field surveys of this study. Previous record codes indicate literature references: 1 = Nguyen et
al. (2010), 2 = Nguyen et al. (2017), 3 = Pham et al. (2018), 4 = Bernardes et al. (2020), 5 = Pham et al. (2020), and 6 = Pham et al. (2022).
. : Red Data Decree | Record evidence Previous
Testudinidae
ai 9
Trionychidae
Palea steindachneri
(Siebenrock, 1906) Sf fw fe fp fmf
near a stream in evergreen forest. This is a new record
for Xuan Nha NR.
Leptobrachella namdongensis Hoang, Nguyen, Luu,
Nguyen, and Jiang, 2019 (Fig. 3E): Four specimens
were found at night on the ground or on stones near a
stream. The surrounding habitat was evergreen forest,
composed of small hardwoods, liane, and shrub.
Leptobrachella ventripunctata (Fei, Ye, and Li, 1990)
(Fig. 3F): One specimen was found on a stone near a
stream and two other specimens were observed along
a forest path at night. This is a new record for Xuan
Nha NR.
Leptobrachium masatakasatoi Matsui, 2013 (Fig. 3G):
Two specimens were found at night on the ground
near a stream in evergreen forest.
Xenophrys maosonensis (Bourret, 1937) (Fig. 3H): Two
specimens were found at night on the ground, near a
stream in evergreen forest.
Microhylidae
Kaloula pulchra Gray, 1831 (Fig. 31): An individual was
observed at night on a bonsai pot in a household garden.
Microhyla_ butleri Boulenger, 1900 (Fig. 3J): One
specimen was found at night on the ground in
meadowlands and other individuals were observed at
night in croplands, and at small puddle edges near the
rice fields and forest edges.
Microhyla heymonsi Vogt, 1911 (Fig. 3K): Two specimens
were found at night on the ground along road edges
and other individuals were observed at night on the
ground in croplands, in meadowlands, croplands, and
forest trails near forest edges, and inside the forest.
Microhyla mukhlesuri Hasan, Islam, Kuramoto,
Kurabayashi, and Sumida, 2014 (Fig. 3L): One
Amphib. Reptile Conserv.
specimen was found at night on the ground near small
puddle edges in rice fields, and other individuals were
observed at night on the ground near small puddle
edges in rice fields, meadowlands, and croplands.
Microhyla pulchra (Hallowell, 1861) (Fig. 3M): Two
specimens were found at night on the ground in
meadowlands near rice fields, and other individuals
were observed at night on the ground in croplands,
around small puddle edges.
Nanohyla marmorata (Bain and Nguyen, 2004) (Fig.
3N): Two specimens were found in the morning on
the forest path. The surrounding habitat was evergreen
forest. This is a new record for Xuan Nha NR.
Dicroglossidae
Fejervarya limnocharis (Gravenhost, 1829) (Fig. 30):
Many individuals were observed at night on the
ground, in meadowlands near rice fields, croplands,
and small puddles at road edges.
Hoplobatrachus rugulosus (Wiegmann, 1834) (Fig. 3P):
Individuals were observed at night on the ground, at
pond edges, and in rice fields.
Limnonectes bannaensis Ye, Fei, Xie, and Jiang, 2007
(Fig. 3Q): Individuals were observed at night on the
ground near streams or water edges in streams in
evergreen forest.
Quasipaa verrucospinosa (Bourret, 1937) (Fig. 3R):
Individuals were observed at night on rocks in streams
or near waterfalls. The surrounding habitat was
evergreen forest.
Ranidae
Amolops cremnobatus Inger and Kottelat, 1998 (Fig.
December 2022 | Volume 16 | Number 2 | e323
Pham et al.
pee er Plate * ite Woe Se
Fig. 3. Amphibian species recorded in Xuan Nha Nature Reserve, Vietnam: (A) Duttaphrynus melanostictus, (B) Boulenophrys
palpebralespinosa, (C) Boulenophrys cf. parva, (D) Leptobrachella eos, (E) L. namdongensis, (F) L. ventripunctata, (G)
Leptobrachium masatakasatoi, (H) Xenophrys maosonensis, (1) Kaloula pulchra, (J) Microhyla butleri, (KK) M. heymonsi, (L)
M. mukhlesuri, (M) M. pulchra, (N) Nanohyla marmorata, (O) Fejervarya limnocharis, (P) Hoplobatrachus rugulosus, (Q)
Limnonectes bannaensis, and (R) Quasipaa verrucospinosa.
Amphib. Reptile Conserv. 225 December 2022 | Volume 16 | Number 2 | e323
Herpetofauna of Xuan Nha Nature Reserve, Vietnam
ad EOF ie — 5
ar < ee ne
f
=
Fig. 4. Additional amphibian species recorded in Xuan Nha Nature Reserve, Vietnam: (A) Amolops cremnobatus, (B) Nidirana
chapaensis, (C) Odorrana nasica, (D) O. tiannanensis, (E) Rana johnsi, (F) Sylvirana guentheri, (G) S. maosonensis, (H) S.
nigrovittata, (1) Kurixalus bisacculus, (J) Polypedates megacephalus, (KK) Raorchestes parvulus, (L) Rhacophorus kio, (M) R.
orlovi, (N) Rhacophorus rhodopus, (O) Zhangixalus feae, (P) Z. pachyproctus, and (Q) Tylototriton pasmansi obsti.
Amphib. Reptile Conserv. 226 December 2022 | Volume 16 | Number 2 | e323
Pham et al.
4A): Two specimens were found at night on rocks in
streams with strong currents. The surrounding habitat
was evergreen forest, composed of small hardwoods,
liane, and shrub.
Nidirana chapaensis (Bourret, 1937) (Fig. 4B): One
specimen was found at night on tree leaves, 30 cm
above the ground, near a stream. Two other individuals
were observed on the ground at a small puddle edge in
evergreen forest.
Odorrana nasica (Boulenger, 1903) (Fig. 4C): One
specimen was found at night on a rock near a waterfall
in evergreen forest.
Odorrana tiannanensis (Yang and Li, 1980) (Fig. 4D):
Two specimens were found at night on the ground
near a stream in evergreen forest.
Rana johnsi Smith, 1921 (Fig. 4E): One specimen was
found at night on the ground near a stream at the forest
edge.
Sylvirana guentheri (Boulenger, 1882) (Fig. 4F):
Individuals were observed at night on the ground or
on leaves, ca. 30-50 cm above the ground near pond
edges and streams. The surrounding habitat was rice
field.
Sylvirana maosonensis (Bourret, 1937) (Fig. 4G): One
specimen was found at night on the ground near a
stream in evergreen forest.
Sylvirana nigrovittata (Blyth, 1856) (Fig. 4H): One
specimen was found at night on the ground near a
stream, and other individuals were observed at night
on the ground, on stones near a stream or at the
water edges in streams. The surrounding habitat was
evergreen forest. The call concerts were regularly
heard in the evening.
Rhacophoridae
Kurixalus bisacculus (Yaylor, 1962) (Fig. 41): One
specimen was found at night on a tree branch near a
stream, and other individuals were observed at night
while sitting on leaves near a stream or near puddles,
ca. 1-2 m above the ground. The surrounding habitat
was mixed evergreen forest of small hardwoods,
bamboo, and shrubs. This is a new record for Xuan
Nha NR.
Polypedates megacephalus Hallowell, 1861 (Fig. 4J):
Two specimens were found at night on the tree
branches near puddles, and other individuals were
observed at night while sitting on leaves or branches
near streams, puddles, and ponds, ca. 0.3—2 m above
the ground. The surrounding habitat was cultivated
land, mixed evergreen forest of small hardwoods,
bamboo, and shrubs.
Raorchestes parvulus (Boulenger, 1893) (Fig. 4K): Two
Specimens were found at night sitting on leaves near
streams, ca. 1-3 m above the ground in evergreen forest.
Rhacophorus kio Ohler and Delorme, 2006 (Fig. 4L):
Individuals were observed at night while sitting on
Amphib. Reptile Conserv.
leaves near puddles, ca. 2-5 m above the ground in
evergreen forest.
Rhacophorus orlovi Ziegler and Kohler, 2001 (Fig. 4M):
Three specimens were found at night while sitting
on leaves near streams, 2—3 m above the ground in
evergreen forest. This is a new record for Xuan Nha
NR.
Rhacophorus rhodopus Liu and Hu, 1960 (Fig. 4N):
Individuals were observed at night while sitting on
leaves near puddles, ca. 2-5 m above the ground in
evergreen forest. This is a new record for Xuan Nha
NR.
Zhangixalus feae (Boulenger, 1893) (Fig. 40):
Individuals were observed at night while sitting on
leaves, 0.5—3 m above the ground; some individuals
found on the ground near streams in evergreen forest.
Zhangixalus pachyproctus Yu, Hui, Hou, Wu, Rao, and
Yang, 2019 (Fig. 4P): Individuals were observed at
night while sitting on leaves, ca. 1-6 m above the
ground, near large puddles in evergreen forest. This is
a new record for Xuan Nha NR.
Caudata
Salamandridae
Tylototriton pasmansi obsti Bernardes, Le, Nguyen,
Pham, Pham, Nguyen, and Ziegler, 2020 (Fig. 4Q).:
Individuals were observed during the daytime in
small streams in evergreen forest. Surrounding habitat
was small hardwoods, bamboo, and shrub.
Reptilia
Squamata
Agamidae
Acanthosaura lepidogaster (Cuvier, 1829) (Fig. 5A): An
individual was observed while sitting on a tree, about
2 m above the ground, and another individual was
seen while crossing a forest path.
Calotes emma Gray, 1845 (Fig. 5B): One specimen was
found in the morning on a forest path in evergreen
forest.
Calotes versicolor (Daudin, 1802) (Fig. 5C): Individuals
were observed during the daytime near cultivated
areas and another road-killed individual was found on
Road 102. Some individuals were seen on the ground
near bushes in a garden.
Gekkonidae
Cyrtodactylus otai Nguyen, Le, Pham, Ngo, Hoang,
Pham, and Ziegler, 2015 (Fig. 5D): Three individuals
were observed at night, on tree branches, near
limestone cliffs at the forest edges.
Gekko palmatus Boulenger, 1907 (Fig. 5E): One specimen
was found and other individuals were observed at
night on limestone cliffs at the forest edges.
December 2022 | Volume 16 | Number 2 | e323
Herpetofauna of Xuan Nha Nature Reserve, Vietnam
2 : -
Fig. 5. Lizard species recorded in Xuan Nha Nature Reserve, Vietnam: (A) Acanthosaura lepidogaster, (B) Calotes emma,
(C) C. versicolor, (D) Cyrtodactylus otai, (E) Gekko palmatus, (F) G. reevesii, (G) Hemidactylus frenatus, (H) H. garnotii, (1)
Hemiphyllodactylus bonkowskii, (J) Takydromus sexlineatus, (IK) Eutropis longicaudatus, (L) E. multifasciatus, (M) Sphenomorphus
indicus, and (N) Tropidophorus baviensis.
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Pham et al.
Gekko reevesii (Gray, 1831) (Fig. 5F): An individual
was observed at night on limestone cliffs, and another
individual was observed on a big tree, about 5 m
above the ground.
Hemidactylus frenatus Duméril and Bibron, 1836 (Fig.
5G): Individuals were observed at night on the wall
near a light in a residential area.
Hemidactylus garnotii Duméril and Bibron, 1836 (Fig.
5H): One specimen was found and other individuals
were observed at night on limestone karst outcrops,
2—3 m above the ground. The surrounding habitat was
secondary forest. This is a new record for Xuan Nha
NR.
Hemiphyllodactylus bonkowskii Nguyen, Do, Ngo,
Pham, Pham, Le, and Ziegler, 2020 (Fig. 51): Two
specimens were found at night on tree branches near
limestone cliffs at forest edges. This is a new record
for Xuan Nha NR and Son La Province.
Lacertidae
Takydromus sexlineatus Daudin, 1802 (Fig. 5J): One
specimen was found during the daytime, on the
ground near bamboo trees in secondary forest.
Scincidae
Eutropis longicaudatus (Hallowell, 1857) (Fig. 5K):
Individuals were found during the daytime on the
ground, garden fences, road edges, and shrubs near
cultivated areas.
Eutropis multifasciatus (Kuhl, 1820) (Fig. 5L): Three
individuals were found during the daytime on the
ground, along road edges near cultivated areas.
Sphenomorphus indicus (Gray, 1853) (Fig. 5M): One
specimen was found in the afternoon on a forest path in
evergreen forest. This is a new record for Xuan Nha NR.
Tropidophorus baviensis Bourret, 1939 (Fig. 5N): One
specimen was found under a carpet of fallen leaves at
the forest edge.
Typhlopidae
Indotyphlops braminus (Daudin, 1803) (Fig. 6A): One
specimen was found in the morning under a rotten
bamboo tree at the forest edge.
Xenopeltidae
Xenopeltis unicolor Reinwardt, 1827 (Fig. 6B): An
individual was observed in the afternoon under a
rotten plank in a garden and another road-killed
specimen was found on Road 102.
Colubridae
Ahaetulla prasina (Bote, 1827) (Fig. 6C): An individual
Amphib. Reptile Conserv.
was found at night on the thick grass in secondary
forest.
Boiga cyanea (Dumeéril, Bibron, and Dumeéril, 1854)
(Fig. 6D): A road-killed specimen was found in the
afternoon on Road 102. The surrounding habitat was
evergreen forest.
Boiga guangxiensis Wen, 1998 (Fig. 6E): An individual
was observed at night on a tree branch near a stream
in evergreen forest.
Boiga multomaculata (Boie, 1827) (Fig. 6F): An
individual was observed at night while moving on the
grass near a stream at the forest edge.
Calamaria pavimentata Dumeéril, Bibron, and Dumeéril,
1854 (Fig. 6G): A road-killed individual was found
in the morning on Road 102. The surrounding habitat
was secondary forest.
Coelognathus radiatus (Boie, 1827) (Fig. 6H): An
individual was observed in the afternoon while
moving across Road 102.
Dendrelaphis pictus (Gmelin, 1789) (Fig. 61): Two
specimens were found in the afternoon near Road
102, an individual crawling on a tree branch and a
road-killed individual on Highway 6. This is a new
record for Xuan Nha NR.
Elaphe moellendorffi (Boettger, 1886) (Fig. 6J): An
individual was observed in the afternoon near the
entrance of a cave at the forest edge.
Elaphe taeniura (Cope, 1861) (Fig. 6K): An individual
was observed in the morning near a large rock at the
forest edge, and another individual was detected in an
agricultural area. This is a new record for Xuan Nha
NR.
Euprepiophis mandarinus (Cantor, 1842) (Fig. 6L): A
road-killed individual was found in the morning on
Highway 6. The surrounding habitat was evergreen
forest.
Gonyosoma coeruleum Liu, Hou, Lwin, Wang, and
Rao 2021 (Fig. 6M): A road-killed specimen (adult
male) was found in the morning on Highway 6. The
surrounding habitat was evergreen forest. This is the
first record of this species in Vietnam. Gonyosoma
coeruleum was recently described by Liu et al. (2021)
from Yunnan Province, China. The new species
closely resembles G. prasinum (Blyth), but it is
differentiated from the latter species by having the
precloacal plate divided, iris blue and inside of mouth
greyish-white in life. Morphological characteristics of
the specimen from Son La Province are as follows:
Snout-vent length: 662 mm; tail length: 242 mm;
head distinguished from neck; pupil rounded; rostral
broader than high; internasals as wide as long:
prefrontal shorter than length of frontal; frontal
pentagonal; parietals longer than wide; nasal paired;
loreal 1/1; supralabials 9/9, fourth to sixth entering
orbit; infralabials 10/10, first to fifth bordering chin
shields; preocular 1/1; postoculars 2/2; anterior
temporals 2/2, posterior temporals 2/2; dorsal scale
December 2022 | Volume 16 | Number 2 | e323
Herpetofauna of Xuan Nha Nature Reserve, Vietnam
3 ee 7d ee
Fig. 6. Snake species recorded in Xuan Nha Nature Reserve, Vietnam: (A) /ndotyphlops braminus, (B) Xenopeltis unicolor, (C)
Ahaetulla prasina, (D) Boiga cyanea, (E) B. guangxiensis, (F) B. multomaculata, (G) Calamaria pavimentata, (H) Coelognathus
radiatus, (1) Dendrelaphis pictus, (J) Elaphe moellendorffi, (WK) Elaphe taeniura, (L) Euprepiophis mandarinus, (M) Gonyosoma
coeruleum, (N) G. frenatum, (O) Lycodon futsingensis, (P) L. meridionalis, (Q) Oligodon fasciolatus, and (R) Oreocryptophis
porphyraceus.
Amphib. Reptile Conserv. 230 December 2022 | Volume 16 | Number 2 | e323
Pham et al.
ae
ae
aS ote
a ‘on 4
Poo \ ae |
Fig. 7. Snake and turtle species recorded in Xuan Nha Nature Reserve, Vietnam: (A) Ptvas korros, (B) Bungarus fasciatus, (C)
Bungarus wanghaotingi, (D) Naja atra, (E) Sinomicrurus macclellandi, (F) Psammodynastes pulverulentus, (G) Hebius chapaensis,
(H) Rhabdophis nigrocinctus, (1) Rhabdophis helleri, (J) Trimerodytes percarinatus, (IK) Pareas hamptoni, (L) Ovophis monticola,
(M) 7rimeresurus albolabris, (N) Platysternon megacephalum, and (O) Manouria impressa.
rows 19-19-15; ventrals 198; cloacal scale paired: Highway 6. The surrounding habitat was evergreen
subcaudals 100, paired. Coloration in preservative: forest.
dorsal surface green; belly greenish (determination Lycodon futsingensis (Pope, 1928) (Fig. 60): One
after Liu et al. 2021). specimen was found at night on the ground while
Gonyosoma frenatum (Gray, 1853) (Fig. 6N): A road- moving near a stream in evergreen forest.
killed specimen was found in the afternoon on Lycodon meridionalis (Bourret, 1935) (Fig. 6P): A
Amphib. Reptile Conserv. 231 December 2022 | Volume 16 | Number 2 | e323
Herpetofauna of Xuan Nha Nature Reserve, Vietnam
road-killed specimen was found in the afternoon on
Highway 6. The surrounding habitat was evergreen
forest.
Oligodon fasciolatus (Gunther, 1864) (Fig. 6Q): An
individual was observed at night on the ground
while moving across a forest trail, and a road-killed
specimen was found on Highway 6. This is a new
record for Xuan Nha NR.
Oreocryptophis porphyraceus (Cantor, 1839) (Fig. 6R):
An individual was observed at night while moving on
the roadside. The surrounding habitat was evergreen
forest.
Ptyas korros (Schlegel, 1837) (Fig. 7A): Five individuals
were found during the daytime on the ground or on
tree branches near bamboo bushes, abandoned fields,
and at the roadside near forest edge.
Elapidae
Bungarus fasciatus (Schneider, 1801) (Fig. 7B): An
individual was observed at night near the ground by a
stream at the forest edge.
Bungarus wanghaotingi Pope, 1928 (Fig. 7C): An
individual was observed near a stream and another
individual was observed in arice field. The surrounding
habitat was secondary forest. Previous records of B.
multicinctus in Xuan Nha NR by Nguyen et al. (2010)
and in Vietnam by Nguyen et al. (2009) should be re-
identified as Bungarus wanghaotingi after Chen et al.
(2021).
Naja atra Cantor, 1842 (Fig. 7D): An individual was
observed in the afternoon on the ground, in a bamboo
bush near Road 102. The surrounding habitat was the
secondary forest.
Sinomicrurus macclellandi (Reinhardt, 1844) (Fig. 7E):
A road-killed specimen was found in the morning on
Highway 6. The surrounding habitat was evergreen
forest.
Lamprophiidae
Psammodynastes pulverulentus (Boie, 1827) (Fig. 7F):
An individual was observed at night on a tree branch
near the forest edge.
Natricidae
Hebius chapaensis (Bourret, 1934) (Fig. G): One
specimen was found at night in a stream in evergreen
forest. This is a new record for Xuan Nha NR.
Rhabdophis nigrocinctus (Blyth, 1856) (Fig. 7H): One
Specimen was found in the afternoon while moving
on the grass near a stream in secondary forest. This is
a new record for Xuan Nha NR.
Rhabdophis helleri (Schmidt, 1925) (Fig. 71): Individuals
were found during the daytime on the ground or
on grass near the roadside, and in rice fields. The
Amphib. Reptile Conserv.
surrounding habitat was secondary forest and
agricultural cultivation areas.
Trimerodytes percarinatus (Boulenger, 1899) (Fig. 7J):
An individual was observed in the afternoon near a
stream. The surrounding habitat was evergreen forest.
Pareatidae
Pareas hamptoni (Boulenger, 1905) (Fig. 7K): One
specimen was found at night sitting on a tree branch
in evergreen forest. This is a new record for Xuan
Nha NR.
Viperidae
Ovophis monticola (Gunther, 1864) (Fig. 7L): One
specimen was found at night while moving across a
forest trail in evergreen forest.
Trimeresurus albolabris Gray, 1842 (Fig. 7M):
Specimens were observed during the daytime on tree
branches at forest edges. The surrounding habitat was
secondary forest and agricultural cultivation areas.
Testudines
Platysternidae
Platysternon megacephalum Gray, 1831 (Fig. 7N): An
individual was observed at night under a rock in a
stream. The surrounding habitat was evergreen forest.
Testudinidae
Manouria impressa (Guenther, 1882) (Fig. 70): An
individual was observed in the afternoon under a wet
carpet of leaves in evergreen forest.
Discussion
The new findings in this study bring the number of
amphibian and reptile species in Xuan Nha NR to 107,
comprising 41 amphibian and 66 reptile species, of
which 21 species are new records for Xuan Nha NR, one
Species 1s a new record for Son La Province, and one
is recorded for the first time from Vietnam. Gonyosoma
coeruleum was recorded for the first time from outside
of China based on a single specimen collected from
Son La Province, Vietnam. This species was recently
described by Liu et al. (2021) from Yunnan Province,
China. Because of morphological ambiguity between
G. coeruleum and G. prasinum, previous records of G.
prasinum in Vietnam should be re-examined to determine
whether they are referrable to G. coeruleum or are, in
fact, true G. prasinum. Hemiphyllodactylus bonkowskii
was recently described by Nguyen et al. (2020). Its
original description was based on specimens found in
Hoa Binh Province, with the type locality approximately
20 km from the new records in Xuan Nha NR.
December 2022 | Volume 16 | Number 2 | e323
Pham et al.
i
i
timber logging, (C) Domestic animal production in the forest, (D, E) Road-killed reptiles and amphibians on the road, and (F) Wildlife
collection for food and trade.
Several of the records provided by Nguyen et al. (2010)
were excluded from the list of Xuan Nha NR in this study,
either because they were based on misidentifications or due
to changes in taxonomy and/or nomenclature. For example,
Leptobrachella_ pelodytoides was formerly reported
from the nature reserve, but has since been assigned to
a different taxon, and L. pelodytoides is considered to be
restricted to Myanmar, southern China, and Thailand (Frost
Amphib. Reptile Conserv.
2021). Previous records of Leptobrachium chapaense,
Amolops_ ricketti, Calotes mystaceus, and Bungarus
multicinctus in Xuan Nha NR, as reported by Nguyen
et al. (2010), could be reidentified as Leptobrachium
masatakasatoi, Amolops cremnobatus, Calotes emma,
and Bungarus wanghaotingi, respectively. Some species
were documented from Xuan Nha NR based on interview
information only, viz. Hylarana macrodactyla, Odorrana
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Herpetofauna of Xuan Nha Nature Reserve, Vietnam
chloronota, Physignathus cocincinus, Varanus salvator,
Python molurus, Ptyas mucosa, Ophiophagus hannah,
Hypsiscopus plumbea, Fowlea flavipunctatus, Cuora
mouhotii, Geoemyda_ spengleri, Mauremys _ sinensis,
Indotestudo elongata, and Palea_ steindachneri. Nine
other species (Occidozyga lima, O. martensii, Hylarana
taipehensis, Eutropis chapaensis, Amphiesma_stolatum,
Rhabdophis chrysargos, Trimeresurus stejnegeri, Cuora
galbinifrons, and Sacalia quadriocellata) were included
in the list here based on the previous records of Nguyen
et al. (2010).
In terms of habitat preferences, most of the amphibians
and reptiles in this survey inhabit the evergreen forest (41
species, or 50% of the total recorded species), followed
by disturbed secondary forest with 33 recorded species
(40.24%), and agricultural areas with 19 recorded species
(23:1:7%: Table:2).
Among the eight survey sites, Kho Hong has the
highest level of species richness with 29 recorded
species; followed by Lay forest with 26 species; the Hen
Pin and Sao Do sites with 23 species; the Nga, Muong
An and So Linh sites with 21 species; and Cong Troi
with 15 species (Table 2). Both of the Kho Hong and Lay
sites are located in the core zone of the Xuan Nha NR
with a large area of evergreen forest (>3,000 hectares)
and the habitat quality is relatively good. Therefore, the
numbers of recorded species are higher than those of the
other sites.
Concerning its herpetofaunal conservation status,
the Xuan Nha NR harbors a high number of threatened
species. Among the 107 species, 19 are listed in the Red
Data Book of Vietnam (Dang et al. 2007), including
three species categorized as CR, 10 as EN, and six as
VU; 18 species are listed in the IUCN Red List IUCN
2022), including six species categorized as CR, five as
EN, five as VU, and two as NT; 14 species are listed in
the Vietnam Governmental Decree No. 84/2021/ND-
CP (2021), including three species in Group IB and 11
species in Group IIB; and 14 species are listed in the
CITES appendices, including one species in Appendix
I and 13 in Appendix II (Table 2). The major threats to
the habitat and populations of amphibians and reptiles
in the Xuan Nha NR are deforestation resulting from
agricultural activities (Fig. 8A), illegal timber logging
(Fig. 8B), free grazing of cattle in the forest (Fig. 8C),
road construction (Fig. 8D—E), and wildlife poaching for
food and trade (Fig. 8F).
Acknowledgements.—We are grateful to the directorates
of Forest Protection Department of Son La Province and
Xuan Nha Nature Reserve for their support of our field
work and issuing relevant permits (permit No. 22/GT
issued on 7 June 2012). We thank TA Sung, LA Sung, CA
Sung, LA Sung (Van Ho District), and CV Nguyen and
CA Lau (Moc Chau Chau District) for their assistance in
the field.
Amphib. Reptile Conserv.
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Anh Van Pham is an Associate Professor of Biology and a Senior Lecturer at the Faculty of Environmental
Sciences, University of Science, Vietnam National University, Hanoi; and a Senior Researcher at the
Center for Biodiversity and Environment Research, Tay Bac University in Vietnam. He obtained his Ph.D.
in 2016 from the Faculty of Biology, Hanoi National University of Education, Vietnam. His research
focuses on the taxonomy and conservation of amphibians and reptiles in Vietnam. He has published one
book and 72 papers, mainly dealing with the herpetodiversity of Vietnam.
Truong Quang Nguyen is a Senior Researcher at the Institute of Ecology and Biological Resources and
a Professor of the Graduate University of Science and Technology, Vietnam Academy of Science and
Technology. He obtained his Ph.D. in 2011 from the Zoological Research Museum Alexander Koenig
and the University of Bonn, Germany (DAAD fellow). From 2011 to 2014, Truong was a Postdoctoral
researcher at the Zoological Institute of the University of Cologne/Cologne Zoo in Germany (Humboldt
Fellow). His research interests are the systematics, ecology, phylogeny, and conservation of reptiles and
amphibians in Southeast Asia. He is the co-author of 14 books and more than 350 papers relevant to
biodiversity research and conservation in Southeast Asia.
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Amphib. Reptile Conserv.
Herpetofauna of Xuan Nha Nature Reserve, Vietnam
Cuong The Pham is a Principal Researcher of the Institute of Ecology and Biological Resources
(IEBR), Vietnam Academy of Science and Technology (VAST). He is member of the Cologne Zoo’s
Biodiversity and Nature conservation projects in Vietnam. Cuong obtained his Ph.D. in 2018 from
the Graduate University of Science and Technology (GUST), Vietnam Academy of Science and
Technology (VAST). He has published 100 papers, mainly dealing with the herpetodiversity of
Vietnam. He is very experienced in biodiversity and field research, and has conducted numerous field
surveys in Vietnam. His research interests are the systematics, ecology, phylogeny, and conservation
of reptiles and amphibians from Vietnam.
Nenh Ba Sung is a researcher at the Center for Biodiversity and Environment Research, Tay Bac
University, Son La, Vietnam. His research focuses primarily on the taxonomy and conservation
of amphibians and reptiles in Vietnam. He has published eight papers, mainly dealing with the
herpetodiversity of Vietnam.
Minh Duc Le has been working on conservation-related issues in Southeast Asia for more than 15
years. His work focuses on biotic surveys, wildlife trade, and the conservation genetics of various
wildlife groups in Indochina. Minh is currently working on projects which characterize the genetic
diversity of highly threatened reptiles and mammals in the region, and he has pioneered the application
of molecular tools in surveying critically endangered species in Vietnam. He has long been involved in
studying the impact of the wildlife trade on biodiversity conservation in Vietnam, and is developing a
multidisciplinary framework to address this issue in the country.
Tao Thien Nguyen is a Senior Researcher at the Institute of Genome Research of the Vietnam
Academy of Science and Technology. His research interests are in the taxonomy, evolutionary origin,
and diversification of amphibians and reptiles, as well the practical elucidation of the phylogeny of
various amphibian and reptile groups. Tao obtained his Ph.D. from Kyoto University, Japan, with a
focus on the molecular and morphological systematics and distribution pattern of various rhacophorid
species. He has extensive experience in the taxonomy and ecology of amphibians and reptiles
throughout Vietnam. Since 2007, he has published more than 120 papers on herpetological topics.
Thomas Ziegler has been the Curator of the Aquarium/Terrarium Department of the Cologne Zoo,
Germany, since 2003. He is also the Coordinator of the Biodiversity and Nature Conservation Projects
of the Cologne Zoo in Vietnam and Laos. As a Zoo Curator and Project Coordinator, Thomas tries to
combine in situ and ex situ approaches, such as linking zoo biological aspects with diversity research
and conservation in the Cologne Zoo, in rescue stations and breeding facilities in Vietnam, and in the
last remaining forests in Indochina. Since February 2009, he has been an Associate Professor at the
Zoological Institute of Cologne University, Germany, and since 2016 he has been an Adjunct Professor.
Photo by Rolf Schlosser.
236 December 2022 | Volume 16 | Number 2 | e323