Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

15(2) [General Section]: 1-9 (e277).

Sa KS

ptile-cons®

Abundance and microhabitat use of the Endangered toad

Rhinella yanachaga (Anura: Bufonidae) in the cloud forest of

Yanachaga Chemillen National Park, Peru

12Shirley Huaman-Trucios, *Vladimir Camel, ‘Edith Orellana Mendoza, *Marcela V. Pyles,

and **Rudolf von May

‘Facultad de Ciencias Forestales y del Ambiente, Universidad Nacional del Centro del Peru, Huancayo, PERU ?Servicio Nacional de Areas

Naturales Protegidas por el Estado - SERNANP, Lima, PERU 2Universidad Cientifica del Sur, Lima, PERU ‘Biology Institute, Sector of Ecology

and Conservation, Federal University of Lavras (UFLA), Minais Gerais, BRAZIL °Biology Program, California State University Channel Islands,

Camarillo, California, USA

Abstract.—The arboreal toad Rhinella yanachaga is an endemic species of the cloud forest of central Peru,

and is categorized as Endangered according to the International Union for Conservation of Nature. The core

habitat of this species is within the Yanachaga-Chemillen National Park, but the status of its populations

remains unknown. Obtaining quantitative data based on field surveys is essential for conserving this species

in the park. In this study, the abundance, size, and microhabitat use of R. yanachaga were examined across

an elevational gradient. Individuals with snout-to-vent length (SVL) 2 20 mm were sampled in four transects

between 2,400 and 2,800 m, in the wet and dry seasons. Using night surveys, individual data were recorded

on sex, SVL, microhabitat, geographic location, relative humidity, and temperature. The abundance of females

and males varied among transects in dry and wet sampling periods. We recorded more individuals in the dry

season and observed that frogs distributed at higher elevations tend to have a larger body size than those at

lower elevations. Most individuals appear to prefer microhabitats composed of leaves and ferns. Additionally,

we observed sexual dimorphism in size, as females were larger than males. These findings contribute to

amphibian conservation programs in Peru.

Keywords. Amphibian, population status, elevational gradient, endemic species, habitat, South America.

Resumen.—El sapo arboreo Rhinella yanachaga es una especie endeémica del bosque nuboso del centro del

Peru y esta clasificada como En Peligro segun la Union Internacional para la Conservacion de la Naturaleza.

El habitat principal de esta especie se encuentra dentro del Parque Nacional Yanachaga-Chemillen, pero el

estado de sus poblaciones es desconocido. La recopilacion de datos cuantitativos de estas poblaciones es

esencial para conservar la especie en el parque. En este estudio, se examino la abundancia, tamano y el uso

de microhabitat de R. yanachaga en un gradiente de elevacion. Se muestreo individuos con longitud de hocico-

cloaca (LHC) 2 20 mm en cuatro transectos distribuidos entre 2,400 y 2,800 msnm, en la estacion humeda

y seca. Mediante monitoreos nocturnos, registramos datos individuales sobre sexo, LHC, microhabitat,

ubicacion geografica, humedad relativa y temperatura. Observamos que la abundancia de hembras y machos

vario entre los cuatro transectos en ambos periodos de muestreo. Registramos mas individuos a mayor altitud

y en la estacion seca, ademas observamos que los individuos distribuidos a mayor elevacion tienden a ser

mas grandes que individuos distribuidos a de elevaciones mas bajas. La mayoria de los individuos parecen

preferir el microhabitat compuesto de hojas y helechos. Ademas, observamos dimorfismo sexual en tamano,

en donde las hembras fueron mas grandes que los machos. Estos hallazgos contribuyen a los programas de

conservacion de anfibios en Peru.

Palabras clave. Anfibio, estado poblacional, bosque de neblina, gradiente de elevacién, especie endémica, habitat,

América del Sur.

Citation: Huaman-Trucios S, Camel V, Orellana Mendoza E, Pyles MV, von May R. 2021. Abundance and microhabitat use of the Endangered toad

Rhinella yanachaga (Anura: Bufonidae) in the cloud forest of Yanachaga-Chemillén National Park, Peru. Amphibian & Reptile Conservation 15(2)

[General Section]: 1-9 (e277).

[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 February 2021; Published: 22 July 2021

Correspondence. *rvonmay@gmail.com (RVM), melanny.ht@gmail.com (SHT), vlad_camel@hotmail.com (VC), eporellana@uncp.edu.pe

(EOM), marcela.pyles@gmail.com (MVP)

Amphib. Reptile Conserv. 1 July 2021 | Volume 15 | Number 2 | e277

Rhinella yanachaga in Peru

Introduction

The cloud forests of Yanachaga-Chemillén National

Park (YCNP), located in the eastern region of the central

Andes of Peru, are considered a hotspot of biodiversity

(Young 2007; Myers et al. 2000). The park is the core

of the larger Oxapampa-Ashaninka-Yanesha Biosphere

Reserve, which aims to maintain cultural and biological

diversity, ecosystem function, and sustainable use of

natural resources in the region (Griesinger 2019). The

YCNP and the buffer zone surrounding the park protect

the habitat of over 40 species of amphibians (Chavez et

al. 2012; Angulo et al. 2016). Most of these species are

known from a small geographic area and are vulnerable

to habitat loss and disease (Aguilar et al. 2010; Chavez

et al. 2012; Jarvis et al. 2015). Conservation of key

areas within the YCNP and its buffer zone is a priority,

because they contain the only known populations of these

endemic amphibians (Lehr and von May 2004; Boano et

al. 2008; Angulo et al. 2019). Obtaining quantitative data

based on field surveys is essential for the monitoring and

protection of the species living in the YCNP.

One of these endemic species is Rhinella yanachaga

Lehr, Pramuk, Hedges, and Cordova, 2007, an arboreal

toad (Bufonidae) distributed from 1,814 to 2,900 m asl

in the cloud forest of YCNP (Lehr et al. 2012). Rhinella

yanachaga is a medium-sized toad with nocturnal habits,

reaching a maximum snout-to-vent length (SVL) of 45.7

mm (Lehr etal. 2007). The species is currently categorized

as Endangered according to the International Union for

Conservation of Nature (IUCN) Red List of Threatened

Species (IUCN 2018), and is currently known from only

two localities—one inside the YCNP and one in the

buffer zone (outside) of the YCNP (Chavez et al. 2012).

75°36'W 75°24'W

Md ri {

Atlantic

Ocean

10°36'S

10°48'S

Pacific

Ocean

75°48'W 75°24'W

Amphib. Reptile Conserv.

Surveys of threatened amphibians such as R. yanachaga

are a priority for the park’s biodiversity monitoring

program, and population status assessments conducted

every 10 years are a priority for global assessments (The

Rules of Procedure for IUCN Red List Assessments

2017-2020; IUCN 2016). Therefore, it is necessary to

have data on the abundance and microhabitat use of this

species.

Here, we present data on the abundance and

microhabitat use of R. yanachaga across an elevational

gradient ina cloud forest in the YCNP. Additionally, given

that seasonality may affect the activity and abundance of

a species, we compared the relative abundance and size of

R. yanachaga between the wet and dry seasons along the

elevational gradient. Whether the number of individuals

and size of R. yanachaga vary across elevation, and

whether seasonality in temperature affects the habitat use

of this species were also assessed. This work provides

data that can be used to further understand the effects of

environmental variables on the distribution of threatened

amphibian populations in the Tropical Andes (Larsen et

al. 2012).

Materials and Methods

Study Area

This study was carried out in the cloud forest sector of

San Alberto within the Yanachaga-Chemillén National

Park, Oxapampa Province, Pasco Department, Peru (Fig.

1). The study area is within the tropical montane forest

ecoregion, locally known as Selva Alta as defined by

Brack (1986). Additionally, the area includes three life

zones as defined by the Holdridge system (ONERN 1976

75°12'W 75°0'W

Legend

Protected Natural Areas

Elevation (m)

ME < 2.500

MO 2,500- 3,500

(7) 3,500 - 4,500

4,500 - 5,500

5,500 - 6,500

75°O'W

75°12'W

Fig. 1. (A) Map of the study area. The white circle indicates the location of the study site (San Alberto) within Yanachaga-Chemillén

National Park, Oxapampa, Pasco; (B) lateral view, (C) ventral view, and (D) dorsal view of Rhinella yanachaga in life. Map by

Vladimir Camel (A), photos by Shirley Huaman-Trucios (B—D).

July 2021 | Volume 15 | Number 2 | e277

Huaman-Trucios et al.

[ONERN = Oficina Nacional de Evaluacion de Recursos

Naturales]). Very Humid Low Montane Tropical Forest,

Low Montane Tropical Rain Forest, and Low Montane

Tropical Humid Forest.

In the study area, in the dry season the level of humidity

is 89.1% + 5.16 and the average temperature 1s 11.7 °C

+1.55, while the wet season has lower humidity levels

(80.3% + 4.57) and a higher average temperature (14.2 °C

+ 1.87).

Data Collection

Four linear transects of 1,550 m x 2 m (length < width)

were established. Each transect was located at one of

the following elevational bands (in m): 2,400—2,500,

2,500-2,600, 2,600—2,700, and 2,700—2,800. Data were

collected using visual encounter surveys at night (1900

to 0000 h) during both the wet season (January—March)

and the dry season (June—July) in 2018. Each transect

was surveyed three times per season. Standard biosafety

protocols were followed to avoid the introduction and

spread of pathogens (Angulo et al. 2006). Protocols

included the disinfection of gloves with 70% ethyl

alcohol after measuring the morphological characteristics

of each individual. Additionally, the field equipment,

including boots, was disinfected in a solution of 4%

sodium hypochlorite (4 mL) diluted in 1 L of water.

Likewise, field instruments, such as the GPS, vernier,

and flashlights, were disinfected with 70% ethyl alcohol.

Three observers participated in each night survey,

and captured the individuals of R. yanachaga observed

in each transect. For each individual of R. yanachaga =

20 mm SVL, the sex, SVL, and elevation were recorded

following the methodology proposed by Lips and Reaser

(1999). The sex of each individual was determined by

examining external characters (Lehr et al. 2007): males

have hypertrophied forearms and females have slim

forearms; the cloaca in males is more protuberant and

ventrally oriented than in females. The following data

were recorded at each capture point: transect location,

coordinates, and microhabitat type (leaves, bromeliads,

ferns, orchids, or moss).

With regards to forest microhabitat categories, the

types considered were arboreal, shrub, and herbaceous

vegetation. The main groups of epiphytes were recorded,

including orchids and bromeliads, as well as ferns and

moss. The orchids evaluated included Epidendrum

sp., and epiphytic bromeliads included Guzmania

jaramilloi, Guzmania melinonis, Aechmea zebrina, and

Tillandsia sp. Ferns included Elaphoglossum sp. and

Campyloneurum sp., and the moss microhabitat included

Sphagnum magellanicum.

Data Analysis

First, the frequency distribution of individuals (males

and females) was visually assessed according to four

Amphib. Reptile Conserv.

altitudinal classes (2,400—2,500, 2,500—2,600, 2,600-

2,700, and 2,700—2,800 m). Subsequently, Generalized

Additive Models (GAM) were used to examine the

relationship between abundance and elevation. The

numbers of male and female individuals found in the

two seasons (dry and wet) were grouped. Subsequently,

Generalized Linear Mixed Models (GLMM) were used to

examine how size varies as a function of four explanatory

variables (microhabitat, elevation, sex, and season)

and three interaction effects (elevation-microhabitat,

microhabitat-sex, and sex-season). Given the possible

lack of independence between the individuals sampled,

the transects and the sampling time were considered as

random factors. The variance homogeneity was verified

by means of residual graphs. Differences in size with

respect to seasons, sex, and microhabitat were accessed

by Tukey’s post hoc tests. A Gamma distribution function

with log link was used to fit the model of size. The effects

and significance of each variable on R. yanachaga size

were accessed from a multi-model inference approach

based on Akaike’s Information Criterion with a

correction for small sample size (AICc) (Burnham and

Anderson 2002). Competing models with delta AICc < 2

were used in conditional model averaging, and averaged

parameter estimates were presented as the final result of

the modeling.

Results

During the study, 226 individuals of R. yanachaga were

recorded, including 103 individuals found in the wet

season and 123 individuals in the dry season. The highest

abundance in the wet season was recorded in the elevation

range of 2,700 to 2,800 m, while the highest abundance

in the dry season was recorded at elevations of 2,600 to

2,700 m (Fig. 2). In both seasons, the lowest abundance

of R. yanachaga was recorded at lower elevations (Fig.

2C). Overall, more males (171) than females (54) were

found during this study (Fig. 2). Additionally, larger

individuals (>32 mm) were less frequent than small

and mid-sized individuals. Most male individuals had

recorded SVL ranging between 24 and 28 mm, whereas

females presented a higher frequency within the range of

28 to 32 mm (Fig. 3).

Individuals of R. yanachaga were found to have

a higher preference for ferns and leaves of shrubs

compared to bromeliads (Table 1). Both females and

males were found to use similar microhabitats, and there

were no significant differences in the abundance between

dry and wet periods (Appendix 2). The abundance

of individuals of both sexes did vary as a function of

elevation. Likewise, the regression analysis showed that

elevation has a positive effect on the size of R. yanachaga

individuals (Table 2), particularly when considering sex

as a determining factor (Table 2). The females tended to

be larger at higher elevations (r? = 0.34, p = 0.01), but

male body size was not correlated with elevation (r? =

July 2021 | Volume 15 | Number 2 | e277

Rhinella yanachaga in Peru

Dry season

A) Mi Female B) i Female

Hi Male @ Male

o 75 55.3% o 75

oO o

s s

3 3

2 2

os os

= £

= =

is) te)

= i

i) @®

2 2

£ £

= =

z z

2,400-2,500 2,500-2,600 2,600-2,700 2,700-2,800

Elevation classes (m asl)

Wet season

—

63.1% @ r2 = 0.40; P= 0.002

Number of individuals

s s

2,400-2,500 2,500-2,600 2600-2700 2,700-2,800 2,400 2,500 2,600 2,700 2,800

Elevation classes (m asl)

Elevation (m asl)

Fig. 2. Number of Rhinella yanachaga individuals per transect, Tl = 2,800-—2,700 m, T2 = 2,700—2,600 m, T3 = 2,600—2,500 m,

and T4 = 2,500-2,400 m, according to the elevation gradient for both sexes, in (A) dry season and (B) wet season. (C) Correlation

between the abundance of Rhinella yanachaga and elevation for both sexes and seasons. The grey band indicates the 95% confidence

limits.

0.003, p = 0.41) (Fig. 4).

Moderate variation in body size of R. yanachaga was

observed between seasons (Fig. 5A—B). Overall, females

(= 31.31 mm + 0.82) tend to be larger than males (=

26.22 mm + 0.50, Fig. 5C). Lastly, average body size of

R. yanachaga varied among microhabitats; individuals

found on bromeliads were larger than those on leaves or

ferns (Fig. 5D).

Discussion

The results support our prediction that relative abundance

and microhabitat use of Rhinella yanachaga vary across

an elevational gradient in the cloud forest of central

Peru. Given that this ecosystem is characterized by high

humidity, provided by fog and rainfall throughout the

year, it supports unique habitats and microhabitats used

by endemic amphibian species (Duellman and Lehr

2009). However, to date, the ecological drivers affecting

the distribution of the genus Rhinella have remained

unclear.

Number of individuals

N oa

wn o

20-24

24-28 28-32 32-36 36-40

Length classes (mm)

Sex HJ Female J male

40-44 44-48

Fig. 3. Numbers of individuals according to sex and length

(SVL) ranges of Rhinella yanachaga in four transects, Tl =

2,800—2,700 m, T2 = 2,700—2,600 m, T3 = 2,600-—2,500 m, and

T4 = 2,500—2,400 m, according to the elevation gradient in the

wet and dry seasons.

Amphib. Reptile Conserv.

The results suggest that relative abundance of R.

yanachaga does not vary across seasons. Several studies

have shown that anurans are more abundant during

the wet season, as higher precipitation favors their

development and reproduction (Arroyo et al. 2003;

Ceron et al. 2020; Linause et al. 2020; Ortega et al.

2011; Narvaes et al. 2009; Zaracho and Lavilla 2015).

For example, in Venezuela, during the high precipitation

season, Hyalinobatrachium duranti showed increased

abundance in a cloud forest (Villa et al. 2019). However,

we found no significant differences between seasons.

This probably reflects the constant presence of mist and

cloudiness, which results in reduced solar radiation,

mesic temperatures, and increased relative humidity

variables that favor amphibian activity throughout the

year (Segev et al. 2012). Similar patterns have been

observed in terrestrial breeding frogs in the genus

Pristimantis (P. miyatai, P. douglasi, and P. merostictus)

in another Andean cloud forest (Arroyo et al. 2003).

45| @ r?=0.34; P=0.01

@ r2= 0.003; P= 0.41 e

Size of R. yanachaga(mm)

2,600 2,650

Elevation (m asl)

2,700 2,750

Sex @Female @ Male

Fig. 4. Correlations between the elevation and size of Rhinella

yanachaga according to sex. The model presents correlation

factors of r?= 0.34; p = 0.01 for females and r? = 0.003; p =

0.41 for males. The colors indicate sex (blue for males and red

for females) and the shaded areas indicate the 95% confidence

limits.

July 2021 | Volume 15 | Number 2 | e277

Huaman-Trucios et al.

Table 1. Microhabitat use by Rhinella yanachaga in the cloud

forest of Yanachaga-Chemillén National Park, Peru.

Number of Numberof Number of

Microhabitat — individuals females males

Leaf (shrub) 110 24 86

Fern 96 22 74

Bromeliad 16 5 11

The different proportions of female and male

individuals across the elevational gradient, particularly

those observed between 2,600 and 2,800 m at both

times of the year, could be related to the availability

of reproductive sites. However, further work (e.g.,

mark-recapture study) is needed to determine whether

R. yanachaga exhibits site fidelity (to reproductive or

retreat sites) at these elevations.

Our results agree with the study of Lehr et al. (2007),

and provide evidence that R. yanachaga exhibits sexual

dimorphism in body size, with females being larger than

males. Sexual dimorphism in body size has phenotypic

importance in the reproductive periods, particularly

because bigger females tend to produce larger eggs or

increased numbers of eggs, and because they may lay eggs

more than once during a reproductive season (Rodrigues

da Silva and Feres 2010). Our data also suggest that the

frequency and size of R. yanachaga individuals increases

at higher elevations. A similar trend has been observed in

terrestrial-breeding frogs in the tropical Andes (von May

et al. 2018; Santa-Cruz et al. 2019). This pattern supports

the prediction of Bergmann’s rule, in which organisms

tend to be larger in colder environments than in warmer

environments (Mayr 1956). The elevation gradient is

one of the most important factors for life that is globally

associated with air temperature, and low temperatures

have an effect on species traits (Korner 2007).

Some plants, such as bromeliads, were found to

support larger individuals of R. yanachaga, on average,

than other plant structures (e.g., leaves or ferns). Climbing

vegetation up to 1.5 m above ground is common in many

anurans (Duellman 1978; Toft and Duellman 1979;

Chavez et al. 2012). Individuals using different plant

structures often remain inactive during the day and

Table 2. Statistical data on the relationship between elevation

and size of Rhinella yanachaga according to GLMM.

Asterisks indicate the level of significance: “*” p < 0.05; “**”

p<0.01; and “***” p< 0.001.

Interaction Estimate Std.error zvalue Pr (> |z|)

(Intercept) 2.652 0.846 3.133 0.001 wee

Sex 0.232 0.745 0.312 0.754

Elevation 0.001 0.0002 2.016 0.043

Elevation = 4991 ~—-0,000009 66.296 ~=-<0,.001.—s*##

Sex

exhibit reproductive activity at night, and this behavior

is similar to that of R. yanachaga with the exception

that male individuals were found on herbaceous or

shrubby vegetation. Additionally, individuals found on

bromeliads were larger than individuals found on other

plants, in both seasons (Table 3, Fig. 5D). Bromeliads

provide a suitable microhabitat for the survival and

breeding of amphibians with predominantly terrestrial

habits (Garcia et al. 2005; Jiménez-Robles et al. 2017).

In summary, to our knowledge, this 1s the first study

reporting the population status and microhabitat use of

R. yanachaga at different elevations in the YCNP. We

found that the relative abundance and body size of this

Species vary across both elevations and seasons. We

confirm that R. yanachaga presents sexual dimorphism

in size, with females larger than males. Our findings

show that the abundance and size of R. yvanachaga

tend to increase at higher elevations. The increased

frequency of both females and males at 2,600—2,800 m

could be attributed to the terrestrial reproduction mode

of R. yanachaga. The abundance of amphibians changes

along the elevation gradient as influenced by the thermal

tolerance of ectothermic species in narrow altitudinal

ranges (Bernal and Lynch 2008; Jiménez-Robles et al.

2017). In addition, we found that R. yanachaga more

frequently uses microhabitats such as leaves and ferns,

but the largest individuals settle in bromeliads. Our data

also indicate that 2,400—2,500 m represents the lower

elevational range limit of R. yanachaga. Finally, given

that R. yanachaga exhibits limited geographic and

elevational distributions, this species could be used in

Table 3. Comparisons of the sizes of individuals of Rhinella yanachaga. Asterisks represent significant differences in the parameters

with the Tukey test after GLMM: “*” p < 0.05; “**” p < 0.01; and “***” p <0.001.

Variable Estimate Std. error t value Pr (> |z|)

Wet season 31.9 2/3 47.86 < 0.001 sa

Females

Dry season 28.8 2.06 -3.405 0.001 sh

Wet season 26 0.585 144.75 < 0.001 cee

Males

Dry season Dhid 0.613 1723 0.084

g Female 31.309 0.824 130.798 < 0.001 ne,

ex.

Male 26.225 0.502 -6.931 < 0.001 nee

Bromeliad 31.319 1.442 74.784 < 0.001 al

Microhabitat Fern 27.145 0.618 -3.013 0.003 ai

Leaf 27.187 0.615 -3.071 0.002 a

Amphib. Reptile Conserv. 5 July 2021 | Volume 15 | Number 2 | e277

Rhinella yanachaga in Peru

ord

Average size (mm)

= = NO NO wo

i=] oa o ol So

Wet season

Dry season

Female sex

C) 35

Average size (mm)

= pas No ho

o oi —] a

Female Male

Sex

Average size (mm)

=—

Average size (mm)

—

NO ow

oi oO

Dry season Wet season

Male sex

i=)

—_

Bromeliad Fern Leaf

Microhabitats

Fig. 5. Comparisons of the sizes of Rhinella yanachaga individuals. (A) Differences in size of females in dry and wet seasons. (B)

Differences in size of males in dry and wet seasons. (C) Differences in size between males and females. (D) Differences in the size

of individuals with respect to microhabitats. The different letters indicate significant differences at p < 0.05 according to the Tukey

test after GLMM. Error bars represent standard errors.

further studies on local adaptation in relation to thermal

physiological limits.

Acknowledgements.—We are grateful to the Servicio

Nacional de Areas Naturales Protegidas (SERNANP)

and the Direction of Yanachaga Chemillén National

Park, especially to Salomé Antezano Angoma and

Rolando Becerra, for providing logistical support and

access to facilities used in this study. We thank park

rangers Elvis Camavilca Rueda, Humberto Cristobal

Espinoza, Alejandro Westreicher Sebastian, and Erick

Medina for providing access to the study area and for

providing support in the field. We thank Dayanne Vilela

Navincopa and Milthon Ninahuanca Chupayo for

providing support during field research and for sharing

their passion for conservation. We also thank Edgar

Lehr, Jifi Moravec, Nelson Rufino de Albuquerque, and

one anonymous reviewer for providing constructive and

helpful comments on the manuscript.

Amphib. Reptile Conserv.

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ecosystems.

environment, and biodiversity.

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biodiversity conservation.

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Shirley Melanny Ross Huaman-Trucios is a Forestry Engineer at the Universidad Nacional del

Centro del Peru and master’s student of Forest Resources Conservation at the Universidad Nacional

Agraria La Molina, Lima, Peru. Currently, Shirley is an official park ranger for the National Service

of Natural Protected Areas, Peru. Her main research interests are biodiversity conservation and

amphibian behavioral ecology in tropical Andes forests.

Vladimir Camel is a Forestry Engineer and is currently pursuing doctoral studies in Biological

Science and Engineering at the Universidad Nacional Agraria La Molina, Lima, Peru. His research

interests include the molecular physiology of plants and conservation of high Andean forest

Edith Orellana Mendoza is a Forestry Engineer and professor in the Area of Biodiversity and

Forest Management at the Faculty of Forestry and Environmental Sciences, Universidad Nacional

del Centro del Peru. Her areas of interest are environmental pollution, the risks of toxics in the

Marcela V. Pyles is a Forestry Engineer who is currently pursuing doctoral studies in Applied

Ecology at the Biology Institute, Sector of Ecology and Conservation, Federal University of Lavras

Rudolf von May is an Assistant Professor in the Biology Program at California State University

Channel Islands, Camarillo, California, USA. His fields of interest include evolutionary ecology and

July 2021 | Volume 15 | Number 2 | e277

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Amphib. Reptile Conserv.

Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

15(2) [Taxonomy Section]: 10—22 (e278).

ptile-cons*

urn:lsid:zoobank.org:pub: D8B4BDF6-C656-460B-83F9-321A8F75E77A

A new lizard of the Liolaemus montanus group that inhabits

the hyperarid desert of southern Peru

‘*Pablo Valladares-Faundez, ?Pablo Franco Leon, *?Cesar Jove Chipana, *Marco Navarro Guzman,

?Javier Ignacio-Apaza, ‘César Caceres Musaja, °Robert Langstroth, **Alvaro Aguilar-Kirigin,

7Roberto C. Gutierrez, and ®°Cristian S. Abdala

'Laboratorio de Zoologia Integrativa, Departamento de Biologia, Facultad de Ciencias, Universidad de Tarapaca, General Velasquez 1775, Arica,

CHILE *Direccion de Investigacion, Universidad Jorge Basadre Grohmann, Avenida Miraflores S/N, Ciudad Universitaria, Tacna, PER U 3Servicio

Nacional Forestal y de Fauna Silvestre, Ministerio de Agricultura y Riego, Tacna, PERU ‘Departamento de Biologia, Facultad de Biologia y

Microbiologia, Universidad Nacional Jorge Basadre Grohmann, Tacna, PERU “Area de Herpetologia, Coleccion Boliviana de Fauna, Campus

Universitario de Cota Cota, Facultad de Ciencias Puras y Naturales, Universidad Mayor de San Andrés, La Paz, Estado Plurinacional de Bolivia,

BOLIVIA °Red de Investigadores en Herpetologia, La Paz, Estado Plurinacional de Bolivia, BOLIVIA ’Museo de Historia Natural, Universidad

Nacional de San Agustin de Arequipa, PERU *Consejo Nacional de Investigacion Cientificas y Técnicas (CONICET) - Unidad ejecutora Lillo

(UEL) - Facultad de Ciencias Naturales e Instituto Miguel Lillo (IML), Universidad Nacional de Tucuman, San Miguel de Tucuman, ARGENTINA

Abstract.—A new lizard of the genus Liolaemus is described from the Tacna region of southern of Peru. This

species belongs to the L. montanus group and was initially thought to be L. poconchilensis and L. insolitus.

However, a series of diagnostic characters differentiate it consistently from these two species and all other

species of the genus. To determine the taxonomic status of these lizards, their phylogenetic relationships were

analyzed, as well as their morphological and ecological characteristics. The results of the analysis support

the conclusion that this population of lizards represents a new species to science, and that the new species

is related to L. nazca and L. chiribaya. The new species has sexual dimorphism and is known from elevations

of ca. 1,000 m above sea level in the hyperarid Pacific deserts, which are populated by scattered Ephedra

americana and Poissonia sp. Due to its highly restricted range and observed habitat loss, we recommend this

species be categorized as Critically Endangered.

Keywords. Tacna, Liolaemidae, reptiles, South America, systematics, taxonomy.

Resumen.—Una nueva especie de lagarto del géenero Liolaemus es descrita para la Region Tacna, sur de Peru.

Esta especie pertenece al grupo L. montanus, la que fue inicialmente confundida con L. poconchilensis y L.

insolitus. Sin embargo, una serie de caracteres diagnosticos la diferencian consistentemente de estas y otras

especies del género. Para determinar su estatus taxonomico, nosotros analizamos sus relaciones filogenéticas,

asi como sus Caracteristicas morfologicas y ecologicas. Nuestros resultados sustentan la conclusion que esta

poblacion es una nueva especie para la Ciencia, e indica que esta nueva especie esta relacionada a L. nazca

and L. chiribaya. La nueva especie presenta dimorfismo sexual, y es conocida en elevaciones cercanas a los

1,000 m sobre el nivel del mar, en el hiperarido desierto del Pacifico con matorral de Ephedra americana y

Poissonia sp. Debido a su distribucion restringida y la pérdida de habitat observada, nosotros proponemos

que sea incluida en la lista de especies amenazadas como En Peligro Critico.

Palabras clave. Tacna, Liolaemidae, lagartos, reptiles, sistematica, taxonomia.

Citation: Valladares-Faundez P, Franco-Leén P, Jove Chipana C, Navarro Guzman M, Ignacio-Apaza J, Apaza JI, Caceres Musaja C, Langstroth R,

Aguilar-Kirigin A, Gutierrez RC, Abdala CS. 2021. A new lizard of the Liolaemus montanus group that inhabits the hyperarid desert of southern Peru.

Amphibian & Reptile Conservation 15(2) [Taxonomy Section]: 10-22 (e278).

[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: 5 November 2020; Published: 12 August 2021

Correspondence. *pvalladares@academicos.uta.cl (PVF), pfrancol@unjbg.edu.pe (PFL), cesarjove@gmail.com (CJC), mnavarro@serfor.

gob.pe (MNG), jmignacionet@gmail.com (JIA), cncaceres@hotmail.com (CCM), pampa_isla@yahoo.de (RL), alvaroaguilarkirigin@gmail.com

(AAK), salamanqueja@gmail.com (RCG), samiryjazmin@gmail.com (CSA)

Amphib. Reptile Conserv. 10 August 2021 | Volume 15 | Number 2 | e278

Valladares-Faundez et al.

Introduction

The richness of reptile species in Peru has been quantified

as 365 species (Carrillo de Espinoza and Icoechea 1995).

However, since that date many new species have been

described for the country (Lehr et al. 2019), particularly

members of the genus Liolaemus (Laurent 1998; Lobo

et al. 2007; Aguilar-Putriano et al. 2013, 2019; Gutiérrez

et al. 2018; Villegas et al. 2020; Chaparro et al. 2020;

Huamani-Valderrama et al. 2020), a group that is very

widespread between central Peru and Tierra del Fuego

of Chile and Argentina. In addition, some Liolaemus

species described from northern Chile have subsequently

been documented for Peru, such as L. poconchilensis

(Langstroth 2011), ZL. chungara, and L. pleopholis

(Valladares et al. 2021).

Lizards from the desert of the Pacific slope of northern

Chile and southern Peru are generally characterized by

the “phrynosaurine” morphotype (Valladares 2004),

and they are recovered in the L. reichei clade in the

phylogeny of Abdala et al. (2020). For example, L.

audituvelatus, L. balagueri, L. chiribaya, L. insolitus, L.

nazca, L. poconchilensis, L. reichei, L. stolzmanni, and

L. torresi present eyelids with a conspicuous comb, eye

diameter greater than length between anterior borders

of eye and rostral, tail shorter than snout-vent length,

head scales poorly differentiated, isognathus jaws, loreal

region depressed and dorsal scales imbricate, smooth,

and with small accompanying scales (1.e., heteronotes).

In Peru, there are known to be four species of the L.

reichei clade: L. balagueri, L. insolitus, L. nazca, and L.

poconchilensis. Males of L. balagueri and L. nazca have

a unique coloration pattern, with ocelli and green scales

on both side of the body, while males of L. chiribaya, L.

poconchilensis, and L. insolitus have blue and orange-

to-red scales, and pronounced sexual dimorphism. They

inhabit sandy or slightly rocky areas, and are associated

with small and restricted vegetation patches. These species

all inhabit coastal desert ecosystems of Chile and Peru with

extreme aridity, very pronounced thermal fluctuations, and

very scant precipitation (Hartley et al. 2005).

During a survey of the biodiversity of arid ecosystems

in southern Peru, a small population of lizards with

particular morphological characteristics was found.

Initially they were thought to be L. poconchiliensis and

L. insolitus, however their large size and color pattern

indicated that this population constitutes a new species

of Liolaemus. In the present paper, these lizards from the

arid coastal desert of southern Peru are described as a

new species, based on a detailed comparison with other

species of the LZ. montanus group and their phylogenetic

relationships, taxonomic position, and conservation

status are then discussed.

Materials and Methods

Phylogenetic analyses. Phylogenetic analyses were

performed using the morphological matrix of Abdala et al.

Amphib. Reptile Conserv.

(2020), which includes 329 characters and 105 terminals

(including Ctenoblepharys adspersa and Phymaturus

palluma as outgroup, and 103 terminals of the Liolaemus

montanus group). Parsimony was used as the optimality

criterion, only selecting the shortest trees or those with

the fewest homoplasies. TNT 1.5 (Tree Analysis Using

New Technology, version 1.5; Goloboff et al. 2003)

was used to generate the phylogenetic hypotheses.

Continuous characters were analyzed following Goloboff

et al. (2006) and were standardized using mkstandb.run.

For this analysis, the value of two was considered as the

highest transformation cost. Heuristic search was used to

find the shortest trees or those with the smallest number

of steps. The matrix was analyzed under equal weight

or under implied weight, and K values from three to 20

were used. One thousand replications were performed

for each search, and 20 trees were saved per replicate.

Symmetric resampling was used to obtain support values

for the results obtained, with 500 replications and using a

deletion probability of 0.33.

Morphology. The morphological characters traditionally

used in Liolaemus taxonomy were examined in this

study, including those of Laurent (1985), Cei (1986,

1993), Etheridge (1993, 1995, 2000), Lobo (2001),

Abdala (2002, 2003, 2007), and Abdala et al. (2019,

2020). The terminology of Smith (1946) was followed

for descriptions of squamation, and that of Frost (1992)

for descriptions of neck-folding. Descriptions of body-

color patterns follow Lobo and Espinoza (1999), Abdala

(2007), and Abdala et al. (2020).

Measurements and scale counts were recorded from

specimens fixed in 10% formalin and preserved in 70%

ethanol. Body and scale measurements were taken with

digital calipers to the nearest 0.02 mm. A binocular

dissecting microscope (10-40X) was used to count and

characterize the scales. Where bilateral, scale count and

measurement data were taken from the right side of the

lizards.

The holotype and paratypes were compared with

other species from the L. montanus group (sensu

Etheridge 1995 and Abdala et al. 2020). Specimens were

measured (Table 1) and compared with other members

of the L. reichei group from adjacent regions (Table 2).

Descriptions of color in life for the new species were

based on observations of freshly collected animals and

photographs taken at the time of capture.

Ecology. The niche study for the new species was

carried out by means of predictive modeling using the

MaxEnt v3.4.1 software, which employs algorithms that

predict the potential distribution of a species in relation

to their environmental conditions (Phillips et al. 2006).

It is considered one of the most efficient programs for

assessing the potential niche of any species (Elith et

al. 2006). The coordinates of the collected individuals

were used along with nine other environmental variables

(Table 3). The AUC statistic was used to validate the

August 2021 | Volume 15 | Number 2 | e278

A new Liolaemus species from Peru

Table 1. Morphological measurements (in mm) of four specimens of Liolaemus basadrei sp. nov. Specimen HP20CBT corresponds

to the proposed holotype.

HP20CBT

Sex Male

Body length 90.6

Tail length 68

Head length 20.4

Head width 18.2

Forelimb length 28.4

Hindlimb length 43.2

Supralabials 10

Infralabials 6

Lorilabials 13

Scales around midbody 79

Scales of the body length 92

Precloacal pores 6

ecological niche model, where values of 0.5—0.7 indicate

low confidence, values of 0.7-0.9 demonstrate a useful

application in the model, and values greater than 0.9

suggest high confidence (Lobo et al. 2007). Likewise,

the Jackknife test was applied, which allows assessment

of the contribution of each variable individually

(Shcheglovitova and Anderson 2013).

Conservation status. The conservation status of

the species has been defined based on the variables

considered in the Conservation Priority Index (CPI)

of Cofré and Marquet (1999) and those of the JUCN

Red List of Threatened Species. Some of the key

HP21CBT HP22CBT HP23CBT

Male Female Female

88.2 63.6 78.7

78.1 53.6 45.1

21 14 15.8

16 10.9 13:9

31 Zoe, 26.6

42 35.7 40.8

8 9 9

7 6 ah

13 1] 13

82 79 74

89 88 86

3 0 0)

variables considered in the CPI were: (a) number of

different ecoregions where the species is found, taken

as indicative of the degree of habitat specialization; (b)

area of geographic distribution of the species (km/”);

endemism, based on the number of countries where the

species 1s present; (e) taxonomic singularity, based on the

degree of monotypy at the levels of genus and family;

(f) body mass; (g) effect of human activities; and (h)

degree of protection, based on the percentage of area of

the ecoregion inhabited by the species which lies within a

protected area (such as national parks, national reserves,

and natural monuments).

Table 2. Morphological measurements (in mm) of six Liolaemus species. The sequence of numbers corresponds to minimum, average (in

parentheses), and maximum values found in the body measurements.

Body length

Tail length

Head length

Head width

Forelimb length

Hindlimb length

Supralabials

Infralabials

Lorilabials

Scales around

midbody

Scales of the body

length

Precloacal pores

L. basadrei sp. nov.

ae)

63.6 (80.3) 90.6

45.1 (61.2) 78.1

14 (17.8) 21

10.9 (14.8) 18.2

23.2 (27.3) 31

35.7 (40.4) 43.2

8 (9) 10

6 (6.5)7

11 (12.5) 13

74 (78.5) 82

86 (88.8) 92

0 (2.3) 6

Amphib. Reptile Conserv.

L. insolitus

67.7

61.9

16.2

14.6

31.4

44.1

L. poconchilensis

(n=4)

47.17 (51.7) 53.83

42.66 (47.2) 53.65

11.34 (13.1) 14.16

9.51 (10.9) 11.53

22.2 (24.8) 27.5

31.15 (34.1) 32.62

L. chiribaya

(n=9)

49.6 (53.3) 68.8

13 (14.8) 16.3

11.4 (12.8) 11.4

20.4 (23.4) 25.8 26.3 (28.8) 30.5

30.9 (33.4) 34.8 38.6 (40.1) 42.2

7 (8.6) 10

55 (61.7) 66

52 (57.4) 61

2 (3.7)5

L. torresi

(n=8)

53.8 (58.1) 64

58.8 (57.4) 74

13 (13.6) 14.5

10.3 (11.02)

11.7

L. reichei

(n= 3)

41.5 (47.7) 50.8

35.7 (39.5) 43.1

10 (10.9) 11.5

8.3 (8.5) 9.7

21.4 (22.6) 24.4

30.1 (31.7) 33.4

9(9)9

6 (6.7) 8

8 (8.7) 9

43 (45) 47

50 (51.7) 54

August 2021 | Volume 15 | Number 2 | e278

Valladares-Faundez et al.

Table 3. Environmental variables and their contributions to the

model of Liolaemus basadrei sp. nov. distribution, obtained

using the MaxEnt algorithm.

Variables Contribution to the

model (%)

Precipitation 0.6

Average temperature 25

Climatic classification 48

Physiography 46.3

Slope 0.3

Geomorphology 0.4

Humidity 0)

Soil type 0.8

Life zone 21

Images and maps. Photographs were taken of live

specimens using a Canon EOS Rebel T71 digital camera.

The distribution map was elaborated in QGIS free

software, using the coordinates from the authors’ own

records, which were taken with a GPS device (datum

WGS84), Garmin inReach Explorer.

Results

Phylogeneticanalyses. The morphological phylogenetic

analysis indicated that the new species belongs to the

Liolaemus reichei clade of the L. montanus group,

nested within a monophyletic subgroup that includes L.

audituvealtus, L. balagueri, L. chiribaya, L. insolitus,

L. nazca, L. poconchilensis, L. reichei, and L. torresi

(Fig. 1).

Twenty trees were saved by each replicate. All resulting

phylogenetic trees showed the same clades as observed

in Fig. 1, and are supported by 25 synapomorphies, six

continuous characters, and 21 discrete characters. All

analyzes showed the new species as sister to the clade (L.

nazca + L. chiribaya), and this clade is supported by 24

all continuous synapomorphies. This clade is at the same

time a basal branching (according to Krell and Cranston

2004) of two large clades, one formed by species that

inhabit Chile and the other by those that inhabit Peru

(except for L. balagueri, which is sister species to the

entire clade). These results were obtained in all trees with

values of k = 3-20. Phylogenetic evidence indicates that

the new species has no direct relationship with L. insolitus.

The new species has a total of 26 autapomorphies, of

which 13 are continuous and 13 are discrete.

Taxonomy

Liolaemus basadrei sp. nov.

(Fig. 2A—D)

urn:lsid:zoobank.org:act:08DE BE00-8856-445A-BBD5-CD2A8D3EC45B

Amphib. Reptile Conserv.

Holotype. HP20CBT, an adult male (Fig. 2A—B) from

the east slope of an unnamed hill east of Locumba

Valley, 17°44°38’S, 70°45’41”W; 897 m, Jorge Basadre

Province, Tacna Region, Peru; collected on 25 January

2019, Pablo Franco, Pablo Valladares-Faundez, Cesar

Chipana, Marco Navarro and Javier Ignacio collectors.

Allotype. HP21CBT, an adult female (Fig. 2C-—D),

from the east slope of an unnamed hill east of Locumba

Valley, 17°45’21”S, 70°45’51”W; 761 m, Jorge Basadre

Province, Tacna Region, Peru; collected on 25 January

2019, same collectors.

Paratypes. Two adults: HP22CBT and HP23CBT,

from the east slope of an unnamed hill east of Locumba

Valley, one male and one female. From the high voltage

tower to the Pan-American highway, on a steep slope

(17°44’50”S, 70°46’06”W); 970 m, same collectors.

Diagnosis. Liolaemus basadrei sp. nov. belongs to the

L. montanus group (sensu Etheridge 1995; Abdala et

al. 2020). This species differs from the species of the L.

boulengeri group of the L. montanus group series by the

absence of a patch of enlarged scales on the posterior

thigh of the hind limb in the new species (Etheridge

1995; Abdala 2007). In relation to the L. montanus

group, L. basadrei sp. nov. differs from L. andinus, L.

annectens, L. cazianae, L. chlorostictus, L. dorbignyi,

L. duellmani, L. eleodori, L. erguetae, L. erroneus, L.

etheridgei, L. evaristoi, L. fabiani, L. famatinae, L.

fittkaui, L. forsteri, L. foxi, L. gracielae, L. griseus, L.

hajeki, L. halonastes, L. huacahuasicus, L. huayra, L.

inti, L. islugensis, L. jamesi, L. juanortizi, L. lenzi, L.

melanogaster, L. montanus, L. molinai, L. multicolor, L.

nigriceps, L. orko, L. ortizi, L. pachecoi, L. pantherinus,

L. patriciaiturrae, L. pleopholis, L. poecilochromus, L.

polystictus, L. pulcherrimus, L. puritamensis, L. galaywa,

L. robertoi, L. robustus, L. rosenmanni, L. ruibali, L.

schmidti, L. scrocchii, L. signifer, L. tajzara, L. thomasi,

L. vallecurensis, L. victormoralesii, L. vulcanus, and L.

williamsi by possessing isognathus jaws and tail shorter

than Snout- Vent Length (SVL). Of the remaining species,

L. basadrei sp. nov. are robust lizards (SVL = 88.2 mm)

differing from L. andinus, L. anqapuka, L. audituvelatus,

L. balagueri, L. cazianiae, L. chiribaya, L. duellmani,

L. eleodori, L. erguetae, L. erroneus, L. etheridgei, L.

evaristoi, L. fabiani, L. famatinae, L. fittkaui, L. foxi,

L. gracielae, L. griseus, L. hajeki, L. halonastes, L.

huacahuasicus, L. islugensis, L. molinai, L. montanus,

L. multicolor, L. nazca, L. orko, L. omorfi, L. ortizi, L.

pantherinus, L. poconchilensis, L. poecilochromus,

L. porosus, L. pulcherrimus, L. reichei, L. robertoi, L.

rosenmanni, L. ruibali, L. smidthi, L. stolzmanni, L.

tajzara, L. thomasi, L. torresi, L. vallecurensis, and L.

williamnsi which are smaller (SVL between 50-80

mm). The dorsal scales on the body are smooth and

subimbricate in Liolaemus basadrei sp. nov., differing

August 2021 | Volume 15 | Number 2 | e278

A new Liolaemus species from Peru

Liolaemus chlorostictus clade

Liolaemus

montanus

group

Liolaemus foxi clade

Liolaemus andinus clade

Liolaemus multicolor clade

Liolaemus poecilochromus clade

Liolaemus ortizi clade

Liolaemus huacahuasicus clade

Liolaemus robustus clade

Liolaemus forsteri clade

Liolaemus arnectens clade

Liolaemus jamesi clade

—— Liolaemus dorbignyi clade

L.poconchiliensis

L.reichei

L.audituvelatus

L.torresi

L.torresiRioLoa

L.afftorresil

L.balagueri

L.basadrei sp. nov.

L.nazca

L.chiribaya

L.affinsolitus6

L.affinsolitusS

—— L.affinsolitus7

61 L.affinsolitus4

L.affinsolitus2

L.affinsolitus3

L.affpoconchiliensis

L.insolitus

Liolaemus reichei clade

Fig 1. Phylogenetic tree obtained for the new species.

from species that have dorsal scales with an evident keel:

L. aymararum, L. etheridgei, L. famatinae, L. fittkaui,

L. griseus, L. huacahuaicus, L. montanus, L. orko, L.

oritizi, L. polystictus, L. pulcherrimus, L. galaywa, L.

signifer, L. tajzara, L. thomasi, L. victormoralesi, and L.

williamsi. Liolaemus insolitus is the most similar among

these lizards to the new species, but it differs principally

by the number of scales along the dorso-thoracic region

(scales between occiput and anterior border of thigh, 63

in L. insolitus versus 86—89 in the new species), number

of ventral scales (70-78 in L. insolitus versus 79-85 in

the new species), and the dorsal pattern in L. insolitus has

fewer dark red scales and more sky-blue scales.

Phylogenetic results indicate that L. basadrei belongs

to the clade of L. reichei (Abdala et al. 2020). L. basadrei

sp. nov. differs from L. angapuka, L. audituvelatus,

L. balagueri, L. chiribaya, L. insolitus, L. nazca, L.

poconchilensis, L. reichei, L. stolzmanni, and L. torresi

because the latter have a smaller size (< 70 mm SVL)

and the new species is over 88 mm. Liolaemus basadrei

sp. nov. also differs from L. balagueri, L. chiribaya, L.

insolitus, L. nazca, L. poconchilensis, L. reichei, and L.

torresi by having a greater number of scales around the

body (74-82 vs. < 72) and a greater number of dorsal

Amphib. Reptile Conserv.

scales on the body (84—92 vs. < 80). The number of ventral

scales is greater than in L. balagueri, L. chiribaya, L.

insolitus and L. nazca (79-85 vs. < 79). The presence of

blue scales on the body also differentiates it from species

that do not have them: L. audituvelatus, L. balagueri, L.

nazca, L. reichei, and L. torresi.

Description of the holotype. Medium-sized lizard,

robust body, limbs short and robust, head triangular and

short, distinct from neck, widest across temporal region,

0.89 times wider (as measured across widest part of

temporal region) than long (as measured from inferior

apex of external auditory meatus to anterior surface of

rostral). Snout short (as measured from tip of snout to

anterior corner or orbit), 0.26 times head length, orbit

(as measured along its greatest horizontal length) short,

0.17 times head length. Nasal region slightly swollen,

convex in profile, rostral narrow, 2.8 times wider than

high, bordered by three postrostrals, semirectangular

and pentagonal, external ones of greater size. Rostral

scale in contact with a lorilabial and a supralabial scale

on each side. Four hexagonal, irregular, and elongated

internasals, external pair meeting nasals. Five medium

and irregular scales between postrostral and internasal.

August 2021 | Volume 15 | Number 2 | e278

Valladares-Faundez et al.

Fig. 2. Dorsal (A) and ventral (B) views of holotype specimen collected in Valle de Locumba, Jorge Basadre Province, Region

Tacna, Peru. Dorsal (C) and ventral (D) views of allotype specimen collected in Valle de Locumba, Jorge Basadre Province, Region

Tacna, Peru.

Nasal scales larger, in contact with one postrostral, one

lorilabial, one internasal, and two irregular postnasals,

and a medium scale between internasal and postrostral.

Nasal is separated from rostral and anterior supralabials

by anterior lorilabials. Posterior nasal rounded and

its anterior part is angled. Nostril oriented postero-

laterally. Dorsal head scales larger, differentiated,

convex; frontonasal region convex in profile. Twenty-

one irregular scales in frontonasal region, five irregular,

convex and smooth prefrontals. Frontals and postfrontals

fragmented and irregular. Two postfrontals meet to

interparietal, which is slightly smaller than adjacent

parietals, irregular, bordered by eight scales, with a

distinct “eye” that corresponds to pineal organ (Fig. 3A).

Elongated, convex and irregular parietals, posterior to

interparietal. Supratemporal region smooth, irregular,

and convex. Temporals larger, convex, juxtaposed, 11

between postocular and anterior margin of ear, 0.43 times

head length. External auditory meatus large, rounded, 2

times higher than wide, bordered by irregular scales,

smaller anteriorly, one largest on the upper side and

not differentiated from posterior temporals, with small

interstitial granules. Orbitals 0.17 times head length.

Supraocular regions large, scales medium size, eight on

each side, 4—5 in a horizontal line across widest part of

supraocular region between superciliaries and frontals.

Fifteen scales form an irregular circum-orbital semicircle.

Seven superciliaries larger, not keeled, four anterior, two

posterior, and one interciliar. Palpebrals small, smooth,

convex and juxtaposed, 11 inner rectangular ciliaries,

outer ciliaries of lower lid 12, outer ciliaries of upper lid

11, third ciliary and three posterior ciliaries triangular, but

not as projecting as those of lower lid, those in middle of

lid more nearly rectangular, not projecting. One preocular

wider than subocular, pentagonal, preceded anteriorly

Amphib. Reptile Conserv.

by a large canthal. Subocular elongated, about 8 times

longer than high and postocular elongate but shorter

than preocular and subocular. Eleven lorilabials, a row

of small scales between the subocular and lorilabials

that start from the loreal scales. Anterior lorilabials

rectangular, posteriors irregular and convex. Six irregular

loreals. Ten supralabials, equal in size to lorilabials. No

supralabials in contact with subocular, and one lorilabial

in contact with subocular (Fig. 3B). Mental large, 1.1

times as wide as rostral, bordered by two infralabials and

two postmentals, not in contact with anterior sublabials.

Four postmentals on each side, infralabials six, gulars

medium size, smooth, semitriangular, convex, imbricate

(Fig. 3C). Ventral scales triangular, similar in size to

dorsal scales, imbricate and smooth. Pectoral scales

imbricate and triangular, on the sides are quadrangular.

Posterior abdominal scales semirectangular. Scales of

precloacal region imbricated and rounded, but wider than

long. Six orange precloacal pores. Dorsal scales of neck

small, smoothly overlapping, slightly concave, smooth

and triangular, with interstitial granules. Dorsal scales

of body larger, rounded or semicircular, smooth and

subimbricate, similar to the lateral scales. Scales around

midbody 79. Middorsal scales from occiput to point even

with anterior margin of thigh 92. Lumbar scales wider

than long, similar in size but less imbricated than dorsal

scales and with interstitial granules. On the sides of the

body, scales are quadrangular.

Lateral nuchal skin folds well-developed and

complex. Two short folds, one originating at superior and

other at inferior margin of auditory meatus, converging

posteriorly to forma V-shaped fold, continuing posteriorly

as longitudinal neck fold, intercepted by oblique neck

fold and antehumeral fold, which reaches half of body.

A fold born in the armpit, projects to the groin. Scales

August 2021 | Volume 15 | Number 2 | e278

A new Liolaemus species from Peru

Fig. 3. Dorsal (A), ventral (B), and lateral (C) views of the head

of holotype HP20CBT.

of lateral neck flat or slightly concave, nonoverlapping.

Below the fold, triangular scales are slightly imbricate,

similar in size to the dorsal neck. Limbs robust and

short. Adpressed hindlimbs reach only middle of body.

Forelimbs 0.32 times SVL and hindlimbs 0.52 times

SVL. Scales of the base of the arm similar to those of the

neck. Brachial scales smooth, triangular and imbricate,

larger in size than dorsal body scales. Antebrachials

tend to be semirectangular and smooth. Elbow scales

semitriangular, and wider than long. Preantebrachials

Amphib. Reptile Conserv.

flat, smaller, rounded, and juxtaposed, with interstitial

granules. Suprafemorals and _ postfemorals larger

and triangular, smooth and imbricate. Prefemorals

small, smooth, convex, juxtaposed. Supratibials and

pretibials longer than wide, imbricate, with interstitial

granules. Infratibials smooth, larger, triangular, and

imbricated. Supratarsals large, smooth, triangular, and

imbricate. Subdigital lamellae of fourth toe 25, with

distal margin slightly tridentate, claws long and slender.

Supracarpals large, smooth, imbricate, wide than longer.

Infracarpals imbricate, somewhat projecting, mucronate,

supradigitals imbricate, keeled and triangular, subdigital

lamellae of fourth finger 19, with distal margin slightly

tridentate, claws long and slender. Tail short and robust,

slightly thickened at the base and somewhat depressed.

The rest is thick and rounded distally. Tail 0.75 times

body length. Dorsal and lateral caudal scales tend to

be irregular, rectangular, with interstitial granules and

imbricate; wider than long, rugose and slightly imbricate

on middle third of tail. Ventral caudal scales triangular on

middle third of tail, but then are rectangular and strongly

imbricate, longer than wider. Autotomic region with 12

scales on dorsal and lateral tail, and eight ventral scales.

Coloration. The holotype has a dark red head and dorsal

body color. Each side of the temporal region and body has

sky blue scales that reach laterally to the tail. Ventrally

there is a heavily variegated coloration, more intense on

the lateral side and throat, ventral side color yellow with

sandy brown spots, a pattern repeated on fore and hind

limbs, and until the end of tail. Dorsal tail dark orange.

Throat predominantly yellow, with sky blue scales and

some red scales.

Variation in morphological measurements and scaling.

Variations based on four specimens, two males and two

females, collected from the same site as the holotype, are

presented in Table 1. The females present a sandy brown

colored head, similar to the sand on which they live. On

the dorsal neck are two medium black spots which are

in parallel along to the dorsal body, where they become

larger and reach to the first part of the tail. Scapular area

shows a short black spot subsequently followed by a

white spot, a pattern which is along the dorso-thoracic

region. Ventrally there is a slightly variegated pattern,

more intense on the throat, ventral side color white with

light gray spots, a pattern repeated on fore and hind limbs,

and until the end of the tail. Female has dorsal scales well

defined, not fragmented, circumorbital semicircles well-

defined, large, and unfragmented subocular, parietals

large, pentagonal, and well-defined. Differences are

mainly in the form of interparietal, which in both females

is hexagonal, while in the males it is irregular. Variation

in the number and form of the scales: temporals eight

between postocular and anterior margin of ear, 13

lorilabials, without a row of small scales between the

subocular and lorilabials, eight supralabials, middorsal

August 2021 | Volume 15 | Number 2 | e278

Valladares-Faundez et al.

70°55'0"W

17°30'0"S

MOQUEGUA

17°40'0"S 17°35'0"S,

17°45'0"S,

PACIFIC

OCEAN

17°50'0"S

17°S5'0"S.

PACIFIC

OCEAN

18°0'0"S

70°55'0"W

Hill fe Sampling (GQ Ecological niche

70°50'0"W 70°45'0"W 70°40'0"W 70°35'0"W 70°30'O"W 70°25'0"W 70°20'0"W

17°30'0"S

17°350"S

JORGE BASADRE

PROVINCE

17°450"S 17°40'0"S

17°50'0"S

TACNA

PROVINCE

17°55'0"S

18°0'0"S

70°50'O"W 7O°45'0"W 7o°40'0"W 70°35'0"W 70°30'0"W 7O°25'0"W 70°20'0"W

Legend

Main roads GZ, Agricultural valleys (~} Provinces

Fig. 4. Current (star) and potential (in gray) distributions of Liolaemus basadrei in the Jorge Basadre Province, Tacna, Peru,

obtained from the MAxEnt algorithms.

scales from occiput to point even with anterior margin

of thigh 88. Elbow scales semitriangular and wider than

long, but lightly keeled. The tail has a spotted pattern.

Forelimb with small dark spots, and hindlimbs variegated

with black and dark brown spots.

The dorsal area of the female is light brown or

pinkish, and the head has dark brown and gray spots with

an irregular shape and order. Lateral area of the head

with dark brown spots that cross the muzzle transversely.

Back of neck and body of the same color as the head,

with large brown spots, arranged two on each side,

bordered by a row of small white scales, a pattern that

is repeated throughout the entire body. Paravertebral

region with small brown spots, while in the lumbar area

a greater number of white scales are observed. Along the

tail, the dorsal pattern is lost and dark brown spots are

observed in an irregular manner and shape, both dorsally

and laterally. Forelimb and hindlimb with light brown

spots irregular in shape and arrangement. Lateral area of

the neck and body white, accompanied by irregular dark

spots. Gular area with gray bands directed towards the

mid-ventral area. Chest with small and very faint gray

spots, white or slightly pink belly, ventral area of the

fore and hind limbs without spots. Ventral area of the tail

white or slightly pink.

Ecology. The knowledge of this species is very poor.

Amphib. Reptile Conserv.

Apparently, its distribution is restricted to the Ephedra

americana and Poissonia sp. desert scrub formation of the

northern Tacna Region, collected in the Locumba valley,

64.5 km north of Tacna (17°45’21”S; 70°45°51”W)

(Fig. 4). Their activity was noted in the morning and

afternoon, and this species thermoregulates at midday by

seeking shade under rocks, cacti, or bushes. Reproductive

phenology, as well as diet and distribution, are unknown.

The new species shares its habitat with a species of

Microlophus, currently under description, of similar

size and mass, and the two species have been observed

utilizing the same cacti as refugia (Fig. 4). While there

are other localities in southern Peru where Liolaemus

and Microlophus can be observed in close proximity,

elsewhere the Microlophus is of larger size and mass

than the Liolaemus. The new species is the largest and

most robust known species of the L. reichei clade and

also the only one known to be associated with cacti. It

is possible that the large size of the new species reflects

its evolution in a resource-rich environment relative to

the other species that are typically found in absolute

desert areas with extremely sparse vegetation. The cacti

likely provide food, water, refuge, and a reduced cost of

thermoregulation. Examination of hawk and owl pellets

from the Locumba Valley has yielded evidence that both

species of lizards are important elements of the local

trophic web (Valladares et al. 2021).

August 2021 | Volume 15 | Number 2 | e278

A new Liolaemus species from Peru

a ae |S ie a! oa Rie

The ecological niche modeling yielded an AUC of 0.988,

indicating a high level of statistical confidence. The most

informative variables for the current ecological niche

of L. basadrei sp. nov. were physiography, the annual

average temperature, and the type of life zone, followed

by the type of climate, precipitation, and slope (Table

3). The remainder of the variables had little intervention

in the model according to the Jackknife test. The area

of the ecological niche of L. basadrei sp. nov. is only

79.76 km?, with distribution exclusively in the Jorge

Basadre and Tacna provinces, specifically in the districts

of Locumba and Inclan, respectively, with a predicted

altitudinal range of 650 to 1,125 m asl (Fig. 4).

Conservation status. According to the CPI variables

considered by Cofré and Marquet (1999), Liolaemus

basadrei sp. nov. 1s a species that inhabits only a

single ecoregion (absolute desert), with an extreme

specialization: known range does not exceed 100 km7,

with an abundance of 7 individuals/km; inhabits only

southern Peru; presents a low taxonomic singularity

(Liolaemus have around 300 species); this species 1s

large, considering both the generic and specific level of

the L. reichei clade (see Table 2); and it has anthropogenic

pressure, because it lives near an interstate highway and

agricultural areas, its habitat area includes high voltage

towers, and its distribution is not within any protected

Amphib. Reptile Conserv.

Fig. 5. Terra typica of Liolaemus basadrei. Valle de Locumba, 897 m, Jorge Basadre Province, Region Tacna, Peru.

aes * igs a =

= <A, See ae

wild areas. All the variables analyzed here indicate that

L. basadrei is a species that should be considered as

Endangered based on the CPI approach. Regarding the

IUCN Red List criteria for evaluating whether a taxon

belongs in a “threatened” category (IUCN 2012, 2019),

we estimate the area of occupancy of L. basadrei to be

less than 10 km?in a single location with ongoing threats

to the extent and quality of its habitat, and we estimate its

population size to be fewer than 250 mature individuals.

Thus, we recommend the category of Critically

Endangered B2ab(ii1); C2a(ii). We have sampled

localities broadly throughout southern Peru and northern

Chile for more than 20 years, and we are confident that

L. basadrei is restricted to an extremely small geographic

area. Over the course of a year, we visited each of the

areas identified as potentially suitable habitat in Fig. 4

and found the species only in the area which includes

the type locality. As summarized in Table 4, all species

of the L. reichei clade assessed to date by the IUCN

are categorized as either Endangered (four species) or

Vulnerable (one species), while five species of the clade

remain to be assessed.

Etymology. We dedicate this species to Jorge Basadre

Grohmann (1903-1980), a distinguished Peruvian

historian and native of Tacna who wrote important works

on the culture and history of Peru. Currently the National

August 2021 | Volume 15 | Number 2 | e278

Valladares-Faundez et al.

Table 4. IUCN conservation status of the species of the L. reichei clade (Abdala et al. 2020).

Species IUCN category IUCN criteria Reference

L. poconchilensis Endangered Blab(iil) Ruiz de Gamboa et al. 2017

L. reichei* Endangered Blab(iii,v) Ruiz de Gamboa and Valladares 2017

L. stolzmanni** Not Evaluated — —

L. audituvelatus Vulnerable Blab(iii); D2 Nufiez et al. 2017

L. torresi Endangered Blab(iii,v) Espejo et al. 2017

L. insolitus Endangered Blab(iii,1v) Aguilar et al. 2017

L balagueri Not Evaluated - -

L. nazca Not Evaluated — =

L. chiribaya Not Evaluated — =

L. anqapuka Endangered*** B HRCA iv) Huamani-Valderrama et al. 2020

L. basadrei sp. nov. Endangered*** B2ab(iil); C2a(il) This work

*The 2017 assessment of L. stolzmanni 1s now applicable to L. reichei, a species which was subsequently resurrected by Valladares

et al. (2018).

**The type locality of L. stolzmanni was restricted to the “transect between Antofagasta and Meyjillones, Chile” by Troncoso-

Palacios and Escobar-Gimpel (2020), who limited its known range to only as far north as Hornitos, approximately 23 NE

of Mejillones.

*** Recommended by the authors of the species.

University of Tacna bears his name, as does one of the

regional provinces of southern Peru.

Discussion

The description of this new species of lizard indicates

that the taxonomy of Liolaemus is still poorly known in

southern Peru, and it is highly probable that additional

species will continue to be discovered (Aguilar-Putriano

et al. 2019; Abdala et al. 2020). Indeed, while Gutiérrez

et al. (2018) indicated that there are a total of 15 species

of the Liolaemus montanus group in Peru, Aguilar-

Putriano (2016, 2019) described five new species of

this group and Valladares et al. (2021) incorporate L.

pleopholis as an element of the Peruvian fauna. Just

recently, Villegas et al. (2020), Chaparro et al. (2020),

and Huamani-Valderrama et al. (2020) described L.

balagueri, L. galaywa, and L. anqapuka, respectively, so

with the addition of L. basadrei sp. nov., the number of

the L. montanus group species in Peru has now reached

The Liolaemus lizards inhabiting the desert and

sandy areas of the lower Pacific slope of northern Chile

and southern Peru are: L. audituvelatus, L. balagueri,

L. chiribaya, L. etheridgei, L. insolitus, L. nazca, L.

reichei, L. poconchilensis, L. stolzmanni, and L. torresi,

some of which have the “phrynosaurian” morphotypes,

and they are distributed from the Atacama (Chile) to

the Arequipa-Ica regions (Peru), and from sea level to

over 3,500 m. Most of these species have scales of very

striking colors, such as sky-blue, red, and yellow, with a

strong sexual dimorphism. Although L. basadrei sp. nov.

Amphib. Reptile Conserv.

inhabits a lowland desert zone and presents characters

of this morphotype, it is larger in size and more robust.

In general, this group of species does not present major

taxonomic controversies and their nomenclatures have

remained stable, perhaps with the exception of L. reichei

and L. stolzmanni (Langstroth 2011; Valladares-Faundez

et al. 2018; Troncoso-Palacios and Escobar-Gimpel

2020). However, Aguilar-Puntriano et al. (2018) found

the phrynosaurian Liolaemus to be paraphyletic within

the L. montanus group when analyzed using only

molecular data.

Regarding the phylogenetic position of the new

species, two clades were recovered within the L. reichei

clade, one composed mainly of lizards that inhabit the

Chilean desert, such as L. poconchilensis, L. reichei, L.

audituvelatus, and L. torresi, and another composed of

lizards living in the Peruvian desert, such as L. balagueri,

L. nazca, L. chiribaya, L. insolitus, and L. basadrei.

Recently L. angapuka (Huamani- Valderrama et al. 2020)

was described as a new species with molecular data. It is

noteworthy that both cladograms, based on molecular or

morphological data, coincide with the two subgroups of

the L. reichei clade, with the same species composition.

From the evolutionary perspective, these species

demonstrate adaptations to the extreme conditions of the

desert; however, the biology and ecology of these lizards

remain unstudied beyond the limited observations made

at the time of collection. While we continue to improve

our taxonomic knowledge, we still lack much of the

important information needed for the conservation of

these species, such as genetic diversity, reproductive

biology, and factors that determine their distribution and

August 2021 | Volume 15 | Number 2 | e278

A new Liolaemus species from Peru

abundance in spatial and temporal perspectives.

Acknowledgements——We thank the Universidad

Nacional Jorge Basadre Grohmann of Tacna, Peru, for

the financing of our research with mining royalty funds.

We also thank the University of Tarapaca, through the

projects FFUTA1799 and UTA Mayor de Investigacion

Cientifica 4723-19. Finally, we thank SERFOR for

issuing the collection permits (AUT-IFS-2019-024) for

scientific research purposes.

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A new Liolaemus species from Peru

Pablo Valladares-Fatindez is a biologist who graduated from the Austral University of Chile, and obtained a Ph.D.

from the University of Chile. Pablo is currently an academic in the Department of Biology, Science Faculty, University

of Tarapaca, in northern Chile. He is interested in the study of vertebrates from arid and high Andean ecosystems,

particularly lizards of the genera Liolaemus and Microlophus, and is developing studies on their taxonomy, systematics,

ecology, and conservation. Pablo is also developing a herpetological collection of northern Chile.

Pablo J. Franco is a Peruvian biologist, a registered researcher at the National Science and Technology Council

(CONCYTEC), and a faculty member at Jorge Basadre Grohmann National University (UNJBG) in Tacna, southern

Peru. He received his degree in Biology at San Agustin National University (UNSA) and holds a Ph.D. Degree in

Environmental Sciences from Santa Maria Catholic University (UCSM), both in Arequipa, Peru. He has authored

or co-authored several peer-reviewed articles on high Andean ecosystems. Pablo currently serves as director of the

General Research Institute of the Jorge Basadre Grohmann National University in Tacna, Peru. He has developed

several research projects on the ecology and biodiversity of high Andean and desert ecosystems in southern Peru.

Cesar A. Jove is a Peruvian biologist who graduated from Jorge Basadre Grohmann National University (UNJBG) in

Tacna, Peru. With experience in managing research and environmental projects, he has participated in research projects

on the flora and fauna associated with high Andean forests and wetlands. He currently works as a research assistant at

the National University of Moquegua (UNAM) in Peru.

_ Marco Alberto Navarro Guzman is a Peruvian biologist who graduated from the Jorge Basadre Grohmann National

; University of Tacna, Peru, as a specialist in biodiversity and conservation. He is interested in the study of arid and high

, Andean ecosystems, particularly in the modeling of ecological niches and habitats of wild flora and fauna species,

| in order to improve their conservation strategies. Marco also works in conservation management in the Regional

Management of Natural Resources and Environmental Management of the Regional Government of Tacna, Peru.

Javier Ignacio-Apaza is a Peruvian who obtained a Bachelor’s Degree from the Jorge Basadre Grohmann National

University, Tacna, Peru. Javier has supported various efforts in the field in evaluations of flora and fauna in the regions

of Tacna and Moquegua, Peru.

Cesar N. Caceres M. is a biologist who graduated from the Jorge Basadre Grohmann National University, with a

Master’s Degree in Tropical Botany from the National University of San Marcos in Peru. He is a specialist in flora and

desert ecosystems, and a member of the Takana-Tacna Herbarium.

~~ Robert Langstroth is a herpetologist, biogeographer, and environmental professional with an M.S. from the University

— of California, Davis (USA) and a Ph.D. from the University of Wisconsin, Madison (USA). His work focuses on the

biogeography and taxonomy of South American lizards, the biogeography of the South American open formations, and

| the application of biodiversity mainstreaming and safeguards to enhance the sustainability of economic development.

* Robert is an associate researcher of the Coleccion Boliviana de Fauna, and currently serves as an IUCN Red List

Taxonomic Authority for the Liolaemidae and as a senior biodiversity and environmental safeguards specialist at a

multilateral development bank in Washington, DC, USA.

’ Alvaro Aguilar-Kirigin is a Bolivian biologist who graduated from the Universidad Mayor de San Andrés, La Paz,

« Bolivia. He has been a researcher at the Coleccién Boliviana de Fauna specializing in herpetology since 2002, and is a

& member of the Bolivian Network of Researchers in Herpetology. He carried out two research internships, in Argentina and

Uruguay, focusing on the systematics and phylogeny of Liolaemus and the latitudinal patterns of seasonal changes in fat

—- body size in 59 species of lizards. He has authored over 35 publications (18 peer-reviewed), 10 book chapters, and seven

- technical cards as part of book chapters, including the descriptions of three species of Liolaemus. Alvaro is interested in

| integrative taxonomy, especially in the genus Liolaemus, because of its phenotypic plasticity in the Andean region. As a

line of research, he is making progress with linear models in the study of classical comparative morphometry. He is also

linked to conservation efforts for the wildlife that inhabit the Amazonian forest in the Department of Beni in Bolivia.

Roberto C. Gutiérrez is a biologist who graduated from the National University of San Agustin de Arequipa of

Peru. Roberto is currently the Curator and Principal Researcher of the Herpetological Collection, Museo Nacional de

Historial Natural, Universidad Nacional de San Agustin, Arequipa, Peru, and Vice President and Founding Member

of the Herpetological Association of Peru (AHP). He is interested in the herpetofauna of the tropical Andes and the

coastal desert, with a special focus on lizards of genus Liolaemus, and is developing studies in the systematics of

amphibians and reptiles, ecology, and conservation. Roberto has conducted several biodiversity inventories, biological

assessments, and biodiversity monitoring programs, and is currently working at the Natural Protected Areas Service of

the Peruvian Ministry of Environment.

Cristian S. Abdala is an Argentinian biologist, a researcher at CONICET, and a professor at the Universidad Nacional

de Tucuman (UNT) in Argentina. Cristian received his Ph.D. degree from UNT, and is a herpetologist with extensive

experience in the taxonomy, phylogeny, and conservation of Liolaemus lizards. He has authored or co-authored over 90

peer-reviewed papers and books on herpetology, including the descriptions of 58 recognized lizard species, mainly in

genus Liolaemus. One species, Liolemus abdalai, has been named in his honor. He has conducted several expeditions

through Patagonia, the high Andes, Puna, and the salt flats of Argentina, Chile, Bolivia, and Peru. From 2016 to 2020,

Cristian has been the president of the Argentine Herpetological Association.

Amphib. Reptile Conserv. 22 August 2021 | Volume 15 | Number 2 | e278

Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

15(2) [General Section]: 23-30 (e279).

New records of the Endangered Szechwan Rat Snake,

Euprepiophis perlaceus (Stejneger, 1929) (Squamata:

Colubridae: Coronellini), from Shaanxi, China

'Shi-Yi Tang, 7?Chen-Liang Li, ‘Yu-Li Li, and '**Bao-Guo Li

'Shaanxi Key Laboratory for Animal Conservation, College of Life Sciences, Northwest University, Xi'an 710069, CHINA *Hubei Broad Nature

Technology Service Co., Ltd., Wuhan 430079, CHINA ?CAS Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences,

Kunming, 650223, CHINA

Abstract.—The Szechwan Rat Snake (Euprepiophis perlaceus Stejneger, 1929) is an Endangered species that is

endemic to China. Previous documentation indicates that it is only distributed in narrow mountainous regions

in Sichuan. However, some recent sighting records indicate the existence of another population located in the

Mts. Qinling, Shaanxi, more than 470 km NW from the original known locality. Here, we report the morphological

details of a live-captured individual of Euprepiophis perlaceus, and provide information on its taxonomy,

distribution, ecology, and conservation implications, along with references to the published literature from

Chinese sources.

Keywords. Asia, conservation, morphology, Qinling Mountains, range extension, Reptilia

Citation: Tang SY, Li CL, Li YL, Li BG. 2021. New records of the Endangered Szechwan Rat Snake, Euprepiophis perlaceus (Stejneger, 1929)

(Squamata: Colubridae: Coronellini), from Shaanxi, China. Amphibian & Reptile Conservation 15(2) [General Section]: 23-30 (e279).

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: 2 August 2020; Published: 29 August 2021

Introduction

The Szechwan Rat Snake (also called Pearl-banded Rat

Snake) was first described by the American herpetologist

Leonhard Stejneger as Elaphe perlacea, based on a

male specimen obtained in Yachow (Ya’an Prefecture),

Szechwan, China, in 1928 (Stejneger 1929), and there

had been no further studies on its distribution from then

until the early part of this century (Zhao 2006; Hu et

al. 2002). This snake was once considered extinct, or

regarded as a sub-species or even just a morphological

variation of the Mandarin Rat Snake, Elaphe mandarina

(Schulz 1989; Zhao 2006), since the location of its type

species is in the areas where Elaphe mandarina is found,

and there are many morphological similarities between

the two species (Schulz 1989, 1996).

The debate over its status as a distinct species has

diminished since three new specimens of Elaphe

perlacea were recorded between 1980 and 1988, from

Wolong National Nature Reserve, Wenchuan County

in Aba Tibetan-Qiang Autonomous Prefecture, and

Hailuogou National Glacier Forest Park, Luding County,

Ganzi Tibetan Autonomous Prefecture (Deng and Jiang

1989). Zhao (1990) reexamined the morphological

characters of the newly found specimens and argued that

Elaphe perlacea should be considered as a valid species

due to some distinctive features compared to Elaphe

mandarina. Schulz (1996) supported this assumption, and

Elaphe perlacea appears on the list of his A Monograph

of the Colubrid Snakes of the Genus Elaphe. Chen et

al. (2014) used multi-locus data obtained from tissue

samples of three Euprepiophis perlaceus (synonym of

Elaphe perlacea) individuals and used coalescent model-

based approaches to clarify the species validity and

explore phylogenetic relationship between this species

and others. The results showed that: “Euprepiophis

perlaceus is a distinct species sister to Euprepiophis

mandarinus (synonym of Elaphe mandarina).” The

genus Euprepiophis contains three species (Euprepiophis

mandarinus, Euprepiophis perlaceus, and Euprepiophis

conspicillata), and has also been recently separated from

the other rat snake lineages (Utiger et al. 2002; Chen et

al. 2014).

Based on the collection of more specimens, the

distribution of Euprepiophis perlaceus was found to

be broader, including two counties in Ya’an Prefecture

(Shimian County and Baoxing County) and another two

counties in Leshan Prefecture (Mabian County and E’ bian

Correspondence. ! sangsy@nwu.edu.cn (SYT), heibao@broadnature.cn (CLL), lily@nwu.edu.cn (YLL), *baoguoli@nwu.edu.cn (BGL)

Amphib. Reptile Conserv.

August 2021 | Volume 15 | Number 2 | e279

Szechwan Rat Snake in Shaanxi, China

County) (Hu et al. 2002; Zhou et al. 2012; Ding et al.

2017). All these sites are within a narrow area in western

Sichuan (Fig. 1, Zhou et al. 2002; Chen et al. 2014).

However, a photograph taken during a field survey by

Northwest Agriculture and Forestry University in 2013

raised the question as to whether Euprepiophis perlaceus

is also located in Ningshan, Ankang Prefecture, Shaanx1,

China (Ding et al. 2017). This would extend its known

distribution by about 470 km NW from the localities

previously reported, and if this is the case, more sighting

records of Euprepiophis perlaceus should be obtained

through extensive surveys in this area. Five years after

the 2013 record, one of the authors confirmed another

record based on a video recording taken during a field trip

on 18 May 2018, at Zhouzhi, Xi’an Prefecture, Shaanx1,

China (Table 1). Nevertheless, no voucher specimen

was available until an extensive search was conducted

during summer 2019, in which the authors obtained a

live individual in Foping County, Hanzhong Prefecture,

Shaanxi Province, China.

Thus, in this study, the morphological characters of

a live Euprepiophis perlaceus individual captured in

Shaanxi are described, followed by an assessment of

all the encounter records recently reported in Shaanxi,

including some unpublished records. In addition, a

preliminary assessment of its distribution, ecology,

and conservation are also discussed based on sources

published in the Chinese literature.

Materials and Methods

The specimen was encountered at 1117 h (GMT + 8)

from a pile of dead leaves at the base of a cliff, near a

cement road, in a valley of Foping County, Hanzhong

Prefecture, Shaanxi, China, on 23 June 2019 (elevation:

1,650 m asl). The surrounding habitat was secondary

deciduous broadleaf forest consisting of high arbors and

shrubs (Fig. 3). The photo of the specimen was taken

with a digital Nikon D810 camera with an AF-S Micro

NIKKOR 60 mm F2.8G lens, and the specimen was

then kept in the Shaanxi Key Laboratory for Animal

Conservation, Northwest University, Xi’an, Shaanxi,

China. The equipment used in taking the measurements

included a caliper (to the nearest 0.1 mm), a measuring

tape (to the nearest | mm for snout-vent lengh (SVL)

and tail length (TL)), and a piece of soft rope. The

total body length, SVL (from the snout to the posterior

margin of the anal plate), and tail length (TL) were

firstly marked on the soft rope and then measured with

the measuring tape. Sex was determined via a Rapti-

zoo SEOO1 Snake sex probe speculum following the

method of Blanchard and Finster (1933) and Fitch

(1960).

Additional visual records of Euprepiophis

perlaceus were collected through browsing local

social media (e.g., “WeChat”) for the snake’s images

and the published records in Chinese sources. We also

interviewed the witnesses or photographers taking the

photos to obtain more information on the locations and

times the photos were taken. The elevations where the

Euprepiophis perlaceus were encountered in Shaanxi

are provided in Table 1, and were obtained according to

location landmarks with Google Earth Pro 7.3.0.3832

(64-bit), when information on the exact locations could

be obtained.

Results and Discussion

This species is characterized by a moss-green color with

paired black bands (1—2 widths of the dorsal scale row)

mixed with yellow-green edges on the dorsum and tail.

The snout and forehead have two black strips extending

through the nostrils and eyes, respectively, both ending

on the supralabials, with a second strip separated into

two branches beneath the eyes. Posterior to the strips,

there are three black V-shaped patterns aligned on the

upper surface of head, occiput, and back. The belly is

greyish white with dark gray blotches. The snout is

obtuse. There is no distinct separation between head

and neck. The eyes are entirely black. Anal is divided

into two parts. Along with the external morphological

characters given in Fig. 2 and Table 2, the description

and measurements of the captured individual are

consistent with those taken by Zhao (1998, 2006) and

Table 1. New distributional records of Euprepiophis perlacea in Shaanxi, China.

Location Month and year

Ningshan, Ankang Prefecture July 2020

Huxian, Xi’an Prefecture May 2020

Ningshan, Ankang Prefecture July 2019

Foping, Hanzhong Prefecture June 2019

Ningshan, Ankang Prefecture June 2019

Zhouzhi, Xi’an Prefecture August 2018

Zhouzhi, Xi’an Prefecture May 2018

Ningshan, Ankang Prefecture June 2017

Ningshan, Ankang Prefecture June 2016

Ningshan, Ankang Prefecture June 2013

Amphib. Reptile Conserv. 24

Elevation (m asl) Reference

- pers. comm.

1,520 pers. comm.

1,650 this study

1,422 Wuet al. 2019

1,790 pers. comm.

1,440 this study

- pers. comm.

1,610 Ding et al. 2017

August 2021 | Volume 15 | Number 2 | e279

Tang et al.

104°E 108°E

38°N 38°N

34°N 34°N

30°N 30°N

Legends

A Previous records

A New localities

==: Province Border

104°E 108°E

Fig. 1. New locations where Euprepiophis perlaceus was found in Shaanxi, including Ningshan, Foping, Zhouzhi,

and Huxian. The previous distribution localities of the species in Sichuan include Ya’an, Wenchuan, Luding, Shimian,

Baoxing, Mabian, and E’bian.

Fig. 2. Dorsal view of Euprepiophis perlaceus captured in Foping County, Hanzhong Prefecture, Shaanxi Province,

China. Photo by Shi-Yi Tang.

Amphib. Reptile Conserv. 25 August 2021 | Volume 15 | Number 2 | e279

Szechwan Rat Snake in Shaanxi, China

Fig. 3. View of the Euprepiophis perlaceus habitat in

Foping, Shaanxi Province, China. Photo by Bin Yang.

Ding et al. (2017) (Table 3).

Records of Euprepiophis mandarinus were also

reported in various plots around our research area

(Wang and Song 2000; S.Y. Tang et al., pers. comm.).

However, Euprepiophis mandarinus has a greater

body length (largest measured specimen: 1,425 mm)

compared with Euprepiophis perlaceus (largest

measured specimen: 1,244 mm) (Zhao 1998). The

upper body and tail are purplish gray or yellowish

brown with conspicuous yellow spots edged by black

diamond circles, which were distinct from Euprepiophis

perlaceus (see the description above). The temporals of

Euprepiophis mandarinus were 2+3, which is different

from Euprepiophis perlaceus and Euprepiophis

conspicillata (temporals: 1+2) (Table 3; Zhao 1998).

The number of dorsal scale rows for Euprepiophis

mandarinus is 23-23-19 (for the number of dorsal scale

rows counted: behind the head-middle ventral-before

the tail), which is different from Euprepiophis perlaceus

(19-19-17) (Table 3). Euprepiophis conspicillata is

endemic to the Japanese archipelago, which has no

distributional overlap with the other two species in the

genus Euprepiophis (Stejneger 1907).

Preliminary research on the range and ecology of

Euprepiophis perlaceus in Sichuan indicated that the

preferred habitats are deciduous broadleaf forest and

mixed evergreen deciduous broad-leaved forest in

temperate mountains with elevations of 1,600—2,800

Amphib. Reptile Conserv.

m asl (Gan et al. 2017; Ding et al. 2017). The habitat

where Euprepiophis perlaceus was found in Shaanxi is

very similar to those reported in Sichuan. Considering

the topography, climate, mountain range alignment,

and the spatial pattern of vegetation types in Southern

Shaanxi, Northern Sichuan, and Southeastern Gansu,

suitable habitats for Euprepiophis perlaceus might be

widely distributed in this area (Zhang 2010; Cheng and

Wang 2019; Fig. 1). As this snake 1s constantly being

encountered by humans in different counties within

the Mts. Qinling (a major mountain range in Southern

Shaanxi, where all the sighting records of Euprepiophis

perlaceus were reported; Fig. 1, Table 1), we believe

the actual distribution areas in Shaanxi are broader than

previously known. In fact, populations of Euprepiophis

perlaceus in the two neighboring provinces may

form a continuous range. This proposition could be

physically confirmed by conducting extensive surveys

to the areas with deciduous broadleaf forests in the

Mts. Qinling. Additional surveys should focus on the

western part of this mountain range, where there are

gaps between the known locations of the neighboring

provinces. Further studies on the morphological and

molecular components, and comparisons with other

species in the same genus, are needed in order to fully

understand the phylogenetic relationships between

the two populations, or sub-populations in varying

geographic scopes (e.g., between sub-populations in

the southern and northern slopes of the Mts. Qinling).

As the main body of the Mts. Qinling, the southern

Shaanxi is famous for its global biodiversity hotspots

and refugia and for many endangered mammals and

birds, particularly during the last glaciation (Wang

et al. 2013). The Chinese Government has invested a

great deal of manpower in the conservation of “four

precious species in the Mts. Qinling” (Giant Panda,

Ailuropoda melanoleuca;, Golden Snub-nosed Monkey,

Rhinopithecus roxellana, Crested Ibis, Nipponia

nippon, and Takin, Budorcas taxicolor). Euprepiophis

perlaceus has been listed as Endangered on the JUCN

Red List of Threatened Species (Zhou et al. 2012), and

the new distribution records in southern Shaanxi caught

our attention for the conservation of this species, as

well as other Threatened or Endangered amphibians

and reptiles in this area. It is necessary to raise the

issues of a conservation strategy for this snake species,

in addition to carrying out further surveys and studies

on its ecology, behavior, and dietary selection. At the

moment, what we know about its conservation status

is that like most other ophidian species, the most likely

threats to Euprepiophis perlaceus could include road

accidents (traffic 1s heavy in the areas), habitat loss,

poaching (for bushmeat), intentional killing due to the

fear of snakes in the local culture, natural disasters

(such as floods), and predation by other animals (Zhou

et al. 2019). Although a series of natural reserves has

been established in the Mts. Qinling, rapid tourism

August 2021 | Volume 15 | Number 2 | e279

Tang et al.

Table 2. Morphological information and pholidosis data of the Euprepiophis perlacea specimen used in this study.

Parameter

Collection locality

Elevation

Sex

Date of collection

Collector

Total body length

Snout to vent length

Tail length

Head length

Head width

Diameter of eye

Eye-nose"

Number of ventrals

Pairs of subcaudals

DORI”

DOR2™

DOR3”™

Number of temporals

Number of supralabials

touching the eyes

Number of infralabials

Number of loreals

Number of pre-oculars

Number of post-oculars

Value or information

Foping, Hanzhong Prefecture, Shaanxi, China

1,650

male

23 June 2019

Shi- Yi Tang

907 mm

725 mm

182 mm

18.1 mm

13.6 mm

3.6mm

6.6 mm

225

3" and 4

— — CO

* Eye-nose: distance from center of the eye to posterior border of the nostril.

**T)OR1: number of dorsal scale rows at one head-length behind the head; DOR2: number of dorsal scale rows at the

position of the middle ventral; DOR3: number of dorsal scale rows at one head-length before the tail.

development would inevitably lead to the expansion

of roads and other artificial constructions, while

increasing human disturbance in this area.

Overharvesting for the pet trade may be another

major challenge to the conservation of Euprepiophis

perlaceus (Zhou et al. 2019). A preliminary

investigation into the underground pet market showed

this snake had become one of the most sought-

after species for reptile collectors. It sells for about

US$400-1,000, probably due to its rarity, mild-temper,

and attractive appearance (Zhou et al. 2019; S.Y. Tang

et al., pers. comm.). To avoid the risk of increased

poaching activity, as suggested by Ngo et al. (2019),

we did not provide the exact localities where the

Euprepiophis perlaceus population was found in this

paper.

In summary, the distribution of Euprepiophis

perlaceus is broader than previously reported.

Unfortunately, this Endangered species has received

Amphib. Reptile Conserv.

very little attention, since no conservation plan or

effort has been proposed so far. Thus, we argue that

appropriate conservation strategies and management

are necessary, and scientific studies on its life-history,

behavior, reproduction, and population genetics are

needed, as proposed by Gan et al. (2017), Ding et al.

(2017), and Zhou et al. (2019). A monitoring system

on the dynamic population profiles of this species

should be established, so that emergency strategies

for its conservation could be applied if a significant

population decline was detected. On the other hand,

more technical programs for captive breeding are also

required (Chen et al. 2017).

Acknowledgements.—We are grateful to Qinglin

Research Station of Endangered Animals, located in

the Foping and Shaanxi Longcaoping Forestry Bureau,

for permission to carry out this study and providing

logistic support. Special thanks to Prof. Fa-Dao Tat,

27 August 2021 | Volume 15 | Number 2 | e279

Szechwan Rat Snake in Shaanxi, China

Table 3. Morphological information and pholidosis data of the three recognized species in the genus Euprepiophis:

Euprepiophis perlaceus, Euprepiophis mandarinus, and Euprepiophis conspicillata.

Species

Distribution

Threat level (UCN)

Number of ventrals

Pair of subcaudals*

DORI”

DOR2™

DOR3”

Number of temporals

Number of supralabials

Euprepiophis perlaceus

China (Sichuan Province

and Shaanxi Province)

Endangered

224-231

57-69

1+2 (1+3 in rare cases)

Euprepiophis mandarinus

China (nearly all central and southern

provinces), northeastern Indo-Chinese

Peninsula

Least Concern

181-237

53-75

2+3

7 (6 or 8 in rare cases)

Euprepiophis conspicillata

Japanese archipelago

Least Concern

200-227

60-76

Dit

1+2 (2+2 in rare cases)

7 (6 or 8 in rare cases)

34 and 4"

1 (lacking in one side in rare

cases)

divided (undivided in rare

rd th rd th

touching the eye Seance earn

Number of infralabials 7-9 9

Number of loreals l 1 (lacking in one side in rare cases)

Number of post-oculars 2 2 (1, 3 or lacking in one/both sides in

rare cases)

Number of pre-oculars 1 1

Anal divided divided

Stejneger 1929; Zhao 1998;

References This study; Zhou et al. Zhao 1998; Ji et al. 2012

2012

* The terminal scute had been excluded.

cases)

Stejneger 1907; Borkin et

al. 2017

** TXOR1: number of dorsal scale rows behind the head; DOR2: number of dorsal scale rows at the position of

the middle ventral; DOR3: number of dorsal scale rows before the tail. For DOR1 and DOR3, the positions of

scale rows counting are different, and for Euprepiophis perlaceus, we counted the scale rows at one head-length

behind the head for DOR1 and at one head-length before the tail for DOR3. Zhao (1998) used similar criteria in

describing Euprepiophis mandarinus, but the scale rows were counted at two head-lengths behind the head (for

DOR1), or before the tail (for DOR3).

*** Stejneger (1907) only generally described number of scale rows of Euprepiophis conspicillata as 21, without

documenting the positions where the scale rows had been counted.

Mr. Bin Yang, Mr. Hai-Tao Zhao, Mrs. Rui Hu, Mr. Yi-

Fei Gao, Mr. Bo Tan, Mr. Yan-Bo Ma, and Mr. Qiang

Cao for their help with artificial feeding, morphological

measurements, and sharing valuable information about

additional localities of the species in Shaanxi. Deepest

regards to Prof. Ru-Liang Pan, Dr. Chang-Cao Wang,

and two anonymous reviewers for their valuable

comments on the original manuscript. This research

was supported by the Postdoctoral Science Foundation

of Northwest University, the National Science

Foundation for Young Scientists of China (31800318),

and the National Key Programme of Research and

Development, Ministry of Science and Technology

(2016YFC0503200). All the works reported here

adhered to the laws of People’s Republic of China on

the protection of wildlife, and our field surveys were

conducted with the approval of Northwest University.

Amphib. Reptile Conserv.

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Amphib. Reptile Conserv.

Szechwan Rat Snake in Shaanxi, China

Shi- Yi Tang has been involved in specimen collection, photography, and behavioral studies

of insects, amphibians, reptiles, and birds since childhood. His research interests lie largely

with taxonomy, distribution, behavioral ecology, and conservation of wild animals across

diverse taxa. Shi-Y1 Tang finished his Ph.D. in 2017 at Wuhan University, China, majoring

in avian behavioral ecology. He spent nearly 20 months in total at various field research

sites in the Qinghai-Tibetan plateau between 2008 and 2016, and had been appointed as a

visiting Ph.D. student in Cornell University (Ithaca, New York, USA) from September 2012

to June 2013. Shi-Yi Tang is currently working as a post-doctoral fellow at Shaanxi Key

Laboratory for Animal Conservation, College of Life Sciences, Northwest University, Xi’ an,

China, where he is involved in several research programs on the ecology and biodiversity

conservation of endangered animal species in Mts. Qinling.

Chen-Liang Li is a herpetologist currently working as the director of Hubei Board Nature

Technology Service Co., Ltd. He obtained his doctoral degree in 2016 at the College of Life

Sciences, Central China Normal University, where he majored in animal behavioral ecology

and conservation. His research interests include the taxonomy, distribution, behavioral

ecology, and conservation of amphibians and reptiles, as well as threatened animal species 1n

other taxa. Chen-Liang Li is currently conducting several projects related to environmental

education for wildlife in China, while promoting a habitat conservation plan for the Critically

Endangered Baer’s Pochard, Aythya baeri.

Yu-Li Li is currently working on her Ph.D. degree under the supervision of Professor Bao-

Guo Li at Shaanxi Key Laboratory for Animal Conservation, College of Life Sciences,

Northwest University (Xi’an, China). Yu-Li finished her M.A.Sc. degree in 2011 at the

Northwest Agriculture and Forestry University. Her work focuses on the ecology, population

genetics, and conservation of endangered animal species in the Mts. Qinling.

Bao-Guo Li is a professor at Shaanxi Key Laboratory for Animal Conservation, College of

Life Sciences, Northwest University (Xian, China). He guides the research of Ph.D. students

as well as M.Sc. students. He graduated in 1982 from the Shaanxi Normal University with

a B.S. in Zoology, and then obtained his M.S. from Northwest University (China) in 1985.

He had been appointed as a visiting professor in Kyoto University (Japan) from May 2001

to April 2002, and a visiting professor in Massey University (New Zealand) in 2007. His

research interests are mainly on the social behavior and conservation biology of endangered

animals in Mts. Qinling. He has been supervising projects supported by NSFC, Pro-Natura

Fund of Japan, COSMO Oil Eco Card Foundation of Japan, Primate Conservation Inc.,

and the Zoological Society of San Diego (California, USA). Prof. Bao-Guo Li has received

many accolades for his contributions to wildlife research and biodiversity conservation in

China.

30 August 2021 | Volume 15 | Number 2 | e279

Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

15(2) [General Section]: 31-39 (e281).

Description of the tadpole and natural history notes of

Incillus spiculatus (Mendelson, 1997), an Endangered toad

endemic to the Sierra Madre de Oaxaca, Mexico

‘Medardo Arreortua, ‘Carlos A. Flores, ‘Pablo Rogelio Simon-Salvador, ‘Hermes Santiago-Dionicio,

and 2’Edna Gonzalez-Bernal

Instituto Politécnico Nacional, CIIDIR Unidad Oaxaca, Laboratorio de Ecologia de Anfibios (ECA), Hornos 1003, Col. Noche Buena, 71230,

Santa Cruz Xoxocotlén, Oaxaca, MEXICO *CONACYT-Instituto Politécnico Nacional, CIIDIR Unidad Oaxaca, Laboratorio de Ecologia de

Anfibios (ECA), Hornos 1003, Col. Noche Buena, 71230, Santa Cruz Xoxocotlan, Oaxaca, MEXICO

Abstract.—Amphibian populations are declining rapidly around the world. However, new amphibian species

keep being discovered, reflecting the still expanding state of our knowledge of this group. Similarly, there is

a lack of information regarding life cycles, particularly among those species that have indirect development

with a free-living larval stage. Many amphibian larvae are still unknown or undescribed, thus impeding a proper

understanding of the biology and habitat use of many species. In this paper, we describe the tadpole of the

Endangered bufonid anuran /ncilius spiculatus, a member of a clade known as forest toads. Also described

are the amplexus behavior of this species observed in nature, and aspects of the natural history of the adult

stage. A tadpole identification key is provided for the forest toad clade of Mexico and Central America. This

information contributes to the understanding of the life history of /. spiculatus, in addition to its diet and

distributional patterns. This article highlights the importance of knowing the complete life cycle of a species

in order to establish effective conservation plans, particularly for those species with limited distributions in

highly managed ecosystems.

Keywords. Anura, forest toads, valliceps group, amplexus, stream breeding, scorpion predation

Citation: Arreortua M, Flores CA, Simén-Salvador PR, Santiago-Dionicio H, Gonzalez-Bernal E. 2021. Description of the tadpole and natural

history notes of Incilius spiculatus (Mendelson, 1997), an Endangered toad endemic to the Sierra Madre de Oaxaca, Mexico. Amphibian & Reptile

Conservation 15(2) [General Section]: 31-39 (e281).

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 August 2020; Published: 26 August 2021

Introduction

In recent years, the continuing discovery of new

amphibian species (Canseco-Marquez et al. 2017;

Jiménez-Arcos et al. 2019; Parra-Olea et al. 2020) and

larval phases (Downie et al. 2015; Kaplan and Heimes

2015; Kohler et al. 2015) has revealed the limited state of

our knowledge regarding amphibians, which are currently

the vertebrate group with the highest risk of extinction

(Beebee and Griffith 2005; IUCN 2020; Scheele et al.

2019; Stuart et al. 2008).

A similar situation is the lack of information that

exists regarding life cycles, in particular for those species

that exhibit indirect development with a free-living larval

stage. These species usually inhabit different habitats

throughout their life cycle and play different ecological

roles in relation to their development stages. For example,

most tadpoles contribute to maintaining healthy water

bodies by consuming algae and breaking down organic

material (Cortés-Gomez et al. 2015), while transferring

energy between aquatic and terrestrial habitats (Flecker

et al. 1999; Kupferberg 1997; Regestert et al. 2008). As

adults, these organisms usually prey on invertebrates,

thus controlling their populations, while at the same time

acting as prey for other organisms (Duellman and Trueb

1994; Stewart and Woolbright 1996). This duality also

means that each life-history stage is exposed to different

risk factors. Thus, when aiming to conserve a species

with a biphasic life cycle, it is essential that we have

thorough knowledge of both life-history stages.

Toads of the genus J/ncilius are anurans with a

biphasic life cycle which inhabit the Americas. Their

geographical distribution ranges from the southern edge

of the United States to northern Colombia (Mendelson

et al. 2011). Currently the genus contains 40 recognized

species, of which 23 have a distribution within Mexico

(AmphibiaWeb 2020; Wilson et al. 2013; Schachat et al.

2016). Among these are the so-called forest toads, a clade

that groups various species that inhabit wet forests and

are sensitive to habitat transformation as detected in their

Correspondence. *“ednagbernal@gmail.com (EGB), medardo.am@hotmail.com (MA), carlosfloresh88@gmail.com (CAF), rogeliosimon-

salvador@gmail.com (PRSS), hermestgo96@gmail.com (HSD)

Amphib. Reptile Conserv.

August 2021 | Volume 15 | Number 2 | e281

Incilius spiculatus in Oaxaca, Mexico

adult stage (Mendelson et al 2011). Despite this known

sensitivity, information on the larval stages of these toads

is incomplete. The forest toad group is composed of 10

species: Incilius aucoinae, I. melanochlorus, I. cristatus,

I. macrocristatus, I. cavifrons, I. spiculatus, I. tutelarius,

I. aurarius, I. leacomyos, and I. campbelli, among which

the larvae of only seven species have been described

(Mendelson et al. 2012; Segura-Solis and Bolafios

2008). The larvae of 1. melanochlorus, I. campbelli, and

I. spiculatus are unknown, reflecting the fact that even

though the description of anuran tadpoles from Latin

America is increasing, there are still many Neotropical

species whose larval stage remains to be described

(Downie et al. 2015; Kaplan and Heimes 2015; Kohler

et al. 2015).

During recent surveys in the northern slopes of the

Sierra de Juarez in Oaxaca, we found an amplectant

pair of Jncilius spiculatus, an endemic species of

southeast Mexico that is restricted to the highlands of

the physiographic sub-province of the Sierra Madre de

Oaxaca (Mendelson 1997; Ortiz-Pérez et al. 2004). This

species occurs mainly in montane cloud forests and is

listed as Endangered (EN) according to the IUCN (IUCN

2020). It was originally described from adult specimens

deposited in scientific collections; however, its breeding

behavior has not been recorded nor has the tadpole been

described, despite extensive fieldwork conducted in the

region (Caldwell 1974; Caviedes-Solis et al. 2015; Delia

etal. 2013; Lips et al. 2004; Mendelson 1997). In addition,

many aspects of the natural history and reproductive

biology of /. spiculatus are still unknown, probably due

to taxonomic confusion of this species with J. cristatus

and I. valliceps, as well as its restricted distribution and

lack of field observations (Mendelson 1997).

In this paper, the tadpole of 7. spiculatus is described

and information on breeding sites, amplexus type, and

clutch size are documented. An identification key for the

tadpoles of the forest toad clade (Mendelson et al. 2011)

in Mexico and Central America is provided, in addition

to observations on adult J spiculatus with comments

on conservation implications that might allow this

endangered toad to persist in the region.

Materials and Methods

Surveys were conducted at San Pedro Yolox

(17.589359°N, -96.551790°W; datum WGS84) and

Santa Cruz Tepetotutla (17.739446°N, -96.558292°W),

both located on the northern slopes of the Sierra Juarez,

Oaxaca, Mexico, within the sub-physiographic province

Sierra Madre de Oaxaca (Ortiz-Pérez et al. 2004).

In February 2019, a pair of 1. spiculatus was found in

amplexus and laying eggs at Rio Coyul, San Pedro Yolox

(17.64015°N, -96.4306°W, 645 m asl). The species was

identified according to the reported distribution and

morphological characteristics described by Mendelson

(1997), particularly the presence of cranial crests,

spiculate tubercles on the limbs, and pale fingertips.

The female body temperature and clutch temperature

Amphib. Reptile Conserv.

were taken with an infrared thermometer. Seventy

eggs were collected from the egg clutch without

disturbing the adult toads (permit FAUT-0074) and

taken to the Amphibian Ecology Laboratory at Centro

Interdisciplinario de InvestigacioOn para el Desarrollo

Integral Regional Unidad Oaxaca (CIIDIR-Oaxaca).

The eggs were kept in glass tanks with aerated water.

The water was partially replaced every two weeks

and tadpoles were fed boiled spinach and lettuce ad

libitum. The room temperature ranged from 23 to 30

°C. Tadpoles were euthanized with 5% lidocaine and

preserved in 10% formalin.

A total of 34 tadpoles at stages 26 to 37 (Gosner

1960) were examined using a microscope (Carl Zeiss

2000-C) and photographed (Canon Powershot GX5)

for their subsequent measurements. For tadpole

morphology, the terminology of Altig (1970, 2007)

was followed. Measurements were made with tpsUtil

and tpsdig2 software (Rohlf 2017, 2019). Photographs

of the oral apparatus were taken specifically at Gosner

stages 24 and 37. The oral formula followed Altig and

McDiarmid (1999). Live coloration and codes were

described following Kohler (2012). All specimen series

were deposited in the Museo de Zoologia Facultad de

Ciencias (MZFC35365, MZFC35366, MZFC35367)

at the Universidad Nacional Autonoma de México.

Larval development time under laboratory conditions

was measured by recording the progress between the

46 Gosner stages until full metamorphosis was reached.

Clutch size. The approximate total number of eggs in

the clutch was calculated by multiplying the average

number of eggs in 10 cm sections of the egg string

(counted at five different sections) by the total length

of the egg string. The total length was an approximate

measurement to avoid disturbing the clutch. In addition,

air and water temperatures were taken, and the river

width was measured with a flexometer.

Adult diet. In order to identify items in the diet, six

adult toads were collected in the field and kept in

plastic boxes with access to water until they defecated,

after which they were released. The fecal samples

were preserved in 70% alcohol and examined with

a microscope (Leica model EZ4 stereoscopic). Food

items or structures were identified with specialized

insect keys (Palacios-Vargas et al. 2014; Rios-

Casanova 2014; Vélez and Vivallo 2018).

Results

Tadpole Description

Average measurements (mm) for Gosner stage

35: body length 13.28, tail length 21.68, tail muscle

height 3.41, maximum tail height 6.09, total length

34.96, tail muscle width 3.31, internarial distance 1.66,

interorbital distance 4.70; measurements for other

Gosner stages are presented in Table 1. The body is

August 2021 | Volume 15 | Number 2 | e281

Arreortua et al.

Table 1. Measurements of the tadpole of /ncilius spiculatus by Gosner stage (averages in mm). Body length (BL), Tail length (TAL),

Tail muscle height (TMH), Maximum tail height (MTH), Total length (TL), Tail muscle width (TMW), Internarial distance (ID),

Interorbital distance (IOD).

Lateral view

Stage BL TAL TMH MTH

26 6.25 9.87 1.38 2.85

27 6.08 9.15 1353 2.84

28 6.61 9.84 152 ee:

29 8.04 11.20 1.82 3.91

30 8.95 12.12 I.95 4.26

3] 8.63 11.77 1.75 4.16

32 8.51 12.80 2A 4.38

33 9:03 13.61 2.74 4.63

34 8.79 13.60 2.14 4.59

3D 13.28 21.68 3.41 6.09

36 12.89 2176 329 390

37 13.90 2218 3.44 6.29

ovoid in dorsal view, widest at about the middle point

and narrower near the tail; depressed in lateral view.

Snout nearly semicircular in dorsal profile, rounded at

the tip in lateral profile. Spiracle sinistral with inner

wall free from body. External nares ovoid situated

nearer to eyes than to snout. Eyes dorsal. Vent tube

medial. Tail rounded at the tip. Caudal musculature

highest at base, gradually tapering to a pointed tip;

dorsal fin reticulated (Fig. 1).

Oral disk small; labial tooth row formula 2(2)/3,

Al slightly longer than other rows; A2 gap narrow,

approximately width of 3—8 teeth, Pl and P2 equal

in length, P3 being the longest posterior row; labial

papillae restricted to lateral portions of oral disc

disposed in two interposed series (Fig. 1A). At stage

24, the larvae show an elongation of the oral apparatus

that protrudes from the body (Fig. 2D—E).

In life, the color of the body is uniformly

Cinnamon Brown (color 43 in Kohler 2012), except

for the ventral part of the mouth where the color

becomes paler. The venter is slightly transparent, with

a counter-clockwise coiled intestine visible. Around

Gosner stage 35, small Cream Yellow (82) dots

appear throughout the body and the iris (Fig. 2G). The

tail fins are transparent with large Cinnamon Brown

(43) pigment granules forming a reticulate pattern on

the dorsal fin. Around Gosner stage 37, the ventral

parts of the limbs are pale Cinnamon Brown (43)

with Cream Yellow (82) dots and dark brown bars

dorsally. In preservative, the tadpole body and the tail

musculature are Natal Brown (49), while the ventral

part of the body is slightly translucent.

Tadpole development required approximately 35

days to complete metamorphosis under laboratory

conditions (Fig. 2H). Three days after collection (8

February 2019), embryonic development reached

Gosner stage 12. Three days later, the embryos

had reached stage 18, and four days after that had

developed into stage 25 tadpoles.

Amphib. Reptile Conserv.

Dorsal view

TL TMW ID IOD

16.12 1.00 0.92 1.87

1523 1.10 0.92 V.79

16.45 127 LETS 2.25

19.25 1.38 1.15 2.26

21.07 LS 1.26 2sSu

20.40 1.45 1.28 2.50

21.31 152 1.32 2.49

22.63 1.68 1.28 2.69

22,39 1.66 | 2,62

34.96 3.31 1.66 4.70

34.66 2.81 159 412

36.63 3.05 1.70 4.84

Adult Breeding Behavior

In February 2019, an amplecting pair of Incilius spiculatus

was observed at 640 m asl in the shallower margins of a

river (Rio Coyul), where the water current was slowed

by the presence of rocks and aquatic vegetation. The Rio

Coyul is a permanent river with an average width of 8.19

m at the site where the amplexus was observed (Fig. 2F).

The toads used vegetation and material on the bottom

of the river to maintain their position in the water during

the amplexus. Mating was observed during the day and

the amplexus was axillary (Fig. 2A—B). At the time of the

observations (1250 h GST), the water temperature was

19.6 °C. The species exhibited an ovipositional string

mode with a double row of eggs arrangement (Altig and

McDiarmid 2007). The estimated clutch size was 4,500

eggs, and the clutch was attached to aquatic vegetation

on rocks at the river margins at about 35 cm depth (Fig.

2C). Amplectant behavior was observed from the time of

encounter until the toads separated (approximately 2.67

h). The female body temperature was 21.0 °C, SVL 85.5

mm, and the clutch temperature was 21.0 °C. In addition

to the amplectant pair, a second male toad was observed

in the water at a distance of 1.0 m. A second egg clutch

was observed in another pool located 3.70 m away; but

the toads that laid this clutch were not observed.

Adult Diet

Fecal samples indicated that Hymenoptera were the

dominant prey (15 individuals, 48.3%), followed by

Coleoptera (7, 22.5%), Scorpiones (6, 19.3%), Orthoptera

(2, 6.4%), and Blattodea (1, 3.2%).

Extension of Elevational Range

Previously, the elevational range reported for /. spiculatus

was from 800—1,689 m asl (Mendelson 1997). During

this survey, two juvenile individuals were observed at

August 2021 | Volume 15 | Number 2 | e281

Incilius spiculatus in Oaxaca, Mexico

Fig. 1. Tadpole of Jncilius spiculatus. (A) Oral disc at Gosner

stage 37, (B) lateral view at Gosner stage 35, and (C) dorsal

view at Gosner stage 35.

Santa Cruz Tepetotutla, Oaxaca, Mexico, in a patch of

primary cloud forest vegetation at an elevation of 1,758

m asl (17.71862°N, -96.55911°W) datum WGS84, in

addition to three individuals in San Pedro Yolox at 682

m asl (17.63622°N, -96.42735°W), 643 m asl (17.64001

°N, -96.43061°W), and 642 m asl (17.64013°N,

-96.43056°W). With these records, the altitudinal range

of this species is now extended as including from 642 to

1,758 m asl.

Discussion

The observations reported here confirm that Jncilius

spiculatus 1s a stream breeder, and that its reproduction

occurs during the dry season, as in the other species in

the forest toad group (Mendelson et al. 2011). With this

description, the number of known forest toad tadpoles is

increased to eight; the only species yet to be described

are [. melanochlorus and I. campbelli (Altig 1970, 1987;

Korky and Webb 1973; Mendelson et al. 1999, 2012;

Segura-Solis and Bolafios 2009; Shannon and Werler

1955). Among the tadpoles of this group, /. tutelarius,

I. macrocristatus, I. leuacomyos, and I. spiculatus share

the oral formula 2 (2) /3, as does I. valliceps (Korky and

Webb 1973; Limbaugh and Volpe 1957; McCranie and

David 2000; Mendelson et al. 1999). Although /. valliceps

is not a forest toad, it is included in the identification key

here because it is sympatric with 1. spiculatus and the two

could be easily confused due to similar morphology. The

difference between the two species is that 1. spiculatus has

an A2 gap that is 3-8 teeth wide, and it has a reticulated

pattern only on its dorsal fin.

Amphib. Reptile Conserv.

A peculiar morphological characteristic of J.

spiculatus present at Gosner stage 24 is an oral apparatus

that protrudes from the body (Fig. 2D—E). As far as we

know, this feature has not been reported for any other

species of anurans. A limiting factor for comparison with

other species is that most descriptions are made from

tadpoles at developmental stages beyond Gosner stage

25, so larval development in earlier stages is generally

unknown. The closest related species for whicha complete

larval development description (from fertilization to

metamorphosis) could be found is /. valliceps, and it

does not have this oral morphology type (Limbaugh and

Volpe 1957). Descriptions of earlier tadpole development

stages should be encouraged because they have proven

to be useful for differentiating species in groups where

the morphological variations of larvae in advanced

stages (beyond Gosner stage 34) are almost non-existent

(Laufer et al. 2013). In addition, we consider that these

observations can contribute to the understanding of

larval ecology. As mouth shape 1s known to be associated

both with habitat type and diet in other amphibians (Altig

and McDiarmid 1999; Van-Buskirk 2009), we suspect

that this structure might be either an adaptation to life in

flowing water that prevents tadpoles from being washed

away (by allowing them to attach to fixed material) or

a foraging adaptation in early development that changes

in the later stages. The diet type at this stage should be

investigated to further elucidate its function.

In relation to breeding behavior, the findings reported

here confirm that /. spiculatus uses lotic systems during

the dry season to reproduce, a consistent pattern among

the forest toad group (Mendelson et al. 1999). With this

new data, the information on reproduction sites for the

ten species of this group is now complete (Mendelson

2011). Reproduction in lotic environments during the

dry season may be related to the flow conditions of the

streams, since this 1s the time when these systems have

slower currents and are shallower. Thus, the eggs are not

washed away and the drying of water bodies does not

represent a risk for the larvae (Kam et al. 1998; Wells

2007).

Based on these field observations, /. spiculatus is

opportunistic and largely insectivorous in its feeding

habits. The feeding strategy of this species is that of a

sit-and-wait predator. Even though the sample size for

the adult diet analysis was small, 1t represents the first

data on the diet of this species, which is composed

of arthropods, including ants, beetles, crickets, and

scorpions. Probably the most noteworthy observation

is the evidence of scorpion consumption, which is

poorly documented in amphibians. While basically

restricted to the Neotropics, all reports of scorpions in

anuran diets are limited to eight species within three

families (Bufonidae, Hylidae, and Leptodactylidae):

Leptodactylus pentadactylus, Leptodactylus bolivianus,

Leptodactylus fuscus, Osteopilus septentrionalis, Boana

pugnax, Peltophryne peltocephalus, Rhinella marina

(Botero-Trujillo 2006; Florez and Banco-Torres 2010),

and Rhinella icterica (Jared et al. 2020). The recent

report of R. icterica as a natural predator of the Yellow

Scorpion (Zityus serrulatus) is interesting, as_ this

scorpion is known for a significant number of poisoning

August 2021 | Volume 15 | Number 2 | e281

Arreortua et al.

Fig. 2. Breeding behavior of /ncilius spiculatus. (A-B) Amplexus (axillary type) and oviposition, (C) egg string staggered in

unilayered tube, (D—E) dorsal and ventral views of the tadpole head at Gosner stage 24 showing the “elongated mouth,” (F) Rio

Coyul, San Pedro Yolox; (G) lateral view of tadpole at Gosner stage 39, and (H) lateral view of metamorphic individual.

incidents involving humans in Brazil (Jared et al. 2020).

A broader dietary analysis of 1 spiculatus should be

undertaken in order to compare possible differences

between ages and sexes, with the aim of determining

different roles in the ecosystem as proposed for other

toad species. For example, preferred prey size is related

to body size and age in /. cristatus: juveniles consume

smaller prey than adults, while females, being larger in

size, consume larger prey items, suggesting different

predator-prey interactions according to age (Gelover et

al. 2001; Oropeza-Sanchez et al. 2018).

Despite the fact that the elevational distribution of

this species is now extended from 642-1,758 m asl,

potential reproductive streams are located at lower

elevations. As lowlands present warmer climates,

fertile soil, and less slope, they are usually attractive for

agriculture and human settlements (Price and Butt 2000;

Slik 2005), which results in clearing and deterioration

of vegetation cover, especially in riparian areas. These

activities contribute to connectivity loss between forest

habitat and breeding sites, creating a habitat split that

is particularly problematic and risky for amphibians

with aquatic larvae (Becker et al. 2007; Price and Butt

2000; Velasco-Murguia et al. 2014). As in other species,

this has several implications for the conservation of /.

spiculatus. First, reproductive adults and metamorphic

individuals emerging from the river are forced to

migrate between forested areas and lotic environments

via disturbed sites, increasing the risks of desiccation

Amphib. Reptile Conserv.

and predation (Oropeza-Sanchez et al. 2018; Todd et al.

2009; Walston and Mullin 2008). Additionally, tadpoles

developing in the river have higher exposure to the

chemicals used in agriculture and other human activities,

such as the extraction of sand and water (Adlassnig et

al. 2013; Sparling et al. 2001). These aspects provide

additional stress factors to the already vulnerable

situation of amphibians, such as J. spiculatus, which

have small distribution areas, aquatic reproduction, and

larval development in lotic systems, making them more

susceptible to habitat transformation and increasing their

risks of population decline or extinction (Becker et al.

2007; Nowakowski 2017).

Increased efforts to describe anuran larval stages

are needed 1n order to complete our knowledge of the

biology of threatened amphibian species. Firstly, this

is necessary to understand the habitat requirements

of a species, and possibly differential stressor factors

throughout the life cycle. Secondly, because tadpoles

remain in water bodies for long time periods, they are

often the only evidence for the presence of amphibians

at many sites, making this life-history stage highly

relevant to rapid inventories that aim to accurately

assess the geographic distribution of this group. For

this reason, the morphological description of tadpoles

allows detection of species that are more difficult to

detect in their adult phase, while reducing the costs

and technical complications of inventories that involve

molecular techniques such as bar coding (Grosjean et al.

August 2021 | Volume 15 | Number 2 | e281

Incilius spiculatus in Oaxaca, Mexico

Key to the tadpoles of the forest toads of Mexico and Central America

la. A2 Gap present...

1b. A2 Gap absent..

2a. Tail fin colotation Variable: known fiom Mexico.

2b. Tail fins light brown with widely dispersed dark brown dots; known from western Costa Rica and Panama............

3a. Known from Sierra Madre Oriental of Veracruz and Puebla,

3b. Known only from Sierra de los Tuxtlas Veracruz,

4a. Tail fins transparent... ccc ccceceeeeeeeees

4b. Tail fins uniformly dark brown..........000.0000000000..

5a. Tail musculature black.....0....c cc ecccceeeeeeeees

5b. Tail musculature brown..........00....cccccccccceccccceeeeeeeeees

6a. Tail musculature partially black with scattered pale areas.

Guatemala...

....L. aucoinae

MexICOt 4... es oe I. cristatus

MEXICO...... 00... cee cece ce essetetsteeeeeel, Cavifrons

5 OE Cia Sd Lee i Ne leh TE ee, Ne See I. tutelarius

Known from southern Mexico to western

1. macrocristatus; I. aurarius

6b. Tail musculature black. Tail fins reticulated and flecked with black. A 22 gap » width about 2 labial teeth. Known only

from north-eastern Honduras..............00... 000 ccc ce cece eens

FERN ee Gil See SO coe. Rn Le I. leucomyos

7a. Dorsal fin has large Cinnamon Brown (43) granules forming a reticulation. A-2 gap width equal to

3-8 labial teeth. Known only from Sierra Madre de Oaxaca...

1. spiculatus

7b. Dorsal and ventral fins with yellow reticulation. A-2 gap wide, width ‘equal to. 10- 15 labial teeth.

Widely distributed across

2015). In addition, morphological data will be useful and

complementary to new and powerful techniques, such as

environmental DNA, for biodiversity inventories in the

coming decades (Beng and Corlett 2020).

A report by the IUCN (IUCN SSC 2020) states that

I. spiculatus is not distributed within protected areas.

However, in our study area, the local community conserves

large areas of the montane cloud forest that is habitat for

I. spiculatus (9,570 ha in the case of the municipality of

San Felipe Usila) under the Indigenous and Community

Conserved Areas (ICCAs) mechanism. ICCAs are areas

governed by indigenous or local communities where

collective action focuses on the governance of common

resources at multiple scales (Bray et al. 2012; Pazos-

Almada and Bray 2018). These social actions contribute

to the maintenance of optimal habitat where the

species can still survive. Communication with the local

community to share findings on reproductive behavior

should increase the chances of improving habitat quality

at lower elevation sites, promote connectivity between

aquatic and terrestrial habitats, and ensure the survival

of this species.

Acknowledgements.—The field work for _ this

publication was funded by CONACYT México through

the project Ciencia Basica #256071. We would like

to thank the authorities of Santa Cruz Tepetotutla and

San Pedro Yolox for their authorization to work in

their community. We also thank Pedro Osorio, Marcial

Hernandez, and Paola Velasco for their support during

Amphib. Reptile Conserv.

southern Mexico and Central AMmMefrica..........0000..0 ccc ceccccceeeeeceeeeeeeeed

valliceps

fieldwork; Camilo Julian and Mayra Miguel for the

scientific illustration of the tadpole; Emilio Martinez

and Eufemia Cruz for allowing us to take tadpole

pictures in their laboratory; and Joseph Mendelson

and Michael Crossland for their helpful comments

on the manuscript. Eggs were collected under permit

FAUT-0074 issued to Fausto Méndez de la Cruz. We

are grateful for comments from Gunter Kohler and an

anonymous reviewer that improved the manuscript. In

memory of Eugui Roy Martinez Pérez.

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Wells KD. 2007. Movements and orientations. Pp. 230— Wilson LD, Johnson JD, Mata-Silva V. 2013. A

267 In: The Ecology and Behavior of Amphibians. conservation reassessment of the amphibians of

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Chicago, Illinois, USA. 1,161 p. Reptile Conservation 7(1): 97-127 (69).

Amphib. Reptile Conserv.

Medardo Arreortia is a Mexican herpetologist interested in the ecology and

conservation of amphibians and reptiles of Mexico. He is currently a postgraduate

student studying the movement ecology and habitat use in amphibians 1n relation to

habitat disturbance. He is a member of the group Ecologia para la Conservacion de

Anfibios (ECA) in Oaxaca, Mexico.

Carlos A. Flores is a biologist currently pursuing a Master’s degree in Conservation

Sciences at CIIDIR-Oaxaca, Mexico. His research focuses on understanding the

effects of introduced exotic fish on native tadpoles, and the implications of invasive

Species introductions for amphibian conservation.

Pablo Rogelio Simén-Salvador is interested in the ecology, natural history, and

conservation of amphibians and reptiles from Mexico. For his Bachelor’s degree,

he designed a method for the collection, storage, and cryopreservation of semen

from snakes from the genus Crotalus. During his Master’s degree, he evaluated the

effect of anthropogenic disturbance on three species of endemic anurans from cloud

forests. His interests include conservation and wildlife photography.

Hermes Santiago Dionicio is currently finishing his Bachelor’s thesis at Instituto

Politecnico Nacional (IPN) CIIDIR-Oaxaca, Mexico. His research is mostly focused

on evaluating shifts in amphibian shelter quality due to habitat disturbance in a

cloud forest. Hermes is interested in the conservation of herpetofauna in general.

Edna Gonzalez-Bernal is the Head of the Amphibian Ecology Lab (ECA) at

CIIDIR-Oaxaca, IPN, Mexico. Her research focuses on amphibian ecology and

biological invasions, with a special interest in the roles that human activities play

in their occurrence.

39 August 2021 | Volume 15 | Number 2 | e281

Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

15(2) [General Section]: 40—49 (e282).

Trends in ovarian development, plasma vitellogenin, and

steroid hormones in female Malaclemys terrapin (Schoepff,

1793) from coastal Louisiana

1.2* Jordan Donini, *“Will Selman, **Steven Pearson, and *’Roldan A. Valverde

'Department of Biological Sciences, Southeastern Louisiana University, 808 North Pine Street, Hammond, Louisiana 70401, USA *Department of

Pure and Applied Sciences, Florida Southwestern State College, 7505 Grand Lely Drive, Naples, Florida 34113, USA *Rockefeller Wildlife Refuge,

Louisiana Department of Wildlife and Fisheries, 5476 Grand Chenier Highway, Grand Chenier, Louisiana 70643, USA *Biology Department,

Millsaps College, 1701 North State Street, Jackson, Mississippi 39210, USA *Louisiana Department of Wildlife and Fisheries, 646 Cajundome

Boulevard, Lafayette, Louisiana 70503, USA °New York State Department of Environmental Conservation, 625 Broadway, Albany, New York 12233,

USA ‘Sea Turtle Conservancy, 4581 NW 6th Street, Gainesville, Florida 32609, USA

Abstract.—The timing of reproductive cycles in reptiles is often linked to environmental correlates, including

temperature and photoperiod. The Diamondback Terrapin (Malaclemys terrapin) is a wide-ranging species that

occurs across multiple climatic regions over the eastern and Gulf coastal areas of the United States. Therefore,

the species may show variation in reproductive cycles according to latitude. To assess the reproductive cycles

of M. terrapin and to improve our understanding of their range-wide variations, terrapins were sampled in the

state of Louisiana during the known nesting seasons from May—August (peak and late nesting period) and

outside of the typical nesting season during the month of October (fall pre-wintering period). Terrapins were

sampled via ultrasonography to assess the development of ovarian follicles and eggs. Blood samples were

collected, and the egg yolk protein vitellogenin and the steroids testosterone and estradiol were measured.

Large pre-ovulatory class follicles were present during the peak nesting season, though the animals showed

fewer (or lacked) follicles in the later portion of the reproductive season. Pre-wintering samples in the fall

showed pre-ovulatory class follicles. Vitellogenin varied significantly across sampling periods, with peak

values occurring during the early portions of the nesting season before decreasing in the late nesting season,

followed by increases in the fall pre-wintering period. The testosterone concentration did not vary over any

of the sampling periods, while estradiol varied significantly across sampling periods, with peak values in

the fall pre-wintering period. These results suggest that M. terrapin in Louisiana likely follow a post-nuptial

reproductive pattern, similar to conspecifics and other emydid turtle species at more northern latitudes.

Keywords. Diamondback Terrapin, vitellogenesis, ovarian cycle, estradiol, testosterone, reproductive cycle

Citation: Donini J, Selman W, Pearson S, Valverde RA. 2021. Trends in ovarian development, plasma vitellogenin, and steroid hormones in female

Malaclemys terrapin (Schoepff, 1793) from coastal Louisiana. Amphibian & Reptile Conservation 15(2) [General Section]: 40-49 (e282).

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: 1 December 2020; Published: 24 August 2021

Introduction Kuchling 1999a). Gonadal steroid hormones are largely

responsible for driving major changes in the reproductive

Reproductive cycles in ectothermic organisms are

largely seasonal and often initiated by environmental

cues, including changes in temperature, photoperiod,

and rainfall (Noeske and Meier 1977; Horseman et al.

1978; Whitter and Crews 1987). Turtles, like other

ectotherms, have reproductive cycles that follow similar

cues (Lewis et al. 1979; Kuchling 1982; Mendonca

and Licht 1986; Kennett 1999) and typically fall under

one of two major categories, depending on whether

gametes are produced prior to (prenuptial cycle) or after

(postnuptial cycle) the reproductive season (Licht 1982;

cycle, with reproductive hormones serving as key

components of gonadal recrudescence, ovulation, and

other reproductive activities (Callard et al. 1976, 1978;

Huot-Daubremont et al. 2003; Al-Habsi et al. 2005).

Non-steroid molecules, such as calcium and the egg yolk

protein vitellogenin (Vtg), may also serve as indicators

of reproductive functions (Rostal et al. 2001; Saka et al.

2011). Specifically, the production of Vtg may be used

as an indicator of reproductive status and reproductive

potential in the female reproductive cycle (Ho et al.

1982; Currylow et al. 2013; Myre et al. 2016).

Correspondence. |*:*Jtdonini@fsw.edu, ** will.selman@millsaps.edu, *° Steven. Pearson@dec.ny.gov, |" Roldan.valverde@selu.edu

Amphib. Reptile Conserv.

August 2021 | Volume 15 | Number 2 | e282

Donini et al.

Though reproductive cycles have been described

in many species of reptiles in terms of both gonadal

recrudescence and hormonal profiles, gaps in the

available information remain for several species, some

which are of conservation concern (Graham et al. 2015).

Diamondback Terrapins (Malaclemys terrapin) are

one such species of conservation interest (Roosenberg

et al. 2019) and there are descriptions of gonadal and

endocrine cycles (Holliday et al. 2018). Terrapins occupy

coastal estuarine habitats across the United States from

mid-coastal Texas, along the northern and eastern Gulf of

Mexico, and up the Atlantic coastline to Massachusetts

(Carr 1952; Ernst and Lovich 2009). Given their

expansive range, populations at different latitudes

may experience varied seasonal and environmental

conditions. Throughout much of their distribution,

Terrapins are exposed seasonally to low temperatures

(Akins et al. 2014), which may serve as a cue for the

production of gametes, similar to other chelonian species

(Ganzhorn and Licht 1983; Mendonca 1987). Following

emergence from winter dormancy, Terrapin nesting is

often observed in the spring through summer (Seigel

1980a; Feinberg and Burke 2003; Harden and Willard

2012). Active breeding and courting, however, have been

observed in both the early fall and during the spring and

summer (Siegal 1980b; Estep 2005).

Along the Northern Gulf of Mexico (NGoM),

Terrapins appear to typically nest from late April to

August (Mann 1995; Borden and Langford 2008:

Coleman et al. 2014; Pearson and Wiebe 2018), and

they likely are exposed to variable thermal conditions

compared to their northern conspecifics, especially in

southern latitudes, where they may experience a shorter

period of inactivity in the winter. Recent studies in the

NGoM have investigated habitat use and reproductive

output (Coleman 2011; Pearson and Wiebe 2018), as

well as some potential threats (Drabeck 2014; Coleman

et al. 2014) to populations in Louisiana, Mississippi, and

Alabama. However, endocrine and gonadal cycles have

never been described in wild Terrapins from this region.

In Louisiana, and throughout their range, Terrapins

have been impacted both historically and in recent

years due to direct human involvement, with some

populations experiencing notable declines (Gibbons

et al. 2001). These impacts include harvesting for food

and the pet trade (Enge 2005; Converse et al. 2017),

habitat destruction and fragmentation, and accidental

by-catch (Wood and Herlands 1997; Lovich et al. 2018).

Therefore, the objective of this study was to investigate

the reproductive cycle of Terrapins in Louisiana, by using

ultrasound and blood sampling, to document ovarian

activity with regard to vitellogenin and sex hormone

concentrations. An improved understanding of the

reproductive physiology of Terrapins in this region could

be valuable for informing stakeholders and conservation

agencies in their decision making towards conservation

goals. Because most known strategies in temperate

Amphib. Reptile Conserv.

chelonians exhibit post-nuptial reproductive cycles, we

suspect that Terrapins in Louisiana will exhibit this same

pattern, with peaks in hormonal and vitellogenin contents

showing elevated concentrations during the nesting

period, then declining as the season progresses before

increasing again in the pre-wintering period in the fall.

Materials and Methods

Study Sites

Terrapins sampled for this study came from two

subpopulations in Louisiana. The first population sampled

was at Rockefeller Wildlife Refuge, with sampling

occurring in both early and late May 2015 and again in

October 2015. A second population was sampled from

June-August 2015 in Terrebonne Parish during nesting

surveys. Primary habitat in these Louisiana study sites

consisted of Smooth Cordgrass (Spartina alterniflora)

and Saltgrass (Distichlis spicata) marshes, as described

by Selman and Baccigalopi (2012) and Selman et al.

(2014), and pocket shell hash beaches in bay estuaries, as

described by Pearson and Wiebe (2018). Terrapins across

the state of Louisiana show similar genetic structure

throughout the region (Petre et al. 2015), and the

populations sampled are at similar latitudes. Thus, data

for the two populations were combined during analyses.

Sample Collection

Terrapins were sampled using three methods: (1)

manual surveys from airboats for locating mud burrows

and mobile Terrapins, (11) using single lead fyke nets

stretched across tidal bayous of saltmarshes (Selman

and Baccigalopi 2012, 2014), and (111) opportunistic

hand capture along nesting beaches. Four females which

were captured and held by a local fisherman for sale and

aquacultural purposes were sampled in August, but it is

unknown how long they had been in captivity. The keeper

provided no information on light or temperature cycles,

but the animals were observed in large Rubbermaid

stock tanks in a storage room with artificial lighting.

According to the keeper, all animals were readily feeding

on invertebrates and fish.

Once captured, females were then bled from the

subcarapacial sinus or dorsal coccygeal vein within

five minutes of handling (to minimize stress response)

using a heparinized 22-gauge needle and 3 ml syringe.

A 0.5—1.5 ml sample of blood was collected from each

individual, depending on its size. Some Terrapins were

bled after a minimum period of 12 h contained in fyke

nets, and the parameters were compared between these

individuals and those sampled by active methods to

assess any stress effects on the hormone values. Whole

blood was immediately placed on ice and centrifuged at

3,000 rpm within 3 h of collection. Plasma was kept on

dry ice while in the field, before storage at —80 °C.

August 2021 | Volume 15 | Number 2 | e282

Female reproductive cycle in Malaclemys terrapin

Fig. 1. Examples of various follicular size classes from different sampling periods of Diamondback Terrapins. (A) Class IT and IV

follicles from late May. (B) Class I follicles from August samples. (C—D). Class II and III follicles from October samples.

Ultrasound

A portable ultrasound (TITAN, Sonosite Inc., Bothell,

Washington, USA) with a 5-8 MHz microconvex

transducer was used to examine ovarian development

and the presence of follicles/eggs in a subset of captured

females. Ovarian follicle diameter was measured to the

nearest 0.1 cm using digital software calipers or using the

program ImageJ (Schneider et al. 2012). Follicles were

assigned to one of four size classes: Class I (< 0.6 cm),

Class IT (0.6—1.0 cm), Class III (1.1-1.6 cm), or Class

IV (> 1.6 cm), adapted from similar classifications by

Lahanas (1982) and Mitchell (1985) (Fig. 1). No follicles

were detected in four of the female Terrapins (n = 2 in

July and n= 2 in August), so these four individuals were

excluded from subsequent follicle analysis.

Hormone and Vitellogenin Concentrations

A modified version of the in-house Vtg enzyme-

linked immunosorbent assay (ELISA) was used as

described by Smelker et al. (2014), using antibodies

developed against Trachemys scripta Vtg. This

antibody exhibits cross reactivity with turtles of the

family Emydidae, including M. terrapin (Donini

et al. 2018). A high-sensitivity commercial ELISA

kit (Enzo Life Sciences, Farmingdale, New York,

USA) was used for measuring both testosterone

(T) and estradiol (E,). Hormone kits were validated

Amphib. Reptile Conserv.

for this species via parallelism tests of M. terrapin

plasma. Samples were run in triplicate, at extraction

volumes from 50—400 ul depending on season and

assay. Hormone extractions were performed via

the methods described by Myre et al. (2016) and

Smelker et al. (2014) using double ether extractions.

Predicted hormone values were corrected for the

amount of plasma used for extraction and buffer

used for reconstitution prior to analysis. Animals

with hormone concentrations below detectable limits

(BDL) were assigned a concentration of 50% of the

lowest detectable limit for the assays (0.007 ng/ml for

E, and 0.0013 ng/ml for T), as has been used in other

assays and experiments of similar design (Flewelling

et al. 2010). Sample sizes varied for analyses of

hormone and Vtg concentrations, due to variations in

available plasma volume from each sample.

Statistical Analysis

A two way Multivariate-Analysis of Variance

(MANOVA) was used to determine whether there were

any effects on the results due to variations in sampling

location, and additionally for capture type (hand vs. trap

capture) to account for potential stress effects on the

hormones. Sampling periods were combined based on

the period in the known nesting season. Samples from

May and a single June sample were categorized as peak

nesting period, while July and August samples were

August 2021 | Volume 15 | Number 2 | e282

Donini et al.

grouped together as late nesting season, and October

samples were categorized as pre-wintering. Levene’s

and Shapiro-Wilk’s tests were used to assess normality

and homogeneity of variance among sampling periods

for the variables (average follicle diameter, Vtg, T, and

E,). Follicle diameter and T data met all parametric

assumptions with no transformations required and

were analyzed using an analysis of variance (ANOVA).

However, Vtg and E, data did not meet the assumptions

of normality and homogeneous variances, and their

skewedness was not within proper parameters to

proceed with normal parametric analysis. As a result,

non-parametric Kruskal-Wallis analyses with a post-

hoc Dwass-Steel-Chritchlow-Fligner test were used

to determine variations of Vtg and E, across sampling

periods. All analyses were performed with SYSTAT

13.0 and all graphical figures were generated using

Sigmaplot 14.0.

Results

Validation of sampling sites and methods. All Terrapins

sampled were adult females, and were captured during the

nesting season (May—August, n = 30) as well as during

periods outside of the known nesting season (October,

n = 9). There was no significant interaction between

season and sampling location (P > 0.05), providing

additional support for treating both sampling regions as

single populations for the analysis, and thus independent

ANOVA were used for each variable. Analysis of

hand captured and trap captured Terrapins determined

there were no significant differences between T and E,

concentrations with regard to capture type (/', ,, = 3.010

P=0.102 and F’ ,, = 3.179 P = 0.084, respectively).

Ultrasound. A subset of 29 females were sampled

via ultrasound. The average follicle diameter did not

significantly vary throughout the sampling periods

(F,4; = 2.234, P = 0.128). Mean follicle size during

the peak nesting period was 1.23 + 0.09 cm, and all

four size classes were observed in May and June. In

the late nesting period samples, individuals either had

very small Class I or II follicles, or they lacked follicles

completely (mean follicle size: 0.714 + 0.05 cm). Mean

follicle size in the October pre-wintering sample was

1.08 + 0.11 cm, again with multiple size classes present

(Fig. 2). No evidence of atretic follicles was observed

in any sampling period. Calcified eggs were visualized

in both peak and late nesting periods, but not in the fall

pre-wintering periods.

Hormone and vitellogenin concentrations. Thirty-

nine individuals were sampled for Vtg, while 21 were

sampled for T, and 34 for E,. The average Vtg intra-assay

coefficient of variation (CV) was 4.9% and the inter-assay

CV was 14.4%. The average T intra-assay CV was 8.66%

and the inter-assay CV was 10.58%. The average intra-

Amphib. Reptile Conserv.

2.5

2.0

S15

r 1.0

ic _——

0.5

0.0 a x ie

g ©) &

s had or

s SS °°

a = oo

5 ; ;

RS 2 cS Pk e RS)

we NS we ev ae

a? @

Q? Vv Q

Fig. 2. Ovarian follicle diameter throughout sampling periods

of female Diamondback Terrapins captured in Louisiana.

Dashed lines within each box indicate the mean of the data,

bold lines within each box indicate the median of the data, and

the upper and lower edges of the boxes represent the 75% and

25% quartiles. T bars represent the minimum and maximum

values. Solid black circles represent outliers. Note n = 4 for late

nesting period, but only two samples were used in the analysis

as the others lacked any detectable follicles. The mean and

median overlap in some categories, so both lines may not be

visible.

assay CV for E, was 9.74% and the inter-assay CV was

12.3%. Samples from Louisiana were run concurrently

with the Florida samples reported in Donini et al.

2018, explaining the similar CV results reported in

both papers. Terrapins had detectable concentrations

of Vtg during all sample periods, ranging from 0.97—

71.95 mg/ml, and significant differences in Vtg were

observed across sampling periods (¥ 7.724; P

= 0.021; df = 2; Fig. 3A). The highest values were

observed during the peak nesting season (28.7 + 3.06

mg/ml for May and June) with a drop occurring in

the late nesting period (July and August, 14.9 + 7.65

mg/ml). There was no significant difference observed

between the late nesting season and pre-wintering

samples (October, 17.47 + 1.04 mg/ml). Likewise,

there was no significant difference in T concentrations

between sampling periods (Ff ,, = 2.541 P = 0.127,

Fig. 3B). Mean T values were 119.53 + 34.04 pg/ml in

the peak nesting period, and 47.61 + 13.90 ng/ml the

pre-wintering sampling periods. Samples from July

and August had low plasma volumes, which prevented

their inclusion in the analysis of T for the late nesting

period. There was significant variation in E, values

across sampling periods (77 = 6.567; P = 0.037; df

= 2; Fig. 3C), with a decrease from the peak nesting

period (4.90 + 1.67 ng/ml) to the late nesting period

(1.06 + 1.06 ng/ml), followed by an increase in the

pre-wintering period (21.48 + 9.07 ng/ml). Data are

summarized in Table 1.

August 2021 | Volume 15 | Number 2 | e282

Female reproductive cycle in Malaclemys terrapin

Discussion

Seasonal follicular cycle. All stages of follicles (I-IV)

and calcified eggs were present through the majority

of the peak nesting period in May and June. Despite

being gravid, females either lacked follicles or showed

only Class I or I follicles during the late nesting

season. Fall pre-wintering samples showed Class I-III

follicles. However, no significant differences between

average follicle size existed among sampling periods.

This general trend in follicular changes throughout the

season is indicative of the post-nuptial cycle observed

in most temperate turtle species, where large follicles

are more common in the early nesting periods, before

being ovulated and/or reabsorbed as the nesting season

concludes, with gonadal recrudescence occurring in the

months following final oviposition (Lewis et al. 1979).

In the late nesting season samples, no females showed

° large preovulatory class follicles, suggesting that their

reproductive output for the season had likely ended.

The small Class I follicles in two of the August samples

likely represent the beginning of the development of

the following year’s clutch, similar to patterns in other

temperate species (Gibbons 1968; Ernst 1971; Robinson

and Murphy 1978; Ganzhorn and Licht 1983).

Vitellogenin (mg/ml)

300

Testosterone (ng/ml)

Seasonal vitellogenin concentrations. The Vtg

concentrations were found to be higher in the peak nesting

0 :

jovial sil season (early May—July) and began to drop as the nesting

s > ae season concluded. Though not statistically significant, the

“3 (*) ‘ t * . é :

Ro ss © increasing pre-winter Vtg concentrations 1s suggestive

Ss be > o> ' ; ;

. PM ¢ of fall follicular proliferation. This apparent “rise” in

S : .

s pas s of the fall, along with the previously presented follicular

increase in size, suggested that follicular recrudescence

likely begins in the transition period between summer

and fall, with the Vtg concentration increasing at this

time, allowing for follicular growth. In Louisiana, we

expected the Vtg trends to resemble those of northern

turtle populations, as Vtg should be highest during the

peak of the reproductive season, before decreasing as the

season concludes. Indeed, this trend is similar to those

reported in Chrysemys picta (Duggan et al. 2001; Gapp

et al. 1979) and in Terrapins in New Jersey (Wolfe 2014)

as the nesting season reached its end in late summer.

An important factor to consider is that the four

individuals sampled in August of the late nesting period

were collected by commercial fishermen and retained

for a potentially extended period of time. It is not known

how long these individuals were in captivity, but they

were confirmed to have been captured during the same

sampling year. Nonetheless, these individuals may have

Estradiol (ng/ml)

Fig. 3. Concentrations of vitellogenin (A), testosterone (B), and estradiol (C) throughout sampling periods of female Diamondback

Terrapins captured in Louisiana. Dashed lines within each box indicate the mean of the data, bold lines within each box indicate the

median of the data, the upper and lower edges of the boxes represent the 75% and 25% quartiles, and bars represent the minimum

and maximum values. Solid black circles represent outliers, and different letters indicate significant differences (P<0.05) between

sampling periods. The mean and median overlap in some categories, so both lines may not be visible.

Amphib. Reptile Conserv. 44 August 2021 | Volume 15 | Number 2 | e282

Donini et al.

skewed our data for this period. Because these individuals

either lacked or had only small previtellogenic or

Class I or II follicles upon ultrasound examination,

this coincided with the decrease in circulating Vtg.

However, reabsorption of developing follicles has

been documented in wild pleurodire species, such as

Psuedemydura umbrina, when brought into captivity

(Kuchling and Bradshaw 1993). The stressors that the

collected terrapins experienced could have potentially

altered their natural cycles. At least two of the individuals

in the fisherman’s possession were captured on nesting

beaches and showed retained eggs. The retention of

eggs and dystocia (egg binding) have both been linked

to environmental and captivity stressors (Buhlman et al.

1995; Kuchling 1999b; Innis and Boyer 2002), which

may have influenced the natural vitellogenic cycles of

these animals. However, as noted by Kuchling (1999b),

some species of turtles are less prone to have altered

reproductive output under captive stress. Close relatives

of the Terrapins (e.g., Chrysemys picta and Trachemys

scripta) along with dissimilar species, like Sternotherus

odoratus, are resilient species and capable of producing

eggs in captivity, even after removal from the wild

(Mendonga and Licht 1986; Bowden et al. 2001). The

lower concentrations of Vtg observed here in August and

the fall corresponded with the findings of Wolfe (2014),

who also found that Terrapins exhibited a quiescent

period in the late summer/fall as nesting was completed.

Therefore, while potentially impaired due to captivity,

we believe the values from captive individuals likely

mimic the natural cycle, as they did not deviate from the

values reported in other studies.

Seasonal sex hormone concentrations. Testosterone

was found in relatively high concentrations in both the

early nesting season and pre-wintering sampling periods,

corresponding to large steroidogenic follicles that were

detected during the same time. However, there was no

significant difference in the T concentrations between

periods. Winters et al. (2016) noticed a distinct decline

in the T concentration of female Terrapins as the nesting

season progressed in New Jersey, something our data was

unable to capture given the lack of plasma available for

assays and sample size as a whole. Lee (2003) showed

peak T values occurring in April, before decreasing in

May and June, in a population of Terrapins in South

Carolina. Lee (2003) also documented basal values of T

from July to August, before the T concentration increased

steadily from September to October. Other temperate

species, such as Graptemys flavimaculata, also exhibited

increased T in the fall and spring, before it decreased in

late summer (Shelby and Mendonca 2001). Terrapins

from Louisiana may exhibit a similar pattern, but our

missing sampling points during the late nesting season

prevented confirmation of this pattern.

Estradiol was found in low concentrations during the

early nesting period, and even lower (near the detectable

Amphib. Reptile Conserv.

limit) during the late nesting season (two samples in

July). These concentrations are drastically lower than

those reported for similar periods in Florida Terrapins

(Donini et al. 2018). The concentrations then increased

to peak values in the fall pre-wintering period. This

hormonal trend is further suggestive of a postnuptial

cycle initiated in fall, with females beginning follicle

development for the following nesting season, similar to

the observations of Lee (2003) in South Carolina. It is also

possible that the low concentrations of E, observed could

be explained by the difference in sampling methods, as

some of the Terrapins in this study were captured via

fyke nets, making it difficult to know capture time prior

to sampling. Thus, the low concentration of reproductive

steroids observed may be explained by stress artifacts,

as glucocorticoids may affect the concentrations of other

hormones in reptiles (Mahmoud et al. 1989; Elsey et al.

1991). However, when these trap-captured samples were

compared to those that were hand captured, no significant

difference existed between the two groups. Further, the

high concentrations of T in similar sampling periods

indicated that stress may not have altered the estradiol

concentrations observed in trap-captured animals.

Additionally, some vertebrates release sex hormones in

brief periods and small concentrations. For instance, only

a single large peak of E, was observed in G. flavimaculata

at a similar latitude in the middle of their known nesting

season (Shelby et al. 2001). E, specifically is only needed

in small doses to initiate vitellogenesis via exogenous

injections (Ho et al. 1981), so it is possible that the

concentrations detected were sufficient to stimulate

vitellogenesis for a subsequent clutch. This possibility is

further supported by peak concentrations of Vtg during

the same time period, indicating that vitellogenesis was

at its peak. Additionally, it is possible that T was still

in the process of aromatization at the time of sampling

in these individuals. Aromatization of T into E, is a

known pathway in the endocrine cycles of turtles (Tsai

et al. 1994: Crews et al. 1996), and the peak estradiol

concentration may have been missed. This differs from

the observations in Donini et al. (2018) for Terrapins from

south Florida, in which E, and T concentrations remained

elevated simultaneously during the nesting season,

coinciding with confirmed multiple clutch productions.

Despite following the same overall method of post-

nuptial reproduction, this may indicate some differences

in reproductive timing in the Terrapins between these

two latitudes, though this is only speculative given

the gaps in sampling data from earlier spring. The low

concentrations of E, in two of the Terrapins sampled in

the late nesting period samples from July coincided with

a lack of follicles, supporting the idea that these animals

had finished producing clutches for the season and were

entering a quiescent phase.

It is legal to harvest Terrapins in Louisiana during a

limited season from 15 April—16 June, but only if the

Terrapins have a carapace length of 6 in (15.2 cm) or

August 2021 | Volume 15 | Number 2 | e282

Female reproductive cycle in Malaclemys terrapin

greater (Louisiana Fishing Regulations 2020). However,

this harvest window overlaps with the major reproductive

periods described herein, so it puts reproductively

active females at the greatest risk of collection given the

timing and harvest size requirements. Consequently, it

may be prudent to revisit this law given the findings of

this paper and other researchers concerning Terrapin

reproduction along the NGoM to ensure the future

survival of this species in the state.

Conclusions

This study is one of very few which quantifies

the endocrinological and ovarian dynamics of the

reproductive cycle in M. terrapin, and it provides novel

data for the species in the NGoM. Overall, the data

presented here suggest a brief late summer quiescent

phase before ovarian recrudescence begins in the fall,

with vitellogenesis occurring into the spring, resulting

in the production of at least one clutch of eggs with the

potential for more. Information gaps still remain in our

knowledge of the endocrine and ovarian cycles of M.

terrapin in this data set, and for the species as a whole.

However, based on the results from this study, we now

have baseline data that suggest a temperate pattern for

the post-nuptial cycle in female Terrapins in the NGoM.

It is possible that conspecifics at higher latitudes follow

similar trends, but additional sampling in these regions,

as well as during more sampling periods, is necessary

to complete a full description of the reproductive cycle

of this species. Though limited, the data presented here

do provide some clarity on the reproductive season and

activity of M. terrapin in Louisiana, and may prove useful

in the potential amendment of collection laws regarding

the size and timing of collection in Louisiana.

Acknowledgments.—We thank Gary Childers and the

SELU Microbiology lab for access to their plate reader,

and Michael Garafolo of ENZO Chemicals for providing

a discounted rate on EJA kits. Funding for this project

was provided by grants through the Diamondback

Terrapin Working Group, The Minnesota Herpetological

Society, the Southeastern Louisiana University Biology

Department Development Fund, and the Rockefeller

Trust Fund. We thank Ryan Chabot, Jacquelyn Coppard,

Gody Godwin, and Lisa Rodriguez for reviewing early

drafts of the manuscript. Research activities for this

project were approved by the Southeastern Louisiana

University IACUC committee (Protocol #30). All

captures and sampling of Terrapins were approved by the

Louisiana Department of Wildlife and Fisheries.

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Amphib. Reptile Conserv.

Jordan Donini is a Professor of Biology at Florida Southwestern State College in Naples, Florida, USA.

Jordan received his B.S. in Biology from Florida Gulf Coast University (Fort Myers, Florida, USA) and his

M.S. from Southeastern Louisiana University (Hammond, Louisiana, USA). His research focuses on the life

history and reproductive ecology of the herpetofauna in the coastal states of the Gulf of Mexico.

Will Selman is an Assistant Professor of Biology at Millsaps College in Jackson, Mississippi, USA.

Will received his B.S. from Millsaps College and his Ph.D. from the University of Southern Mississippi

(Hattiesburg, Mississippi, USA). The research that he and his undergraduate students pursue focuses on

turtle life history and ecology in the southeastern United States, and the distribution and population status

of herpetofauna in Mississippi and the region. He is a member of the IUCN Tortoise and Freshwater Turtle

Specialist Group, on the Board of Advisors for the American Turtle Observatory, and the Chelonian Section

Co-Editor for Herpetological Conservation and Biology. Will also co-edited a recent issue of Chelonian

Conservation and Biology dedicated to the conservation and biology map turtles and sawbacks of the genus

Graptemys. Photo by Sophie Wolf.

Steven Pearson is an Ecologist with an interest in the anthropogenic impacts on plant and animal communities.

He completed his Bachelor of Science in Environmental Studies from the Richard Stockton College of New

Jersey (Galloway, New Jersey, USA), and worked for several years as a seasonal biologist with plants,

raptors, mammals, and reptiles before attending Drexel University (Philadelphia, Pennsylvania, USA) for his

Ph.D. At Drexel, Steven studied spatial resource use and dietary overlap between the non-native Trachemys

scripta elegans and the other members of the turtle community. After completing his Ph.D., he worked with

the Louisiana Department of Wildlife and Fisheries studying Malaclemys terrapin population and nesting

ecology, and determining the short-term and long-term impacts of oil and gas spills on aquatic environments

and organisms. Steven currently resides in New York, where he works with the New York Department of

Environmental Conservation as a Research Scientist, focusing on studying the abundance, distribution, and

management of aquatic invasive species.

Roldan A. Valverde is a Professor of Biology at Southeastern Louisiana University (Hammond, Louisiana,

USA) and Scientific Director of the Sea Turtle Conservancy. Roldan received his B.S. in Marine Biology at

the Universidad Nacional of Costa Rica, and his Ph.D. at Texas A&M University (College Station, Texas,

USA). He conducted post-doctoral training at the University of Michigan (Ann Arbor, Michigan, USA).

His current interests include the stress and reproductive endocrinology of sea turtles. Through his research,

Roldan collaborates with researchers in several parts of the USA, Latin America, and Europe.

49 August 2021 | Volume 15 | Number 2 | e282

Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

15(2) [General Section]: 50—58 (e283).

Effect of anthropogenic habitat disturbance on the nesting

ecology of the Wood Turtle (Glyptemys insculpta)

12,*Alexandra VIk, ‘Elizabeth Bastiaans, ‘Daniel Stich, and ‘Donna Vogler

'Department of Biology, State University of New York-College at Oneonta, 108 Ravine Parkway, Oneonta, New York, 13820 USA *Department of

Biology, Randolph-Macon College, 114 College Avenue, Ashland, Virginia, 23005 USA

Abstract.—In species that lack parental care beyond nesting, the fitness of the mother depends on the

selection of a high-quality nest site. Unfortunately, given the importance of nest site selection, anthropogenic

habitat degradation continues to decrease the availability of high-quality nest sites. This study focuses on

nest-site selection by a population of Endangered Wood Turtles (Glyptemys insculpta) in a disturbed site with

a high amount of human activity and invasive plant species. Logistic regression was used to examine nest-

site microhabitat characteristics such as soil composition, moisture, temperature, slope, vegetation type and

cover, canopy cover, and distances to water and vegetation. Wood Turtle nest site microhabitat characteristics

were also characterized in a protected site and compared to those of the disturbed site using a series of t-tests

and x? tests. Soil composition and a slight slope were the most important factors for Wood Turtle nest-site

selection at the disturbed site. Turtles at the disturbed site preferred a high amount of sand and small gravel,

with little or no larger gravel or clay. The disturbed site had a higher maximum temperature overall, with an

average of 35 °C versus 28 °C at the protected site. The turtles at both sites nested in sandy habitat, while the

nests at the protected site had higher moisture content than those at the protected site and lacked gravel. Since

is it common for Wood Turtles to use anthropogenic habitat, identifying, protecting, and managing nesting

sites are essential to Wood Turtle conservation efforts. To enhance the overall nesting success of these turtles

in disturbed areas, artificial nest sites could be judiciously placed and used by the turtles. Artificial nest sites

could be managed to improve the nesting success of this Endangered turtle species and, also, potentially

reduce adult loss by modifying the upland movements of adult females during the nesting season.

Keywords. Connecticut, Emydidae, fragmentation, habitat management, human disturbance, New York, USA

Citation: VIkA, Bastiaans E, Stich D, Vogler D. 2021. Effect of anthropogenic habitat disturbance on the nesting ecology of the Wood Turtle (Glyptemys

insculpta). Amphibian & Reptile Conservation 15(2) [General Section]: 50-58 (e283).

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 September 2020; Published: 24 August 2021

Introduction

Investment in parental care varies across taxa, with

some animals watching over and defending their young

for many years, while other animals have minimal

interactions with their offspring after birth (Gross 2005).

Clutton-Brock (1991) defines parental care as any type

of parental investment in the offspring after eggs have

been deposited or young have been born. For species

that do not provide direct parental care to their offspring,

strategies to increase the survival of the hatchlings may

include allocating energy to eggs in the form of lipid

reserves (Nagle et al. 2003; Kamel and Mrosovsky 2005)

or selecting a high-quality nest environment (Kolbe and

Janzen 2002). Habitat characteristics associated with

nest sites, such as temperature (Weisrock and Janzen

1999), can have direct effects on offspring survival and

phenotypes (Kolbe and Janzen 2002). Because turtles

are long-lived animals which require many years to

reach sexual maturity and have high egg and hatchling

mortality with no parental care beyond nesting, nest site

selection may be important for population persistence

since the nest site may directly influence nest success

(Lovich et al. 1990; Congdon et al. 1993; Horne et al.

2003). Unfortunately, given the importance of nest site

selection by turtles, anthropogenic habitat degradation

continues to decrease the availability of high-quality nest

sites, which could cause turtles to delay nesting and/or

nest in an unfavorable habitat (Walde et al. 2007). Due

to habit losses caused by anthropogenic disturbances,

reptiles are declining globally (Gibbons et al. 2000).

Turtles are particularly threatened by the increasing

Correspondence. *v/kalexandra@gmail.com (AV), Elizabeth. Bastiaans@oneonta.edu (EB), Daniel.Stich@oneonta.edu (DS),

Donna. Vogler@oneonta.edu (DV)

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Vik et al.

pressures of anthropogenic disturbances (Williams

1999). The International Union for Conservation of

Nature (IUCN) lists 148 of the 356 turtle species as

either Vulnerable, Endangered, or Critically Endangered

(Turtle Conservation Coalition 2018).

This study compares Wood Turtle (G/yptemys

insculpta) nest site selection between an anthro-

pogenically altered nesting site and a protected nesting

site. The Wood Turtle is currently under review for

protection under the Endangered Species Act (U.S. Fish

and Wildlife Service, 2019) and listed as Endangered by

the IUCN (IUCN 2016). The Wood Turtle is particularly

vulnerable to habitat loss and fragmentation because it is

a long-lived animal that displays low vagility and high

site fidelity (Garber and Burger 1995). Since the Wood

Turtle prefers open canopy forested areas, Kaufmann

(1992) speculated that this species might benefit from the

increased habitat openings created by humans. However,

anthropogenically generated habitat openings are often

the sites of other human impacts, which may reduce the

survival of Wood Turtle eggs laid there (Saumure 2004).

Wood Turtles require a variety of habitats (Arvisais

et al. 2004). Studies in Pennsylvania (Kaufmann 1992)

and Ontario (Foscarini 1994) showed that Wood Turtles

selected their habitat nonrandomly relative to availability

(Arvisais et al. 2004). They are known as an “edge

species” according to Kaufmann (1992), with a strong

selection of riparian habitat within 300 m of streams

(Arvisais et al. 2004). Wood Turtles often use forested

areas with openings in the canopy to allow for foraging

on herbaceous undergrowth and/or slugs (Lee 1999).

During the reproductive season, turtles require additional

areas of habitat. For example, gravid females travel

hundreds of meters seeking nest sites, hatchlings migrate

from nests to water, and males may travel in search of a

mate (Bol 2007).

Depending on latitude, the Wood Turtle nesting

season occurs between late May and mid-July (Arvisais

2002). Females construct nests on sandy beaches, railway

embankments, agricultural fields, and gravel quarries;

selecting for well-drained, sloped, and exposed areas

close to a water source (Harding and Bloomer 1979;

Foscarini 1994; Walde et al. 2007). The turtles spend a

few hours to several days exploring suitable nest sites

(A. VIk, pers. obs.). The time investment in finding a

nest site indicates that females are selective about where

they lay their eggs, likely to increase hatchling success

(Hughes et al. 2009). Unlike some other turtles, Wood

Turtles have genetic sex determination rather than

temperature-dependent sex determination (Ewert and

Nelson 1991). This suggests that females select nesting

locations based on maximizing hatchling survival rather

than balancing the sex ratio of the clutch (Hughes et al.

2009). Therefore, identifying, protecting, and managing

nesting sites are essential to Wood Turtle populations

because female Wood Turtles are highly sensitive to

disturbance prior to the initiation of egg laying (Walde et

Amphib. Reptile Conserv.

al. 2007). Furthermore, our lack of knowledge about the

nesting ecology and reproductive behavior of this species

hinders conservation efforts (Bury 2006; McCallum

and McCallum 2006). The goal of this study was to

locate and characterize Wood Turtle nesting habitat at

two Wood Turtle occupied sites, one disturbed and one

protected, to increase our knowledge of the usefulness of

anthropogenic sites and better inform the management of

these areas.

Materials and Methods

Study sites. The disturbed study site, located in the

Susquehanna watershed, was a park used for recreation

activities such as hiking, soccer, softball, picnics, and

angling. The forest consisted of mixed deciduous Oak-

Maple-Birch-Sycamore (Quercus, Acer, Betula, and

Platanus). The floodplains were mainly composed

of Spotted Knapweed (Centaurea), Common Lady’s

Thumbprint (Persicaria), Mugwort (Artemesia), and

Goldenrod (Solidago). A highly invasive plant species

native to Asia, Japanese Knotweed (Fallopia japonica),

dominated the floodplains and forests forming dense

stands that excluded most other vascular plants and

shrubs. Litter invaded the Wood Turtle habitat and

vegetation in the park was periodically mowed (A. VIk,

pers. obs.). On the other side of the creek, across from the

park, was a field that was mowed periodically for hay and

included a building supply store which provides masonry

products to the public. Daily uses of the supply store

include the operation of boom trucks, tractor trailers, box

trucks, and concrete mixers.

The protected site was located in the Great Swamp

Wildlife Management Area (WMA), Putnam County,

Connecticut, bordering New York. This area is managed

by the New York State Department of Environmental

Conservation, with an emphasis on habitat preservation

and restoration for the benefit of native species (NYS

DEC 2021). This WMA covers 444 acres of the Great

Swamp, which encompasses natural Wood Turtle nesting

habitat that is monitored by the staff, and free from

anthropogenic disturbances.

The exact study location of each site has been omitted

from this article to prevent illegal collection of the Wood

Turtles, but is available upon request at the authors’

discretion.

Data collection. At both the disturbed and protected

sites, Wood Turtles were captured along the shoreline in

the spring and summer of 2017 and 2018. The individual

adult and juvenile turtles captured were weighed, sexed

based on plastron concavity, and aged by counting

growth annuli on dorsal scutes (Harding and Bloomer

1979). Measurements (+ 0.01 mm) of the carapace

and plastron lengths were taken using calipers. Turtles

smaller than 180 mm were considered juveniles (Walde

1998). To establish a unique identification for each turtle,

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Nesting ecology of Glyptemys insculpta

Table 1. List and descriptions of covariates that were used in

the first subset of Wood Turtle nesting habitat selection models.

Covariate Covariate descriptions

Soil composition large gravel (> 5 cm), small gravel

(<2 mm), sand, clay

Temperature (°C) Average, maximum

notches were filed using a Dremel tool along the edge

of the scutes with notch codes provided by New York

Department of Environmental Conservation (DEC) and

Connecticut Department of Energy and Environmental

Protection (DEEP). Each turtle weighing at least 400 g

was fitted with a radio transmitter (Advanced Telemetry

Systems, Isanti, Minnesota, USA), which was glued

with epoxy gel to the rear marginal scutes of the

carapace. The transmitter weighed approximately 16 g

and never exceeded 5% of body mass. All procedures

were reviewed and approved by the SUNY Oneonta

Institutional Animal Care and Use Committee (IACUC

#2018-25), DEC (DEC Scientific permit #2136), and

DEEP (DEEP Scientific permit # 1718008).

In May—August, the spring and summer active

season of the turtles, 14 turtles at the disturbed site were

located by radiotelemetry every other day during the

pilot season in 2017. In 2018, 17 Wood Turtles were

tracked. Turtles were located between 0800 and 2000

h (most of the location events were during 0800-1400

h). Beginning on 26 May 2018, excursions were made

between 1700 and 2030 h to observe any nesting female

behavior (Ernst et al. 1994; Walde et al. 2007). The first

signs of nesting occurred on 28 May 2018 at 2000 h. The

turtle was sniffing and throwing dirt on her carapace,

which indicates nesting behavior (Harding and Bloomer

1979). Because Wood Turtles are known to start nest

activity at approximately 1700 h or later (Walde et al.

2007), radio tracking began every day from 1200-1500

h to locate turtle nesting grounds and avoid disturbing

nesting females. In the evening, once nesting females

were located, observations were made from concealed

locations to prevent the females from abandoning their

nests. If a Wood Turtle stayed in the nesting ground past

2030 h, observations continued until the turtle retreated

to the stream (Walde et al. 2007).

Eighteen Wood Turtles were tracked at the protected

site every other day during the nesting season by one of

the Great Swamp biologists. Known nesting sites were

checked daily during 1900-2100 h beginning 26 May,

while 30 May marked the beginning of the nesting

season at this site. Once the nesting season was initiated,

the same protocols were followed for observations at the

disturbed and protected sites.

At both sites, after a female was done nesting, the

turtle eggs were excavated, and microhabitat variables

were measured (Tables 1 and 2). The eggs at the disturbed

site were placed in vermiculite in an incubator at 28 °C,

and were then used in another study (Janzen and Morjan

Amphib. Reptile Conserv.

Table 2. List and descriptions of landscape nest covariates

that were used in second subset of Wood Turtle nesting habitat

selection models.

Covariate Covariate descriptions

Vegetation bare, herbaceous, woody

Canopy open, partial, full

Vegetation nest cover none, partial, full

2002), while the eggs at the protected nest site were left in

the ground with an exclosure placed over the nest. Many

of the nests at the unprotected site were found by digging

in suitable Wood Turtle nesting habitat, which included

floodplains with sand and/or small gravel present with

little vegetation or canopy cover. Soil samples (445 g)

were collected at approximately 10 cm depths from all

nests to measure grain size and moisture content (Hughes

et al. 2009). A sieve was used to separate 400 g of soil

into three different categories of large gravel (> 5 cm),

small gravel (< 2 mm), and sand (Table 1). Clay was

separated from the sand by adding water to the sample,

mixing the contents, and leaving it sit for two days to

allow separation. The amount of soil in each category

was expressed as a percentage. To determine moisture

content, 45 g of the sand separated out from the soil

sample was placed in a small tin, which was placed 1n an

Isotemp Programmable Muffle Furnace 650-750 Series

(Fisher Scientific, Dubque, Iowa, USA) for two weeks

at 110 °C (Hughes et al. 2009). After two weeks, the soil

samples were weighed again to determine how much

moisture weight was lost.

When all observed nesting activity ceased on 27 June,

waterproof iButton (ButtonLink, LLC, Whitewater,

Wisconsin, USA) temperature dataloggers were placed 15

cm deep at the site of each nest, which is the approximate

nest depth of Wood Turtles (Foscarini 1994; Walde 1998;

Compton 1999; this study). To prevent disturbance of

the eggs at the protected site, temperature loggers were

placed approximately 10 cm from the clutch and 15 cm

deep. Temperatures were recorded at 4-hour intervals

during the incubation period until 20 August when all

hatchlings had hatched. The dataloggers were placed in

15-inch PCV pipes and waterproofed by cementing a

coupler to each end of the PCV pipe.

Other microhabitat variables recorded in a radius of 1

m (around the nest) included: slope, canopy cover, nest

cover, vegetation type, and distances to nearest vegetation

and aquatic habitat (Table 2). At the disturbed site, habitat

was measured both at the nest location and at a nearby

randomly selected unused nest habitat with availability

at the same place and time, based on a random compass

bearing and a random distance selected uniformly from

~0.3—17 m (Compton 2002; Dragon 2014).

Data Analysis

Disturbed site. To estimate the probability of Wood

Turtles using specific nesting microhabitat in the

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Vik et al.

Table 3. Candidate model selection statistics for Wood Turtle nesting choice first subset. K is the number of parameters in each of

the models. AICc is the AIC score corrected for sample size. AAIC is the difference in AICc between the best model and each of the

other models. AIC wt is the probability that a given model is the best model in the candidate set.

Model

Soil PC 1 + soil PC 2

Soil PC 2

Soil PC 1

Average

Maximum temperature

Moisture

Maximum temperature + average

Maximum temperature + average + soil PC 1 + soil PC 2 + moisture

disturbed site, logistic regression in the Ime4 (Bates et al.

2015) package in R (R Core Team 2013) was used based on

a binary response (1 = used, 0 = random). A set of models

were fit using maximum likelihood estimation. A total of

16 models were constructed using a priori combinations

of explanatory variables. The explanatory variables were

divided into two subsets used to make models: (1) nest

characteristics, including soil composition, moisture

content, and temperature (Table 3); and (2) landscape

features, including slope, canopy cover, amount of nest

cover, type of vegetation and distances from the nearest

vegetation and aquatic habitat (Table 4).

Due to the small sample size of nesting turtles and the

soil variables being intercorrelated, a Principal Component

Analysis (PCA) was used on the soil variables to reduce

the dimensionality. The four soil variables (large gravel,

small gravel, sand, and clay) were grouped into two PC

axes that explained 81% of the variation combined in soil

composition (Table 5). The logistic regression model for

the nest characteristics subset was constructed using 10

paired nest locations due to the loss of two temperature

loggers in a flash flood. The landscape model consisted

of 12 paired nest locations. Akaike’s Information Criterion

(AIC) was used to rank each competing model using the

AlICcmodavg package (Mazerolle 2017). The model with

the lowest AIC score was considered the best supported

(Burnham and Anderson 2002).

Comparisons of the disturbed and protected sites. To

determine if nest site microhabitat characteristics differed

K AICe AAIC AIC wt

3 DI23 0.00 0.54

2 26.68 1.44 0.26

2 29.26 4.03 0.07

2 29:99. 4.76 0.05

2 30.61 5.38 0.04

2 31.89 6.66 0.02

3 32.77 7.53 0.01

6 34.32 9.09 0.01

between the disturbed and protected sites, a series of

t-tests and y? tests were conducted in jamovi (Jamovi

Project 2018). The statistical tests were conducted only

using actual turtle nests. Multiple t-tests were used to

identify differences in the variables: “temperature,”

“slope,” “distance vegetation,” “distance water,” “soil

composition,’ and “moisture” between the disturbed

and protected sites. The variables “distance vegetation”

and “distance water” were log-transformed due to the

violation of normality and equal variances. Since moisture

and soil microhabitat variables were correlated, a second

PCA analysis comparison was performed between the

two sites that grouped the four soil explanatory variables

and moisture together on habitat that was used for nesting

(Table 6). The variables with an eigenvalue above one

were then used in a ¢-test to compare soil compositions

of the two nest sites. Chi-square tests were performed on

the categorical variables “vegetation,” “canopy,” and “nest

cover” to determine whether the frequency of various

categories differed between disturbed and protected sites.

Since multiple statistical tests were performed, Bonferroni

correction was used to adjust the p-value to 0.003 to

minimize type I errors.

Results

Twelve nests were observed at the disturbed nest site and

seven at the protected nest site. The number of eggs in each

nest ranged from one to 16 (8.3 + 4.84) at the disturbed site

and eight to nine at the protected site (7.67 + 0.70). Most

Table 4. Candidate model selection statistics for Wood Turtle nesting choice second subset. Variable definitions are as indicated in Table 3.

Model

Slope degree

Slope degree + vegetation

Vegetation

Nest cover

Distance vegetation

Distance water

Canopy

Slope degree + vegetation + distance vegetation + canopy + nest

cover + distance water

Amphib. Reptile Conserv.

K AICce AAIC AIC wt

2 32.21 0.00 0.48

4 33:25 1.04 0.29

3 34.81 2.60 0.13

2 37.59 5.38 0.03

2 37.64 5.43 0.03

2 37.83 5.62 0.03

4 40.40 8.19 0.01

10 53.63 21.43 0.00

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Nesting ecology of Glyptemys insculpta

Table 5. Loading matrix from a Principal Component Analysis

(PCA) of four microhabitat variables measured at N = 10

disturbed Wood Turtle nest sites and N = 10 random paired

locations.

Covariate PC1 PC2

Large gravel -0.98 0.12

Small gravel 0.42 0.79

Sand 0.85 -0.50

Clay 0.57 0.37

female turtles started nest construction at approximately

1930 h, corresponding to sunset, and completed their

nests 2—3 hours later. Warm humid rainy days stimulated

nesting activity from multiple turtles at the same time (A.

Vik, pers. obs.).

Disturbed site. In 2018, 12 Wood Turtle nest sites were

located at the disturbed site. In 2017 and 2018, Wood

Turtle nesting began on 28 May and ended approximately

19 June. For the nest characteristics subset, “soil PC

2” was the most important predictor of nesting habitat

selection based on its inclusion in both top models. The

best model indicated significant effects of both “soil PC

1” (GLM: ¥°7, = 4.23, P = 0.03) and “soil PC 2” (GLM: y’,

= 6.82, P = 0.009) (Table 3). This model suggested that

the likelihood of Wood Turtles using habitat increased

when there was a high amount of small gravel and sand

along with lower amounts of large gravel and clay. Turtles

were more likely to use habitat with high values of “soil

PC 1,” which corresponded to minimal amounts of large

gravel and a higher amount of sand in addition to small

gravel and clay. The second-best model contained the

explanatory variable “soil PC 2.” This model indicated

that there was a higher probability of use when there was

a high amount of small gravel and no clay present.

The presence of a slope, which ranged from 7—50°,

was the most significant predictor variable of nesting

habitat selection for the landscape subset of models

(GLM: y= 5.63, P = 0.01) (Table 4). The use of nesting

habitat was reduced when zero slope was present. The

second-best model contained the explanatory variables

“slope” and “vegetation.” Slope in combination with

herbaceous vegetation resulted in a higher likelihood of

Wood Turtles selecting for that particular habitat. The

turtles were least likely to select nesting habitat with no

vegetation or slope present.

Comparisons of Disturbed and Protected Sites

Soil composition and moisture. In the overall

comparison between selected nest habitat at the disturbed

and protected nest sites, soil composition and moisture

principal component variables were _ significantly

different (¢ = 3.72, df = 15, P = 0.002). The principal

component variable revealed that at the protected site,

turtles were more likely to select sandy habitat with

Amphib. Reptile Conserv.

Table 6. Loading matrix from a Principal Component Analysis

(PCA) of five microhabitat variables measured at N = 10

disturbed Wood Turtle nest sites and N = 7 protected Wood

Turtle nest sites.

Covariate PC1 PC2

Large gravel -0.94 0.0019

Small gravel -0.78 0.34

Sand 0.97 -0.21

Clay 0.45 -0.76

Moisture 0.70 0.58

a higher amount of moisture and clay and no gravel

compared to the disturbed site. At the disturbed site, the

nests had more small gravel and less moisture and clay.

Temperature. The maximum temperature was also

significantly different between the disturbed and protected

field sites (t = 7.04, df = 12, P = 0.001). Although the

disturbed site had lower nest temperatures during the

morning hours, there was a higher maximum temperature

with an average of 35 °C compared to the protected site

with an average maximum temperature of 28 °C. The

minimum average temperatures at the disturbed and

protected sites were 15 °C and 19 °C, respectively (¢

= -3.42, df = 12, P = 0.005), which did not reach the

threshold for a statistically significant difference after

Bonferroni correction. The average temperatures were

24 °C at the disturbed site and 22 °C at the protected site

(¢ = 2.70, df= 12, P =0.019).

Landscape features. Since the amounts of canopy and

vegetation nest cover were low at both the disturbed and

protected sites, there was no significant difference in

canopy cover (7 = 0.62, df = 1, P = 0.43) or vegetation

nest cover (7 = 0.31, df= 1, P=0.58). The turtles at both

sites selected for bare nesting ground with no vegetation

present (x? = 7.28, df = 3, P = 0.06). The average slopes

for the nests at the disturbed and protected sites were

13.40° and 14.17°, respectively (¢ = -0.16, df= 17, P=

0.87). Distance of vegetation from each nest site averaged

15.24 cm for the disturbed site and 22.86 cm for the

protected site (¢ = -0.74, df = 14, P = 0.47). The turtles

at both the disturbed and protected sites nested on the

floodplains or close to a water source (t = -0.11, df = 17,

P=0.91). Although the maximum distance to the nearest

water from nests was 69 m at the protected site and 24

m at the disturbed site, the average at the protected site,

including two outlier nests, was 20 m (+ 11.16) compared

to 4 m (+ 1.4) at the disturbed site.

Discussion

Wood Turtles are known to select nesting habitat that

is open, slightly sloped, and well-drained (Walde et al.

2007; Hughes et al. 2009), which the results presented

here supported. Nest site selection at the disturbed site

was nonrandom based on microhabitat characteristics.

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Vik et al.

Both disturbed and protected nest sites consisted of open

canopy, sandy patches, and little or no vegetation.

Soil composition. The soil composition appeared to be

one of the most important factors when selecting nest

habitat at the disturbed site. The turtles preferred to

nest in soil that was primarily composed of sand, with

some small gravel and clay but limited large gravel. This

pattern is most likely related to thermoregulation and

drainage because sandy soils warm up more quickly in

the sun and do not hold water as well as soils rich in

organic substrates (Brady and Weil 2002).

At both field sites, females selected nesting areas

based on the same microhabitat characteristics. However,

the selected nest habitat differed in soil composition

between the disturbed and protected sites. Due to the

absence of random points at the protected field site, it 1s

not clear whether this difference represents differences

in nesting preferences between the two turtle populations

or differences in soil composition between the two sites.

While turtles in both sites nested in sandy habitats, the

female turtles at the protected nest site selected for higher

moisture content with no gravel.

Temperature. Although temperature was not a significant

predictor of nest site selection in the disturbed habitat,

other literature has shown its importance in nest selection

in various turtle species (Compton 1999; Hewavisenthi

and Parmenter 2002; Hughes et al. 2009). There was a

significant difference in the maximum temperature of nest

sites between the two sites. Overall, the disturbed site had

warmer nest temperatures. Compton (1999) suggested that

in the northern portion of the Wood Turtle’s range, finding

nest sites that encourage successful hatchling incubation

is critical. To increase development rate, the Wood Turtles

in the northern range select for warm and variable nest

temperatures rather than a narrow temperature range

(Compton 1999; Hughes et al. 2009), which was seen in

the disturbed nest site in this study. The disturbed site had

lower nest temperatures during the morning hours as well,

causing high temperature variation, which may promote

shorter incubation periods (Hughes 2009). Although

northern Wood Turtle populations are known to select

for warm nest temperature, a maximum temperature of

35°C at the disturbed site may potentially be harmful to

hatchlings by decreasing their survival rate. In some

cases, embryonic mortality of nests may increase with

high incubation temperatures (Matsuzawa et al. 2002:

Hawkes et al. 2007; Maulany et al. 2012). For example,

a study found that by incubating freshwater Mary River

Turtle (E/usor macrurus) eggs at 32 °C, hatchling

success was lower (Micheli-Campbell et al. 2011); and

the same was true for Chinese Three-keeled Pond Turtle

(Chinemys reevesii) eggs exposed to temperatures above

32 °C (Du et al. 2007).

Amphib. Reptile Conserv.

Landscape features. Wood turtles at both sites selected

for slightly sloped habitat. Many turtle species use slope

as an environmental nesting cue (Schwarzkopf and

Brooks 1987; Horrocks and Scott 1991). Slope may

reflect a change in elevation making it an important cue

(Horrocks and Scott 1991). A change to a greater slope

could indicate that the turtle has reached an elevation that

increases the probability of hatching success for her nest

(Wood and Bjorndal 2000).

At the disturbed site, 42% of the turtles selected nest

sites with no vegetation, while 58% chose nests near

small herbaceous plants. The most common plants the

turtles nested next to were Spotted Knapweed (Centaurea

stoebe) and Common Lady’s Thumbprint (Persicaria

pensylvanica). Nesting near herbaceous vegetation may

be advantageous if it provides a concealing structure for

females without shading the nest (Harding and Bloomer

1979; Hughes et al. 2009). The herbaceous root system

may also help prevent slope erosion caused by rainfall

(Buhlmann and Osborn 2011). Alternatively, vegetation

can have a negative impact on the nests due to root

invasion and reduced sunlight exposure, leading to egg

mortality (Congdon et al. 2000; Behler and Castellano

2005). Root invasion and shading were common problems

at the disturbed site, especially as the vegetation grew.

Anthropogenic nest sites. It is common for Wood Turtles

to use anthropogenic nest sites, such as agricultural fields,

yards, clear-cuts, railway embankments, and roadsides

(Congdon et al. 2000; Saumure et al. 2007). Although

human-impacted nesting sites may provide appropriate

canopy openings, this disturbed habitat can negatively

affect the turtles (Kolbe and Janzen 2002). Nesting

in an anthropogenic site increases the probabilities of

nests being walked on, predation, collecting, mortality

associated with crossing roads, shading and/or root

invasion by invasive plant species (Garber and Burger

1995). In addition, anthropogenic disturbances could

cause Wood Turtles to delay nesting and/or to nest

in unfavorable habitat since this species is extremely

sensitive to disturbance prior to egg laying (Walde et al.

2007). Turtle use of human impacted areas, however,

indicates that conservation measures can be taken to

mitigate such negative effects. Artificial nesting mounds

could be built that enhance nesting success (Beaudry

et al. 2010). If actively managed, these mounds could

potentially reduce exposure to many of the common

threats that nesting females face (Buhlmann and Osborn

2011).

Conclusions

Because Wood Turtles are long-lived organisms with

delayed sexual maturity, populations may require a

long time to recover; and so conservation biologists

seeking to manage them face a pressing challenge in

August 2021 | Volume 15 | Number 2 | e283

Nesting ecology of Glyptemys insculpta

a world that is undergoing rapid changes (Garber and

Burger 1995; Kolbe and Janzen 2002). Thus, efforts to

understand what effects human impacts have on Wood

Turtle nesting habitat and population dynamics 1s

crucial. It is also important to recognize which factors

contribute to suitable Wood Turtle nesting habitat for the

persistence and conservation of this species (Kolbe and

Janzen 2002). To help protect this Endangered turtle, our

research provides data that identifies the microhabitat

variables Wood Turtles are selecting for in a nest habitat.

Future studies should include a “false nest” subset, 1.e.,

nests constructed by the female but then abandoned.

This might provide more evidence as to what habitat

the female is actively selecting for and/or rejecting,

which could improve our ability to protect or construct

appropriate nesting habitat for this Endangered species.

Acknowledgments.—Alexander Robillard provided

knowledge, comments, and guidance during this project.

We thank Hannah Harby and Timothy Gochenour for

their field contributions and photography. Previous drafts

of this manuscript were reviewed by Donna Vogler, Sean

Robinson, Jeffrey Heilveil, and Russell Burke. Funding

for this work was supported by Hudson River Foundation

(79063, 2017), Western New York Herpetological

Society (80415, 2018), Riverbanks Society (79530,

2017), International Herpetological Symposium (79454,

2017), American Wildlife Conservation Fund (77108,

2017), and Rhode Island Zoological Society (80007,

2017). All procedures were reviewed and approved by

the SUNY Oneonta Institutional Animal Care and Use

Committee (IACUC) and DEC (DEC Scientific permit

#2136 and IACUC #2018-25).

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Alexandra VIk obtained her M.S. in Biology from State University of New York-College at

Oneonta. She has a B.S. in Biology from James Madison University (Harrisonburg, Virginia,

USA), with a concentration in Ecology and Environmental Studies. Her research interests lie in

reproductive behavior and how anthropogenic disturbances are affecting wildlife. She now teaches

molecular biology and the scientific method at Randolph-Macon College (Ashland, Virginia, USA).

Elizabeth Bastiaans is a professor at State University of New York-College at Oneonta. She

completed her B.A. at the University of Chicago (Chicago, Illinois, USA), her Ph.D. at the University

of California, Santa Cruz, and a postdoctoral fellowship at the University of Minnesota, Twin Cities

(Minneapolis-St. Paul, Minnesota, USA). Elizabeth’s previous research focused on sexual signal

evolution in Mexican montane lizards and life history evolution in tropical crickets. In this work,

she used methods such as capture-mark-recapture studies, mate choice trials, aggression trials,

maintenance of lizards in captivity, spatial analyses, DNA sequencing, and molecular phylogenetics.

As a postdoctoral fellow at the University of Minnesota, Elizabeth studied the reproductive behavior,

life history, and immune physiology of Pacific Field Crickets (7eleogryllus oceanicus).

Daniel Stich is a professor at State University of New York-College at Oneonta. He earned his B.T.

in Fisheries and Aquaculture at the State University of New York, Cobleskill College of Agriculture

and Technology, an MLS. in Fish and Wildlife Conservation at the Virginia Polytechnic Institute and

State University (Blacksburg, Virginia, USA), and a Ph.D. in Wildlife Ecology at the University of

Maine (Orono, Maine, USA). He previously worked with NOAA Fisheries as a contracted fishery

biologist studying the effects of dam passage performance standards and lake connectivity on

alosines (shad and herring) in the Northeast, and continues to collaborate with federal agencies

on related issues. Daniel uses data-driven approaches to answer questions about a wide range of

species and topics that range in breadth from physiology of individual organisms to population-

level responses to management actions. These approaches make use of modern quantitative and

computer-based modeling techniques to address complex problems faced by both local and regional

resource managers, and are extensively supplemented by field and laboratory research.

Donna Vogler was born and educated in the Midwestern United States, with a B.S. from The Ohio

State University (Columbus, Ohio, USA), and an M.S. from Iowa State University (Ames, Iowa,

USA), before working for the U.S. Fish and Wildlife Service in Washington, DC, USA. Donna

earned a Ph.D. from Pennsylvania State University (University Park, Pennsylvania, USA) in

Botany, and was a postdoctoral researcher at the University of Pittsburgh (Pittsburgh, Pennsylvania,

USA) before joining the SUNY-Oneonta faculty in 2000. Donna’s recent research topics include

demographic studies of invasive plant species (e.g., Marsh Thistle, Cirsium palustre), floral

mechanisms related to self vs. outcross pollination, and using Wood Turtle habitat communities and

vegetation management at regional airports to reduce wildlife hazards.

Amphib. Reptile Conserv.

August 2021 | Volume 15 | Number 2 | e283

Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

15(2) [General Section]: 59-71 (e284).

Herpetofauna of Marechal Newton Cavalcanti Instruction

Center, a hotspot Atlantic Forest fragment in Pernambuco,

north-eastern Brazil

Leonardo P.C. Oitaven, Danilo S. Barreto, Mariana M. de Assungao, José R. de O. Santos,

Alan P. Araujo, *Geraldo J.B. de Moura

Laboratorio de Estudos Herpetologicos e Paleoherpetologicos, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n,

Dois Irmdos, CEP 52171-900, Recife, Pernambuco, BRAZIL

Abstract.—Determining the richness and composition of species in an area provides indispensable information

for understanding their natural history, habitat requirements, and other ecological interactions; in addition to

improving our knowledge of their geographic distributions and a better understanding of their ecophysiological

restrictions. The development of strategies that reconcile human population growth with biodiversity

conservation is a current challenge for humanity, especially in areas with exceptionally high historical rates

of destruction, such as the Atlantic Forest. This work contributes to our understanding of the biodiversity of

the Atlantic Forest in the state of Pernambuco, Brazil, by documenting the anuran and reptile species found

in the largest Atlantic Forest remnant in the state: the Integral Conservation Protection Rainforest Unit of

the Marechal Newton Cavalcanti Instruction Centre (CMINIC). Sampling was carried out between August 2008

and December 2009, and a total of 83 species were recorded, including 30 anuran amphibians and 53 reptiles

(three testudines, 19 lizards, two amphisbaenians, 27 snakes, and two crocodilians). Most of the species that

were recorded are widely distributed in the Atlantic Forest, although at the state, national and international

levels, three of the anurans (10%) and four of the reptiles (7.5%) are in the threatened conservation status

classifications. The occurrence of species listed on national and state lists in categories representing critically

endangered, endangered, and vulnerable status in this region reinforces the need for conservation actions, and

the necessity of obtaining better knowledge about the area, which continues to be poorly studied even today.

Keywords. Lissamphibia, Sauropsida, richness, diversity, herpetology, South America

Citation: Oitaven LPC, Barreto DS, de Assungao MM, Santos JRO, Araujo AP, de Moura GJB. 2021. Herpetofauna of Marechal Newton Cavalcanti

Instruction Center, a hotspot Atlantic Forest fragment in Pernambuco, north-eastern Brazil. Amphibian & Reptile Conservation 15(2) [General Section]:

59-71 (e284).

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: 30 October 2020; Published: 26 August 2021

Introduction

The production of updated lists which detail the richness

and composition of the species in an area are indispensable

for studying diversity, ecosystem compositions, and

Species distributions (Pedrosa et al. 2014; Freitas et

al. 2017). Moreover, such lists are indispensable for

developing conservation initiatives, because they provide

not only present-day information, but also historic

information on the species composition of an area in a past

state of preservation (Freitas et al. 2017). The accumulated

information brings together records of the occurrence (or

disappearance) of species, as well as the occurrence of

Species 1n various threat status categories, in areas that may

have undergone changes due to anthropogenic degradation,

climate shifts, or other modifications (Pedrosa et al. 2014).

Correspondence. “geraldo.jbmoura@ufrpe.br

Amphib. Reptile Conserv.

Through documenting biodiversity, researchers can

contribute to the development of effective management

plans for the conservation of individual species, as well

as the ecosystems they inhabit (Dixo and Verdade 2006;

Pereira et al. 2015). This is particularly important for

the Atlantic Forest biome which has been extensively

degraded since the period of Brazilian colonization

(Dixo and Verdade 2006; Palmeira and Goncalves

2015). As a result of human population growth, the

forest fragments are highly exposed to predators and

the anthropogenic degradation of fauna and flora, as

well as soil and water pollution (Dixo and Verdade

2006). This situation makes the knowledge of the

fauna from this ecosystem a top priority for creating

conservation plans (Condez et al. 2009; Palmeira and

Goncalves 2015).

August 2021 | Volume 15 | Number 2 | e284

Herpetofauna in an Atlantic Forest hotspot in Brazil

The Atlantic Forest biome is known to harbor a high

richness of anurans (530 species, or 53.6% of the anuran

species in Brazil, Santos et al. 2016; Costa and Beérnils

2018) and reptiles (200 species, or 23.7% of reptile

species in Brazil, Palmeira and Gongalves 2015; Costa

and Bérnils 2018). This diversity has been attributed to

the great variety of habitats and microhabitats in this

domain, which also favor a number of specialist species,

as well as endemics (Condez et al. 2009; Palmeira and

Gongalves 2015). This work contributes to our knowledge

of the biodiversity in the Atlantic Forest of Pernambuco,

by providing a list of the anurans and reptiles found in the

largest Atlantic Forest remnant in the state, the Integral

Conservation Protection Rainforest Unit of the Marechal

Newton Cavalcanti Instruction Center (CMINIC).

Materials and Methods

Study area. This study was conducted at the Marechal

Newton Cavalcanti Instruction Center (CIMNC;:

7.8312°S, 35.1033°W), which is the largest Atlantic

Forest fragment of the mesoregion in the rainforest

region of the state of Pernambuco, northeastern Brazil

(Guimaraes 2008; Lucena 2009). It encompasses a

total area of 7,342 ha, including the cities of Aracgoiaba,

Paulista, Igarassu, Paudalho, and Tracunhaem (Lucena

2009), and is approximately 42 km from the state capital

of Recife (Fig. 1). Itis mostly characterized by a relatively

homogeneous conservation state, composed of secondary

forests with medium-to-advanced stages of regeneration,

with some parts of the area also showing traces of initial

regeneration and recent disturbance (Guimaraes 2008).

The relief in the region is strongly undulating, and

the elevation ranges from 60 to 254 m asl. The climate

is tropical with dry summers and an average annual

temperature of 25.2 °C. The rainy season begins in

February and ends in October, with an average annual

rainfall of 1,634 mm (Guimaraes 2008).

Field sampling. Sampling efforts were carried out

from August 2008 through December 2009, totaling

one year and five months of uninterrupted sampling.

Three different sampling strategies were employed:

a passive method through pitfall traps (Condez et al.

2009); active searches limited by time; and searches by

third parties (1.e., by locals). These three complementary

methods were used in order to maximize the diversity

of species encountered (Condez et al. 2009; Palmeira

and Gongalves 2015). The naming of species on the list

follows Amphibian Species of the World 6.0, an Online

Reference (Frost 2019) and Costa and Bérnils (2018).

Specimens were collected under a scientific permit

issued by IBAMA/RAN (088/07).

For pitfall samplings, a total of two trap lines were

installed, each composed of ten 60-L buckets, interconnected

by 110 m of a 50 cm-high fence, which remained active for

518 days (August 2008 through December 2009), for a total

sampling effort of 10.360 d/bucket. The active searches

were conducted from August 2008 through December

2009, for a total of 24 searches, each one being 9 h in

duration. These were divided into three stages of 3 h each

at nightfall (1600-1900 h), at night (2000-2300 h), and at

dawn (0430-0730 h), and were always conducted by three

collectors, totaling a sampling effort of 648 person-h.

42 40 38 6 4M 32 3

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Fig. 1. Atlantic Forest fragment of Marechal Newton Cavalcanti Instruction Center (CIMNIC), Pernambuco, Northeastern Brazil. A

few other Ecological Reserves located in Pernambuco State, as well as other states in Northeastern Brazil, are also shown.

Amphib. Reptile Conserv.

August 2021 | Volume 15 | Number 2 | e284

Oitaven et al.

gyrinaethes (Peixoto, Caramaschi, and Freire, 2003); (B) Phyllodytes edelmoi (Peixoto, Caramaschi, and Freire, 2003); (C)

Phyllodytes luteolus (Wied-Neuwied, 1824); (D) Pristimantis ramagii (Boulenger, 1888); (E) Pithecopus nordestinus (Caramaschi,

2006); (F) Dendropsophus elegans (Wied-Neuwied, 1824); (G) Scinax cretatus (Nunes and Pombal, 2011); (H) Scinax eurydice

(Bokermann, 1968); (1) Scinax x-signatus (Spix, 1824); (J) Dermatonotus muelleri (Boettger, 1885); (IX) Elachistocleis ovalis

(Schneider, 1799); (L) Stereocyclops incrassatus (Cope, 1870). Photos: M.A. Freitas.

One specimen of each species was collected and

euthanized with lidocaine application to the ventral region

(anuran) or intramuscular ketamine injections (reptiles).

The specimens were fixed in 10% formaldehyde, and

later preserved in 70% ethanol. All of the collected

specimens were deposited at the UFRPE (Universidade

Federal Rural de Pernambuco) herpetological and

paleoherpetological collection, although for some species

only visual and photographic records were obtained. The

species conservation status categories were determined

using the classification of the International Union for

Conservation Nature Red List of Threatened Species

(IUCN 2017) as well the Brazilian National (MMA

2014) and Pernambuco State lists (SEMAS 2015, 2017)

Amphib. Reptile Conserv.

of threatened amphibian and reptile classifications.

The information on these lists has been combined into

a comprehensive list at the laboratory’s website (LEHP

2018). When collections were only obtained from third

parties, or represent just one individual captured for a

species without accounting, the data were insufficient to

generate a reliable sampling curve.

Results

In total, 30 anuran amphibians and 53 reptile species were

recorded, which included three testudines, 27 snakes, 19

lizards, two amphisbaenians, and two crocodilians (Figs.

2-6).

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Herpetofauna in an Atlantic Forest hotspot in Brazil

2 et

tl ;

Fig. 3. Additional anuran species found in the Marechal Newton Cavalcanti Instruction Center Atlantic Forest fragment. (A) Boana

crepitans (Wied-Neuwied, 1824); (B) Leptodactylus troglodytes (A. Lutz, 1926); (C) Leptodactylus natalensis (A. Lutz, 1930); (D)

Dendropsophus branneri (Cochran, 1948); (E) Boana faber (Wied-Neuwied, 1821); (F) Boana raniceps (Cope, 1862); (G) Boana

semilineatus (Spix, 1824); (H) Boana albomarginatus (Spix, 1824); (I) Leptodactylus latrans (Linneaus, 1758); (J) Leptodactylus

marmoratus (Steindachner, 1867); (IX) Leptodactylus mystacinus (Burmeister, 1861); (L) Leptodactylus fuscus (Schneider, 1799);

(M) Leptodactylus vastus (A. Lutz, 1930); (N) Physalaemus cuvieri (Cruz and Pimenta, 2004); (0) Dendropsophus haddadi (Bastos

and Pombal, 1996); (P) Dendropsophus minutus (Peters, 1872). Photos: M.A. Freitas.

Regarding the conservation status of the reported and 45 (85%) were LC (Table 1; MMA 2014; SEMAS

anuran species for the roughly comparable categories at 2015, 2017; IUCN 2017; LEHP 2018).

the three levels (state, national, and international), three With respect to the sampling methods, 67 species were

(10%, Phyllodytes acuminatus, Phyllodytes edelmoi, collected by active search, 33 by passive search, and 24 by

and Phyllodytes gyrinaethes) were in the threatened _ third parties (Table 1). All anuran species were collected

categories, one (3.3%) was Near Threatened (NT), three —_ by active search, with 18 collected only by active search,

(10%) were Data Deficient (DD), and 23 (76.7%) were — while the remaining 12 species were collected by both

Least Concern (LC). Among reptiles, four species were __ passive and active searches. For lizards, 11 species were

threatened (7.5%, two lizards, Strobilurus torquatus collected through active searching exclusively, while

and Cercosaura ocellata, and two snakes, Siphlophis — eight species were also captured by passive search.

compressus and Lachesis muta), four (7.5%) were DD __ Testudines were not collected by active search, with one

Amphib. Reptile Conserv. 62 August 2021 | Volume 15 | Number 2 | e284

Oitaven et al.

Table 1. Herpetofauna recorded between August 2008 and December 2009 at Marechal Newton Cavalcanti Instruction Center,

Pernambuco, Northeastern Brazil. Type of record: CP = Passive collection; CA = Active collection; CT = Collected by third parties;

Conservation status codes listed below for either the international, national or state levels: LC = limited concern; DD = insufficient

data; NA = not evaluated; NT = near threatened; CT = critically threatened; EN = endangered; VU = vulnerable.

Sampling

Conservation status method

International

Taxon Voucher (IUCN) National State CA CP CT

Amphibia: Anura

Craugastoridae

Pristimantis ramagii (Boulenger, 1888) 0591-0592 LC LC Le xX

Hylidae

Dendropsophus branneri (Cochran, 1948) 0593 Le LC LC xX

Dendropsophus elegans (Wied-Neuwied, 1824) 3466 EC LE LC xX

Dendropsophus haddadi (Bastos and Pombal, 1996) VR LG Le he x

Dendropsophus minutus (Peters, 1872) 2495 LC LC LC xX

Boana albomarginatus (Spix, 1824) 2496 LG Le LE xX

Boana crepitans (Wied-Neuwied, 1824) 3789 Le LC Ee x

Boana faber (Wied-Neuwied, 1821) VR EC Re. Le x

Boana raniceps (Cope, 1862) 3451-3452 LG Le he xX

Boana semilineatus (Spix, 1824) 3596 LC LC Le x

Phyllodytes acuminatus (Bokermann, 1966) VR LG Le EN x

Phyllodytes edelmoi (Peixoto, Caramaschi, and Freire, 2003) VR DD NT EN xX

Phyllodytes gyrinaethes (Peixoto, Caramaschi, and Freire, 2003) VR DD CR EN xX

Phyllodytes luteolus (Wied-Neuwied, 1824) VR LC |b LC x

Pithecopus nordestinus (Caramaschi, 2006) 2546-2547 DD Le Le x

Scinax cretatus (Nunes and Pombal, 2011) VR Le Le LC x

Scinax eurydice (Bokermann, 1968) 3477-3478 Le LC Ee x

Scinax x-signatus (Spix, 1824) 2552-2553 LC RE. Le xX

Leptodactylidae

Physalaemus cuvieri (Cruz and Pimenta, 2004) 3401-3402 LC LC Le x xX

Leptodactylus fuscus (Schneider, 1799) 3556-3557 LG Le Le x x

Leptodactylus marmoratus (Steindachner, 1867) 3568 Le Le Le xX x

Leptodactylus mystacinus (Burmeister, 1861) VR LC |G Le x x

Leptodactylus natalensis (A. Lutz, 1930) 2651 LC |b LC x x

Leptodactylus latrans (Linneaus, 1758) 0840 LC LC VG x x

Leptodactylus troglodytes (A. Lutz, 1926) VR Le Le Le x x

Leptodactylus vastus (A. Lutz, 1930) 1328 Le LC jh oe x x

Mycrohylidae

Dermatonotus muelleri (Boettger, 1885) 3542 LC LC LC x x

Elachistocleis ovalis (Schneider, 1799) VR LC LC LC x x

Stereocyclops incrassatus (Cope, 1870) 0588-0590 Le Le LC x xX

Ranidae

Lithobates palmipes (Spx, 1824) 0852 UC LE LC x xX

Reptilia: Testudines

Knosternidae

Kinosternon scorpioides (Linneaus, 1766) VR Le Le Le x x

Mesoclemmys tuberculata (Ltiederwalt, 1926) VR NA LC Le x

Phrynops geoffroanus (Schweigger, 1812) VR NA Le. LC x xX

Amphib. Reptile Conserv. 63 August 2021 | Volume 15 | Number 2 | e284

Herpetofauna in an Atlantic Forest hotspot in Brazil

Table 1 (continued). Herpetofauna recorded between August 2008 and December 2009 at Marechal Newton Cavalcanti Instruction

Center, Pernambuco, Northeastern Brazil. Type of record: CP = Passive collection; CA = Active collection; CT = Collected by third

parties; Conservation status codes listed below for either the international, national or state levels: LC = limited concern; DD =

insufficient data; NA = not evaluated; NT = near threatened; CT = critically threatened; EN = endangered; VU = vulnerable.

Sampling

Conservation status method

International

Taxon Voucher (IUCN) National State CA CP CT

Reptilia: Squamata (lacertids)

Leiosauridae

Enyalius catenatus (Wied-Neuwied, 1821) VR Le Le LC x

Phyllodactylidae

Gymnodactylus darwinii (Gray, 1845) 0587 Le LC 1 x x

Dactyloidae

Norops fuscoauratus (D'Orbigny, 1837) VR LC LC LC xX

Norops punctatus (Daudin, 1802) 0567 LG LC Le xX

Tropiduridae

Tropidurus hispidus (Spix, 1825) 3600 LC LC LC xX

Tropidurus semitaeniatus (Spix, 1825) VR LG LC ie xX

Strobilurus torquatus (Wiegmann, 1834) VR Le Le VU xX

Teiidae

Ameiva ameiva (Linneaus, 1758) VR LC LC LC x xX

Ameivula ocellifera (Spix, 1825) 2540 LC LC LC xX x

Kentropyx calcarata (Spix, 1825) 0694 LC LC LC x x

Salvator merianae (Dumeril and Bibron,1839) VR LC Le LC x

Gymnophythalmidae

Acratosaura mentalis (Amaral, 1933) VR LC LC LC x x

SoHo i caeoya eT Xavier Freire, Machado VR LC LC LC x x

Cercosaura ocellata (Wagler, 1830) VR LC LG. VU x x

Gekkonidae

Hemidactylus mabouia (Moreau de Jonnés, 1818) VR LC Le LC x

Iguanidae

Iguana iguana (Linneaus, 1758) 0831 LG Le LC xX

Polychrotidae

Polychrus acutirostris (Spix, 1825) VR LC Le Ee x

Polychrus marmoratus (Linneaus, 1758) VR LC Ee LC x

Coleodactylus meridionalis (Boulenger, 1888) 2865, 2869 LC LE Le x x

Reptilia: Squamata (Amphisbaenians)

Amphisbenidae

Amphisbaena alba (Liennaeus, 1758) VR LC Le Le x x

Amphisbaena vermiculares (Wagler, 1824) 4468 NA Le | xX x

Reptilia: Squamata (snakes)

Boidae

Boa constrictor (Linneaus, 1758) VR NA LC Le xX

Epicrates cenchria (Linneaus, 1758) VR NA Le LC x xX

Colubridae

Chironius flavolineatus (Jan, 1863) 0549 NA LE Le x

Dendrophidion atlantica (Freire, Caramaschi, and Gongalves, 2010) 0546 NA LC NA x x

Spilotes pullatus (Linneaus, 1758) 0554 NA Le LC x x

Tantilla melanocephala (Linneaus, 1758) 0547 NA Le LC x x

Amphib. Reptile Conserv. 64 August 2021 | Volume 15 | Number 2 | e284

Oitaven et al.

Table 1 (continued). Herpetofauna recorded between August 2008 and December 2009 at Marechal Newton Cavalcanti Instruction

Center, Pernambuco, Northeastern Brazil. Type of record: CP = Passive collection; CA = Active collection; CT = Collected by third

parties; Conservation status codes listed below for either the international, national or state levels: LC = limited concern; DD =

insufficient data; NA = not evaluated; NT = near threatened; CT = critically threatened; EN = endangered; VU = vulnerable.

Sampling

Conservation status method

International

Taxon Voucher (IUCN) National State CA CP CT

Dipsadidae

Boiruna sertaneja (Zaher, 1996) VR NA 1 Le x x x

Erythrolamprus almadensis (Wagler, 1824) VR NA LC LC x

Erythrolamprus poecilogyrus (Wied-Neuwied, 1825) 4466 NA LE LC x

Erythrolamprus viridis (Wagler, 1824) 0564, 0566 Le Le Ee x

Helicops angulatus (Linneaus, 1758) VR NA LC LC xX

Oxybelis aeneus (Wagler, 1824) 4969 NA LC LC x

Oxyrhopus petolarius (Linneaus, 1758) 4492 NA Le LC xX

Oxyrhopus trigeminus (Dumeéril, Bibron, and Dumeril, 1854) 0552 NA Le Le x x x

Philodryas olferssi (Lichtenstein, 1823) VR NA LG. Le x x

Philodryas patagoniensis (Girard, 1825) 0556 NA Le Le x

Sibon nebulatus (Linneaus, 1758) 0553 NA Le NA x

Sibynomorphus neuwiedi (Ihering, 1911) 0550 NA Le LE x x x

Siphlophis compressus (Daudin, 1803) 0565 LC Le VU xX

Thamnodynastes pallidus (Linneaus, 1758) 0548 LC Le LC xX

Xenodon merremii (Wagler, 1824) 0555 NA Le LC x

Elapidae

Micrurus ibiboboca (Merrem, 1820) 0560-0562 NA Le DD x x

Micrurus leminiscatus (Linneaus, 1758) VR NA LC DD xX xX

oe eat bre oe Jr. Feitosa, Costa-Prudente, 0563 NA LC DD x x

Typhlopidae

Amerotyphlops brongersmianus (Vanzolini, 1976) VR NA LC LC x

Viperidae

Crotalus durissus (Linneaus, 1758) 0558 LC Le i x x x

Lachesis muta (Linneaus, 1766) 0559 NA LC VU xX

Reptilia: Crocodylia

Alligatoridae

Caiman latirostres (Daudin, 1802) VR NA Le Le. x x

Paleosuchus palpebrosus (Cuvier, 1807) VR Le. Le DD x x

Total 68 33 24

species exclusively captured using a specifictrap(funnel Discussion

trap), and the other two captured by funnel traps and

third parties. For crocodilians and amphisbaenians, the

traps did not prove to be an adequate collection method,

with all four species captured by active search or third

parties. The snake species showed the greatest variation

in method suitability. Of the 27 snake species, four

were captured by all three methods, while three species

were found by passive search, five by active search, and

seven by third parties. Eight of the snake species were

collected using at least two of the collecting methods

(Fig. 7).

Amphib. Reptile Conserv.

To the best of our knowledge, this study represents the

first initiative to catalog the diversity of herpetofauna in

the CMNIC area. Several other studies in similar Atlantic

Forest remnants (by biome and phytophysiognomy),

which covered the same seasons and had similar sample

efforts, reported less richness (Fig. 1). These studies

were conducted in Serra do Urubt (69 species; 8.5666°S,

35.6166°W; 207 km from our study site; Roberto

et al. 2017), Mata do Junco (59 species; 10.5416°S,

37.0583°W; 649 km from our study site; Morato et al.

August 2021 | Volume 15 | Number 2 | e284

Herpetofauna in an Atlantic Forest hotspot in Brazil

act

a) ee

2011), Gurjau Ecological Reserve (62 species; 8.2291°S,

35.0597°W; 77 km from our study site; Santos et al.

2016; Silva et al. 2017), and Mata do Buraquinho (51

species; 7.145°S, 34.865°W; 110 km from our study site;

Santana et al. 2008). However, at these study sites, the

thinning curves were not stabilized, which indicates that

the diversity could have been even higher.

Based on the inventories published for the Brazil

Northeast Atlantic Forest, the richness of the anurans

and reptiles shows great diversity in various remnants

of this ecosystem (Palmeira and Gongalves 2015; Santos

et al. 2016). In conjunction with the intrinsic aspects of

the biological potential of the locality (i.e., microclimate,

succession history, etc.), the reported richness also

depends on methodological aspects, such as capture

Amphib. Reptile Conserv.

Fig. 4. Testudines, amphisbaenians, and crocodilians found in the Marechal Newton Cavalcanti Instruction Center Atlantic Forest

fragment. (A) Phrynops geoffroanus (Schweigger, 1812); (B) Kinosternon scorpioides (Linneaus, 1766); (C) Mesoclemmys

tuberculata (Luederwalt, 1926); (D) Amphisbaena vermiculares (Wagler, 1824), (E) Amphisbaena alba (Liennaeus, 1758); (F)

Caiman latirostris (Daudin, 1802); (G) Paleosuchus palpebrosus (Cuvier, 1807). Photos: M.A. Freitas.

strategies and sampling effort. The data reported here

suggests that this area 1s important for conservation, due

to the high representation of the species richness (214

sp.) in the state (38.8%) (Martins-Sobrinho et al. 2016;

SEMAS 2015). Most of the recorded species (74.6%) are

widely distributed in the Atlantic Forest (Dias et al. 2014;

Palmeira and Gongalves 2015; Roberto et al. 2017), as

well as other domains (Pedrosa et al. 2014). However,

some of the species reported locally in this study, 10% of

anurans and 7.5% of reptiles, represent some threatened

status categories, reinforcing the need for conservation

actions in this region.

Considering the sampling methods, this study revealed

that all of the methods used were complementary, being

affected by several factors such as species habits (Freitas

August 2021 | Volume 15 | Number 2 | e284

Oitaven et al.

! ne Bad

Fig. 5. Lac

ertid species found in the Marechal Newton Cavalcanti Instruction Center Atlantic Forest fragment. (A) Enyalius catenatus

(Wied-Neuwied, 1821); (B) Gymnodactylus aff. darwinii (Gray, 1845); (C) Norops fuscoauratus (D'Orbigny, 1837); (D) Tropidurus

hispidus (Spix, 1825); (E) Tropidurus semitaeniatus (Spix, 1825); (F) Ameiva ameiva (Linneaus, 1758); (G) Ameivula ocellifera

(Spix, 1825); (H) Salvator merianae (Dumeril and Bibron, 1839); (I) Kentropyx calcarata (Spix, 1825); (J) Cercosaura ocellata

(Weagler, 1830); (IK) Hemidactylus mabouia (Moreau de Jonnés, 1818); (L) Jguana iguana (Linneaus, 1758); (M) Coleodactylus

meridionalis (Boulenger, 1888); (N) Polychrus marmoratus (Linneaus, 1758); (O) Strobilurus torquatus (Wiegmann, 1834).

Photos: M.A. Freitas.

et al. 2017). Pit traps are very useful in the Atlantic Forest

due to the rarity of some of the species. In addition,

some of the places are difficult to access, especially

for terrestrial and fossorial species such as those in

the families Microhylidae (Crump and Scott 1994),

Gymnophytalmidae (Garda et al. 2014), and Elapidae

Amphib. Reptile Conserv.

(Viana and Mendes 2015). The active search represents

a good method for sampling species with arboreal habits

(Mesquita et al. 2015), large size (Pedrosa et al. 2014), or

species-specific vocalizations (Crump and Scott 1994).

Due to the aquatic habitat and difficult conditions for

visualizing the individuals through the water, the passive

August 2021 | Volume 15 | Number 2 | e284

Herpetofauna in an Atlantic Forest hotspot in Brazil

Fig. 6. Snakes species found in the Marechal Newton Cavalcanti Instruction Center Atlantic Forest fragment. (A) Boa constrictor

(Linneaus, 1758); (B) Epicrates cenchria (Linneaus, 1758); (C) Chironius flavolineatus (Jan, 1863); (D) Dendrophidion atlantica

(Freire, Caramaschi, and Gongalves, 2010); (E) Spilotes pullatus (Linneaus, 1758); (F) Tantilla melanocephala (Linneaus, 1758);

(G) Erythrolamprus almadensis (Wagler, 1824); (H) Erythrolamprus poecilogyrus (Wied-Neuwied, 1825); (1) Erythrolamprus

viridis (Wagler, 1824); (J) Helicops angulatus (Linneaus, 1758); (IK) Oxybelis aeneus (Wagler, 1824); (L) Oxyrhopus petolarius

(Linneaus, 1758); (M) Oxyrhopus trigeminus (Dumeril, Bibron, and Dumeril, 1854); (N) Philodryas olferssi (Lichtenstein, 1823);

(O) Philodryas patagoniensis (Girard, 1825); (P) Sibynomorphus neuwiedi (Ihering, 1911); (Q) Siphlophis compressus (Daundin,

1803); (R) Xenodon merremii (Wagler, 1824); (S) Thamnodynastes pallidus (Linneaus, 1758); (T) Micrurus leminiscatus (Linneaus,

1758); (U) Micrurus ibiboboca (Merrem, 1820); (V) Amerotyphlops brongersmianus (Vanzolini, 1976); (W) Crotalus durissus

(Linneaus, 1758); (X) Lachesis muta (Linneaus, 1766). Photos: M.A. Freitas.

Amphib. Reptile Conserv. 68 August 2021 | Volume 15 | Number 2 | e284

Oitaven et al.

35 im Anura

Reptiles

Number of species

Active search Passive search Collected by third parties

Fig. 7. Comparative evaluation of the sampling methods for

anurans and reptiles recorded at Marechal Newton Cavalcanti

Instruction Center (CMNIC) Atlantic Forest fragment, from

August 2008 through December 2009.

search by funnel trap represents the best option for

Testudines, as well as crocodilians (Balestra et al. 2016).

The results obtained here are consistent with those from

studies which used similar methods (Morato et al. 2011;

Dias et al. 2014; Palmeira and Goncalves 2015; Santos

et al. 2016), revealing that the various kinds of methods

used are governed by the sample effort, in conjunction

with the species-specific and environmental conditions

(Pedrosa et al. 2014).

Considering that this study represents the first effort

to identify the herpetofauna diversity in this region, the

results are able to reveal gaps in the knowledge, raising

the awareness of the region’s size and unexplored areas.

In addition, this work reinforces the need for more data

on the fauna that inhabit this study site, especially the

herpetofauna given its high diversity in this biome, which

will be useful for more accurate wildlife conservation

and environmental projects, because surveys such as

this one increase the number of species registered in the

area. We strongly recommend that long-term studies be

conducted in this area, in a further attempt to describe the

entire herpetofauna, which could include the addition of

new species to the list, in addition to the possibility of

new species records for the State of Pernambuco.

Acknowledgements.—The authors would like to thank

FACEPE for financial assistance, the CMINIC project,

and IBAMA Institute for the permit issued (088/07).

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[Accessed: 31 October 2020].

Roberto IJ, de Oliveira CR, de Araujo Filho JA, de

Oliveira HF, Avila RW. 2017. The herpetofauna of the

Serra do Urubu mountain range: a key biodiversity

area for conservation in the Brazilian Atlantic

forest. Papéis Avulsos de Zoologia 57(27): 347-373.

Santana GG, Vieira WLS, Pereira-Filho GA, Delfim FR,

Lima YCC, Vieira KS. 2008. Herpetofauna em um

fragmento de Floresta Atlantica no Estado da Paraiba,

Regiado Nordeste do Brasil. Biotemas 21(1): 75-84.

Santos JRO, O1taven LPC, Aratyo AP, Moura GJB.

2016. Anfibios (Anura e Gymnophiona) do refugio de

vida silvestre “Matas do sistema Gurjau,” estado de

Pernambuco, Nordeste do Brasil. Revista Nordestina

de Zoologia 10(1): 83-96.

Silva TL, Barbosa GG, Oliveira CN, Rodrigues GG.

2017. Répteis do refugio de vida silvestre “Matas

do sistema Gurjau,” Pernambuco, Brasil. Revista

Nordestina de Zoologia 11(1): 43-47.

Viana PF, Mendes DMM. 2015. Feeding behavior

and first record of Rhinatrema bivittatum (Guérin-

Méneville, 1829) as part of the diet of the Ribbon

Coral Snake, Micrurus lemniscatus (Linnaeus, 1758)

in the Central Amazon region (Serpentes: Elapidae).

Herpetology Notes 8: 445-447.

August 2021 | Volume 15 | Number 2 | e284

Amphib. Reptile Conserv.

Oitaven et al.

Leonardo Pessoa Cabus Oitaven is currently serving as a Ph.D. student, associated with the

Laboratorio de Estudos Herpetologicos e Paleoherpetologicos (LEHP), Department of Biology,

Universidade Federal Rural de Pernambuco (UFRPE), Recife, Pernambuco, Brazil. Leonardo is

obtaining his Ph.D. from the Ciéncia Animal Tropical program (PGCAT) at UFRPE and his research

interests include various aspects of the ecology of reptiles and amphibians. He has authored articles

and book chapters on the herpetofauna of Pernambuco state (Brazil), and has been working in snake

husbandry, including captive rearing of venomous snakes for research and venom extraction for

serum production.

Danilo Sé Barreto obtained his Bachelor’s degree in Biology from Universidade Federal Rural de

Pernambuco (UFRPE) in Recife, Pernambuco, Brazil. Danilo has been developing various research

interests in herpetology, with an emphasis on snakes.

Mariana Miranda d'Assunc4o obtained her Bachelor’s degree in Biology from Universidade

Federal Rural de Pernambuco (UFRPE) in Recife, Pernambuco, Brazil. Currently she is a Specialist

in Environmental Management at the Faculdade Frassinetti do Recife (FAFIRE) in Recife,

Pernambuco, Brazil. She has also been developing a variety of research interests in herpetology,

with an emphasis on snakes.

José Ricardo de Oliveira-Santos obtained his Master’s degree in Ecology from Universidade do

Estado da Bahia (UNEB), Salvador, Bahia, Brazil. Currently, he is working ona Ph.D. in the Ciéncia

Animal Tropical (PGCAT) program at Universidade Federal Rural de Pernambuco (UFRPE). José

has acted as an anti-racism activist, as well as Professor in the Departamento de Educacéo, Campus

VII of UNEB. Currently, he is developing projects on the hematologic and biochemichal patterns

of endemic anuran species from Brazil, with the aim of verifying the effects of anthropic actions

on wildlife. In addition, has developed various electronic media-based science communication

projects, using the podcast Rapadura com Ciéncia and YouTube, as well as Instagram.

Alan Pedro Aratjo is currently a Ph.D. student in the Ecology and Evolution program at

Universidade Federal de Goias (UFG) in Goidania, Goias, Brazil, and has previously obtained a

Biology and Ecology Master’s degree. He has been developing studies on anurans associated with

bromeliads, with an emphasis on acoustic community and phoretic relationships.

Geraldo Jorge Barbosa de Moura currently works as a Professor and Researcher at the Universidade

Federal Rural de Pernambuco (UFRPE), teaching and guiding undergraduate students in on-site

courses in the Biological Sciences, as well as Stricto Sensu Academic Graduate Programs at the

Master’s and Ph.D. levels in Ecology, Tropical Animal Science, and Environmental Sciences; in

addition to guiding the Graduate Programs in Environmental Planning at Universidade Catolica do

Salvador (UCSAL), Human Ecology at Universidade do Estado da Bahia (UNEB), and Geosciences

and Paleontology at Universidade Federal do Ceara (UFC). He has extensive experience in

research, mainly in the areas of Behavior, Ecology, Paleontology, Environmental Management, and

Theoretical-Clinical Psychoanalysis and Teaching. Geraldo also serves as a member of the Editorial

Boards of various national and international journals.

71 August 2021 | Volume 15 | Number 2 | e284

The herpetofauna of Veracruz, Mexico

SF,

Introductory Page. Crotalus mictlantecuhtli Carbajal-Marquez, Cedefio- Vazquez, Martinez-Arce, Neri-Castro, and Machkour-

M’Rabet, 2020. The Veracruz Neotropical Rattlesnake is a cryptic state endemic species in the Crotalus durissus species complex,

which recently was described. This rattlesnake is distributed in the southern portion of the state of Veracruz, and eventually might be

found in northeastern Oaxaca and western Tabasco. This species occurs at elevations from near sea level to 1,200 m. The describers

indicated that this rattlesnake “inhabits mostly open dry areas with rocky outcrops in tropical deciduous forest and seasonal rain

forest along the Atlantic versant” (Carbajal-Marquez et al. 2020: 465). The conservation status of this species has not been evaluated

by the IUCN or by SEMARNAT; however, we calculated its EVS value as 16, placing it in the middle portion of the high vulner-

ability category. This individual was photographed in the vicinity of La Antigua, in the municipality of the same name. Photo by

Isaac Ajactle-Tequiliquihua.

Amphib. Reptile Conserv. 72 September 2021 | Volume 15 | Number 2 | e285

Amphibian & Reptile Conservation

15(2) [General Section]: 72-155 (e285).

Official journal website:

amphibian-reptile-conservation.org

The herpetofauna of Veracruz, Mexico:

composition, distribution, and conservation status

‘Lizzeth A. Torres-Hernandez, ‘Aurelio Ramirez-Bautista, 7Raciel Cruz-Elizalde, *Uriel Hernandez-

Salinas, *Christian Berriozabal-Islas, Dominic L. DeSantis, “Jerry D. Johnson, ‘Arturo Rocha,

8Eli Garcia-Padilla, °Vicente Mata-Silva, °Lydia Allison Fucsko, and ‘Larry David Wilson

'Laboratorio de Ecologia de Poblaciones, Centro de Investigaciones Biologicas, Instituto de Ciencias Bdsicas e Ingenieria, Universidad Auténoma del

Estado de Hidalgo, Km 4.5 Carretera Pachuca-Tulancingo, 42184 Mineral de La Reforma, Hidalgo, MEXICO ?2Laboratorio de Zoologia, Facultad

de Ciencias Naturales, Universidad Autonoma de Querétaro, Avenida de las Ciencias S/N, Santa Fe Juriquilla, C. P. 76230, Querétaro, Querétaro,

MEXICO ?Instituto Politécnico Nacional, CIIDIR Unidad Durango, Sigma 119, Fraccionamiento 20 de Noviembre II, Durango 34220, MEXICO

‘Programa Educativo de Ingenieria en Biotecnologia, Universidad Politécnica de Quintana Roo, Av. Arco Bicentenario M 11, Lote 1119-33, Sm

255, 77500 Canciin, Quintana Roo, México y Universidad de Quintana Roo, Departamento de Administracion turistica, Playa del Carmen Cancun,

Quintana Roo, MEXICO *Department of Biological and Environmental Sciences, Georgia College and State University, Milledgeville, Georgia 31061,

USA °Department of Biological Sciences, The University of Texas at El Paso, El Paso, Texas 79968-0500, USA "Department of Biological Sciences, El

Paso Community College, El Paso, Texas 79927, USA *Oaxaca de Juarez, Oaxaca 68023, MEXICO °Department of Humanities and Social Sciences,

Swinburne University of Technology, Melbourne, Victoria, AUSTRALIA "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 state of Veracruz, Mexico, currently consists of 359 species, including

76 anurans, 45 caudates, one caecilian, one crocodylian, 217 squamates, and 19 turtles. The distribution

of the herpetofaunal species are catalogued here among the four recognized physiographic regions in

the state. The total number of species ranges from 179 in the Sierra de Los Tuxtlas to 236 in the Sierra

Madre Oriental. The number of species shared among the four physiographic regions ranges from 100

between the Gulf Coastal Lowlands and the Transmexican Volcanic Belt, to 190 between the Sierra Madre

Oriental and the Transmexican Volcanic Belt. A similarity dendrogram based on the Unweighted Pair Group

Method with Arithmetic Averages (UPGMA) depicts two distinct clusters, one between the Sierra Madre

Oriental and the Transmexican Volcanic Belt, and the other between the Gulf Coastal Lowlands and the

Sierra de Los Tuxtlas. The former cluster reflects two adjacent regions in highland environments that

share a substantial number of herpetofaunal species, and the latter cluster shares a sizeable number

of wide-ranging, generalist, lowland species found on the Atlantic and Pacific versants of Mexico and

Central America. The level of herpetofaunal endemism is relatively high, with 182 of 359 species either

endemic to Mexico or to Veracruz. The distributional categorization of the total herpetofauna is as follows:

169 non-endemic species; 138 country endemic species; 44 state endemic species; and eight non-native

species. The 169 non-endemic species are allocated to the following distributional categories: MXCA (89),

MXSA (30), MXUS (29), USCA (11), USSA (four), and OCEA (five). The principal environmental threats to

the herpetofauna of Veracruz include deforestation, livestock, roads, water pollution, myths and other

cultural factors, diseases, invasive species, and illegal commerce. The conservation status of each native

species was evaluated using the SEMARNAT, IUCN, and EVS systems, of which the EVS system proved to

be the most useful. The Relative Herpetofaunal Priority method was employed to determine the rank order

significance of the four regions, and this identified the Sierra Madre Oriental as the region of greatest

importance. Only six protected areas exist in Veracruz, most of which are located in the Gulf Coastal

Lowlands, the region of least conservation significance. The area of greatest significance, the Sierra Madre

Oriental, does not contain any protected areas. A total of 265 species have been recorded within the six

protected areas, of which 138 are non-endemics, 89 are country endemics, 31 are state endemics, and

seven are non-natives. Finally, we provide a set of conclusions and recommendations to enhance the

prospects for the future protection of the herpetofauna of Veracruz.

Keywords: Anurans, caudates, physiographic regions, protected areas, protection recommendations, squamates, turtles

Resumen.—La herpetofauna de Veracruz, Mexico, comprende 359 especies, incluidas 76 anuros, 45

caudados, una cecilido, un cocodrilido, 217 escamosos y 19 tortugas. Catalogamos la distribucion de las

especies de herpetofauna en cuatro regiones fisiograficas reconocidas. El numero total de especies varia

de 179 en la Sierra de Los Tuxtlas a 236 en la Sierra Madre Oriental. El numero de especies compartidas

Correspondence. /izzeth.torres97@gmail.com (LATH), ramibautistaa@gmail.com (ARB), cruzelizalde@gmail.com (RCE), uhernndez3@

gmail.com (UHS), christianberriozabal@gmail.com (CBI), dominic.desantis@gcsu.edu (DLD), jjohnson@utep.edu (JDJ), turvrocha@gmail.com

(AR), eligarcia_18&@hotmail.com (EGP), vmata@utep.edu (VMS), lydiafucsko@gmail.com (LAF), bufodoc@aol.com (LDW)

Amphib. Reptile Conserv. 73 September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

entre las cuatro regiones fisiograficas varia de 100 entre las Tierras Bajas Costeras del Golfo y el Cinturon

Volcanico Transmexicano a 190 entre la Sierra Madre Oriental y el Cinturon Volcanico Transmexicano.

Un dendrograma de similitud basado en el Método de Grupos de Pares no Ponderados con Promedios

Aritméticos (UPGMA) muestra dos grupos distintos, uno entre la Sierra Madre Oriental y el Cinturon

Volcanico Transmexicano y el otro entre las Tierras Bajas Costeras del Golfo y la Sierra de Los Tuxtlas. El

primer grupo refleja las dos regiones que comparten un numero sustancial de especies de herpetofauna

de ambientes de tierras altas en areas adyacentes, y el ultimo grupo comparte un numero considerable de

especies de tierras bajas generalistas de amplio rango que se encuentran en las vertientes del Atlantico

y Pacifico de Mexico y America Central. El nivel de endemismo de la herpetofauna es relativamente alto,

de 359, 182 especies son endemicas de Mexico o Veracruz. De la herpetofauna total, la clasificacion de

distribucion es la siguiente: 169 especies no endémicas; 138 especies endemicas al pais; 44 especies

endemicas al estado; y ocho especies exoticas. Las 169 especies no endémicas se asignan a las siguientes

categorias de distribucion: MXCA (89); MXSA (30); MXUS (29); USCA (11); USSA (cuatro); y OCEA (cinco).

Las principales amenazas ambientales para la herpetofauna de Veracruz incluyen la deforestacion, la

ganaderia, las carreteras, la contaminacion del agua, los mitos y otros factores culturales, las enfermedades,

las especies invasoras y el comercio ilegal. El estado de conservacion de cada especie nativa se evaluo

utilizando los sistemas SEMARNAT, IUCN y EVS, de los cuales el sistema EVS resulto mas util. Se utilizo

el metodo de Prioridad Relativa de la Herpetofauna para determinar el orden de importancia de las cuatro

regiones, con la mayor importancia asignada a la Sierra Madre Oriental. Solo existen seis areas protegidas

en Veracruz, la mayoria de las cuales estan ubicadas en las Tierras Bajas Costeras del Golfo, la region de

menor importancia para la conservacion. La zona de mayor importancia, la Sierra Madre Oriental, no tiene

areas protegidas dentro de ella. Se registra un total de 265 especies dentro de las seis areas protegidas,

de las cuales 138 son no endémicas, 89 son endemicas del pais, 31 son endemicas del estado y siete

son no nativas. Finalmente, se brinda un conjunto de conclusiones y recomendaciones para mejorar las

perspectivas de proteccion futura de la herpetofauna de Veracruz.

Palabras Clave: Anuros, caudados, regiones fisiograficas, areas protegidas, recomendaciones de _ proteccion,

escamosos, tortugas

Citation: Torres-Hernandez, LA, Ramirez-Bautista A, Cruz-Elizalde R, Hernandez-Salinas U, Berriozabal-Islas C, DeSantis DL, Johnson JD, RochaA,

Garcia-Padilla E, Mata-Silva V, Fucsko LA, and Wilson LD. 2021. The herpetofauna of Veracruz, Mexico: composition, distribution, and conservation

status. Amphibian & Reptile Conservation 15(2) [General Section]: 72-155 (e285).

[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: 31 March 2021; Published: 29 September 2021.

ature is the metaphorical goddess of all existence to the southeast by Chiapas, and to the east by Tabasco.

that lies beyond human control. Humanity is blessed Its surface area covers 71,826 km’, which ranks 11" in

to the extent we love her, and her products, from the _ size among the 32 federal entities or states in Mexico.

sweet descent of her sunsets to the tantrums of her — The population in 2020 was 8,062,597, ranking 3" in the

thunderstorms, and from the empty vast space beyond country, with a population density of 110 people/km’,

her biosphere to the seething diversity within it, of which — which was 10" in the country (http://inegi.org.mx;

we ourselves are a recent chance addition.” Accessed: 3 April 2021).

The highest mountain in Mexico is the stratovolcano

E. O. Wilson (2020) — Pico de Orizaba (or Citlaltépetl), with an elevation of

5,747 m, which lies along the border of Veracruz and

Introduction neighboring Puebla (Woolrich-Pifia et al. 2017), traversing

the caldera at the peak (http://maps.google.com; Accessed:

Veracruz includes 212 municipalities and is a narrow, 8 June 2020). This imposing volcano lies on the eastern

elongate, crescent-shaped state in Mexico (Fig. 1) _ periphery of the Transmexican Volcanic Belt (TVB), a

that extends 650 km (from north to south) along the — roughly 1,000 km-long volcanic arc in central Mexico that

southwestern coast of the Gulf of Mexico, and varies in —_ extends from near the Gulf of Mexico to near the Pacific

width from 32 to 212 km. The state is situated entirely | Ocean at latitudes between 18°30’N and 21°30’N.

within the tropics, but at its northernmost extent lies only In addition to the TVB, Veracruz also harbors elements

160 km south of the Tropic of Cancer at latitude 23.43663° — of three other physiographic regions, including the Gulf

N. The state is bordered to the north by Tamaulipas, to | Coastal Lowlands (GCL), the Sierra Madre Oriental

the west by San Luis Potosi, Hidalgo, Puebla, and Oaxaca, (SMO), and the Sierra de Los Tuxtlas (SLT). The GCL

Amphib. Reptile Conserv. 74 September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

extends along the entire length of the state and lies between

the shore of the Gulf of Mexico and the lower limits of the

SMO and the TVB. Herein, the same cut-off point (200 m)

for the upper limit of the GCL was used as in Johnson et al.

(2010, 2015a) and Cruz-Saenz et al. (2017) for the Pacific

Coastal Plain in Chiapas and Jalisco, respectively.

The SMO is a narrow and elongate mountain range

in eastern Mexico that extends from near the Rio

Grande along the border of Texas (in the United States)

and Coahuila (in Mexico) southward along the eastern

periphery of the Central Plateau (= Mesa Central) through

Nuevo Leon, southwestern Tamaulipas, eastern San Luis

Potosi, northeastern Querétaro, eastern Hidalgo, and

northern Puebla, where it joins the eastern extension of the

TVB to the west of the GCL (Lemos-Espinal and Dixon

2013; Ramirez-Bautista et al. 2014; Nevarez-de los Reyes

et al. 2016; Woolrich-Pifia et al. 2017; Lazcano etal. 2019).

The SLT is an isolated volcanic belt and mountain range

in southeastern Veracruz that contains Volcan Santa Marta

and Volcan San Martin Tuxtla, both above 1,700 m in

elevation. This range is separated from the Transmexican

Volcanic Belt to the northwest by about 250 km and from

the Central American Volcanic Belt to the southeast by

about 330 km (http://www.wikipedia.org; Accessed: 8

June 2020).

Because of its geographic position, Veracruz

encompasses the broadest range of elevations of any state

in Mexico, from sea level along the eastern coast of the

Gulf of Mexico to the peak of Pico de Orizaba at almost 6

km above sea level along its western border.

Materials and Methods

Our Taxonomic Position

In this paper, we maintain the same taxonomic position as

explained in previous works on other parts of Mesoamerica

(e.g., 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; Ramirez-Bautista et al.

2020). Consult Johnson (2015b) for a statement of this

position, with special reference to the subspecies concept.

System for Determining Distributional Status

We used the same system developed by Alvarado-Diaz et

al. (2013) for the herpetofauna of Michoacan to determine

the distributional status of members of the herpetofauna of

Veracruz. 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), and Ramirez-Bautista et al. (2020)

utilized this system, which consists of the following four

categories: SE = endemic to state (in this case Veracruz);

CE = endemic to Mexico; NE = not endemic to Mexico;

Amphib. Reptile Conserv.

and NN = non-native in Mexico.

Systems for Determining Conservation Status

To evaluate the conservation status of the herpetofauna

of Veracruz, we employed the same 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-Saenz

et al. (2017), Gonzalez-Sanchez et al. (2017), Lazcano et

al. (2019), and Ramirez-Bautista et al. (2020). Detailed

descriptions of these three systems appear in earlier papers

in this series (e.g., Alvarado-Diaz et al. 2013; Johnson

et al. 2015a; Mata-Silva et al. 2015), and thus 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 published in

Amphibian & Reptile Conservation. The basic format

for 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 resumed with a paper on the herpetofauna

of Oaxaca (Mata-Silva et al. 2015), and that same year

with a paper on the herpetofauna of Chiapas (Johnson et

al. 2015a). Three entries in the MCS appeared tn 2016, on

Tamaulipas (Teran-Juarez et al. 2016), Nayarit (Woolrich-

Pifia et al. 2016), and Nuevo Leon (Nevarez-de los Reyes

et al. 2016). Three more entries appeared 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), followed by another

in 2019, on Coahuila (Lazcano et al. 2019). Finally, one

entry appeared in 2020, on Hidalgo (Ramirez-Bautista et

al. 2020). Consequently, this paper on the herpetofauna of

Veracruz is the 12" entry in this series.

Physiography and Climate

Physiographic Regions (Fig. 1)

The distribution of the herpetofauna of Veracruz was

analyzed using the classification system of physiographic

regions (= physiographic provinces of INEGI 2000

and CONABIO 2008). According to these sources, the

state contains four regions (Fig. 1), as briefly described

below. Note that Veracruz falls within the biogeographic

area described by Holt et al. (2013) as the “Panamanian

Realm” (Tropical Mexico and Central America), which

supersedes previous traditional classifications by other

biogeographers.

September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

se°c'o"w sr-oo"w Se°oo"wW ss°0'o"wW oo'o"wW

Tamaulipas

Gulf of Mexico

19°O'0"N

18°0'0"N

Torn

Oaxaca

0 25 50 100 150 200

es Kilometers

16°0'O°N

Se°0'O"W sroo"w seo" W sSoorw aorw

Physiographic regions

BP Gult Coastal Lowlands (GCL)

Ae we Sierra de Los Tuxtlas (SLT)

eee Z Sierra Madre Oriental (SMO)

metas Transmexican Volcanic Belt (TVB)

Fig. 1. Location in Mexico and physiographic regions of Veracruz, Mexico. Abbreviations: GCL = Gulf Coastal Lowlands; SLT =

Sierra de Los Tuxtlas; SMO = Sierra Madre Oriental; and TVB = Transmexican Volcanic Belt.

Gulf Coastal Lowlands (GCL). In Mexico, this region

(Figs. 2-3) extends from the Rio San Fernando in

Tamaulipas southeastward to the Rio Candelaria, located

on the Yucatan Peninsula (Morrone 2001). This region

covers various-sized Atlantic versant portions of the states

of Tamaulipas, San Luis Potosi, Veracruz, Hidalgo, Puebla,

Oaxaca, Chiapas, Tabasco, Campeche, Yucatan, and

Quintana Roo. In Veracruz, the GCL is located between

25°52717.02”N, -94°04'11.48"°W, and 20°55°36.56’N,

-90°18°06.7"W, at elevations ranging from about sea

level to 200 m (Espinosa et al. 2008). The mean annual

precipitation in this region ranges from 1,000—2,000

mm, whereas the average annual temperature is 21.2 °C.

Numerically dominant vegetation types include tropical or

subtropical evergreen forest, scrub, sub-deciduous forest,

and dry forest (CONABIO 2008; Wilson and Johnson

2010), depending on the elevation and amount of rainfall.

Sierra de Los Tuxtlas (SLT). In Veracruz, this physiographic

region (Fig. 4) is bordered to the north and east by the Gulf

of Mexico, to the east and southeast by the Olmec region,

and to the west by the Papaloapan region (CONABIO

2008). The SLT (18°42’36” to 18°03’00”N, -95°25’48”

to -94°34’12”W) contains four municipalities: Catemaco,

Amphib. Reptile Conserv.

Hueyapan de Ocampo, San Andrés Tuxtlas, and Santiago

Tuxtla (Gonzalez-Soriano et al. 1997). This region has a

surface area of 3,484.34 km? (4.1% of state’s territory),

and due to their combined size, the municipalities of

San Andrés Tuxtlas and Hueyapan de Ocampo comprise

56.6% of its territory. The region is volcanic in origin, and

because of its proximity to the Gulf of Mexico it generates

a sizable amount of precipitation, making it one of the

rainiest regions in Mexico (Table 2). The elevations of

the steep-sided volcanic cones range from 200—1,700 m

(CONABIO 2008). The climate of the region ranges from

humid tropical to humid subtropical, depending on the

elevation. The average temperature ranges from 21.5—27.3

°C, and the annual rainfall is over 4,500 mm. Even though

rainfall is frequent throughout the year, there is arecognized

“rainy season” from May to February, and a “dry season”

from March to May (CONABIO 2008). The driest month

generally 1s May, and wettest months are either August,

September, October, or November. The region contains

such lush vegetation as tropical and subtropical evergreen

forest, but 1t has been subjected to intense agricultural

exploitation since pre-Hispanic times (Gonzalez-Soriano

et al. 1997). The most important agricultural products are

corn, beans, sugar cane, and tobacco. Fishing and raising

September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

Fig. 2. Gulf Coastal Lowlands. Vegetation in the vicinity of El

Salmoral, municipality of La Antigua. Photo by Isaac Ajactle-

Tequiliquihua.

eo;

Fig. 4. Sierra de Los Tuxtlas. Cloud forest at the top of Volcan

San Martin. Photo by Eli Garcia-Padilla.

ce Se

Fig. 6. Transmexican Volcanic Belt. Vegetation on the “roof

of Mexico,” Volcan Pico de Orizaba or “Citlatépetl.” Photo by

Jorge Gonzalez Sanchez.

livestock are common in areas that have been transformed

into grassland, in addition to industrial activities and

tourism.

Sierra Madre Oriental (SMO). The Sierra Madre Oriental

(Fig. 5) is an extensive mountain system that extends for

about 1,350 km from the Rio Grande on the northwest, to

about the Isthmus of Tehuantepec in northeastern Oaxaca

on the southeast (Campbell 1999). Collectively, this area

constitutes 2.84% of the land in Mexico (Morrone 2001;

CONABIO 2008). In Veracruz, the northern limit of the

SMO lies at 25°36’23.13”N, -100°17°38.99"W and the

Amphib. Reptile Conserv.

ss 4 L } a fe Bite ” SL

Fig. 3. G

ulf Coastal Lowlands. Mangrove forest during the

dry season in the vicinity of Tumilco, municipality of Tuxpam.

Photo by Uriel Hernandez-Salinas.

2 7 cae

Fig. 5. Sierra Madre Oriental. Montane cloud forest in the mu-

nicipality of Tatatila. Photo by Fidel Lopez Guzman.

southern limit at 17°28’45.86’N, -96°04’34.85”W. The

upper elevations of the SMO in Veracruz range from

2,500-3,700 m (CONABIO 2008). To the east, the SMO

is bordered by the GCL, and to the west by a very small

portion of the Northern Plateau Basins and Ranges (NB;

Wilson and Johnson 2010), the Mesa Central (MC; which

includes a small portion of TVB), and the Sierra Madre del

Sur (SUR) (Campbell 1999). The SMO contains portions

of 22 municipalities. This region is geologically complex

and consists mostly of sedimentary and metamorphic

rocks from the Cretaceous and Jurassic (CONABIO

2008). The mean annual precipitation varies considerably,

ranging from 400-800 mm in montane cloud forests

in the municipalities of Xalapa and Chiconquiaco

(CONABIO 2008) to 220 and 234 mm in drier areas in the

municipalities of Perote and Las Vigas, respectively. The

average annual temperature for the region 1s 17.4 °C, and in

winter and summer ranges from 4—28 °C in montane areas,

and from 10-40 °C in temperate valleys. On the wetter

slopes, the numerically dominant vegetation communities

are coniferous forest (28%), oak forest (26%), and cloud

forest (8%), while xerophilous scrub (16%) occurs in the

drier areas (CONABIO 2008).

Transmexican Volcanic Belt (TVB). The Transmexican

Volcanic Belt (Fig. 6) is a volcanic arc located in the Mesa

Central (Campbell 1999) that slightly tilts in a northwest

to southeast direction and extends from Nayarit on the

September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

Pacific versant (Ferrusquia-Villafranca 2007; CONABIO

AO i a

pas aS BY oOMmN O&O NAO CoCo 2008), and then parallels the northern slope of the Balsas

oF ae = NAKED OND COMO KUN ere : :

Ses Be oe ae os aa =n Basin into Veracruz, where it converges with the SMO

& oF a near Pico de Orizaba. This belt 1s formed by a set of

8 a 3 S b volcanoes of different ages (Miocene to Plio-Pleistocene),

Bs s< 2 = aRaA RAN _LA@n 4fa ane i pocsonce ue Soon ee Peet aN,

§ 3 8 : 3 aaa 2aGa cla “la -98 37 42.45 W and 21f53 40.02 N, -105°36’09.80”"W.

ESoxu| A This region occupies 8% of Mexico’s surface area, and

o 2 Sh a ranges in elevation from 1,000—5,747 m. In Veracruz,

3 q's 3 3 2 mz ae the TVB reaches elevations from 1,500—5,747 m. Within

3 g 2 < 5 co — 2 as = uae % + the TVB are Pico de Orizaba, Cofre de Perote, Sierra

Ree LL 5 = - ee de Zongolica, and Sierra de Chiconquiaco (CONABIO

SOs 2008). The mean annual precipitation ranges from 581—

Ns = is EJ m Wa ry 2,236 mm, and the mean annual temperature is 15.3 °C

9Sa0 i Bee ee eters Ei ee (Suarez-Mota et al. 2014). Numerically dominant natural

gg fe a Ee SE EOS SE RUN SUN vegetation communities are represented primarily by

a S 7 coniferous forest (31%) and oak forest (28%), with the

= =e os bs remainder composed of subalpine scrub and subtropical

Bb = = E = mMHo wmMo mto ofn dry forest; disturbed areas such as farmland and pastures

2 ie = = aan Aaa =A ald have replaced the natural vegetation.

fav <s ag & N

sk oY :

Bb 23 Climate

a Ow ~

£8<5| 6 (Soe S83 5228 225] am ni

ies 3 Ait OE Ae lees igh Col perature. The monthly minimum, mean, and

2 5S & ll bas a a a ap maximum temperatures for a single locality are indicated

SAZ ys _ _ " y in each of the four recognized physiographic regions in

O€ ER: = SE eye MoO eae Osea Veracruz in Table LL The elevations for these localities

c z g S = CERYC ECUO aces: Pen range from 40 m in the city of Veracruz to 3,000 m at

7 = 3 a Orizaba. The mean annual temperature is highest at

SSE , LOG de Se Sag EE Veracruz (40 m asl) in the GCL at 27.3 °C, followed by

28 a = BAD AGT NAS aww San Andrés oe ‘Se as : a Bae as eae ie

BSEy 4 aA ed Huayacocotla (2, m asl) in the SMO at 21. , wit

a. = = Ee the lowest mean temperature of 16.6 °C at Orizaba in the

5 ais ep |omt anit can noo TVB (3,000 m asl).

3 bc cs &] = |Aas Aaa Tan F248 In the four physiographic regions in Veracruz, the

q ae s minimum annual temperatures range from 4.3—10.7 °C

z - fs g a || Noo la Rell pastaw lower than the maximum annual temperatures (Table

ay S 'S 5 = la aa saa 228 22a 1). The mean minimum monthly temperatures peak

E ie 6 & in May (SLT and SMO), June (GCL), or September

& SBS] . siby ef im hat (TVB), and reach their lowest levels in January (GCL,

Seat ee || cee [Pecuthee e ty Cee eet, Se SLT, and SMO) or December (TVB). The mean monthly

Ea See. |inem [isa eee eo ee temperatures are highest in May (TVB), July (GCL), and

g 8 sé August (SLT and SMO), and lowest in January (GCL,

E E oe c 1 re a ” SMO, and TVB) or February (SLT).

Sa a Fee alt eune et esr ioe ae a — | |

ee Ae es ee (PG a as Precipitation. As typical in tropical climates, the

5 5 re E a precipitation regime in Veracruz is partitioned into a six-

a 5 s at month wet season that extends from May to October, and

= 0 : s tEan nA, cen Loa a dry season of similar length, from November to April

PERS) € [Fan =SN Ooa SSA (Table 2). The mean monthly precipitation is highest in

eee) "> September (GCL), October (SLT, TVB), or November

eee Ss]. (SMO), and lowest in January (GCL, SLT, TVB) or

8 Sols Rectgee o £ 5 3 February (SMO). During the rainy season (May to

688 = & 5 ge 2 as = g % S October) from 58.8 to 76.5% of the annual precipitation

= = 2 : g 2 = 2 : 3 S 5 z q occurs. The annual rainfall ranges from 267.6 mm in the

2ees| ea sR 8 2 Ss TVB to 2,218.8 mm in the SLT (Table 2).

£586) ™ e

SOR xo

Amphib. Reptile Conserv. 78 September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

™

No. 1. Jncilius cavifrons (Firschein, 1950). The Mountain

Toad is a state endemic species restricted in distribution to the

Sierra de los Tuxtlas physiographic region (Frost 2020). This

individual was found at Los Tuxtlas, in the municipality of

San Andrés Tuxtla. Wilson et al. (2013a) calculated its EVS

as 13, placing it at the upper limit of the medium vulnerability

category. Its conservation status has been established as

Endangered by the IUCN, and as Special Protection (Pr) by

SEMARNAT. Photo by Christian Berriozabal-Islas.

No. 2. 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 (Frost 2020). This

individual was found at Comapa, in the municipality of the same

name. We determined its EVS as 11, placing it in the middle of

the medium vulnerability category. Its conservation status has

not been assessed by either the IUCN or SEMARNAT. Photo

by Aaron Arias Hernandez.

No. 3. Craugastor alfredi (Boulenger, 1898). Alfred’s Rainfrog

is a non-endemic species distributed from central Veracruz,

Mexico, to western El Petén, Guatemala (Kohler 2011). This

individual was encountered at Los Tuxtlas, in the municipality

of San Andrés Tuxtla. Wilson et al. (2013a) calculated its EVS as

11, placing it in the middle of the medium vulnerability category.

Its conservation status has been evaluated as Vulnerable by the

IUCN, but this species has not been assessed by SEMARNAT.

Photo by Christian Berriozabal-Islas.

Amphib. Reptile Conserv.

No. 4. Craugastor rhodopis (Cope, 1867). The Polymorphic

Robber Frog is a country endemic species found in western

Veracruz and adjacent Hidalgo and Puebla, as well as in central

and southeastern Chiapas and adjacent Oaxaca (Frost 2020).

This individual was found at Huayacocotla, in the municipality

of the same name. Wilson et al. (2013a) determined its EVS as

14, placing it at the lower limit of the high vulnerability category.

Its conservation status has been assessed as Vulnerable by the

IUCN, but this species has not been evaluated by SEMARNAT.

Photo by Christian Berriozabal-Islas.

September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

ges Recent Literature on the Veracruz Herpetofauna

== iso) = — — —

S.ss S Ot ANN ent on

— m | 4 ee nN: Oe mn a) ' i

- 8 = EJESEG 4eG BAR CAS Our knowledge of the Mexican herpetofauna continues

— Sn oo A ee S eh oe Noe] . Ts

ee oe ea “a ae a to expand. As of this writing, several modern state-

Gres Be am ‘

2 Sooo level treatments have appeared, in book form in some

oe) a N Som >

OS ‘ >| 2 SiS eA nm end ee cases and as lengthy papers in others. Although the

BaOaASs = ON. Paine oe. Seuss herpetofauna of Veracruz is one of the most diverse in

o 20 Desh aa N \O

SS Se gl EBs Unset De Bs || Tene etn try, it has not und h t

a22u| 8 LS e entire country, it has not undergone such a recen

is 2 a treatment. Toward this end, a summary of the pertinent

oO : j oy

ZOES ie literature is assembled here to document the composition

ayo < 2 —~ = —~ :

s 3 2 =) = Soe Oe ee Ra of the herpetofauna of Veracruz (Table 3). The literature

5-25 l 2 OO ae atten etek: ONE citations are organized in this table in alphabetical order

=& = e| Z for each of the physiographic regions, and then by year

=a oO : :

ost 5 of publication.

> omen ip ann aN a — of

oS So 2 Sy oe SRS SS oo OG, al

Ty eS PGi S sio "st ONS ‘ ike

TR AN | Blaam Sunn = Saye Composition of the Herpetofauna

#2o _ ieee SESE EO a Se

Cen oS

eca oh

Sesame Families

Press be

son fs > ie Ze a} oe ,

S 5 2 gees oe 2 ee a oi The herpetofaunal species in Veracruz are classified in

2S o-9 Sp Meee ee ee en oa oh MS =

voEAZsS!l Blannmn ant Han AVS 51 families, including 11 families of anurans, four of

> nm Ov cm) ae bas a ‘ 1: 13

gSEsa| a salamanders, one of caecilians, one of crocodylians, 25

Ym VY 2 3 . :

BALES of squamates, and nine of turtles (Table 4). This total

een! Ux , qe

BSE! g ya he px & figure represents 85.0% of the 60 herpetofaunal families

O: > Ios Sgr NAY So 6 ‘ é

eosn| fe SYR SSS SS a art known from Mexico (Wilson et al. 2013a,b; J. Johnson,

ee) 2 [kes Sas San oe unpub. data, 19 March 2020). Of the 16 amphibian

8 E 2 3 families, 72.1% (88) of the 122 species (Tables 5—6) are

= sx z ee ee in the families Bufonidae (nine), Hylidae (29), Ranidae

N & So lo oma) 7 ‘ i on

Se or Blast gxXAS CMzX Sor eight), and Plethodontidae (42). Among the 35 families

oO 6U) Te) |[eies donee GES: Res ee, ecm Kaas :

£5 2S i ~ = a of reptiles, 70.0% (166) of the 237 species (Table 5) are

7 oO : E Pas . allocated to the families Anguidae (10), Dactyloidae

» & = S eee ee ht 18), Phrynosomatidae (20), Colubridae (41), Dipsadidae

255 %| Bl-“58 Sun 62S sux ;

2's = & me |PAs= san Fea TS (46), Natricidae (14), and Viperidae (17).

oOo oO

= Uv pa

ones

Gen og —~ fam ie = G

EASES a rere ata en (0 Tone) enera

Sue! s |=e8 ssh FSR acy

on Oo oOo FR Ne eel eee = wat

SOEs ‘<i cm One hundred and forty-two herpetofaunal genera are

YU SF

eessa| —_ a yan ems _ represented in Veracruz, including 32 genera of anurans,

aso5k FE LTONnN ORR ante tom

2 eés Bloons raw onN ore 10 of salamanders, one of caecilians, one of crocodylians,

=O ara — nim m st 4 0 Gerke aan =n

mar 84 of squamates, and 14 of turtles (Table 4). These 142

Sess aioe

Ags enera comprise 66.0% of the 215 recorded from Mexico

esas SIlnamo oka +6Rn whoo

Sa Soa | pha [oe ee eee Neher (J. Johnson, unpub. data, 19 March 2020). Among the

<s89E S Arn Hn Aw © aan eat ;

ER ZE| = ~ ~ ~ LY amphibians (Table 5), the species are most numerous

a0} a UV YO . aie .

ei in the genera Jncilius (seven species), Craugastor

So 8 o> >

= RB

No) i) p> : :

% ER = ae a i oa 11), Eleutherodactylus (seven), Lithobates (eight),

Ss @ > >

eee] 2B ISSSs wae BSS GaS| Chi ion (10), Pseud 10), and Thori

Seat OP | alee, | sey Roa re en ee eMac iropterotriton (10), Pseudoeurycea (10), an orius

poli Rens aa = a re ine). Among the reptiles (Table 5), the most speci

BILE) & (nine). Among the reptiles (Table 5), the most speciose

2 3S 2s = genera are Norops (18 species), Sceloporus (17), Tantilla

a5 5 : az |aARQ+t Coto nen Naa (five), Coniophanes (five), Geophis (eight), Rhadinaea

é Tigeeet| fey (PSone Cee Eevee BeOS (seven), Thamnophis (11), and Crotalus (10).

geo

SoS Species

See ee || RE elie See ie sé So The herpetofauna of Veracruz consists of 359 species,

2 8 & ; s 2 Y e : 4 oe 5 5 including 76 anurans, 45 salamanders, one caecilian,

23 2 a 2 & 4 2 a 2 . BS one crocodylian, 217 squamates, and 19 turtles (Table

iS #e = = 4). The current numbers of native species in these six

Amphib. Reptile Conserv. 80 September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

| ¢ Ae pe 5 : ai

es - . a)

on .

tat _ . 5

. or. ¥ % Pa

‘ . ~My ed ~ : 25 “ 4

fo f 4 < Se a , © \ ail

e Sool P BY one a : ia —

No. 5. Craugastor vulcani (Shannon and Werler, 1955). The

Volcan San Martin Rainfrog is a state endemic species restricted

in distribution to the Sierra de Los Tuxtlas physiographic

region (Frost 2020). This individual was encountered at Los

Tuxtlas, in the municipality of San Andrés Tuxtla. Wilson et

al. (2013a) calculated its EVS as 17, placing it in the middle

of the high vulnerability category. Its conservation status has

been determined as Endangered by the IUCN, but this species

has not been evaluated by SEMARNAT. Photo by Christian

Berriozabal-Islas.

No. 6. Megastomatohyla mixomaculata (Taylor, 1950). The

Variegated Treefrog is a country endemic species only known

from the municipalities of Coscomatepec, Zongolica, and Los

Reyes in central Veracruz, and in the Sierra Negra region of

southeastern Puebla, Mexico, at elevations from 900 to 1,650

m (Frost 2020). This individual was photographed at Finca

Santa Martha, in the municipality of Los Reyes. Wilson et

al. (2013a) ascertained its EVS as 14, placing it in the lower

portion of the high vulnerability category. Its conservation

status has been assessed as Endangered by the IUCN, and as

Threatened (A) by SEMARNAT. Photo by Jesse Hosman.

No. 7. Rheohyla miotympanum (Cope, 1863). The Small-eared

Treefrog is a country endemic species distributed from “Nuevo

Leon and Coahuila (Sierra Madre Oriental) to Guanajuato

(Sierra Santa Rosa), Hidalgo, and Oaxaca, adjacent Veracruz,

and central Chiapas” (Frost 2020). This individual was found

at El Potrero, in the municipality of Acultzingo. Wilson et al.

(2013a) determined its EVS as 9, placing it at the upper limit

of the low vulnerability category. Its conservation status has

been judged as Near Threatened by the IUCN, but this species

has not been evaluated by SEMARNAT. Photo by Bruno

Rosas Fragoso.

Amphib. Reptile Conserv.

No. 8. Scinax staufferi (Cope, 1865). Stauffer’s Long-nosed

Treefrog is a non-endemic species occurring in savannas

and sub-humid forest in lowlands to moderate elevations

from southern Tamaulipas, Mexico, southward to Nicaragua

on the Caribbean versant, and from Guerrero, Mexico, to

northwestern Costa Rica on the Pacific; it also occurs in

disjunct areas along the Pacific lowlands of western to central

Panama (Frost 2020). This individual was found at Misantla,

in the municipality of the same name. Wilson et al. (2013a)

ascertained its EVS as 4, placing it in the low vulnerability

category. Its conservation status has been assessed as Least

Concern by the IUCN, and this species is not listed by

SEMARNAT. Photo by Bruno Rosas-Fragoso.

September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

Table 3. Summary of the literature documenting the composition and physiographic distribution of the herpetofauna of Veracruz,

Mexico.

Phy goesap tic Documentation

region

Aguilar-Lopez and Canseco-Marquez (2006); Aguilar-Lopez and Pineda (2015); Aguilar-Lopez et al. (2010, 2015, 2016,

2020); Altamirano-Alvarez and Soriano-Sarabia (2010); Avila-Najera et al. (2018); Badillo-Saldafia et al. (2018); Barrio-

Amoros (2019); Bury and Whelan (1984); Campbell and Lamar (1989, 2004); Carbajal-Marquez et al. (2020); Cazares-

Hernandez (2015); Chambers and Hillis (2020); Chavez-Lugo (2015); de la Torre-Loranca et al. (2006); Dixon and Lemos-

Espinal (2010); Duellman (1958, 2001); Duellman and Trueb (1986); Escobedo-Galvan and Gonzalez-Salazar (2011);

Flores-Villela (1998); Frost (2020); Garcia-Vazquez et al. (2010); Guzman-Guzman (2011); Iverson (1992); Johnson et

al. (2010); Jones and Lovich (2009); Klauber (1972); Lemos-Espinal and Dixon (2013); Marquez (1994); McCranie et al.

Gulf Coastal (2020); Méndez-de la Cruz and Casas-Andreu (1992); Mendoza-Henao et al. (2020); Meza-Lazaro and Nieto-Montes de

Lowlands Oca (2015); Morales-Mavil et al. (2017); Myers et al. (2017); Ochoa-Ochoa and Flores-Villela (2011); Oliver-Lopez et al.

(2009); Ordéfiez-Gomez and Valadez-Azua (2008); Palacios-Aguilar and Flores-Villela (2020); Pérez-Higareda and Smith

(1991); Pineda-Arredondo (2015); Ramirez-Bautista et al. (2006, 2009, 2010, 2014); Ramirez-Gonzalez and Canseco-

Marquez (2015); Reyes- Velasco et al. (2020); Rossman et al. (1996); Roze (1996); Ruane et al. (2014); Sanchez-Juarez

(2002); Scarpetta et al. (2015); SEMARNAT (2018); Smith and Taylor (1966); Solis-Zurita et al. (2019); Uribe-Pefia et

al. (1999); Valverde and Rouse-Holzwart (2017); Vazquez-Diaz and Quintero-Diaz (2005); Werler and Dixon (2000);

Wilson (1970); Wilson et al. (2010, 2013a,b); Wright and Wright (1957); Yafiez-Arenas et al. (2016).

Avila-Najera et al. (2018); Badillo-Saldafia et al. (2014, 2018); Barrio-Amorés (2019); Bury and Whelan (1984); Campbell

and Lamar (2004); Carbajal-Marquez et al. (2020); Chambers and Hillis (2020); de la Torre-Loranca et al. (2006); Dixon

and Lemos-Espinal (2010); Duellman (1958, 2001); Flores-Villela (1998); Frost (2020); Garcia-Vazquez et al. (2010);

Guzman-Guzman (2011); Iverson (1992); Johnson et al. (2010); Lemos-Espinal and Dixon (2013); McCranie et al. (2020);

Mendoza-Henao et al. (2020); Meza-Lazaro and Nieto-Montes de Oca (2015); Ochoa-Ochoa and Flores-Villela (2011);

Oliver-Lopez et al. (2009); Palacios-Aguilar and Flores-Villela (2020); Pérez-Higareda and Smith (1991); Pérez-Higareda

et al. (2007); Pineda-Arredondo (2015); Ramirez-Bautista (1977); Ramirez-Bautista and Nieto-Montes de Oca (1997);

Ramirez-Bautista et al. (2006, 2009, 2010, 2014); Ramirez-Gonzalez and Canseco-Marquez (2015); Rossman et al. (1996);

Roze (1996); SEMARNAT (2018); Sherbrooke and Lazcano- Villareal (1999); Sherbrooke (2003); Smith and Taylor

(1966); Solis-Zurita et al. (2019); Urbina-Cardona et al. (2006); Uribe-Pefia et al. (1999); Vazquez-Diaz and Quintero-

Diaz (2005); Werler and Dixon (2000); Wilson et al. (2010, 2013a,b).

Sierra de Los

Tuxtlas

Avila-Najera et al. (2018); Bury and Whelan (1984); Campbell and Lamar (1989, 2004); Canseco-Marquez and Gutiérrez-

Mayén (2010); Canseco-Marquez et al. (2016); Castillo-Juarez et al. (2020); Cazares-Hernandez et al. (2018); Ceron-de

la Luz (2010); Chacon-Juarez and Vasquez-Cruz (2018); Chambers and Hillis (2020); Contreras-Calvario et al. (2019);

Cruz-Elizalde et al. (2020); de la Torre-Loranca et al. (2006, 2019); Dixon and Lemos-Espinal (2010); Duellman (1958,

2001); Ernst and Ernst (2003); Flores-Villela (1998); Frost (2020); Garcia-Bafiuelos et al. (2020); Garcia-Castillo et al.

(2018); Garcia-Morales et al. (2017); Guzman-Guzman (2011); Iverson (1992); Johnson et al. (2010); Jones and Lovich

Sierra Madre (2009); Klauber (1972); Lara-Hernandez and Vasquez-Cruz (2020); Lemos-Espinal and Dixon (2013); Lemos-Espinal

Oriental et al. (2019); Macario-Cueyatcle et al. (2019); McCranie et al. (2020); Mendoza-Henao et al. (2020); Meza-Lazaro and

Nieto-Montes de Oca (2015); Ochoa-Ochoa and Flores-Villela (2011); Oliver-Lopez et al. (2009); Paredes-Garcia et al.

(2011); Peralta-Hernandez et al. (2019); Pérez-Higareda and Smith (1991); Pérez-Sato et al. (2018); Pineda-Arredondo

(2015); Ramirez-Bautista et al. (2006, 2009, 2010, 2014); Reyes-Velasco et al. (2020); Rossman et al. (1996); Roze (1996);

SEMARNAT (2018); Sherbrooke (2003); Sherbrooke and Lazcano- Villareal (1999); Smith and Taylor (1966); Solis-Zurita

et al. (2019); Uribe-Pefia et al. (1999); Vasquez-Cruz and Canseco-Marquez (2020); Vasquez-Cruz et al. (2018, 2019,

2020a,b); Wilson et al. (2010, 2013ab); Wright and Wright (1957).

Avila-Najera et al. (2018); Bello-Sanchez et al. (2014); Bury and Whelan (1984); Campbell and Lamar (1989, 2004):

Canseco-Marquez and Gutiérrez-Mayén (2010); Canseco-Marquez et al. (2016); Carbajal-Marquez et al. (2020); Castillo-

Juarez et al. (2020); Cazares-Hernandez et al. (2018); Cerén-de la Luz (2010); Chacon-Juarez and Vasquez-Cruz (2018);

Chambers and Hillis (2020); Conant (2003); Contreras-Calvario et al. (2019); de la Torre-Loranca et al. (2006, 2019); Dixon

and Lemos-Espinal (2010); Duellman (1958, 2001); Duellman and Trueb (1986); Ernst and Ernst (2003); Flores-Villela

(1998); Frost (2020); Garcia-Bafiuelos et al. (2020); Garcia-Castillo et al. (2018); Garcia-Morales et al. (2017); Gonzalez-

Romero and Murrieta-Galindo (2008); Gonzalez-Zamora et al. (2018); Guzman-Guzman (2011); Iverson (1992); Johnson

et al. (2010); Kelly-Hernandez et al. (2020); Klauber (1972); Lara-Hernandez and Vasquez-Cruz (2020); Lemos-Espinal

and Dixon (2013); Lemos-Espinal et al. (2019); Macario-Cueyatcle et al. (2019); McCranie et al. (2020); Mendoza-Henao

et al. (2020); Meza-Lazaro and Nieto-Montes de Oca (2015); Murrieta-Galindo et al. (2013); Ochoa-Ochoa and Flores-

Villela (2011); Oliver-Lopez et al. (2009); Orddfiez-Gomez and Valadez-Azua (2008); Palacios-A guilar and Flores-Villela

(2020); Paredes-Garcia et al. (2011); Parra-Olea et al. (2020); Peralta-Hernandez et al. (2019); Pérez-Higareda and Smith

(1991); Pérez-Sato et al. (2018); Pineda-Arredondo (2015); Ramirez-Bautista et al. (2006, 2009, 2010, 2014); Reyes-

Velasco et al. (2020); Rossman et al. (1996); Roze (1996); Sandoval-Comte et al. (2017); SEMARNAT (2018); Smith and

Taylor (1966); Solis-Zurita et al. (2019); Uribe—Pefia et al. (1999); Vasquez-Cruz and Canseco-Marquez (2020); Vasquez-

Cruz et al. (2018, 2019, 2020a,b); Wilson et al. (2010, 2013a,b); Yafiez-Arenas et al. (2016).

Transmexican

Volcanic Belt

Amphib. Reptile Conserv. 82 September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

No. 9. Triprion spinosus (Steindachner, 1864). The Coronated

Treefrog is a non-endemic species with a disjunct distribution

in humid forests, primarily in the premontane zone, in eastern

Mexico (Tabasco, Veracruz, Puebla, Oaxaca, and Chiapas,

800—2,068 m asl), Guatemala, northeastern Honduras (95 m

asl), the Atlantic versant of Costa Rica and western Panama,

and from southwestern Costa Rica to west-central Panama on

the Pacific slopes, at elevations from 350 to 1,330 m (Frost

2020). This individual was found at Finca Santa Martha,

in the municipality of Los Reyes. Wilson et al. (2013a)

ascertained its EVS as 14, placing it in the lower portion of

the high vulnerability category. Its conservation status has

been assessed as Least Concern by the IUCN, and this species

is not listed by SEMARNAT. Photo by Jesse Hosman.

ia ls rs et ae ae

No. 11. Lithobates vaillanti (Brochi, 1877). Vaillant’s Frog

is a non-endemic species occurring at 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, at elevations from 0 to

1,700 m (Frost 2020). This individual was photographed in

the vicinity of Catemaco, in the municipality of the same

name. Wilson et al. (2013a) determined its EVS as 9, placing

it in the higher portion of the low vulnerability category. Its

conservation status has been assessed as Least Concern by the

IUCN, and this species is not listed by SEMARNAT. Photo by

Christian Berriozabal-Islas.

Amphib. Reptile Conserv.

No. 10. Agalychnis taylori Funkhouser, 1957. The Northern

Red-eyed Treefrog is a non-endemic species occurring from

“west-central Honduras north through Guatemala along the

Atlantic lowlands of Oaxaca and southern Veracruz, Mexico”

(Frost 2020). This individual was encountered at Los Tuxtlas,

in the municipality of San Andrés Tuxtla. Wilson et al. (2013a)

ascertained its EVS as 11, placing it in the middle of the

medium vulnerability category. Its conservation status has

been assessed as Least Concern by the IUCN, and this species

is not listed by SEMARNAT. Photo by Eli Garcia-Padilla.

No. 12. Aquiloeurycea cafetalera Parra-Olea, Rovito,

Marquez-Valdelmar, Cruz, Murrieta-Galindo, and Wake,

2010. The Coffee Grove Salamander is a country endemic

species known to occur in the municipalities of Chocoman,

Zongolica, Los Reyes, Tequila y Union, and Progreso in

Veracruz (Frost 2020), as well as in Puebla (Woolrich et

al. 2017). This individual was encountered at Finca Santa

Martha, in the municipality of Los Reyes. Johnson et al.

(2017) calculated the EVS as 17, placing it in the middle of

the high vulnerability category. Its conservation status has not

been determined by either the IUCN or SEMARNAT. Photo

by Matthieu Berroneau.

September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

Table 4. Composition of the native and non-native herpetofauna of Veracruz, Mexico.

ay Sa

Gymnophiona

Subtotal

122

Crocodylia

Squamata

groups in Mexico are, respectively, 408, 154, three, three,

885, and 51 (J. Johnson, unpub. data, 6 July 2020). The

359 herpetofaunal species in Veracruz comprise 26.7%

of the 1,347 species in the entire Mexican herpetofauna

(J. Johnson, unpub. data, 6 July 2020). In all the species

listed in the text, those that are country (Mexico)

endemics are indicated by (*) and those that are state

(Veracruz) endemics are indicated by (**).

Veracruz shares a border with seven other Mexican

states, 1.e., Tamaulipas, San Luis Potosi, Hidalgo, Puebla,

Oaxaca, Chiapas, and Tabasco (Fig. 1). Studies of the

herpetofauna of five of these seven states (Tamaulipas,

Hidalgo, Puebla, Chiapas, and Oaxaca) have appeared

thus far in the MCS (Teran-Juarez et al. 2016; Ramirez-

Bautista et al. 2020; Woolrich-Pifia et al. 2017; Johnson

et al. 2015a; and Mata-Silva et al. 2015, respectively).

The herpetofaunas of each of these five states include,

respectively, 184, 203, 267, 330, and 442 species, and

the number of composite species increases from north

to south. The state area/species richness ratios for

these five states are as follows: Tamaulipas (80,249

km/?/184 = 436.1); Hidalgo (20,813/203 = 102.5); Puebla

(34,306/267 = 128.5); Chiapas (73,311/330 = 222.2); and

Oaxaca (93,757/442 = 212.1). The comparable figure for

Veracruz is 200.1 (71,826/359), which is most similar to

that for Oaxaca. This relationship ranges from highest

to lowest among the six states in the following order:

Tamaulipas, Chiapas, Oaxaca, Veracruz, Puebla, and

Hidalgo.

Patterns of Physiographic Distribution

Here, we recognize four physiographic regions in

Veracruz (Fig. 1) and document the distribution of the

herpetofauna among these four regions in Table 5, and

summarize the data in Table 6.

The total number of species in each of these four

regions ranges from a low of 179 in the Sierra de Los

Tuxtlas (SLT) to 236 in the Sierra Madre Oriental (SMO).

The intermediate figures are 222 for the Transmexican

Volcanic Belt (TVB) and 190 for the Gulf Coastal

Lowlands (GCL). The percentage of the entire state

herpetofauna comprising each of the four physiographic

regions is, in order of size (236/359) 65.7% (SMO),

Table 5. Distribution of the herpetofaunal species of Veracruz, Mexico, by physiographic region. See text for descriptions of these

regions. * = species endemic to Mexico; ** = species endemic to Veracruz; and *** = non-native species.

Physiographic regions of Veracruz Number

taxa Gulf Coastal Sierrade Los SierraMadre Transmexican ot regions

Lowlands Tuxtlas Oriental Volcanic Belt occupied

Anura (76 species)

Bufonidae (9 species)

Anaxyrus compactilis* xX xX 2

Incilius cavifrons** x x 2

Incilius cristatus* xX x xX >

Incilius macrocristatus xX |

Incilius marmoreus* x x x 3

Incilius nebulifer xX xX xX 3

Incilius occidentalis* xX xX 2

Incilius valliceps xX xX xX xX 4

Rhinella horribilis xX xX xX xX 4

Centrolenidae (1 species)

Hyalinobatrachium viridissimum xX xX xX xX 4

Craugastoridae (11 species)

Craugastor alfredi x x x xX 4

Craugastor berkenbuschii* x xX xX xX 4

Craugastor decoratus* xX xX 2

Amphib. Reptile Conserv. 84 September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

re | Pad eee eo; : ;

No. 13. Bolitoglossa platydactyla (Gray, 1831). The Broad-

footed Salamander is a country endemic species distributed

from “southern Tamaulipas and eastern San Luis Potosi south

through Hidalgo to southern Veracruz, Puebla, Oaxaca, and

extreme northeastern Chiapas” (Frost 2020). This individual

was found at Siete Palmas, in the municipality of Ixcatepec.

Wilson et al. (2013a) determined its EVS as 15, placing in

the lower portion of the high vulnerability category. Its

conservation status has been evaluated as Least Concern by

the IUCN, and as Special Protection (Pr) by SEMARNAT.

Photo by Christian Berriozabal-Islas.

No. 15. /sthmura gigantea (Taylor, 1939). The Giant False

Brook Salamander is a country endemic species known

from the La Joya-Jalapa region of Veracruz into northeastern

Hidalgo (Frost 2020). This individual was found on the

road between Zongolica and Tequila, in the municipality of

Zongolica. Wilson et al. (2013a) determined its EVS as 16,

placing it in the middle of the high vulnerability category.

Its conservation status has been calculated as Critically

Endangered by the IUCN, but this species has not been

evaluated by SEMARNAT. Photo by Matthieu Berroneau.

Amphib. Reptile Conserv.

No. 14. Bolitoglossa rufescens. The Common Dwarf

Salamander is a non-endemic species found from “extreme

eastern San Luis Potosi...south through Veracruz, and,

provisionally east of the Isthmus of Tehuantepec in Chiapas

to Belize and northwestern Honduras” (Frost 2020). This

individual was encountered at Los Tuxtlas, in the municipality

of San Andrés Tuxtla. Wilson et al. (2013a) calculated its

EVS as 9, placing it at the upper limit of the low vulnerability

category. Its conservation status was determined as Least

Concern by the IUCN, and as Special Protection (Pr) by

SEMARNAT. Photo by Christian Berriozabal-Islas.

No. 16. Pseudoeurycea werleri Darling and Smith, 1954.

Werler’s False Brook Salamander is a country endemic

species “known from the Sierra de Los Tuxtlas, southern

Veracruz...and the northern slopes of the Sierra de Juarez

[sic] about Vista Hermosa, northern Oaxaca” (Stuart et al.

2008). This individual was located on Volcan San Martin, in

the municipality of San Andrés Tuxtla. Wilson et al. (2013a)

ascertained its EVS as 17, placing it in the middle of the

high vulnerability category. Its conservation status has been

determined as Endangered by the IUCN, and as Special

Protection (Pr) by SEMARNAT. Photo by Eli Garcia-Padilla.

September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

Table 5 (continued). Distribution of the herpetofaunal species of Veracruz, Mexico, by physiographic region. See text for

descriptions of these regions. * = species endemic to Mexico; ** = species endemic to Veracruz; and *** = non-native species.

Physiographic regions of Veracruz Number

Le Gulf Coastal Sierrade Los SierraMadre Transmexican of Peeluus

Lowlands Tuxtlas Oriental Volcanic Belt Groupie’

Craugastor laticeps x xX 2

Craugastor loki x x xX xX 4

Craugastor megalotympanum** x 1

Craugastor mexicanus* x xX 2

Craugastor pygmaeus xX x xX xX 4

Craugastor rhodopis* x x xX xX 4

Craugastor spatulatus* xX x 2

Craugastor vulcani** x xX 2

Eleutherodactylidae (7 species)

Eleutherodactylus cystignathoides xX xX 2

Eleutherodactylus leprus xX xX 2

Eleutherodactylus longipes* xX l

Eleutherodactylus nitidus* x xX W2

Eleutherodactylus planirostris*** x xX xX 3

Eleutherodactylus verrucipes* xX xX 2

Eleutherodactylus verruculatus** xX xX 2

Hylidae (29 species)

Bromeliohyla dendroscarta* xX xX xX 3

Charadrahyla nephila* xX 1

Charadrahyla taeniopus* xX xX 2

Dendropsophus ebraccatus xX xX xX 3

Dendropsophus microcephalus xX xX xX xX 4

Dryophytes arenicolor xX l

Dryophytes euphorbiaceus* xX xX 2

Dryophytes eximius* xX x xX 3

Dryophytes plicatus* xX xX 2

Duellmanohyla chamulae* xX l

Ecnomiohyla valancifer** x 1

Exerodonta bivocata* x 1

Megastomatohyla mixomaculata* xX xX xX 3

Megastomatohyla nubicola** x xX 2

Ptychohyla zophodes* xX x 2

Quilticohyla zoque* xX 1

Rheohyla miotympanum* xX xX x x 4

Sarcohyla arborescandens* xX xX 2

Sarcohyla bistincta* x x 2

Sarcohyla pachyderma** xX 1

Sarcohyla siopela* xX xX 2

Scinax staufferi x x x x 4

Smilisca baudinii xX x x x 4

Smilisca cyanosticta x x xX xX 4

Tlalocohyla godmani* x x 2»

Tlalocohyla loquax xX xX xX xX 4

Tlalocohyla picta xX p46 xX xX 4

Trachycephalus vermiculatus xX xX xX xX 4

Triprion spinosus xX »4 xX xX 4

Leptodactylidae (3 species)

Engystomops pustulosus xX x 2

Leptodactylus fragilis xX xX x xX 4

Leptodactylus melanonotus xX xX xX xX 4

Amphib. Reptile Conserv. 86 September 2021 | Volume 15 | Number 2 | e285

Table 5 (continued). Distribution of the herpetofaunal species of Veracruz, Mexico, by physiographic region. See text for

Torres-Hernandez et al.

descriptions of these regions. * = species endemic to Mexico; ** = species endemic to Veracruz; and *** = non-native species.

Taxa

Microhylidae (3 species)

Gastrophryne elegans

Hypopachus ustus

Hypopachus variolosus

Phyllomedusidae (2 species)

Agalychnis callidryas

Agalychnis moreletii

Ranidae (8 species)

Lithobates berlandieri

Lithobates brownorum

Lithobates catesbeianus***

Lithobates johni*

Lithobates maculatus

Lithobates montezumae*

Lithobates spectabilis*

Lithobates vaillanti

Rhinophrynidae (1 species)

Rhinophrynus dorsalis

Scaphiopodidae (2 species)

Scaphiopus couchii

Spea multiplicata

Caudata (45 species)

Ambystomatidae (1 species)

Ambystoma velasci*

Plethodontidae (42 species)

Aquiloeurycea cafetalera*

Aquiloeurycea cephalica*

Aquiloeurycea praecellens**

Bolitoglossa alberchi*

Bolitoglossa mexicana

Bolitoglossa occidentalis

Bolitoglossa platydactyla*

Bolitoglossa rufescens

Bolitoglossa veracrucis*

Chiropterotriton aureus **

Chiropterotriton casasi**

Chiropterotriton ceronorum*

Chiropterotriton chiropterus*

Chiropterotriton chondrostega*

Chiropterotriton lavae**

Chiropterotriton nubilus**

Chiropterotriton perotensis**

Chiroterotriton terrestris *

Chiropterotriton totonacus**

Isthmura corrugata**

Isthmura gigantea*

Isthmura naucampatepetl**

Parvimolge townsendi**

Pseudoeurycea firscheini*

Pseudoeurycea gadovii*

Pseudoeurycea granitum**

Amphib. Reptile Conserv.

Physiographic regions of Veracruz Number

Gulf Coastal Sierra de Los Sierra Madre ‘Transmexican of regions

Lowlands Tuxtlas Oriental Volcanic Belt pemupied

Xx Xx 2

xX xX xX XxX 4

Xx Xx Xx Xx 4

xX xX Xx Xx 4

xX 4 xX xX 4

Xx xX xX xX 4

xX xX 2

xX XxX XxX xX 4

xX 1

XxX xX 2

Xx Xx p

xX b 4 2

xX Xx Xx 4 4

xX xX 2

xX Xx xX 3

xX xX 2

Xx xX 2

XxX 1

xX Xx Xx xX 4

xX 1

Xx Xx xX xX 4

xX XxX xX xX 4

Xx 1

xX 1

Xx 1

xX 1

Xx 1

xX 1

4 1

xX 1

Xx 1

xX Xx wi

xX Xx 2

xX xX 2

xX Xx 2

XxX xX 2

87 September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

Table 5 (continued). Distribution of the herpetofaunal species of Veracruz, Mexico, by physiographic region. See text for

descriptions of these regions. * = species endemic to Mexico; ** = species endemic to Veracruz; and *** = non-native species.

Physiographic regions of Veracruz Number

Taxa Gulf Coastal Sierra de Los

Lowlands Tuxtlas

Pseudoeurycea leprosa*

Pseudoeurycea lineola**

Pseudoeurycea lynchi*

Pseudoeurycea melanomolga*

Pseudoeurycea nigromaculata**

Pseudoeurycea orchimelas**

Pseudoeurycea werleri*

Thorius dubitus*

Thorius lunaris**

Thorius magnipes**

Thorius minydemus**

Thorius munificus**

Thorius narismagnus**

Thorius pennatulus**

Thorius spilogaster**

Thorius troglodytes**

Salamandridae (1 species)

Notophthalmus meridionalis xX

Sirenidae (1 species)

Siren intermedia xX

Gymnophiona (1 species)

Dermophiidae (1 species)

Dermophis mexicanus x

Crocodylia (1 species)

Crocodylidae (1 species)

Crocodylus moreletii xX

Squamata (217 species)

Anguidae (10 species)

Abronia chiszari**

Abronia graminea*

Abronia reidi**

Abronia taeniata* x

Barisia imbricata*

Gerrhonotus liocephalus xX

Gerrhonotus ophiurus*

Mesaspis antauges**

Ophisaurus ceroni**

Ophisaurus incomptus*

Corytophanidae (4 species)

Basiliscus vittatus

Corytophanes hernandesii

Laemanctus longipes

xxx

Laemanctus serratus

Dactyloidae (18 species)

Norops alvarezdeltoroi*

Norops barkeri*

Norops beckeri

Norops biporcatus

xx mK KM

Norops compressicauda*

Norops cymbops*

Norops duellmani**

Amphib. Reptile Conserv. 88

x x x

of regions

Sierra Madre Transmexican :

occupied

Oriental Volcanic Belt

Kx x KK KM

x x KK

| RO Oe ee NO OO ae LO an \O oS)

x xX xX

x xX x xm mK ~<

~< xx KK MK ~<

FeENNANWENE

x x XK

NN BD

PFNFEFWNHN =

September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

Table 5 (continued). Distribution of the herpetofaunal species of Veracruz, Mexico, by physiographic region. See text for

descriptions of these regions. * = species endemic to Mexico; ** = species endemic to Veracruz; and *** = non-native species.

Taxa

Norops laeviventris

Norops lemurinus

Norops naufragus*

Norops petersii

Norops purpuronectes*

Norops rodriguezii

Norops sagrei***

Norops schiedii**

Norops sericeus

Norops tropidonotus

Norops uniformis

Dibamidae (1 species)

Anelytropsis papillosus*

Diploglossidae (4 species)

Celestus enneagrammus*

Celestus ingridae**

Celestus legnotus*

Celestus rozellae

Eublepharidae (1 species)

Coleonyx elegans

Gekkonidae (3 species)

Hemidactylus frenatus***

Hemidactylus mabouia ***

Hemidactylus turcicus***

Iguanidae (2 species)

Ctenosaura acanthura

Iguana iguana

Mabuyidae (1 species)

Marisora lineola

Phrynosomatidae (20 species)

Holbrookia propinqua

Phrynosoma braconnieri*

Phrynosoma orbiculare*

Sceloporus aeneus*

Sceloporus aureolus*

Sceloporus bicanthalis*

Sceloporus cyanogenys

Sceloporus formosus*

Sceloporus grammicus

Sceloporus internasalis

Sceloporus jalapae*

Sceloporus megalepidurus*

Sceloporus mucronatus *

Sceloporus salvini*

Sceloporus scalaris*

Sceloporus serrifer

Sceloporus spinosus*

Sceloporus teapensis

Sceloporus torquatus*

Sceloporus variabilis

Scincidae (5 species)

Amphib. Reptile Conserv.

Gulf Coastal

Lowlands

Physiographic regions of Veracruz Number

Sierra de Los Sierra Madre =‘ Transmexican oh rezions

Tuxtlas Oriental Volcanic Belt occupied

xX Xx Xx 3

Xx Xx Xx 4

xX 1

xX Xx Xx 4

4 2

xX 2

Xx Xx 2

xX xX b 4 4

Xx Xx xX 3

xX 2

Xx xX 2

XxX xX 2

xX 1

Xx 1

XxX Xx xX 4

xX 2

Xx xX 3

xX 2

Xx xX XxX 4

Xx 2

Xx xX xX 4

xX xX bs

xX xX 2

XxX XxX wi

xX 1

xX xX 2

Xx 1

XxX XxX 2

4 xX 3

xX Xx 2

xX xX 2

Xx xX 2

xX x 2

xX xX xX 3

xX xX 2

XxX 2

Xx xX 2

xX xX xX 4

xX xX Z

Xx Xx Xx 4

89 September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

Table 5 (continued). Distribution of the herpetofaunal species of Veracruz, Mexico, by physiographic region. See text for

descriptions of these regions. * = species endemic to Mexico; ** = species endemic to Veracruz; and *** = non-native species.

Taxa

Plestiodon brevirostris*

Plestiodon copei*

Plestiodon lynxe*

Plestiodon sumichrasti

Plestiodon tetragrammus

Sphaerodactylidae (2 species)

Gonatodes albogularis

Sphaerodactylus glaucus

Sphenomorphidae (3 species)

Scincella cherriei

Scincella gemmingeri*

Scincella silvicola*

Teiidae (5 species)

Aspidoscelis costata*

Aspidoscelis deppii

Aspidoscelis gularis

Aspidoscelis guttatus*

Holcosus amphigrammus*

Xantusiidae (5 species)

Lepidophyma flavimaculatum

Lepidophyma pajapanense*

Lepidophyma sylvaticum*

Lepidophyma tuxtlae*

Lepidophyma zongolica*

Xenosauridae (3 species)

Xenosaurus grandis*

Xenosaurus rectocollaris*

Xenosaurus tzacualtipantecus*

Boidae (1 species)

Boa imperator

Colubridae (41 species)

Coluber constrictor

Conopsis acuta*

Conopsis lineata*

Conopsis nasus*

Dendrophidion vinitor

Drymarchon melanurus

Drymobius chloroticus

Drymobius margaritiferus

Ficimia olivacea*

Ficimia publia

Ficimia streckeri

Ficimia variegata*

Lampropeltis polyzona

Lampropeltis triangulum

Leptophis ahaetulla

Leptophis mexicanus

Masticophis flagellum

Masticophis mentovarius

Masticophis schotti

Mastigodryas melanolomus

Amphib. Reptile Conserv.

Gulf Coastal

Lowlands

xx KX

x x MK MK

~ xX XM

Km KKM KK KK KK

Physiographic regions of Veracruz Number

Sierra de Los Sierra Madre =‘ Transmexican oh rezions

Tuxtlas Oriental Volcanic Belt occupied

Xx Xx 2

Xx Xx Xx 3

xX XxX 3

xX Xx Xx 3

Xx 1

xX Xx Xx 4

xX Xx xX 4

xX Xx 2

Xx xX 2

xX xX 3

xX Xx xX 4

xX XxX xX 4

xX 2

xX p

xX 2

Xx 2

xX Xx 83

4 xX XxX 3

xX 1

Xx 1

xX xX xX 4

xX xX w

xX xX 2

xX 1

xX Xx xX 4

xX 2

Xx xX x 4

XxX xX xX 3

xX 2

Xx 2

XxX xX xX 4

Xx xX XxX 4

Xx 2

xX 2

xX Xx 3

90 September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

Table 5 (continued). Distribution of the herpetofaunal species of Veracruz, Mexico, by physiographic region. See text for

descriptions of these regions. * = species endemic to Mexico; ** = species endemic to Veracruz; and *** = non-native species.

Physiographic regions of Veracruz Number

of regions

Taxa Gulf Coastal Sierra de Los Sierra Madre Transmexican :

occupied

Lowlands Tuxtlas Oriental Volcanic Belt

Oxybelis aeneus x xX xX

Oxybelis fulgidus x xX

Pantherophis emoryi xX

Phrynonax poecilonotus x x

Pituophis deppei* xX

x xX

Pituophis lineaticollis

Pseudelaphe flavirufa x xX

Salvadora bairdi* x

Salvadora grahamiae

Senticolis triaspis

Spilotes pullatus

Stenorrhina degenhardtii

xx KKK KK

x x x

~ rx

Stenorrhina freminvillii

Tantilla bocourti*

Tantilla rubra

Tantilla schistosa xX xX

Tantilla shawi*

Kx KKK KK KK

x x x XK

Tantilla slavensi**

Tantillita lintoni x

Trimorphodon biscutatus

x x XK

WNRE EP RNNF KR KR RNWWNWNNN W

~ x x

Trimorphodon tau*

Dipsadidae (46 species)

Adelphicos quadrivirgatum

Adelphicos visoninum

Amastridium sapperi

Chersodromus liebmanni*

Clelia scytalina

Coniophanes bipunctatus

Coniophanes fissidens

xx KKK

Coniophanes imperialis

Coniophanes quinquevittatus

Coniophanes taeniatus*

Kx mK Km MK MK KM OM

Conophis lineatus

xxx mK KK KM

Conophis morai**

Diadophis punctatus xX

Geophis bicolor*

Geophis blanchardi*

xx KKM MK

Geophis carinosus xX xX

Geophis chalybeus** x

Geophis juliai** xX

Geophis lorancai*

Geophis mutitorques*

Geophis semidoliatus*

Imantodes cenchoa

Imantodes gemmistratus

Leptodeira frenata

Leptodeira maculata

Leptodeira polysticta

Leptodeira septentrionalis

Ninia diademata

Ninia sebae

FFA NAPNWHWrRKNWRYKNNK NN FwWN FH HHPwWwW He W

KK MK MK KM

KKM KM MM KM

x xX xX

x mx x

Amphib. Reptile Conserv. 91 September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

Table 5 (continued). Distribution of the herpetofaunal species of Veracruz, Mexico, by physiographic region. See text for

descriptions of these regions. * = species endemic to Mexico; ** = species endemic to Veracruz; and *** = non-native species.

Taxa

Oxyrhopus petolarius

Pliocercus elapoides

Rhadinaea cuneata*

Rhadinaea decorata

Rhadinaea forbesi**

Rhadinaea fulvivittis*

Rhadinaea macdougalli*

Rhadinaea marcellae*

Rhadinaea quinquelineata*

Rhadinella schistosa*

Sibon dimidiatus

Sibon linearis**

Sibon nebulatus

Tretanorhinus nigroluteus

Tropidodipsas fasciata

Tropidodipsas sartorii

Xenodon rabdocephalus

Elapidae (4 species)

Micrurus diastema*

Micrurus elegans

Micrurus limbatus**

Micrurus tener

Leptotyphlopidae (4 species)

Epictia phenops

Epictia resetari*

Rena dulcis

Rena myopica*

Natricidae (14 species)

Nerodia rhombifer

Storeria dekayi

Storeria storerioides*

Thamnophis chrysocephalus*

Thamnophis conanti*

Thamnophis cyrtopsis

Thamnophis eques

Thamnophis godmani*

Thamnophis marcianus

Thamnophis proximus

Thamnophis pulchrilatus*

Thamnophis scalaris*

Thamnophis scaliger*

Thamnophis sumichrasti*

Sibynophiidae (1 species)

Scaphiodontophis annulatus

Typhlopidae (2 species)

Amerotyphlops tenuis

Virgotyphlops braminus***

Viperidae (17 species)

Agkistrodon taylori*

Bothrops asper

Cerrophidion petlalcalensis*

Amphib. Reptile Conserv.

Gulf Coastal

Lowlands

xx KX

xx mK KK

Physiographic regions of Veracruz Number

Sierra de Los Sierra Madre =‘ Transmexican oF regions

Tuxtlas Oriental Volcanic Belt occupied

xX 2

xX Xx XxX 4

Xx XxX 3

xX Xx Xx 4

XxX 1

Xx Xx 2

xX XxX z

Xx 1

xX 1

Xx 1

Xx XxX 2

Xx 1

xX 2

xX Xx xX 4

XxX 2

xX XxX Xx 4

Xx Xx xX 4

xX 1

Xx 1

Xx Xx 3

xX XxX 2

xX 2

Xx 2

xX xX 3

xX xX 2

Xx xX 2

xX p.4 2

xX 1

xX xX 2

xX xX ws

xX xX 2

XxX xX xX 4

xX 1

xX D4 2

xX 1

xX xX 2

xX xX 3

XxX xX xX 4

xX xX XxX 4

Xx 2

XxX Xx xX 4

xX xX 2

92 September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

Table 5 (continued). Distribution of the herpetofaunal species of Veracruz, Mexico, by physiographic region. See text for

descriptions of these regions. * = species endemic to Mexico; ** = species endemic to Veracruz; and *** = non-native species.

Physiographic regions of Veracruz

Taxa Gulf Coastal

Lowlands

Crotalus aquilus*

Crotalus atrox x

Crotalus intermedius* xX

Crotalus mictlantecuhtli** XxX

Crotalus molossus

Crotalus polystictus*

Crotalus ravus*

Crotalus scutulatus

Crotalus totonacus*

Crotalus triseriatus*

Metlapilcoatlus nummifer*

Metlapilcoatlus olmec xX

Ophryacus smaragdinus*

Ophryacus undulatus*

Testudines (19 species)

Cheloniidae (4 species)

Caretta caretta

Chelonia mydas

Eretmochelys imbricata

x x Kx xX

Lepidochelys kempii

Chelydridae (1 species)

Chelydra rossignonii xX

Dermatemyidae (1 species)

Dermatemys mawii x

Dermochelyidae (1 species)

Dermochelys coriacea xX

Emydidae (3 species)

Terrapene mexicana* x

Trachemys scripta*** x

Trachemys venusta x

Geoemydidae (1 species)

Rhinoclemmys areolata xX

Kinosternidae (5 species)

Kinosternon acutum x

Kinosternon flavescens x

Kinosternon herrerai* x

Kinosternon leucostomum x

Kinosternon scorpioides x

Staurotypidae (2 species)

Claudius angustatus

Staurotypus triporcatus

Testudinidae (1 species)

Gopherus berlandieri xX

(222/359) 61.8% (TVB), (190/359) 52.9% (GCL), and

(179/359) 49.9% (SLT). The average percentage of

occupancy is 57.6%, or somewhat in excess of one-half

of the number of Veracruz’s herpetofaunal species.

The numbers of amphibian species in the SMO and

TVB (Table 6) are very similar to each other (57 and

56 anurans of 76; 28 and 31 salamanders of 45; 0 and

Amphib. Reptile Conserv.

Sierra de Los

Number

of regions

Transmexican E

occupied

Volcanic Belt

Sierra Madre

Tuxtlas Oriental

Kx KM KKK XK

x KKK MK

NNNNNNNNKENWWEE

x xX

xx KK

NNN N

NNN Ww

one caecilian of one; and totals of 85 and 88 of 122,

respectively). The numbers of reptile species in these

two regions (Table 6), however, are relatively dissimilar

when compared to the situation with amphibians (0 and

0 crocodylians of one; 151 and 132 squamates of 217; 0

and two turtles of 19; and totals of 151 and 134 of 237,

respectively).

93 September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

Table 6. Summary of distributional occurrence of the herpetofaunal families in Veracruz, Mexico, by physiographic province. GLC

= Gulf Coastal Lowlands; SLT = Sierra de los Tuxtlas; SMO = Sierra Madre Oriental; and TVB = Transmexican Volcanic Belt.

Family

Bufonidae

Centrolenidae

Craugastoridae

Eleutherodactylidae

Hylidae

Leptodactylidae

Microhylidae

Phyllomedusidae

Ranidae

Rhinophrynidae

Scaphiopodidae

Subtotal

Ambystomatidae

Plethodontidae

Salamandridae

Sirenidae

Subtotal

Dermophiidae

Subtotal

Total

Crocodylidae

Subtotal

Anguidae

Corytophanidae

Dactyloidae

Dibamidae

Diploglossidae

Eublepharidae

Gekkonidae

Iguanidae

Mabuyidae

Phrynosomatidae

Scincidae

Sphaerodactylidae

Sphenomorphidae

Tetidae

Xantusiidae

Xenosauridae

Subtotal

Boidae

Colubridae

Dipsadidae

Elapidae

Leptotyphlopidae

Natricidae

Sibynophiidae

Typhlopidae

Viperidae

Subtotal

Cheloniidae

Chelydridae

Dermatemyidae

Dermochelyidae

Emydidae

Geoemydidae

Kinosternidae

Staurotypidae

Testudinidae

Subtotal

Total

Sum Total

Amphib. Reptile Conserv.

Number of

species

NR oNwWwRr

—

HAeunvwnanSenv-s- Ze oec-Re-

WEAN NHwWHEHHERBYANHNYN Be Fl Saevynraenv-- | Hevse- Vera] FoeH-unvwgerara

Distributional occurrence

SLT SMO TVB

4 7 v3

1 l 1

8 8 8

2 5 4

15 23 22

3 2 2

2 2 2

p) 5 6

] ae —

— 2, D:

44 57 56

—- 1 1

11 26 30

ee 1 un

11 28 31

l —- l

1 — 1

56 85 88

| = —_

1 =— —

3 6 f

3 2 3

12 9 7

— 1 1

l 2 1

l 1 l

3 — 1

2 l 1

l l 1

4 17 17

2 > 4

l l l

3 3

2 4 4

eS) 2, 1

| 3 1

42 58 53

1 1 1

22 26 23

32 32 25

8 3 2

Z 4 —

| 13 11

1 — 1

2 2 2

3 (2 14

67 93 79

4 =

l = —

1 — =

1 ~- 1

l —— —

3 ~- i

2 a —

13 — 2

123 151 134

179 236 222

September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

No. 17. Abronia graminea. The Sierra de Tehuacan Arboreal

Alligator Lizard is a country endemic species distributed in

central Veracruz, eastern Puebla, and Oaxaca (Uetz et al.

2020). This individual was found at Finca Santa Martha,

in the municipality of Los Reyes. Wilson et al. (2013b)

determined its EVS as 15, placing it in the lower portion of the

high vulnerability category. Its conservation status has been

assessed as Endangered by the IUCN, and as Threatened (A)

by SEMARNAT. Photo by Matthieu Berroneau.

No. 19. Gerrhonotus ophiurus Cope, 1867. The Snake Lizard

is acountry endemic species distributed from central San Luis

Potosi south to eastern Querétaro, Hidalgo, Tlaxcala, northern

Veracruz, and Puebla (Lemos-Espinal and Dixon 2013). This

individual was discovered at Comapa, in the municipality

of the same name. Wilson et al. (2013b) determined its EVS

as 12, placing it in the middle of the medium vulnerability

category. Its conservation status has been determined as Least

Concern by the IUCN, but this species has not been evaluated

by SEMARNAT. Photo by Aaron Arias.

Amphib. Reptile Conserv.

No. 18. Barisia imbricata. The Transvolcanic Alligator

Lizard is a country endemic species that occurs broadly in the

Sierra Madre Oriental and Transmexican Volcanic Belt from

Hidalgo south to Oaxaca, and west to Jalisco and Michoacan

(Ramirez-Bautista et al. 2014). This individual was located at

San Isidro, in the municipality of Mariano Escobedo. 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 determined as Least Concern by the IUCN, and

as Special Protection (Pr) by SEMARNAT. Photo by René

Avalos-Vela.

.. : Ae |

No. 20. Ophisaurus ceroni Holman, 1965. Ceron’s Glass

Lizard is a state endemic species distributed in the Gulf Coastal

Lowlands physiographic region (Uetz et al. 2020). This

individual was located at Cuitlahuac, in the municipality of

the same name. Wilson et al. (2013b) calculated its EVS as 14,

placing it at the lower limit of the high vulnerability category.

Its conservation status has been assessed as Endangered by

the IUCN, and as Threatened (A) by SEMARNAT. Photo by

Matthieu Berroneau.

September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

The members of the Veracruz herpetofauna occupy

from 1-4 of the four physiographic regions, as follows:

one (86; 24.0%), two (153; 42.6%), three (45; 12.5%),

and four (75; 20.9%). The mean regional occupancy 1s

2.3, meaning that each species, on average, inhabits only

slightly more than one-half of the physiographic regions

located in the state.

A large proportion of the herpetofauna is found in

one or two regions (239 species, or 66.6% of the total).

This situation is of significant conservation importance,

as discussed below in the section on conservation status.

The number of species found in a single region varies

from 16 in the SLT to 27 in the GCL. The 27 single-

region species in the GCL are:

Incilius macrocristatus

Eleutherodactylus longipes*

Duellmanohyla chamulae*

Exerodonta bivocata*

Quilticohyla zoque*

Bolitoglossa veracrucis*

Siren intermedia

Ophisaurus ceroni**

Norops alvarezdeltoroi*

Norops compressicauda*

Norops purpuronectes*

Celestus rozellae

Holbrookia propinqua

Gonatodes albogularis

Aspidoscelis deppii

Coluber constrictor

Conopsis acuta*

Lampropeltis triangulum

Leptophis ahaetulla

Masticophis flagellum

Adelphicos visoninum

Crotalus atrox

Dermatemys mawii

Terrapene mexicana*

Trachemys venusta

Kinosternon flavescens

Gopherus berlandieri

Sixteen of the 27 GCL single-region species (59.3%)

are non-endemics, 10 (37.0%) are country endemics

(indicated by asterisks) and one (3.7%) is a state endemic.

As expected, the largest number of these lowland-

inhabiting species ranges outside the limits of Mexico.

The 25 single-region species in the SMO are as follows:

Sarcohyla pachyderma**

Chiropterotriton aureus **

Chiropterotriton terrestris*

Thorius lunaris**

Thorius magnipes**

Amphib. Reptile Conserv.

Thorius minydemus**

Thorius munificus**

Norops naufragus*

Celestus legnotus*

Sceloporus aureolus*

Sceloporus cyanogenys

Plestiodon tetragrammus

Xenosaurus rectocollaris*

Xenosaurus tzacualtipantecus*

Tantilla shawi*

Geophis chalybeus**

Geophis mutitorques*

Rhadinaea forbesi**

Rhadinaea marcellae*

Rhadinaea quinquelineata*

Rhadinella schistosa*

Micrurus tener

Thamnophis conanti*

Thamnophis cyrtopsis

Thamnophis pulchrilatus*

Thirteen of the 25 SMO single-region species (52.0%)

are Mexican endemics, eight (32.0%) are state endemic

species, and four (16.0%) are non-endemic species. As

expected, the largest number of these species in this

montane region are Mexican endemics, with the next

largest number being state endemics, for a total of 21

endemic taxa (84.0%).

The 18 single-region species in the TVB are as follows:

Dryophytes arenicolor

Lithobates johni*

Chiropterotriton casasi**

Chiropterotriton ceronorum*

Chiropterotriton chiropterus*

Chiropterotriton chondrostega*

Chiropterotriton lavae**

Chiropterotriton nubilus**

Chiropterotriton perotensis**

Chiropterotriton totonacus**

Isthmura corrugata**

Thorius spilogaster**

Ophisaurus incomptus*

Stenorrhina freminvillii

Geophis bicolor*

Thamnophis scaliger*

Crotalus aquilus*

Crotalus polystictus*

Nine of the 18 single-region TVB species (50.0%) are

country endemics, seven (38.9%) are state endemics, and

two (11.1%) are non-endemics. Again, it was expected

that the largest number of these species in this montane

region would be Mexican endemics, with the next largest

number being state endemics, for a total of 16 endemic

taxa (88.9%).

September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

No. 21. Corytophanes hernandezii (Wiegmann, 1831).

Hernandez’s Helmeted Basilisk is a non-endemic species

ranging from southeastern San Luis Potosi south to

northwestern Honduras (Kohler 2008). This individual was

located at Los Tuxtlas, in the municipality of San Andrés

Tuxtla. Wilson et al. (2013b) assessed its EVS at 13, placing

it at the upper limit of the medium vulnerability category. Its

conservation status has been determined as Least Concern by

the IUCN, and as Special Protection (Pr) by SEMARNAT.

Photo by Christian Berriozabal-Islas.

=e , tg 5 an r . < > —

No. 23. Celestus enneagrammus (Cope, 1861). The Huaxteca

Lesser Galliwasp is a country endemic species found in

the states of Veracruz, Puebla, Oaxaca, and Chiapas (Uetz

et al. 2020). This individual was located at Tequila, in

the municipality of the same name. Wilson et al. (2013b)

ascertained its EVS as 14, placing it at the lower limit of the

high vulnerability category. Its conservation status 1s indicated

as Least Concern by the IUCN, and as Special Protection (Pr)

by SEMARNAT. Photo by René Avalos-Vela.

Amphib. Reptile Conserv.

- ‘< 3 :

No. 22. Norops barkeri Schmidt, 1939. Barker’s Anole is a

country endemic species found in the region of the Isthmus

of Tehuantepec in Veracruz, Tabasco, Oaxaca, and Chiapas

(Kohler 2008). This individual was found at Los Tuxtlas, in

the municipality of San Andrés Tuxtla. Wilson et al. (2013b)

determined its EVS as 15, placing in the lower portion of the

high vulnerability category. Its conservation status has not

been evaluated by either the IUCN or SEMARNAT. Photo by

Christian Berriozabal-Islas.

No. 24. Sceloporus salvini Gunther, 1890. Salvin’s Spiny

Lizard is a country endemic species that ranges into Veracruz

and Oaxaca (Uetz et al. 2020). This individual was discovered

at Tepexilotla, in the municipality of Chocaman. Wilson et

al. (2013b) determined its EVS as 15, placing it in the lower

portion of the high vulnerability category. Its conservation

status has been evaluated as Data Deficient by the IUCN, and

as Threatened (A) by SEMARNAT. Photo by René Avalos-

Vela.

September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

Fig. 7. UPGMA generated dendrogram illustrating the similar-

ity relationships of species richness among the herpetofaunal

components in the four physiographic regions of Veracruz

(based on the data in Table 7; Sokal and Michener 1958). Simi-

larity values were calculated using Duellman’s (1990) Coef-

ficient of Biogeographic Resemblance (CBR).

The 16 single-region species in the SLT are as follows:

Craugastor megalotympanum**

Charadrahyla nephila*

Ecnomiohyla valancifer**

Bolitoglossa alberchi*

Bolitoglossa occidentalis

Pseudoeurycea orchimelas**

Pseudoeurycea werleri*

Thorius narismagnus**

Abronia chiszari**

Abronia reidi**

Norops duellmani**

Celestus ingridae**

Dendrophidion vinitor

Tantilla slavensi**

Sibon linearis**

Micrurus limbatus**

Eleven of the 16 single-region SLT species (68.8%) are

state endemics, three (18.8%) are country endemics,

and two (12.5%) are non-endemics. Given the isolation

of this montane region relative to others in the vicinity,

this is also the expected pattern, with the prevalence of

state endemics versus the other distributional categories

represented. In total, this region supports 14 endemic

taxa (87.5%).

In summary, of the 86 single-region species in

Veracruz, 24 (27.9%) are non-endemics, 35 (40.7%)

are Mexican endemics, and 27 (31.4%) are state

endemics. Of the four physiographic regions, the SMO

has the greatest conservation significance given that it

encompasses the greatest overall number of species (236

of 359, or 65.7%), the greatest numbers of country and

state endemics (130 [109 and 21, respectively] of 182, or

71.4%), and the second highest number of single-region

species (25 of 86, or 29.1%).

A Coefficient of Biogeographic Resemblance (CBR)

matrix was constructed for assessing the herpetofaunal

similarity relationships (Duellman 1990) among the

four physiographic regions in Veracruz (Table 7) and

those data were used to create a UPGMA dendrogram

(Fig. 7; Sokal and Michener 1958). The SMO contains

the greatest amount of species richness (236 species)

and the SLT the least (179 species). The mean species

richness value for all four regions is 206.8. The number

of shared species between each regional pair ranges

from a high of 190 between the SMO and TVB, to a

low of 100 between the TVB and GCL. The mean value

of shared species among all four regions is 123.0. The

lowest number of shared species between the TVB and

GCL (100 species) was expected, as these two regions

are completely separated from each other by the SMO

and are environmentally different on an elevational scale.

The GCL, with an elevational range from sea level to

about 200 m, contains tropical evergreen forest, scrub,

sub-deciduous forest, and tropical dry forest (CONABIO,

2008). Conversely, with a limited geographic area within

Veracruz, the TVB contains primarily coniferous and

oak forest vegetation with the remainder comprised of

subalpine scrub, cloud forest, xerophilous scrub, and

tropical dry forest. The elevations for the TVB range

from 1,000 m in sloping river valleys to 5,700 m on the

highest volcanic peak. The TVB and SMO share the most

Table 7. Pair-wise comparison matrix of Coefficient of Biogeographic Resemblance (CBR) data of herpetofaunal relationships for

the four physiographic regions in Veracruz, 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. 7 for the UPGMA dendrogram produced from the

CBR data.

Gulf Coastal Sierra de Los Tuxtlas Sierra Madre Transmexican

Lowlands Oriental Volcanic Belt

Gulf Coastal Lowlands 190 137 105 100

Sierra de Los Tuxtlas 0.74 179 104 102

Sierra Madre Oriental 0.49 0.50 236 190

Transmexican Volcanic Belt 0.49 0.51 0.83 222

Amphib. Reptile Conserv.

September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

LR)

-—. ° Z wa

7 ' ’

. 2. <=.

No. 25. Scincella cherriei (Cope, 1893). The Brown Forest

Skink is a non-endemic species occurring from Veracruz

to western Panama (Uetz et al. 2020). This individual was

found at Los Tuxtlas, in the municipality of San Andrés

Tuxtla. Wilson et al. (2013b) calculated its EVS as 8, placing

it in the upper portion of the low vulnerability category. Its

conservation status has not been assessed by either the IUCN

or SEMARNAT. Photo by Christian Berriozabal-Islas.

ete. “3

No. 27. Sphaerodactylus glaucus (Cope, 1866). The Collared

Dwarf Gecko is non-endemic species occurring from Veracruz,

Tabasco, Oaxaca, and Chiapas in Mexico, through the Yucatan

Peninsula and northern Guatemala to the interior of western

Honduras, at elevations from 200 to 1,000 m (Kohler 2008).

This individual was found at Los Tuxtlas, in the municipality

of San Andrés Tuxtla. Wilson et al. (2013b) determined its

EVS as 12, placing it in the medium vulnerability category.

This species has not been assessed by either the IUCN or

SEMARNAT. Photo by Christian Berriozabal-Islas.

Amphib. Reptile Conserv.

No. 26. Lepidophyma tuxtlae Werler and Shannon, 1957. The

Tuxtla Tropical Night Lizard is a country endemic species

distributed from the Sierra de Los Tuxtlas to the El Ocote region

of Chiapas (K6éhler 2008). This individual was located at Los

Tuxtlas, in the municipality of San Andrés Tuxtla. Wilson et

al. (2013b) determined its EVS as 11, placing it in the middle

of the medium vulnerability category. Its conservation status 1s

designated as Data Deficient by the IUCN, and as Threatened

(A) by SEMARNAT. Photo by Christian Berriozabal-Islas.

No. 28. Boa imperator Daudin, 1803. The Central American

Boa Constrictor is a non-endemic species occurring in Central

America (including South American populations in the

Choco of Colombia and Ecuador [and probably Peru], and

North American populations along the Gulf coast of Mexico

(west of the Isthmus of Tehuantepec; Card et al. 2016). This

individual was encountered at Los Tuxtlas, in the municipality

of San Andrés Tuxtla. We calculated its EVS as 10, placing

it at the lower limit of the medium vulnerability category. Its

conservation status has not been determined by the IUCN or

SEMARNAT. Photo by Christian Berriozabal-Islas.

September 2021 | Volume 15 | Number 2 | e285

The herpetofauna of Veracruz, Mexico

species (190), which also was expected because they are

directly adjacent to each other in Veracruz and share

many of the same montane environments in their limited

geographic ranges within the state. The SLT and GCL

share the second largest number of species (137). The

SLT is an isolated mountainous region with a maximum

elevation of 1,700 m, which is nearly surrounded by

lowland habitats, some of which ascend upward to an

elevation of 200 m into lower montane areas on volcanic

slopes. Pairwise comparisons of the aligned regions in

order from highest to lowest species richness (underlined

values) and their corresponding numbers of shared

species (in parentheses) are as follows:

SMO 236: TVB (190), SLT (104), GCL (105)

TVB 222: SMO (190), SLT (102), GCL (100)

GCL 190: SLT (137), SMO (105), TVB (100)

SLT 179: GCL (137), SMO (104), TVB (102)

In general, the pattern indicates how species richness

values within each of the four biogeographic regions of

Veracruz equate to numbers of shared species among

the other three regions. There is a higher correlation of

species richness values to the numbers of shared species

between regions that are in contact with each other, but

also a correlation between regions that share ecological

parameters. Interestingly, the two regions that share the

second highest number of species (137) are a highland

region (SLT) and a lowland region (GCL), which is

probably due to the GCL containing many generalist

species that tolerate both montane and non-montane

environments at low to moderate elevations. The fact that

the GCL shares fewer species with the SMO and TVB

gives credibility to the premise that regions separated by

ecological barriers will share fewer species than they will

with regions in direct contact.

The following data show the ranges and mean numbers

of shared species (bold in parentheses) for each of the

four regions, and are arranged according to increasing

species richness (underlined values) in each region:

Sierra Madre Oriental, SMO (236): 104—190 (133)

Transmexican Volcanic Belt, TVB (222): 100-190

(130.7)

Gulf Coastal Lowlands, GCL (190): 100-137 (114)

Sierra de Los Tuxtlas, SLT (179): 102-137 (114.3)

The mean numbers of shared species compared to the

species richness in the four regions indicate that higher

Species richness in a pairwise comparison tends, with one

exception, to translate into higher reciprocal numbers when

all the regional pairs are totaled. The comparison between

the SMO and TVB are 1* and 2™ in species richness and 1°

and 2" in the average value of shared species, respectively.

The minor exception is that the GCL, a lowland region,

is 3™ in species richness but last (4) in the mean number

of shared species, whereas the SLT is lower in species

Amphib. Reptile Conserv.

richness but slightly higher in the mean numbers of shared

species. Apparently, the size of the region has an important

effect on species richness, and the ecological variability

(highlands vs. lowlands) has an important effect on the

average number of shared species in Veracruz.

Regarding area, the GCL in Veracruz is by far larger

than all three mountainous areas combined (SMO,

TVB, and SLT), but is 3“ in species richness; it has 11

more species than the SLT. The total area of the SLT is

much smaller compared to the other three regions and

it is located only within a small portion of southeastern

Veracruz, whereas the other three regions have much

larger ranges outside of the state.

Based on the data in Table 7, a UPGMA dendrogram

(Fig. 7) depicts herpetofaunal similarity resemblance

patterns in a hierarchical fashion among the four

physiographic regions of Veracruz (Fig. 1). The

dendrogram is composed of two distinct clusters: one

comprising two montane regions (SMO and TVB) at the

0.83 level, and the other containing one montane region

(SLT) and one lowland region (GCL) at the 0.74 level.

The two clusters connect with each other at the 0.50

level. Regions in both clusters have portions adjacent

to each other somewhere in their total ranges, and the

GCL surrounds the SLT to a varying degree only in

southeastern Veracruz. Many of the shared species with

the GCL contain wide-ranging generalist species that

occur all along the Gulf lowlands from Tamaulipas and

the adjacent USA into the Yucatan Peninsula of Mexico

and northern Central America, and a few enter northern

South America (Wilson and Johnson 2010). In our

opinion, those lowland generalist species are the main

reason why the SLT clusters with the GLC instead of

with the SMO, even though the GLC and SMO share

borders along the northern half of Veracruz.

Distribution Status Categorizations

This analysis of the distributional status of the members

of the Veracruz herpetofauna utilizes the same system

employed by Alvarado-Diaz et al. (2013) and all the other

entries in the MCS (see above). The four categories 1n this

system are non-endemic, country endemic, state endemic,

and non-native. The data are presented based on these

categories in Table 8, and summarized in Table 9.

In descending order of size, the numbers of species in

each of these categories are non-endemics: 169 (47.1%),

country endemics: 138 (38.4%), state endemics: 44

(12.3%), and non-natives: 8 (2.2%). The herpetofauna

of Veracruz, therefore, resembles several other state

herpetofaunas covered previously in the MCS in that

the largest number of species fall into the non-endemic

category, 1.e., 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. 2017); and Coahuila (Lazcano et al. 2019). In other

September 2021 | Volume 15 | Number 2 | e285

Torres-Hernandez et al.

No. 29. Spilotes pullatus Linnaeus, 1758. The Tropical Tree

Snake is a non-endemic species found from Tamaulipas

southward through Central America and South America to

Argentina on the Atlantic versant, and from the Isthmus of

Tehuantepec to Ecuador on the Pacific versant (Lemos-

Espinal and Dixon 2013). This individual was found at Los

Tuxtlas, in the municipality of San Andrés Tuxtla. Wilson et

al. (2013b) determined its EVS as 6, placing it in the middle of

the low vulnerability category. Its conservation status has not

been determined by either the IUCN or SEMARNAT. Photo

by Christian Berriozabal-Islas.

No. 31. Clelia scytalina (Cope, 1867). The Mexican Snake

Eater is a non-endemic species ranging from southern Mexico

to Guatemala and Belize (Kohler 2008). This individual was

found at Los Tuxtlas, in the municipality of San Andrés Tuxtla.

Wilson et al. (2013b) determined its EVS as 13, placing it

at the upper limit of the medium vulnerability category. Its

conservation status has not been determined by either the

IUCN or SEMARNAT. Photo by Christian Berriozabal-Islas.

Amphib. Reptile Conserv.

me EE ee =e

No. 30. Adelphicos quadrivirgatum Jan, 1862. The

Mesoamerican Earth Snake is a non-endemic species

distributed from Tamaulipas to Honduras on the Atlantic

versant, and from Oaxaca to Guatemala on the Pacific versant

(Lemos-Espinal and Dixon 2013). This individual was located

at Los Tuxtlas, in the municipality of San Andrés Tuxtla.

Wilson et al. (2013b) ascertained its EVS as 10, placing it

at the lower limit of the medium vulnerability category. Its

conservation status has been calculated as Least Concern by

the IUCN, and as Special Protection (Pr) by SEMARNAT.

Photo by Christian Berriozabal-Islas.

No. 32. Jmantodes cenchoa (Linnaeus, 1758). The Blunt-

headed Treesnake is a non-endemic species occurring at

low and moderate elevations (up to 1,600 m) on the Atlantic

versant from southern Tamaulipas, southward through

Central and South America to Argentina. It also occurs along

the Pacific lowlands and premontane slopes from Chiapas

to Guatemala. In the Yucatan Peninsula, it is known from

southern Campeche and Quintana Roo, but apparently is

absent from the arid north-western region of the peninsula

(Heimes 2016). This individual was found at Los Tuxtlas, in

the municipality of San Andrés Tuxtla. Wilson et al. (2013b)

determined its EVS as 6, placing it in the low vulnerability

category. Its conservation status has not been determined by

either the IUCN or SEMARNAT. Photo by Eli Garcia-Padilla.

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The herpetofauna of Veracruz, Mexico

Table 8. Distributional and conservation status measures for members of the herpetofauna of Veracruz, Mexico. Distributional

Status: CE = endemic to country of Mexico; SE = endemic to state of Veracruz; 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://www.mesoamericanherpetology.com),

as follows: 3 = species distributed only in Mexico and the United States; 4 = species found only in Mexico and Central America;

6 = species ranging from Mexico to South America; 7 = species ranging from the United States to Central America; 8 = species

ranging from the United States to South America; and 9 = Oceanic species. Environmental Vulnerability Scores (taken from

Wilson et al. 2013a,b): low (L) vulnerability species (EVS 3-9); medium (M) vulnerability species (EVS 10-13); and high (H)

vulnerability species (EVS 14-19). IUCN categorization: CR = Critically Endangered; EN = Endangered; VU = Vulnerable; NT =

Near Threatened; LC = Least Concern; DD = Data Deficient; and 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 nba ease IUCN SEMARNAT

Taxon Vulnerability ow

status Category (score) categorization status

gory

Anaxyrus compactilis* CE H (14) LE NS

Incilius cavifrons** SE M (13) EN Pr

Incilius cristatus* CE H (14) CR Pr

Incilius macrocristatus NE4 M (11) VU NS

Incilius marmoreus * CE M (11) EN NS

Incilius nebulifer NE3 L (6) CR NS

Incilius occidentalis* GE M (11) EG NS

Incilius valliceps NE4 L (6) Le NS

Rhinella horribilis NE7 L (3) NE NS

Hyalinobatrachium viridissimum NE4 M (11) NE NS

Craugastor alfredi NE4 M (11) VU NS

Craugastor berkenbuschii* CE H (14) NT Pr

Craugastor decoratus* CE H (15) VU Pr

Craugastor laticeps NE4 M (12) NT Pr

Craugastor loki NE4 M (10) Le NS

Craugastor megalotympanum** SE H (18) CR Pr

Craugastor mexicanus* CE H (16) LG NS

Craugastor pygmaeus NE4 L(9) VU NS

Craugastor rhodopis* CE H (14) VU NS

Craugastor spatulatus* CE H (16) EN Pr

Craugastor vulcani** SE H (17) EN NS

Eleutherodactylus cystignathoides NE3 M (12) LC NS

Eleutherodactylus leprus NE4 M (12) VU NS

Eleutherodactylus longipes* CE H (15) VU NS

Eleutherodactylus nitidus* CE M (12) LC NS

Eleutherodactylus planirostris*** NN — — —

Eleutherodactylus verrucipes* GE H (16) VU Pr

Eleutherodactylus verruculatus** SE H (18) DD NS

Bromeliohyla dendroscarta* CE H (17) CR Pr

Charadrahyla nephila* CE M (13) VU NS

Charadrahyla taeniopus* CE M (13) VU A

Dendropsophus ebraccatus NE6 M (12) LC NS

Dendropsophus microcephalus NE6 L (7) LG NS

Dryophytes arenicolor NE3 L (7) Le NS

Dryophytes euphorbiaceus* CE M (13) NT NS

Dryophytes eximius* CE M (10) Le NS

Dryophytes plicatus* CE M (11) LG A

Duellmanohyla chamulae* CE M (13) EN Pr

Ecnomiohyla valancifer** SE H (18) Cre PE

Exerodonta bivocata* CE H (15) DD NS

Megastomatohyla mixomaculata* CE H (14) EN A

Megastomatohyla nubicola** SE H (14) EN A

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Torres-Hernandez et al.

Table 8 (continued). Distributional and conservation status measures for members of the herpetofauna of Veracruz, Mexico.

Distributional Status: CE = endemic to country of Mexico; SE = endemic to state of Veracruz; 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://www.mesoamericanherpetology.

com), as follows: 3 = species distributed only in Mexico and the United States; 4 = species found only in Mexico and Central

America; 6 = species ranging from Mexico to South America; 7 = species ranging from the United States to Central America; 8 =

species ranging from the United States to South America; and 9 = Oceanic species. Environmental Vulnerability Scores (taken from

Wilson et al. 2013a,b): low (L) vulnerability species (EVS 3-9); medium (M) vulnerability species (EVS 10-13); and high (H)

vulnerability species (EVS 14-19). IUCN categorization: CR = Critically Endangered; EN = Endangered; VU = Vulnerable; NT =

Near Threatened; LC = Least Concern; DD = Data Deficient; and 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 onli eae IUCN SEMARNAT

Taxon Vulnerability th

status Category (score) categorization status

gory

Ptychohyla zophodes* CE M (13) DD NS

Ouilticohyla zoque* CE H (14) NE NS

Rheohyla miotympanum* CE L(9) NT NS

Sarcohyla arborescandens* CE M (11) EN Pe

Sarcohyla bistincta* CE L (9) Le Pr

Sarcohyla pachyderma** SE H (15) CR Pr

Sarcohyla siopela* CE H (15) CR NS

Scinax staufferi NE4 L (4) LC NS

Smilisca baudinii NE7 L(3) Ee NS

Smilisca cyanosticta NE4 M (12) NT NS

Tlalocohyla godmani* CE, M (13) VU A

Tlalocohyla loquax NE4 L(7) Le NS

Tlalocohyla picta NE4 L (8) LG NS

Trachycephalus vermiculatus NE6 L (4) LG NS

Triprion spinosus NE4 H (15) Le NS

Engystomops pustulosus NE6 L (7) Le NS

Leptodactylus fragilis NE8 L (5) LC NS

Leptodactylus melanonotus NE6 L (6) LC NS

Gastrophryne elegans NE4 L (8) LC Pr

Hypopachus ustus NE4 L (7) LE Pr

Hypopachus variolosus NE7 L (4) LC NS

Agalychnis taylori NE6 M (11) LG NS

Agalychnis moreletii NE4 L (7) CR NS

Lithobates berlandieri NE3 L-C) Le Pr

Lithobates brownorum NE4 L (8) NE Pr

Lithobates catesbeianus*** NN — — —

Lithobates johni* CE H (14) EN P

Lithobates maculatus NE4 LS) Le NS

Lithobates montezumae* CE M (13) LC Pr

Lithobates spectabilis* CE M (12) Le NS

Lithobates vaillanti NE6 L(Q) LG NS

Rhinophrynus dorsalis NE7 L (8) Le Pr

Scaphiopus couchii NE3 L (3) LE. NS

Spea multiplicata NE3 L (6) LG NS

Ambystoma velasci* CE M (10) LG Pr

Aquiloeurycea cafetalera* CE H (17) NE NS

Aquiloeurycea cephalica* CE H (14) L¢ A

Aquiloeurycea praecellens** SE H (18) CR A

Bolitoglossa alberchi* CE H (15) VU NS

Bolitoglossa mexicana NE4 M (11) IBS) Pr

Bolitoglossa occidentalis NE4 M (11) LG. Pr

Bolitoglossa platydactyla* CE H (15) LG PE

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