Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

12(1) [General Section]: 1-4 (el50).

New distributional records of the Toad-headed Pitviper

Bothrocophias hyoprora (Amaral, 1935) in Brazil

^uciana Silva de Oliveira, 2 lvanei Souza Araujo, 3 Ana Lucia da Costa Prudente, 4 Rafael de Fraga,

5 Alexandre Pinheiro de Almeida, and 6 Alexandre Cordeiro Ascenso

13 ’ 6 Setor de Herpetologia, Departamento de Zoologia, Museu Paraense Emilio Goeldi, Avenida Perimetral, 1901, 66077-830, Belem, Para, BRAZIL

2 Setor de Entomologia, Departamento de Zoologia, Museu Paraense Emilio Goeldi, Avenida Perimetral, 1901, 66077-830, Belem, Para, BRAZIL

4 Universidade Federal do Oeste do Para, Instituto de Ciencias e Tecnologia das Aguas, Av. Mendonca Furtado 2946, 68040-050, Santarem, Para,

BRAZIL 5 Universidade Federal do Amazonas, Programa de Pos-Graduacao em Zoologia, Av. General Rodrigo Octavio Jordao Ramos 3000,

69077-000, Manaus, Amazonas, BRAZIL

Keywords. Viperidae, snake, Amazonian herpetofauna, Canutama, Altamira, distribution extension

Citation: Oliveira LS, Araujo IS, Prudente ALC, Fraga R, Almeida AP, Ascenso AC. 2018. New distributional records of the Toad-headed Pitviper

Bothrocophias hyoprora (Amaral, 1935) in Brazil. Amphibian & Reptile Conservation 12(1) [General Section]: 1-4 (el 50).

NonCommercialNoDerivatives 4.0 International License, which permits unrestricted use for non-commercial and education purposes only, in any

medium, provided the original author and the official and authorized publication sources are recognized and properly 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-reptiie-conservation. org>.

Received: 06 July 2017; Accepted: 04 October 2017; Published: 21 January 2018

The genus Bothrocophias Gutberlet and Campbell

2001 is a monophyletic entity composed of six species:

Bothrocophias andianns (Amaral, 1923), B. campbelli

(Freire- Lascano, 1991), B. colombianus (Rendahl and

Vestergren, 1941), B. hyoprora (Amaral, 1935), B.

microphthalmus (Cope, 1875), and B. myersi Gutberlet

and Campbell, 2001 (Carrasco et al. 2012). It is widely

distributed in tropical lowland forests of the Amazon

basin of Colombia, Ecuador, Peru, Bolivia, and Brazil

(Campbell and Lamar 2004; Fenwick et al. 2009;

Carrasco et al. 2012; Wallach et al. 2014).

Among the Bothrocophias species, the Toad-head

Pitviper (B. hyoprora) exhibits the widest distribution,

occurring in lowland Amazonian forests of Colombia,

Ecuador, Peru, Bolivia, and Brazil (Campbell and Lamar

2004; Cisneros-Heredia et al. 2006). In the Brazilian

Amazon, the species is broadly distributed from the

western Amazonas to the eastern middle Tapajos River,

also occurring at the states of Acre, Ronddnia, and Mato

Grosso (Bernarde et al. 2011; Mendes-Pinto and Souza

2011; Carvalho et al. 2013). According to the available

literature, Bothrocophias hyoprora is often found on the

leaf litter near water bodies (Campbell and Lamar 2004),

and feeds upon centipedes, anurans, lizards, and rodents

(Martins and Oliveira 1998; Martins et al. 2002).

We herein report two vouchered specimens and

an additional non-collected specimen of B. hyoprora

from southwestern Para and southern Amazonas,

which is located in northern Brazil (Fig. 1). An adult

male of B. hyoprora (MPEG 24662, snout-vent length

366 mm, tail length 82 mm) was collected on 2 April

2011 by L. Drummond, H. Costa, and J. Tonini, in an

ombrophilous dense forest located in Jardim do Ouro,

eastern part of the Itaituba municipality, state of Para,

Brazil (6.26190°S, 55.90621°W; WGS 84; 237 m). The

specimen is deposited in the herpetological collection

“Oswaldo Rodrigues da Cunha,” Museu Paraense Emilio

Goeldi, Belem, Brazil - MPEG. An adult male (INPA-H

33106, snout-vent length 347 mm, tail length 63 mm;

Fig. 2) was collected on 24 April 2013 by Alexandre

Almeida and F. Assungao, in a dense forest in the Floresta

Estadual Canutama, a Conservation Unit on Canutama

municipality, southern Amazonas, on the right bank of the

Paisse River (6.49514°S, 64.56611°W; WGS 84; 75 m).

This specimen is deposited in the herpetological section

of the Zoological Collections of the Instituto Nacional

de Pesquisas da Amazonia, Manaus, Brazil - INPA-H.

An adult B. hyoprora (UF 157255; Fig. 3) was found

on 18 April 2016 by Ivanei Araujo and Edson Reis in a

preserved forest transect in the of the Chapleau mining

company, concession (7.550479°S, 55.034344; WGS 84;

238 m), Altamira municipality, Para state, Brazil. This

record corresponds to a photographic voucher specimen

deposited at the Florida Museum of Natural History-UF.

The register represented by the MPEG specimen

extends the known distribution of Bothrocophias

hyoprora ca. 190 km south from the last known record,

which was at FLONA Trairao, Para. The University of

Co rres pon den CO. 1 lucorallus09@gmail. com, 2 araujois@yahoo. com. hr, 2 prudente@museu-goeldi. hr, 4 r. defraga@gmail. com,

5 alexandre. dealmeida@hotmail. com, 6 emurinus@hotmail. com (corresponding author)

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | el 50

Oliveira et al.

- 70 ° 0 ' - 60 ° 0 '

Fig. 1. Known geographic range of Bothmcophias hyoprora in South America: white circles = literature data, red star = type

locality, red squares = records from Jardim do Ouro, Itaituba, Para, Brazil (MPEG 24662) and from Floresta Estadual Canutama,

Canutama, Amazonas, Brazil (INPA-H 33106), red triangle = record from Chapleau mining company concession, Altamira, Para,

Brazil (UF 157255).

Fig. 3. Adult Bothmcophias hyoprora (UF 157255) from

Altamira, Para, Brazil. Photography by Ivanei S. Araujo.

Fig. 2. Adult Bothmcophias hyoprora (INPA-FI 33106) from

Canutama, Amazonas, Brazil. Photography by Vimcius T. de

Carvalho.

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | e150

New distributional records of Bothrocophias hyoprora

Florida photographed specimen expands the distribution

ca. 270 km southeast (Mendes-Pinto and Souza 2011).

Both records fill a distributional gap in the Xingu-

Tapajos interfluve, located in southeast Para. The INPA

specimen fills an important gap on southern Amazonas,

at the Jurua-Purus interfluve, one of the most unexplored

region of Amazonia concerning the herpetofauna. These

records provide new distribution data about this rare

species in the Brazilian Amazon. The UF record is the

first for the municipality of Altamira. Despite being

considered abundant at the Andean slopes of Colombia,

Peru, and Ecuador, Bothrocophias hyoprora records are

very uncommon in Brazil, with few specimens being

registered for central and western Amazon. However, the

lack of registers is most likely due to scarcity of field

work rather than low demographic of the species in the

region (Carvalho et al. 2013).

Acknowledgements. —We thank the Conselho

Nacional de Desenvolvimento Cientifico e Tecnologico

(CNPq) and the Fundagao Amazonia de Amparo a

Estudos e Pesquisas (FAPESPA) for financial support

to A C.A. (process 134389/2011-5 and 440413/2015-

0), and A.L.C.P. (CNPq processes Pq 305475/2014-

2, CNPq-PROTAX 440413/2015-0 and FAPESPA-

PROTAX 2016/111449). We also thank Murilo Pastana

for the English review, and Francisco Dal Vechio for the

confirmation of identification of the photograph from

Altamira’s specimen.

Literature Cited

Amaral A. 1923. New genera and species of snakes.

Proceedings of the New England Zoological Club 8:

85-105.

Amaral A. 1935. Novas especies de ophidios da

Colombia. Estudos Sobre Ophidios Neotropicos.

Memdrias do Institnto Butantan 9: 222-225.

Bernarde PS, Amaral ES, Vale MAD. 2011. Squamata,

Serpentes, Viperidae, Bothrocophias hyoprora

(Amaral, 1935): Distribution extension in the state

of Acre, northern Brazil. Check List 6: 813-814.

Campbell JA, Lamar WW. 2004. The Venomous Reptiles

of the Western Hemisphere. Cornell University

Press, Ithaca, New York, USA. 870 p.

Carrasco PA, Mattoni Cl, Leynaud GC, Scrocchi GJ.

2012. Morphology, phylogeny and taxonomy of

South American bothropoid pitvipers (Serpentes,

Viperidae). Zoologic a Script a 41: 1-15.

Carvalho VT, Fraga R, Eler ES, Kawashita-Ribeiro RA,

Feldberg E, Vogt R, Carvalho MA, Noronha JC,

Condrati LH, Bittencourt S. 2013. Toad-headed

pitviper Bothrocophias hyoprora (Amaral, 1935)

(Serpentes, Viperidae): New records of geographic

range in Brazil, hemipenial morphology, and

chromosomal characterization. Herpetological

Review 44(3): 410—414.

Cisneros-Heredia DF, Borja MO, Proano D, Jean-

Marc T. 2006. Distribution and natural history of

the Ecuadorian toad-headed pitvipers of the genus

Bothrocophias (Squamata: Serpentes: Viperidae:

Crotaline). Herpetozoa 19: 17-22.

Cope ED. 1875. Report on the reptiles brought by

professor James Orton from the middle and upper

Amazon and western Peru. Journal of the Academy

of Natural Sciences ofPhiladelphia N.S. 8: 159-183.

Fenwick AM, Gutberlet-Jr RL, Evans JA, Parkinson

CL. 2009. Morphological and molecular phylogeny

and classification of South American pitvipers,

genera Bothrops , Bothriopsis , and Bothrocophias

(Serpentes: Viperidae). Zoological Journal of the

Linnean Society 156: 617-640.

Freire-Lascano A. 1991. Dos nuevas especies de

Bothrops en el Ecuador. Publicaciones Trabajos

Cientificos del Ecuador, Universidad Tecnica de

Machala2\ 1-11.

Gutberlet-Jr RL, Campbell JA. 2001. Generic recognition

for a neglected lineage of South American pitvipers

(Squamata: Viperidae: Crotalinae), with the

description of a new species from the Colombian

Choco. American Museum Novitates 3316: 1-15.

Martins M, Oliveira ME. 1998. Natural history of snakes

in forests of the Manaus region, Central Amazonia,

Brazil. Herpetological Natural History 6 \ 78-150.

Martins M, Marques OA, Sazima I. 2002. Ecological

and phylogenetic correlates of feeding habits in

Neotropical pitvipers of the genus Bothrops. Pp.

307-328 In: Biology of the Vipers. Editors, Schuett

GW, Hoggren M, Douglas ME, Greene HW. Utah,

Eagle Mountain Publishing, Eagle Mountain, Utah,

USA. 580 p.

Mendes-Pinto TJ, Souza SM. 2011. Preliminary

assessment of amphibians and reptiles from Floresta

Nacional do Trairao, with a new snake record for

the Para state, Brazilian Amazon. Salamandra 47:

199-206.

Rendahl H, Vestergren G. 1941. Notes on Colombian

snakes. Arkiv for Zoologi 33A: 1-16.

Wallach V, Williams KL, Boundy J. 2014. Snakes of the

World: A Catalogue of Living and Extinct Species.

Taylor and Francis, CRC Press, Boca Raton, Florida,

USA. 1,237 p.

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | el 50

Oliveira et al.

|' ^ i

Luciana Silva de Oliveira received her Master’s degree in zoology in 2014 from the Federal

University of Para and the Emilio Goeldi Museum of Para (MPEG), and now works with inventories

\ r M of Amazonian herpetofauna. Eler research interests include monitoring wildlife in the Amazon,

systematics and genetics of amphibians and reptiles, and techniques and procedures of natural history

Ivanei Souza Araujo received his Master’s degree in 2006 from the Federal University of Para and the

Emilio Goeldi Museum of Para (MPEG), and works as a biodiversity and conservation consultant of

Amazonian insects and mammals. His current research is focused on monitoring wildlife for biological

conservation, as well as army ants, dung beetles, and butterflies, as a research associate of the MPEG.

Ana Lucia da Costa Prudente is a titular researcher at the Emilio Goeldi Museum of Para, Brazil

(MPEG), and is a teacher and advisor in the postgraduation programs of zoology (in a covenant with

the Federal University of Para) and of Biodiverstiy and Evolution (from Emilio Goeldi Museum

of Para). She is current chief of the zoology coordination from MPEG, current vice coordinator of

research and postgraduation at the MPEG, and curator of the herpetological collection from MPEG

since 2000. Her current research focuses on the systematics, taxonomy, and biogeography (mainly

with snakes) of animals, Amazon basin, and morphology of reptiles.

Rafael de Fraga is a professor at the Federal University of the West of Para (UFOPA - ICTA). He

received a Master’s degree in ecology in 2009, and a doctoral degree in 2016 in ecology from the

National Institute of Amazonian Researches (INPA). His current research focuses on ecology with an

emphasis in herpetology, acting mainly on metrics estimates of diversity (e.g., taxonomic, functional,

and phylogenetic), niche theory, and theory of ecological gradients.

Alexandre Pinheiro de Almeida received his Master’s degree in 2011 from the Federal University of

Amazonas, and now works with inventories of Amazon Herpetofauna. His research interests include

monitoring wildlife in the Amazon, ecology and taxonomic aspects of amphibians and reptiles, and

wildlife management.

Alexandre Cordeiro Ascenso is a doctoral research fellow at the Biodiversity and Evolution Program

at the Emilio Goeldi Museum of Para, Brazil (MPEG). His current research focuses on the systematics

and taxonomy of a species complex of neotropical snakes (Erythrolamprus reginae ), with strong

interests in the study of natural history, genetics, biogeography, and conservation of amphibians and

reptiles.

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | e150

Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

12(1) [General Section]: 5-14 (el51).

On the occurrence of Hemiphractus scutatus (Spix, 1824)

(Anura: Hemiphractidae) in eastern Amazonia

1 ’ 2 ’ 3 Leandro Joao Carneiro de Lima Moraes and 24 Dante Pavan

l Programa de Capacitaqao Institutional, lnstituto National de Pesquisas da Amazonia - INPA, Manaus, AM, BRAZIL 2 Ecosfera Consultoria e

Pesquisa em Meio Ambiente Ltda., Sao Paulo, SP, BRAZIL

Abstract.—Hemiphractus Wagler, 1828 is part of Hemiphractidae Peters, 1862, a family that harbors species of

frogs characterized by the deposition of eggs on the females’ dorsum. Both the genus Hemiphractus and the

species Hemiphractus scutatus (Spix, 1824) are only known to the Andean mountain range and western half of

the upper Amazon Basin. Herein, we provide the first records of H. scutatus from the eastern Amazonia (middle

Tapajos River region, Para State, Brazil), which extends its geographic range ca. 1,000 km from nearest known

occurrence record and are among the lowest known levels for the species elevational range. Comparisons of

morphologic and molecular data with available voucher specimens and published information on the species

revealed variation that we interpret as intraspecific polymorphism. Phylogenetic analysis of a fragment of the

mitochondrial gene 16S recovered the newly discovered specimens as most closely related to samples from

Peru. These results add new evidence in the known biogeographic patterns of the genus and species, and

ongoing plans to build hydroelectric plants in the middle Tapajos River region can negatively affect this unique

population.

Keywords. Biogeography, conservation, geographic range, marsupial frogs, morphology, Para State, phylogenetic

relationships

Citation: Moraes LJCDL, Pavan D. 2018. On the occurrence of Hemiphractus scutatus (Spix, 1824) (Anura: Hemiphractidae) in eastern Amazonia.

Amphibian & Reptile Conservation 12(1) [General Section]: 5-14 (el51).

cialNoDerivatives 4.0 International License, which permits unrestricted use for non-commercial and education purposes only, in any medium, provided

the original author and the official and authorized publication sources are recognized and properly 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-

reptiie-conservation.org>.

Received: 02 August 2017; Accepted: 28 September 2017; Published: 30 January 2018

Introduction

According to the latest phylogenetic revisions (Castro-

viejo-Fisher et al. 2015; Duellman 2015), the family

Hemiphractidae Peters, 1862 is considered monophy-

letic and include the genera Cryptobatrachus Ruthven,

1916 (six species), Gastrotheca Fitzinger, 1843 (70 spe¬

cies), Stefania Rivero, 1968 (19 species), Flectonotus

Miranda-Ribeiro, 1926 (two species), Fritziana Mello-

Leitao, 1937 (five species), and Hemiphractus (six spe¬

cies). Members of this family inhabit humid Neotropi¬

cal forests in different elevational zones: Central Amer¬

ica, Choco, Andes, mountainous Caribbean coast, the

island of Trinidad and Tobago, Amazonia, and the Atlan¬

tic Forest (Castroviejo-Fisher et al. 2015; Duellman

2015). These frogs share a unique reproductive mech¬

anism, with deposition of eggs on the females’ dorsum

(Duellman 2015). In Amazonia, this characteristic seems

to be relevant to define hemiphractid geographic ranges,

as they are more diverse and abundant in the west, which

may be a result of ideal climatic conditions for its life

cycle in this region (Bernal and Lynch 2013; Duellman

2015), such as the lower seasonality and higher annual

rainfall (Sombroek 2001).

The species of the genus Hemiphractus are terrestrial

and arboreal frogs with well-modified and ornamented

skulls (Trueb 1974), which are distributed throughout

Central America, East of Andes and in the extreme west¬

ern Amazon basin (Frost 2017): H. bnbahis (Jimenez la

Espada, 1870), H.fasciatus Peters, 1862, H. helioi Sheil,

and Mendelson III, 2001, H. johnsoni (Noble, 1917), H.

proboscideus (Jimenez de la Espada, 1870), and H. scu¬

tatus (Spix, 1824). The latter is the type species of the

genus and inhabits a wide elevational range along the

western Amazon Basin and Andean mountain range, in

Bolivia, Peru, Ecuador, and Brazil (Spix 1824; Myers

and Carvalho 1945; Trueb 1974; Duellman and Lynch

1988; Rodriguez and Duellman 1994; Ruiz-Carranza

et al. 1996; Sheil and Mendelson III 2001; Lehr 2001;

Moravec et al. 2002; Coloma et al. 2004; Duellman 2005;

Correspondence, 2 leandro.jclm(a),gmail.com (corresponding author); 4 dtpavan@yahoo.com.br

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | e151

Moraes and Pavan

Colombia

Brazil

Tapajos

Bolivia

Jamanxim<

W80°

W60°

W70°

W60°

W50°

W40°

W80°

South America

Peru

Fig. 1. Known distribution of (a) genus Hemiphractus (in purple) and (b) Hemiphractus scutatus (dots), highlighting new locality of

occurrence in middle Tapajos River region, Para State, Brazil (red dots) and localities of sequences included in molecular analysis

(yellow dots). The region of new records is zoomed in (c), showing the sampling sites where H. scutatus was present (red) and not

recorded (white).

Lynch 2005; Cisneros-Heredia 2006; Glaw and Franzen

2006; Munoz-Saravia 2008; Souza 2009; von May et al.

2009; Beirne and Whitworth 2011; Bernarde et al. 2011;

Catenazzi et al. 2013; Ortiz 2013; Almendariz etal. 2014;

Castroviejo-Fisher et al. 2015; Frost 2017; GBIF 2017;

Rainforest Conservation Fund 2017; SpeciesLink 2017).

Herein we present the first records of Hemiphrac¬

tus scutatus from the middle Tapajos River region, Para

State, Brazil. These records are the easternmost known

localities of occurrence reported for this species and the

genus, and are among the lowest known elevational lev¬

els for the species distribution. We also present a phylo¬

genetic tree based on mtDNA gene 16S for some Hemi¬

phractus species, and discuss on the biogeographic

implications of these records and conservation of this

population.

Material and Methods

The amphibian survey was conducted on the middle

Tapajos River region, Para State, Brazil. This river is one

of the largest tributaries of the Amazon River (Sioli 1968)

and is located in eastern Amazonia. The climate in this

region have a high seasonality (Sombroek 2001), with

average annual temperature of 26 °C and total annual

rainfall exceeding 2,400 mm (Wang et al. 2017), with

driest months from June to August (Alvares et al. 2013).

We survey for amphibians in 11 sampling sites with four

km long, installed in both banks of the Tapajos River and

its tributary the Jamanxim River. Each sampling site cov¬

ered humid primary Terra Firme forests, which does not

suffer the seasonal riverine flood pulse effect (Junk et al.

1989) and riparian forests (Fig. 1). We used complemen¬

tary sampling methods (Heyer et al. 1994), such as pitfall

traps (600 trap nights) and diurnal and nocturnal active

searches (more than 340 days). Six field campaigns were

conducted along July 2012 and November 2013.

Aiming to better understand the relevance of these

records in the general context of the geographic and ele¬

vational distribution of the species, we survey for its

occurrence data available in the literature (Spix 1824;

Myers and Carvalho 1945; Trueb 1974; Duellman and

Lynch 1988; Rodriguez and Duellman 1994; Ruiz-Car-

ranza et al. 1996; Sheil and Mendelson III 2001; Lehr

2001; Moravec et al. 2002; Coloma et al. 2004; Duellman

2005; Lynch 2005; Cisneros-Heredia 2006; Glaw and

Franzen 2006; Munoz-Saravia 2008; Souza 2009; von

May et al. 2009; Beirne and Whitworth 2011; Bernarde

et al. 2011; Catenazzi et al. 2013; Almendariz et al. 2014;

Castroviejo-Fisher et al. 2015; Frost 2017; Rainforest

Conservation Fund 2017; AP Lima, pers. comm.) and

online databases (Ortiz 2013; GBIF 2017; SpeciesLink

2017), mostly with associated vouchers in zoological

collections, obtaining a total of 77 georeferenced locali¬

ties of occurrence.

Morphologic data survey

We analyzed morphologic data traditionally used in the

taxonomy of the genus (Trueb 1974), obtaining qualita¬

tive characters of external morphology and quantitative

characters using a caliper to the nearest 0.1 mm: snout-

vent length (SVL); forearm length from proximal edge

of palmar tubercle to outer edge of flexed elbow (FAL);

hand length from proximal edge of palmar tubercle to

tip of finger III (HA); tibia length from proximal edge of

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | e151

Occurrence of Hemiphractus scutatus in eastern Amazonia

Fig. 2. Specimens of Hemiphractus scutatus from middle Tapajos River region, Para State, Brazil, (a) Female, 76.1 mm SVL,

INPA-H38116; (b) Male, 57.8 mm SVL, INPA-H38117; (c) Female, 61.7 mm SVL, 1NPA-H38118.

flexed knee to heel (TL); foot length from proximal edge

of inner metatarsal tubercle to tip of Toe IV (FL); head

width at level of angle of jaw (HW); head length from

angle of jaw to tip of snout (HL); eye diameter (ED);

internarial distance (IN); diameter of tympanum (DT);

interorbital distance (10) and thigh length (THL). We

compared the measurements with information available

from the literature and voucher specimens deposited at

the Collection of Amphibians and Reptiles (INPA-H) of

the Instituto Nacional de Pesquisas da Amazonia (INPA),

Manaus, Amazonas, Brazil (Appendix SI), where the

new specimens were also deposited (under accession

numbers INPA-H 38116-38118).

Molecular data protocols

We extracted the genomic DNA from two specimens

liver tissue samples conserved in absolute ethanol using

the phenol-chloroform protocol (Sambrook and Rus¬

sel 2001). The 16S mtDNA gene, a standard marker for

amphibians (Vences et al. 2012), was amplified via the

Polymerase Chain Reaction (PCR). The PCR amplifica¬

tion used a mix with final volume of 25 pi: 4 pi of 1.25

M dNTPs, 2.5 pi of 10X amplification buffer (75mM Tris

HC1, 50 mM KC1, 20 mM (NH 4 ),S0 4 ), 1.0 pi of 50 mM

MgCl 2 , 1.0 pi of DNA in a concentration of 250 ng/pl,

0.25 pi of each primer (/ASar and /ASbr - Palumbi et

al. 1991) in a concentration of 200 ng/ul, 0.25 pi of Taq

DNA polymerase 5 U/pL and 15.75 pL of ddH,0. Reac¬

tion conditions had an initial heating step at 94 °C for

five minutes, 30 cycles of denaturation at 94 °C for 30 s,

primer annealing at 50 °C for 60 s, and extension at 72 °C

for 120 s, followed by a final extension at 72 °C for seven

minutes. PCR products were purified with ExoSAP-IT

(USB Corporation) and submitted to a sequencing reac¬

tion following BigDye Terminator Cycle Sequencing Kit

(Applied Biosystems, EUA) protocols. The sequences

were obtained in the automated sequencer ABI PRISM

3500 (Applied Biosystems, EUA) and deposited in Gen-

Bank (accession numbers MG011478, MG011479).

The sequences were aligned using the MUSCLE algo¬

rithm, implemented in MEGA 6.06 (Tamura et al. 2013)

and corrected manually, obtaining a 524 bp alignment.

Using the same software, we generated a maximum like¬

lihood phylogenetic tree, constructed through a general

time reversible model with a gamma distribution of rate

variation (GTR+G), selected as the best DNA evolution

model for the alignment by Bayesian Information Cri¬

terion (BIC), as well as to calculate two inter and intra¬

specific genetic distances: uncorrected-pairwise and

Kimura-2-Parameter (K2P) (Kimura 1980). Additional

sequences were obtained in GenBank, including the two

distinct lineages of H. scutatus identified by Castroviejo-

Fisher et al. (2015) (Table 3). The statistical support for

the tree nodes was estimated by bootstrapping (5,000

replicates).

Results

New records of Hemiphractus scutatus

We found three specimens of H. scutatus in two of the

11 sampling sites (Figs. 1-3). It was a rare species in the

sampling, recorded at a ratio of one specimen in about

each 300 days of sampling, while the most abundant

syntopic terrestrial frogs were from genera Adenomera

Steindachner, 1867, Pristimantis Jimenez de la Espada,

1870, Allobates Zimmermann and Zimmermann, 1988,

and Rhinella Fitzinger, 1826, with 2,700 specimens

recorded in this same sampling effort. The three spec¬

imens of H. scutatus were only recorded by the active

searches, and exclusively in Terra Firme forests (Fig. 4).

On 28 September 2012 one female voucher speci¬

men was collected by D. Pavan close to a large tree and

under a palm leaf, on the left bank of Tapajos River, at

19:15 h (76.1 mm SVL; 05°02’S, 56°53’W, 62 m above

mean sea level, hereafter referred as asl). On 16 Octo¬

ber 2012 a male voucher specimen was collected on the

same riverbank by LJCL Moraes hidden inside the leaf-

litter at 21:05 h, distant ca. 51 km in straight line from

the first record (57.8 mm SVL; 04°39’S, 56°37’W, 60

m asl). On 28 April 2013 a second female voucher spec¬

imen was collected also hidden inside the leaf-litter on

the same riverbank by J. Cassimiro at 21:30 h (61.7 mm

SVL; 04°40’S, 56°37’W, 83 m asl), distant ca. 50 km in

straight line from the first record and 430 m from the sec¬

ond record. No evidence of reproductive activity or gap¬

ing posture (Trueb 1974) was observed.

These three records represent the easternmost known

localities of occurrence of H. scutatus , extending the geo-

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | e151

Moraes and Pavan

Fig. 3. Dorsal and ventral views of voucher specimens of Hemiphractus scutatus from middle Tapajos River region, Para State,

Brazil, (a) Female, 76.1 mm SVL, INPA-H38116; (b) Male, 57.8 mm SVL, INPA-H38117. Scale bar = 20 mm.

graphic range of the species and the genus Hemiphractus.

They are distant ca. 1,000-1,500 km from the previously

known easternmost points of the species occurrence,

in Ronddnia (INPA-H 15398, 15399) and Amazonas

States, Brazil (GBIF 2017; SpeciesLink 2017) (Fig. 1).

Considering only the Amazon Basin at South of Ama¬

zon River, these new records even extend to the East the

geographic range of the family Hemiphractidae. Further¬

more, the elevation level in which these specimens were

recorded are among the lowest known elevation for the

species (60, 62, and 83 m asl; Fig. 5), and two of them

(60 and 62 m asl) also extend downwards the known ele-

vational range of this species, since there are no docu¬

mented records of individuals below 70 m asl.

Morphologic variation and molecular relation¬

ships

The morphologic data confirms the identification of our

specimens in accordance to the literature (Trueb 1974)

and voucher specimens. Qualitative characters include

the triangular head, canthus rostralis rounded in sec¬

tion; tympanum large and vertically ovoid; oblique rows

of tubercles on dorsal surfaces of forearm and hind limb

(less pronounced in female specimens); small triangu¬

lar fleshy proboscis, dorsoventrally flattened, on tip of

snout; eyelids granular with one (female specimens) or

three (male specimen) prominent fleshy conical tuber¬

cles; single bony projection at the angle of the jaw;

slightly enlarged tubercles at the knee and small tuber¬

cles at calcaneum (divergent from the absence of calcar

projections reported by Trueb 1974 and Rodriguez and

Duellman 1994); fingers and toes with vestigial adhe¬

sive discs, well-developed round subarticular tubercles

and basal webbing; thenar tubercle elliptical and outer

palmar tubercle diffuse, flat and cordiform; no evidence

of nuptial pads in male specimen; toes also with well-

developed round subarticular tubercles and about one-

fourth webbed; inner metatarsal tubercle well-developed

and elliptical, and outer metatarsal tubercle indistinct;

shagreened skin on dorsum and granular on flanks, abdo¬

men and ventral surfaces of thighs.

Dorsal coloration in life varies from reddish brown

(INPA-H38116 and 38118) to pale tan background with

dark mottling (INPA-H38117), with two dark vertebral

spots; dark suborbital marks from the lower margin of

the eye expanding posteroventrally but not reaching the

lip (more pronounced in INPA-H38117 than in INPA-

H38116 and 38118) and scattered dark spots in the tym¬

panic region. Ventrally, gular coloration varies from uni¬

formly brown (INPA-H38116 and 38118) to mottled

(INPA-H38117), with a pale mid-ventral stripe reach-

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | e151

Occurrence of Hemiphractus scutatus in eastern Amazonia

Fig. 4. Aerial (a) and inside (b) view of the Hemiphractus

scutatus habitat (Terra Firme forest) in middle Tapajos River

region, Para State, Brazil, also showing the BR-230 highway.

ing the pectoral region; same gular color reaches the pec¬

toral region, and becomes less pigmented posteriorly. A

finely dark venate pattern covers the flank areas above

the forelimb; forelimbs and hind limbs varies from uni¬

formly brown (INPA-H38116 and 38118) to tan (INPA-

H38117), with dark transverse bands, reaching the dor¬

sal surface of hands (more evident in INPA-H38117); iris

bronze and darker ventrally, with a longitudinally cross¬

ing reddish area and pupil horizontal. Regarding quanti¬

tative characters, most of the measurements of the middle

Tapajos River specimens agree with the known morpho¬

metric range of the species (Table 1), also showing the

sexual dimorphism in body size. The only divergence is

a small HW compared to SVL in female INPA-H38116.

The 16S mtDNA tree for Hemiphractus species

shows, as the results presented by Castroviejo-Fisher

et al. (2015), two distinct lineages of H. scutatus. The

middle Tapajos River population is more related to the

lineage from Peru (Figs. 6, 7), as the sequences have a

higher genetic similarity (more than 97%) compared to

sequence from Colombia, near the country’s border with

Brazil (93%) (Fig. 7).

Discussion

The presence of possible cryptic taxa under the name H.

scutatus was suggested based on the results of a phylogeny

3 , 200 - 3,400

3 , 000 - 3,200

2 , 800 - 3,000

~ 2 , 600 - 2,800

</)

” 2 , 400 - 2,600

7 T 2 , 200 - 2,400

« 2 , 000 - 2,200

(O 7 7

£ 1 , 800 - 2,000

= 1 , 600 - 1,800

| 1 , 400 - 1,600

| 1 , 200 - 1,400

I 1,000-1,200

800 - 1,000

600-800

400-600

200-400

0-200

0 5 10 15 20 25

Number of individuals

Fig. 5. Variation in number of individuals of Hemiphractus

scutatus recorded along its known elevational range (60-3,300

m above mean sea level). The specimens from middle Tapajos

River region, Para State, Brazil are recorded among the lowest

known elevation for the species.

of molecular and morphologic data (Castroviejo-Fisher

et al. 2015), since two genetically distant intraspecific

lineages were found. Although we initially worked with

the hypothesis that specimens from middle Tapajos

River were a new taxon, the morphologic and molecular

analysis readily rejected this. Regarding the morphology,

despite the possibility of strong variation due to large

geographic distance to known distribution area, most

of the qualitative and quantitative data of the specimens

from middle Tapajos River were inside the known range

for the species (Trueb 1974; Rodriguez and Duellman

1994) and other voucher specimens (Table 1). The

slightly divergences in colors, shapes, and morphometric

characters between this specimens and the known for the

species may be part of intraspecific variation. Regarding

the molecular data, despite the high geographic distance

between the populations from middle Tapajos River

and Peru (more than 2,300 km), there is a low genetic

distance between the sequences from these regions

(between 2% and 3%). As Castroviejo-Fisher et al.

(2015) highlighted, the genetic distance between the

sequences from Colombia and Peru, and now including

the distance of Tapajos sequences, are high and may

indicate cryptic speciation (more than 7%). As overall

similarity in external morphology and pronounced

morphologic variation are common events inside the

genus Hemiphractus (Trueb 1974), further broader

studies and integrative taxonomic revisions may indicate

the extent of morphologic and molecular variability of

this species and reveal the taxonomic status of these

genetically distant lineages.

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | e151

Moraes and Pavan

Table 1. Morphologic measurements (mm) of Hemiphractus scutatus specimens recorded in middle Tapajos River region

(highlighted), compared to literature data and other voucher specimens from herpetological collection of Institute Nacional de

Pesquisas da Amazonia, Brazil (INPA-H). Literature: a Trueb 1974, n = 8 males and 15 females; b Rodriguez and Duellman 1994.

Measurements

Literature

Male

INPA-H38117

Male

Literature

Female

INPA-H 15399

Female

INPA-H15398

Female

INPA-H38116

Female

INPA-H38118

Female

SVL

36.9-62 ab

57.8

60.4-8 l ab

62.5

73.6

76.1

61.7

FAL

12.7

12.2

15.7

16.4

12.9

16.3

21.3

17.6

15.5-27.5 a

25.1

23.7-38.3 a

21.2

34.5

27.6

26.2

25.5

30.1

26.7

17.5-30 a

28.3

25.7-42.9 a

36.3

20.8-37.5 a

34.2

34.4-52.8 a

43.3

41.6

37.5

5.6

7.3

5.6

3.8

4.5

4.8

5.2

3.3

4.9

4.7

3.7

14.6

14.4

17.6

17.8

17.3

THL

28.2

29.7

38.2

34.4

29.2

TL/SVL (%)

42.3-48 a

39.3-47.6 a

HL/SVL (%)

47.6-52.3 a

42.7-53.3 a

HW/SVL (%)

56.6-65.5 a

57.1-65.7 a

Biogeography

After more than 190 years since the original description

of H. scutatus (Spix 1824) we recorded this species in the

eastern Amazonia, emphasizing the lack of knowledge

about the general biogeographic patterns of Amazonian

amphibians, which can be mainly generated by sampling

difficulties, especially in cases of secretive species. Large

forested regions in the Amazonia remain unexplored and

have the potential to harbor new species or expanding

species distributions (Azevedo-Ramos and Galatti 2002).

Therefore, the recognition of broader biogeographic pat¬

terns to Amazonian amphibians, as areas of endemism

historically recognized in the biome to other vertebrates

(e.g., Cracraft 1985; Boubli et al. 2014) depends on the

continued expansion of the sampling effort and new anal-

itical techniques that is currently being held in the biome.

Our new records for H. scutatus bring new informa¬

tion to a biogeographic idea historically recognized on

the low representation of Hemiphractidae in the east¬

ern Amazonia, probably due to increased seasonality in

this region (Sombroek 2001; Duellman 2015). Species of

this family that have greater environmental plasticity, as

appears to be the case of H. scutatus (the species of the

genus with the widest known geographic and elevational

range) may reach the preserved forests in this region and

establish viable populations, although in less abundance

in relation to the more climatically constant (Wang et al.

2017) and humid environments of western Amazonia.

Regarding elevational occurrence, although H. scuta¬

tus has already been recorded in high elevations at the

Andean mountain range (GBIF 2017), a greater number

of individuals is known for the Amazonian lowlands, and

67% of 77 published localities of occurrence are below

600 m asl (Fig. 5). This wide elevational range rein¬

force the high environmental plasticity, as the life-his¬

tory strategies of amphibian populations in high and low¬

lands may drastically differ (Morrison and Hero 2003).

The knowledge on the drivers of elevational variation in

the distribution of Amazonian amphibians is still incipi-

Table 2. Sequences from GenBank with accession numbers. In

bold are sequences generated from this study.

Taxon

16S

Hemiphractus bubal us

DQ679412

Hemiphractus fasciatus

KC014899

Hemiphractus fasciatus

KC014900

Hemiphractus fasciatus

KC129336

Hemiphractus fasciatus

KC129337

Hemiphractus fasciatus

KC 129338

Hemiphractus fasciatus

KC 129339

Hemiphractus fasciatus

KC 129340

Hemiphractus fasciatus

KC129341

Hemiphractus fasciatus

KC 129342

Hemiphractus fasciatus

KC 129343

Hemiphractus helioi

AY843594

Hemiphractus helioi

KR270431

Hemiphractus proboscideus

DQ679413

Hemiphractus scutatus

DQ679414

Hemiphractus scutatus

KR270432

Hemiphractus scutatus

MG011478

Hemiphractus scutatus

MG011479

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | e151

Occurrence of Hemiphractus scutatus in eastern Amazonia

Hemiphractus

100

scutatus (Para, Brazil) MG011479

scutatus (Para, Brazil) MG011478

scutatus (Peru) DQ679414

scutatus (Colombia) KR270432

— proboscideus DQ679413

- bubalus DQ679412

100

1 h(

helioi KR270431

helioi AY843594

fasciatus KC129339

fasciatus KC129338

fasciatus KC 129343

j- fasciatus KC 129342

* fasciatus KC129341

, fasciatus KC014900

P fasciatus KC014899

4 fasciatus KC 129340

'> fasciatus FJ784476

fasciatus KC 129337

fasciatus KC129336

Stefania riae JQ742172

Stefania evansi AY843767

0.03

Fig. 6. Maximum likelihood phylogenetic tree of Hemiphractus species based in a fragment of the 16S mtDNA gene, with GenBank

accession numbers. Only bootstrap values >80% are shown (5,000 replicates). For Hemiphractus scutatus , sample localities are in

parentheses and specimens from middle Tapajos River region, Para State, Brazil are highlighted.

ent (Siqueira and Rocha 2013) and the H. scutatus may

be a target taxon for future studies testing this gradient.

Conservation

Hemiphractus scutatus is considered as “Least Con¬

cern” by IUCN due to its wide distribution and presum¬

ably large and stable populations (Coloma et al. 2004).

However, this species is rarely recorded and have poorly

known population dynamics to define its conservation

status, that can even vary along its wide geographic

and elevational range. As the Amazon region has suf¬

fered increasing anthropic impact through the advance

of cities and highways, forests fragmentation and habitat

loss (Feamside 2015), the H. scutatus may have declin¬

ing populations in most of its distribution, since they

are dependents of undisturbed forests (Rodriguez and

Duellman 1994).

The specimens of H. scutatus from middle Tapajos

River region may represent a unique population, recorded

near and within a federal conservation unit (Parque

Nacional da Amazonia), same pattern already described

for Peruvian populations (von May et al. 2009), reinforc¬

ing the need to maintain large protected forest areas in

the Amazonia and adequate land-use on the unprotected

(Laurance et al. 2001). In addition to these threats, the

biome has been target of dam construction in its larger

rivers (Latrubesse et al. 2017), which can negatively

affect the biodiversity of the surrounding forests (Moraes

et al. 2016). The population of H. scutatus from Tapa¬

jos River is in the region affected by the construction of

a large hydroelectric plant, part of a complex planned for

the basin (Fearnside 2015), thus the implementation of

this project may affect the viability of this population.

Conclusion

The discovery of the first specimens of H. scutatus from

eastern Amazonia sheds new insights into ecology, bio¬

geography, taxonomy, and conservation of these remark¬

able frogs. To better understand the population status

and the total distribution range of this taxon in Amazo¬

nia, we need more long-term field studies, with standard¬

ized protocols, complementary sampling and broader

approaches.

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | e151

Moraes and Pavan

0.14

+! 0.12

£.0.10

E 0.08

^ 0.06

= 0.04

OS 0.02

Hsc/Hbu Hsc/Hpr Hsc/Hfa Hsc/Hhe Col/Per Col/Tap Per/Tap Tap/Tap

comparisons

Fig. 7. Inter and intraspecific genetic distances (mean ±

standard deviation of pairwise and K2P distances) calculated

for a fragment of I6S mtDNA gene of Hemiphractus species

and populations. (Hsc) Hemiphractus scut at us; (Hpr)

Hemiphractus proboscideus (Hfa) Hemiphractus fasciatus;

(Hhe) Hemiphractus heJioi; (Col) Colombia; (Per) Peru; (Tap)

middle Tapajos River region, Para State, Brazil. GenBank

accession numbers of sequences are in Table 2.

Acknowledgements. —We thank MC Barros and

members of GENBIMOL Molecular Biology Labora¬

tory of the Universidade Estadual do Maranhao - campus

Caxias (UEMA) for assistance with the molecular data

survey; LF Storti, J Cassimiro, JO Gomes, M Hoffman,

TFD Rodrigues, JMB Ghelere, AB Barros, and ES Brito,

for help in sampling; CNEC WorleyParsons Engenharia

S.A., for financial and logistical support and FP Wer-

neck, AAA Silva, and R Vogt, for allowing the specimens

examination at the herpetological collection of INPA.

The individuals were collected under permit 066/2012

provided by Instituto Brasileiro do Meio Ambiente e dos

Recursos Naturais Renovaveis (IBAMA). The Conselho

Nacional de Desenvolvimento Cientifico e Tecnologico

(CNPq, Brazil) provided a scholarship to LJCL Moraes.

Literature Cited

Almendariz A, Simmons JE, Vaca-Guerrero J, Brito J.

2014. Overview of the herpetofauna of the unex¬

plored Cordillera del Condor of Ecuador. Amphib¬

ian & Reptile Conservation 8: 45-64 (e82).

Alvares CA, Stape JL, Sentelhas PC, Gongalves JLM,

Sparovek G. 2013. Koppen’s climate classification

map for Brazil. Meteorologische Zeitschrift 22(6):

711-728.

Azevedo-Ramos C, Galatti U. 2002. Patterns of amphib¬

ian diversity in Brazilian Amazonia: Conservation

implications. Biological Conservation 103(1): 103—

111 .

Beirne C, Whitworth A. 2011. Frogs of the Yachana

Reserve. Global Vision International, Exeter, United

Kingdom. 109 p.

Bernal MH, Lynch JD. 2013. Thermal tolerance in

anuran embryos with different reproductive modes:

Relationship to altitude. The Scientific World Jour¬

nal 2013: 1-7.

Bemarde PS, Machado RA, Turci LCB. 2011. Herpe¬

tofauna da area do Igarape Esperanqa na Reserva

Extrativista Riozinho da Liberdade, Acre - Brasil.

Biota Neotropica 11(3): 117-144.

Boubli JP, Ribas CC, Lynch Alfaro J, Silva MNF, Pinho

GM, Farias IP. 2015. Spatial and temporal patterns

of diversification on the Amazon: A test of the river¬

ine hypothesis for all diurnal primates of Rio Negro

and Rio Branco in Brazil. Molecular Phylogenetics

and Evolution 82: 400^-12.

Catenazzi A, Lehr E, von May R. 2013. The amphibians

and reptiles of Manu National Park and its buffer

zone, Amazon basin and eastern slopes of the Andes,

Peru. Biota Neotropica 13(4): 269-283.

Cracraft J. 1985. Historical biogeography and patterns of

differentiation within the South American avifauna:

Areas of endemism. Ornithological Monographs

36; 49-84.

Castroviejo-Fisher S, Padial Jr. JM, Silva HR, Rojas-

Runjaic FJM, Medina-Mendez E, Frost DR. 2015.

Phylogenetic systematics of egg-brooding frogs

(Anura: Hemiphractidae) and the evolution of direct

development. Zootaxa 4004: 1-75.

Cisneros-Heredia DF. 2006. La Herpetofauna de la

Estacion de Biodiversidad Tiputini, Ecuador: Diver-

sidad & Ecologia de los Anfibios & Reptiles de una

Comunidad Taxonomicamente Diversa. B.Sc. The¬

sis, Universidad San Francisco de Quito, Quito,

Ecuador. 129 p.

Coloma LA, Ron S, Azevedo-Ramos C. 2004. Hemi¬

phractus scutatus. The IUCN Red List of Threat¬

ened Species 2004: e.T55371A11299534.

Duellman WE. 2005. Cusco Amazonico: The Lives of

Amphibians and Reptiles in an Amazonian Rainfor¬

est. Comstock Publishing Associates, Cornell Uni¬

versity Press, Ithaca, New York, USA. 488 p.

Duellman WE. 2015. Marsupial Frogs. Gastrotheca and

Allied Genera. Johns Hopkins University Press, Bal¬

timore, Maryland, USA. 432 p.

Duellman WE, Lynch JD. 1988. Anuran amphibians

from the Cordillera de Cutucu, Ecuador. Proceed¬

ings of the Academy of Natural Sciences, Philadel¬

phia 140(2): 125-142.

Fearnside PM. 2015. Amazon dams and waterways: Bra¬

zil’s Tapajos basin plans. Ambio 44(5): 426^139.

Frost DR. 2017. Amphibian Species of the World: An

Online Reference. Version 6.0. American Museum

of Natural History, New York, New York, USA.

Available: http ://research. amnh. org/herpetology/

amphibia/index.html [Accessed: 03 May 2017],

GBIF. 2017. Hemiphractus scutatus (Spix, 1824) spe¬

cies page. Available: http://www.gbif.org/spe-

cies/2429986 [Accessed: 03 May 2017],

Glaw F, Franzen M. 2006. Type catalogue of amphibians

in the Zoologische Staatsammlung Munchen. Spixi-

ana 29: 153-192.

Heyer WR, Donnelly MA, Mcdiarmid RW, Hayek LC,

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | e151

Occurrence of Hemiphractus scutatus in eastern Amazonia

Foster MS. 1994. Measuring and Monitoring Bio¬

logical Diversity: Standard Methods for Amphibi¬

ans. Smithsonian Institution Press, Washington, DC,

USA. 384 p.

Junk WJ, Bayley PB, Sparks RE. 1989. The flood pulse

concept in river-floodplain systems. Canadian Spe¬

cial Publication of Fisheries and Aquatic Sciences

106: 110-127.

Kimura MA. 1980. A simple method for estimating evo¬

lutionary rates of base substitutions through com¬

parative studies of nucleotide sequences. Journal of

Molecular Evolution 16(2): 111-120.

Latrubesse EM, Arima EY, Dunne T, Park E, Baker VR,

d’Horta FM, Wight C, Wittmann F, Zuanon J, Baker

PA, Ribas CC, Norgaard RB, Filizola N, Ansar A,

Flyvbjerg B, Stevaux JC. 2017. Damming the rivers

of the Amazon basin. Nature 546: 363-369.

Laurance WF, Cochrane MA, Bergen S, Fearnside PM,

Delamonica P, Barber C, D’Angelo S, Fernandes T.

2001. The future of the Brazilian Amazon. Science

29E 438-439.

Lehr E. 200E New records for amphibians and reptiles

from Departamentos Pasco and Ucayali, Peru. Her-

petological Review 32: 130-132.

Lynch JD. 2005. Discovery of the richest frog fauna in

the world—an exploration of the forests to the north

of Leticia. Revista de la Academia Colombiana de

Ciencias 29(113): 581-588.

Morrison C, Hero JM. 2003. Geographic variation in

life-history characteristics of amphibians: A review.

Journal of Animal Ecology 72: 270-279.

Moraes LJCL, Pavan D, Barros MC, Ribas CC. 2016.

The combined influence of riverine barriers and

flooding gradients on biogeographical patterns for

amphibians and squamates in south-eastern Amazo¬

nia. Journal of Biogeography 43(11): 2,113-2,124.

Moravec J, Tuanama IA, Burgos AM. 2002. Amphibians

recently recorded from the surroundings of Iquitos

(Departamento Loreto, Peru). I. Hylidae. Casopis

Narodmho Rada, pfirodovedna 171: 29-44.

Munoz-Saravia A. 2008. Geographic distribution: Hemi¬

phractus scutatus. Herpetofogicaf Review 39: 233.

Myers GS, Carvalho AL. 1945. Notes on some new or lit¬

tle-known Brazilian amphibians, with an examina¬

tion of the history of the Plata salamander, Ensatina

platensis. Boletim do Museu Nacional, Nova Serie,

Zoologia 35: 1-24.

Ortiz DA. 2013. Hemiphractus scutatus. In: Amphibi-

aWebEcuador. Version 2016.0. Editors, Ron SR,

Guayasamin JM, Yanez-Munoz MH, Merino-Vit-

eri A, Ortiz DA, Nicolalde DA. 2016. Museo de

Zoologia, Pontificia Universidad Catolica del Ecua¬

dor, Ecudaor. Available: http://zoologia.puce.edu.

ec/ vertebrado s/anfibios/F ichaE specie. aspx? Id=12 7 5

[Accessed: 03 May 2017],

Rainforest Conservation Fund. 2017. Species Data

Sheets, Reptiles & Amphibians, Hemiphractus scu¬

tatus. Available: http://www.rainforestconservation.

org/species-data-sheets/frogs/hemiphractus-scutatus

[Accessed: 03 May 2017],

Rodriguez LO, Duellman WE. 1994. Guide to the Frogs

of the Iquitos Region, Amazonian Peru. Peruvian

Field Guides Series No Sp 22 (Book 22). Asociacion

de Ecologia y Conservacion, Amazon Center for

Environmental Education and Research and Natural

History Museum, The University of Kansas, Law¬

rence, Kansas, USA. 89 p.

Ruiz-Carranza PM., Ardila-Robayo MA, Lynch JD.

1996. Lista actualizada de la fauna de Amphibia de

Colombia. Revista de la Academia Colombiana de

Ciencias Exactas, Fisicas y Naturales 20: 77,365-

77,415.

Sambrook JD, Russel W. 2001. Molecular Cloning: A

Laboratory Manual. 3 rd edition. Cold Spring Harbor

Laboratory Press, Cold Spring Harbor, New York,

USA. 999 p.

Sioli H. 1968. Hydrochemistry and geology in the Bra¬

zilian Amazon region. Amazoniana 1: 267-277.

Siqueira CC, Rocha CFD. 2013. Altitudinal gradients:

concepts and implications on the biology, the distri¬

bution and conservation of Anurans. Oecologia Aus-

tralisYl : 282-302

Sombroek W. 2001. Spatial and temporal patterns of

Amazon rainfall - Consequences for the planning

of agricultural occupation and the protection of pri¬

mary forests. Ambio 30: 388-396.

Souza MB. 2009. Anfibios: Reserva Extrativista do Alto

Junta e Parque Nacional da Serra do Divisor, Acre.

IFCH, Campinas, Brazil. 76 p.

SpeciesLink. 2017. SpeciesLink. Centro de Referencia

em Informagao Ambiental, CRIA. Available: http://

splink.cria.org.br [Accessed: 03 May 2017],

Spix JBV. 1824. Animalia nova sive Species novae Tes-

tudinum et Ranarum quas in itinere per Brasiliam

annis MDCCCXVII-MDCCCXX jussu et auspiciis

Maximiliani Josephi I. Bavariae Regis. F.S. Hiib-

schmann, Munchen, Germany. 29 p.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M,

Kumar S. 2013. MEGA6: Molecular Evolutionary

Genetics Analysis Version 6.0. Molecular Biology

and Evolution 30: 2,725-2,729.

Trueb L. 1974. Systematic relationships of Neotropical

horned frogs, genus Hemiphractus (Anura: Hyli¬

dae). Occasional Papers of the Museum of Natural

History, the University of Kansas 29: 1-60.

Vences M, Nagy ZT, Sonet G, Verheyen E. 2012. DNA

barcoding amphibians and reptiles. Pp. 79-107 In:

DNA Barcodes: Methods and Protocols. Methods in

Molecular Biology Series. Editors, Kress WJ, Erick¬

son DL. Humana Press, Inc., New York, New York,

USA. 470 p.

von May R, Siu-Ting K, Jacob JM, Muller MM, Gagliardi

G, Rodriguez LO, Donnelly MA. 2009. Species

diversity and conservation status of amphibians in

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | e151

Moraes and Pavan

Madre de Dios, southern Peru. Herpetological Con¬

servation and Biology 4(1): 14-29.

Wang X, Edwards LR, Auler AS, Cheng H, Kong X,

Wang Y, Cruz FW, Dorale JA, Chiang HW. 2017.

Hydroclimate changes across the Amazon lowlands

over the past 45,000 years. Nature 541: 204-207.

Appendix SI.

Specimens examined. Hemiphractus scutatus (n = 5): BRAZIL: Rondonia: Abuna esquerda, Porto Velho (65°20’S 09 o 3LW),

INPA-H15398, Jirau esquerda, Porto Velho, 1NPA-H15399 (64°44’S 09°20’W); Para: Left bank of middle Tapajos River, Itaituba

(05°02’S 56°53’W), 1NPA-H38116, Left bank of middle Tapajos River, Itaituba (04°39’S 56°37’W), INPA-H38117. Left bank

of middle Tapajos River, Itaituba (04°40’S 56°37’W), 1NPA-H38118. 1NPA-H = Collection of Amphibians and Reptiles of the

Institute Nacional de Pesquisas da Amazonia, Manaus, AM, Brazil.

Leandro J.C.L. Moraes has a B.S. in biology from the Universidade Federal de Sao Carlos (campus

Sorocaba, Brazil) and a Master’s degree in ecology at Institute Nacional de Pesquisas da Amazonia-

INPA, Manaus, AM, Brazil. Currently he is a researcher at the same institution. His research fields

include diversity, taxonomy, biogeography, evolution, and conservation of Neotropical amphibians

and reptiles.

Dante Pavan has a B. S. in biology from the Universidade de Sao Paulo - USP, Sao Paulo, Brazil and a

Master’s and Doctoral degrees in zoology at the same institution. He works mainly with environmental

impact studies, analyzing and predicting the anthropic impacts on amphibians and reptiles from diverse

Brazilian biomes.

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | e151

Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

12(1) [General Section]: 15-17 (el52).

Sighting of the Himalayan Trinket Snake, Orthriophis

hodgsonii Gunther (1860) (Reptilia: Colubr dae), in Sahastra

Dhara, Uttarakhand: A new elevational record

^bhishek Singh and 2 Ritesh Joshi

1 Endangered Flora and Fauna on Earth Conservation Team, Vasant Vihar, Dehradun, Uttarakhand, INDIA 2 Conservation & Survey Division,

Ministry of Environment, Forest & Climate Change, New Delhi, INDIA

Abstract .—In 2016, two individuals of Orthriophis hodgsonii (Himalayan Trinket Snake) were observed from

the Sahastra Dhara area, Uttarakhand, India, confirming the occurrence of this species in the Garhwal region.

This report provides the lowest elevational record (835 m) of Orthriophis hodgsonii from its previously known

distribution range (1,000-3,200 m).

Keywords. Geographic distribution, north India, Garhwal region, range extension, Sauria, conservation

Citation: Singh A, and Joshi R. 2018. Sighting of the Himalayan Trinket Snake, Orthriophis hodgsonii Gunther (1860) (Reptilia: Colubridae), in

Sahastra Dhara, Uttarakhand: A new elevational record. Amphibian & Reptile Conservation 12(1) [General Section]: 15-17 (e152).

NoDerivatives 4.0 International License, which permits unrestricted use for non-commercial and education purposes only, in any medium, provided

the original author and the official and authorized publication sources are recognized and properly 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-

reptiie-conservation.org>.

Received: 06 September 2016; Accepted: 21 December 2016; Published: 31 January 2018

Of the four species in the genus Orthriophis found across

the world ( Orthriophis mollendorffi, O. taeniurus, O.

hodgsonii , and O. cantoris ), three are found in India (O.

taeniurus, O. hodgsonii, and O. cantoris ) (Utiger et al.

2002; Whitaker and Captain 2004). The Himalayan Trin¬

ket Snake ( Orthriophis hodgsoni) is native to India, Ne¬

pal, and China (Tibet) (Whitaker and Captain 2004). In

India, this species is distributed in Jammu and Kashmir

northern Punjab, Himachal Pradesh, Uttarakhand, Bihar,

Northern, West Bengal Sikkim and Meghalaya, ranging

from the elevation of 1,000-3,200 m (Smith 1943; Das

2002; Whitaker and Captain 2004; Sharma 2007).

On 1 April 2016 (11:10 hours), a Himalayan Trinket

Snake (sex unknown) was recorded from a small barren

plot, located close to human settlements in the Sahastra

Dhara area near Dehradun (30°23'07.4"N, 78°07'40.5"E,

831.4 m; Fig. 1). The spot was near the protected forest

of the Mussoorie Forest Division. Some of the plants in

this area where the snakes were seen are: Murray a koe-

nigii (Curry Tree), Lantana camara (Fantana), Jatropha

curcas (Ban Arandi), and Datura stramonium (Jimson

Weed). Both snakes (including the one recorded below)

were photographed and visually identified based on de¬

scriptions given by Smith (1943), Sharma (2007), and

Whitaker and Captain (2004). No scalation data was

recorded. Thereafter, on 18 August 2016 (13:20 hours),

an individual of unknown sex was observed far from

where the first specimen was recorded (30°23'05.5"N,

78°07'44.6"E, 839.4 m; Figs. 2 and 3). Both sightings

were during the summer season and near the Sahastra

Dhara.

Husain and Ray (1995) first recorded this species from

Pauri, Chamoli, and Nainital districts of the Uttarakhand

State. Thereafter, Whitaker and Captain (2004) recorded

this species from Mussoorie, Almora, and Nainital dis¬

tricts of Uttarakhand State, at an elevation ranging from

1,000-3,200 m. Smith (1943), Sharma (2003) and Bahu-

guna (2010) also corroborated the presence of the Hima¬

layan Trinket Snake in the State. Vasudevan and Sondhi

(2010) had only included the Himalayan Trinket Snake

in a checklist of snakes of Uttarakhand but no description

and locality records were stated.

We herein confirm the occurrence of the Himalayan

Trinket Snake in the Uttarakhand State, Garhwal re¬

gion (Sahastra Dhara-a perennial river) and provide the

first record of its presence below 1,000 m. The Sahastra

Dhara is located in northern India at 29°26'-31°28'N and

77°49'-80°06'E and falls within the Himalaya Biogeo¬

graphic Zone and located in the West Himalaya Province.

The largest portion of this area is in the Shivalik’s Bio¬

geographic Subdivision, which constitutes an important

repository of reptilian fauna.

The Himalayan Trinket Snake has not yet been as¬

sessed by the IUCN Red Fist. Increasing development

Correspondence. ' ngoeffect@gmail.com ; 2 riteshJoshi2325@yahoo.com (Corresponding author)

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | el 52

Singh and Joshi

Fig. 1. Himalayan Trinket Snake, Orthriophis hodgsonii, near Sahastra Dhara.

Fig. 2. Close-up of the head of a Himalayan Trinket Snake recorded from Sahastra Dhara.

and anthropogenic activities across the riparian corri¬

dors, shrinkage of natural water sources inside protected

areas, expansion of the road network across a long chain

of protected habitats, and lack of awareness among the

local people were some of the observed threats that could

potentially lead to population decline of the species.

Acknowledgements. —The authors would like to

acknowledge the anonymous reviewers, including Mr.

Ashok Captain, a renowned Indian herpetologist and

conservationist, who provided valuable input and com¬

ments on the previous versions of the manuscript and

contributed significantly to improve the manuscript to its

present form. Thanks are due to Mr. Sudhakar Sharma

and Mr. Raj Shekhar Singh for assisting us in collecting

field data.

Literature Cited

Bahuguna A. 2010. Reptilia. Pp. 445-503 In: Fauna of

Uttarakhand. (Part 1) Vertebrates. State Fauna Se¬

ries 18. Editor, Director, Zoological Survey of India,

M-Block, New Alipore, Kolkata 700 053. Zoologi¬

cal Survey of India, Kolkata, India. 621 p. Available:

http:// faunaofindia. nic. in/PDF Volumes/sfs/062/index,

pdf [Accessed: 31 January 2018],

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | el 52

Himalayan Trinket Snake new elevation record

Fig. 3. Himalayan Trinket Snake in its natural habitat in the Sahastra Dhara area.

Das I. 2002. A Photographic Guide to the Snakes and

Reptiles of India. New Holland Publishers, London,

United Kingdom. 144 p.

Husain A, Ray P. 1995. Reptilia. Pp. 159-167 In: Fauna

of Western Himalaya (Part-2)-Himachal Pradesh. Hi¬

malayan Ecosystem Series (Part I). Editor, Director,

Zoological Survey of India, Kolkata, India. Published

by the Director, Zoological Survey of India, Kolkata,

India. 359 p. Available: http://faunaofindia.nic.in/PD-

FVolumes/ess/021/index.pdf [Accessed: 31 January

2018],

Rodgers WA, Panwar HS, Mathur VB. 2002. Wildlife

Protected Areas in India: A review. Executive Sum¬

mary. Wildlife Institute of India, Dehradun, India. 44

P-

Sharma RC. 2003. Handbook: Indian Snakes. Editor,

Director, Zoological Survey of India, Kolkata, India.

Publisher, Zoological Survey of India, Kolkata, India.

292 p.

Sharma RC. 2007. The Fauna of India and the Adjacent

Countries: Reptilia, Volume 2: Sauria. Editor, Direc¬

tor, Zoological Survey of India, Kolkata, India. Pub¬

lisher, Zoological Survey of India, Kolkata, India. 410

p. Available: http://faunaohndia.nic.in/PDFVolumes/

h/037/index.pdf [Accessed: 31 January 2018],

Smith MA. 1943. The Fauna of British India, Ceylon and

Burma including the Whole of the Indo-Chinese Sub-

region, Reptilia and Amphibia Volume III. Serpents.

Taylor and Francis, London, England. 583 p.

Utiger U, Helfenberger N, Schatti B, Schmidt C, Ruf M,

Ziswiler V. 2002. Molecular systematic and phylog-

eny of old and new world ratsnakes, Elaphe AUCT.,

and related genera (Reptilia, Squamata, Colubridae).

Russian Journal of Herpetology 9(2): 105-124.

Vasudevan K, Sondhi S. 2010. Amphibians and Reptiles

of Uttarakhand, India. Wildlife Institute of India,

Dehradun, Uttarakhand, India. 94 p.

Whitaker R, Captain A. 2004. Snakes of India, The Field

Guide. Draco Books, Chennai, India. 481 p.

Abhishek Singh graduated from the Subharti University, India in 2009. He is the chairman of the non

governmental organization Endangered Flora and Fauna on Earth Conservation Team (EFFECT). His

research interests are the ecology and taxonomy of reptiles in northern India, and particularly serpents

and threatened species. He is also associated with TRAFFIC India (The Wildlife Trade Monitoring

Network). The past six years, he has been actively involved in providing training in the identification

and rescue of various poisonous and non-poisonous snakes, as well as other wildlife, to the staff of the

State Forest Department of Uttarakhand State.

Ritesh Joshi is a scientist presently working for the Ministry of Environment, Forest and Climate

Change, Government of India. He has a bachelor, master’s, and doctorate degree in environmental

sciences from India universities. Dr. Joshi is actively involved in research on wildlife in protected

areas of northern India. His research interest includes ecology and behavior of wildlife, especially

mammals and serpents. He has published three books on wildlife and more than 75 research papers in

various national and international scientific journals. He has also published nearly 50 scientific articles

in scientific magazines on wildlife and conservation of the environment. The Department of Official

Fanguages, Ministry of Home Affairs, Government of India, has honored Ritesh with the Rajiv Gandhi

National Award for his book. Wildlife of Uttarakhand and Conservation. This award was given to him

by the Hon’ble President of India in 2015.

Amphib. Reptile Conserv.

January 2018 | Volume 12 | Number 1 | el 52

Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

12(1) [General Section]: 18-26 (el53).

Captive management, reproduction, and comparative

larval development of Klappenbach’s Red-bellied Frog,

Melanophryniscus klappenbachi Prigioni and Langone, 2000

1 ’ 2 Nils Behrand ^Dennis Rodder

1 Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, D - 53113 Bonn, GERMANY

Abstract. —In this study, we report on the successful keeping, breeding, and rearing of Klappenbach’s Red-

bellied Frog, Melanophryniscus klappenbachi Prigioni and Langone, 2000. Breeding and spawning took place

after a relatively dry period without using a brumation period. To initiate mating behavior the toads were

introduced into a rain chamber with a raised water level and constant irrigation in accordance with the toad’s

natural habitat and heavy rainfalls. The fast developing tadpoles started metamorphosis after 19 days at a

constant water temperature of 23 °C and pH values between 6.5 and 7.9. A higher pH value led to slightly faster

growth irrespective if tadpoles were reared singly or in groups.

Keywords. Amphibians, Anura, captive breeding, conservation breeding, environmental factors, spawning

Citation: Behr N, Rodder D. 2018. Captive management, reproduction, and comparative larval development of Klappenbach’s Red-bellied Frog,

Melanophryniscus klappenbachi Prigioni and Langone, 2000. Amphibian & Reptile Conservation 12(1) [General Section]: 18-26 (el 53).

cialNoDerivatives 4.0 International License, which permits unrestricted use for non-commercial and education purposes only, in any medium, provided

the original author and the official and authorized publication sources are recognized and properly credited. The official and authorized publication

credit sources, which will be duly enforced, are as follows: official journal

reptile-conservation. org>.

Received: 02 January 2017; Accepted: 28 August 2017; Published: 01

Introduction

The genus Melanophryniscus Gallardo, 1961 is current¬

ly represented by 29 species which have been reported

from southern Bolivia and southern Brazil in the north

over Paraguay to Uruguay and northern Argentina in the

south. They are commonly referred to as South American

Redbelly Toads due to the red or orange flash markings

upon their ventral bodies, hands, and feet (Frost 2016).

Species of this genus have been divided into three phe¬

notypic species groups based on morphological charac¬

teristics: the Melanophryniscus tumifrons , M. moreirae ,

and M. stelzneri groups (Cruz and Caramaschi 2003).

Klappenbach’s Red-bellied Frog (M klappenbachi Pri¬

gioni and Langone, 2000) is part of the Melanophrynis¬

cus stelzneri group (Cruz and Caramaschi 2003), which

currently includes eight more species, i.e., M. atroluteus

(Miranda-Ribeiro, 1920), M cupreuscapularis (Cespe-

dez and Alvarez, 2000), M. dorsalis (Mertens, 1933),

M. fulvoguttatus (Mertens, 1937), M. krauczuki (Baldo

and Basso, 2004), M. montevidensis (Philippi, 1902), M.

rubriventris (Vellard, 1947), and M. stelzneri (Weyen-

bergh, 1875).

Klappenbach’s Red-bellied Frog is characterized by a

yellow stripe between the eyes or two to three large yel¬

low blotches forming a distinct interocular band. Its dor-

COrrespondence. 2 s6nibehr@uni-bonn.de; 3 <7 roedder@leibniz-zfmk

title Amphibian & Reptile Conservation ; official journal website <amphibian-

May 2018

sal and ventral surfaces are covered with small and large,

irregularly formed yellow blotches on a black base color

(see Fig. 1A and B) (Kwet et al. 2005). Adults of this di¬

urnal species reach an average size of 2.5 to 3.0 cm (Pri¬

gioni and Langone 2000). Melanophryniscus klappenba¬

chi inhabits usually dry environments, such as shrubland

habitats, in north-eastern Argentina and Paraguay at 50

to 100 m above sea level (Bland 2015; Frost 2016). Af¬

ter heavy rainfalls explosive breeding takes place in the

emerging ephemeral water bodies (Aquino et al. 2004).

Fast development of tadpoles increases the probability of

completing metamorphosis before water bodies dry out

(Kurth et al. 2013).

Currently Klappenbach’s Red-bellied Frog is listed as

Least Concern by the IUCN Red List of Threatened Spe¬

cies, due to its wide distribution, large and stable popula¬

tions, and its tolerance for habitat modification (Aquino

et al. 2004).

Although it was once a popular species in the pet trade

it does not seem to be regularly reproduced in captivity

(Bland 2015; Aquino et al. 2004). Amphibians are one of

the most threatened animal taxa with more than one third

of the currently described species (ca. 7,520) recognized

as threatened with extinction (Frost 2016; Hoffmann et

al. 2010; Stuart et al. 2004). For threatened species ex

situ captive-breeding programs are relevant instruments

.de (Corresponding author)

Amphib. Reptile Conserv.

May 2018 | Volume 12 | Number 1 | el 53

Behr and Rodder

Fig. 1. Melanophrynisens klappenbachi. (A) Dorsal and (B) ventral view of an adult female. (C) Amplexus. (D) Egg clump attached

to moss. (E) Contrasting photo of a tadpole, used for evaluating the growth.

in learning more about a species and to build up assur¬

ance populations against extinction (Gawor et al. 2011).

Kurth et al. (2013) have already reported on repro¬

ductive cues and larval development in M. klappenbachi ,

while Bland (2015) has given a short report of rearing

captive bred M. klappenbachi. However, both papers did

not consider influences of differing water parameters or

group sizes on the development of young tadpoles.

Herein, we present captive management conditions at

the animal keeping facility of the Zoological Research

Museum Alexander Koenig (ZFMK), Bonn, Germany,

experiences in breeding without the use of a brumation

period, and rearing tadpoles. Further this paper reports on

the influence of different pH values and group sizes for

growth and mortality rates of early developmental stages

of Klappenbach’s Red-bellied Frog.

Materials and Methods

Captive management and breeding

The basis for the breeding stock used in this study was

built up by a group of eight M. klappenbachi purchased

from a pet shop in 2011, which were imported from Para¬

guay according to the vendor. The group of adult toads

were housed in a terrarium measuring 120 x 50 x 50 cm

(L x w x H) in the animal keeping facility of the ZFMK.

The terrarium bottom was covered with a six cm thick

filter pad which was diagonally cut in the front, result¬

ing in a water surface of 120 x 12 cm. There was at least

a water level of two cm depth in the tank at all times,

including the dry phase. Previous setups have revealed

that toads were not able to swim for long periods of

time, thus water levels needed to be shallow or a num¬

ber of aquatic plants provided to prevent drowning. The

complete ground and all three side walls were covered

with Hygrolon®, a novel synthetic material that is non-

decomposable and mimics the features of dead cellulose

cells. This material is highly hygroscopic and used to en¬

sure high air humidity.

The terrarium setup for the frogs was automatically

misted three times per day for 30 seconds and air hu¬

midity varied between 70% and 80%. The setup was

equipped with different plants, i.e., Ficuspiimila , Bego¬

nia sp., Neoregelia schnltesiana, Pilea sp., an undefined

fast-growing Venezuelan tendril, and different mosses.

Additionally leaf litter, pieces of cork bark, and roots

were added to the terrarium in order to provide hiding

and climbing space for the toads. Photoperiod was set to

daylight between 8:00 and 20:00 h, as lighting LED light

Amphib. Reptile Conserv.

May 2018 | Volume 12 | Number 1 | el 53

Klappenbach’s Red-bellied Frog, Melanophryniscus klappenbachi

Fig. 2. Keeping and rearing M. klappenbachi. (A) Terrarium

of the adult group housing eight specimens. (B) Rearing of the

tadpole test groups in a climate chamber. (C) Rearing containers

for the young toadlets.

strips (Solar Stinger 1,100 mm Sunstrip Dimmable Driv¬

er). Temperatures varied between 22 °C and 26 °C. Toads

were fed flightless fruit flies ( Drosophila melanogaster

and D. hydei) and rarely with pinhead crickets ( Acheta

domestica and Gryllus assimilis ). All prey was dusted

with mineral or vitamin powder (i.e., herpetal Amphib,

herpetal Mineral + Vitamin D3, and herpetal Complete

Terrarium) and gut loaded with fresh vegetables or fruit

puree before being fed to the toads.

To artificially initiate breeding season toads were

placed into a second terrarium measuring 60 x 50 x 70

cm. The breeding terrarium was filled with water to a

depth of six to seven cm and equipped with a few pieces

of xaxim, a big root, and some plants (i.e., Spathipyllnm

sp., some mosses, and Microsorum pteropns ) to provide

small areas above the water. Temperature and lighting

were the same as described above. In this tank a perma¬

nent rain system was installed that irrigated the back wall

of the terrarium all day long. After successful mating and

spawning, when the males stopped calling and the pairs

did not exhibit amplexus any longer, all toads were trans¬

ferred into the first terrarium again.

The spawn was divided into four aquariums measur¬

ing 30 x 30 x 30 cm filled with osmosis water to a depth

of about 20 cm. Water temperature varied between 22 °C

and 25 °C. A few aquatic plants (Java Fern, Microsorum

pteropus ) and small aquatic snails (Bladder Snails, Phy-

sella sp., and Ramshorn Snails, Planorbella sp.) were

added into each aquarium.

Table 1. Water parameters of the different pH value groups.

Comparative setup

For rearing tadpoles water with various pH values was

used: osmosis water with a measured pH of 6.5-7.0 and

pond water with a measured pH of 7.7-8.0. To obtain

water with a reduced pH value a small amount of peat

was added to the osmosis water, until a pH of 5.5-5.8

was obtained. Afterwards water was filtered to remove

the remaining peat. Table 1 lists the additionally mea¬

sured water parameters.

Once tadpoles had hatched, a total of 108 larvae were

randomly chosen and divided into different groups. All

tadpoles were transferred into plastic boxes measuring

10 x 10 x 10 cm filled with a water depth of eight cm. Ev¬

ery box was equipped with a single aquatic plant (either a

small Java Fern, Microsorum pteropus , or a short branch

of Hornwort, Ceratophyllum sp.) to provide shelter and

one aquatic snail (either Bladder Snails, Physella sp., or

Ramshorn Snails, Planorbella sp.) to remove remaining

food. For each pH value there were two different group

sizes of either one tadpole or five tadpoles per box, to de¬

termine if group size influenced individual growth rate.

Six samples were set up for each group size, so that a

total of twelve boxes and 36 tadpoles were exposed to

each pH value.

All tadpoles were kept in a climate chamber (Versa¬

tile Environmental Test Chamber MLR-352H-PE) under

standardized conditions. The temperature was set to 23

°C and the photoperiod was set to daylight between 6:00

and 18:00 h each day. Inside the climate chamber boxes

of different group sizes and pH values were placed ran¬

domly (see Fig. 2 B). The larvae were fed every second

day with a mixture of pulverized fish food dissolved in

water. Additionally one object slide overgrown with a

thin layer of algae was placed in every box and renewed

every three days. Two thirds of entire water content was

exchanged every second day. All boxes were checked

daily to remove deceased tadpoles and later to transfer

metamorphosed froglets to a terrestrial setup.

Newly morphed toads were relocated into plastic

containers measuring 33 x 21 x 28 cm. Two layers of

Hygrolon® were used as ground layer to ensure high air

humidity in rearing containers. One side of the boxes was

placed on a heightened surface, so a height difference of

10 cm was formed from one end of the box to the other

and a water part with a depth of 1-2 cm was created (see

Fig. 2 C). As a result, a humidity gradient was created

in the box, letting toads choose their preferred humidity.

Containers were equipped with a small plant (undefined

Venezuelan tendril) and some oak leaf litter.

NQ 2 [mg/L] NQ 3 [mg/L] NH 4 [mg/L] Cu [mg/L] KH [°dH] GH [°dH] pH

Osmosis water <0.05 7.5 <0.05 <0.1 3 5 6.5-7.0

Pond water <0.05 <0.5 <0.05 <0.1 9 8 7.7-8.0

Peat water <0.05 7.5 <0.05 <0.1 3 5 5.5-5.8

Amphib. Reptile Conserv.

May 2018 | Volume 12 | Number 1 | el 53

Behr and Rodder

Fig. 3. Developing coloration in young toadlets of different ages. (A) Recently metamorphosed toadlet. (B) Ten days after

metamorphosis. (C) Twenty-three days after metamorphosis. (D) Two months after metamorphosis.

Data collection and evaluation

Photos of each single tadpole were taken three times:

first, on the day they were transferred into the boxes, sec¬

ond, five days later and third, one week later when the

first tadpoles had already grown hind legs. Photos were

taken with a digital camera (Olympus TG-2). Tadpoles

were individually transferred into a petri dish placed on

a transparent glass plate lightened from below thus in¬

creasing the contrast between tadpole and its surround¬

ings (see Fig. 1 E).

To evaluate the growth of tadpoles the digital image

analysis tool SAISAQ (Kurth et al. 2014) was used. This

tool is programmed on the open source statistics platform

R (R Developmental Core Team 2016) and facilitates the

semiautomatic processing of standardized image files

computing the surface area of a tadpole, which is highly

correlated with its body mass (Kurth et al. 2014). As this

method is non-invasive it is ideally suited for repeated

measurements on live animals.

Results

Breeding

Within one hour after relocating adult toads into the

breeding terrarium males began to call. The first amplex-

us could be observed only a few hours after relocating

toads. Klappenbach’s Red-bellied Frogs show an axil¬

lary amplexus. Eggs were found on the second day in the

breeding tank. Spawn was mainly deposited in clumps of

10-30 eggs, some clumps were attached to the plants or

xaxim pieces under water and some were just deposited

in the water without any such attachment. Often next to

egg clutches were a few single eggs. Eggs were greyish

and had a diameter of 1.5-2.0 mm surrounded by a ge¬

latinous capsule. The last recorded spawn was produced

on the ninth day after transfer to the breeding terrarium.

No amplexus was observed after egg laying and females

appeared slimmer. After two more days in which no am¬

plexus was achieved and no more spawn was deposit-

May 2018 | Volume 12 | Number 1 | el 53

Amphib. Reptile Conserv.

Klappenbach’s Red-bellied Frog, Melanophryniscus klappenbachi

Mortality [%]

•P-l

-P-5

0-1

-0-5

3 3

■a

■»-*

* 4 -

I-

-Q

i p-i

l P-5

0-1

10-5

19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36

Time [d]

Fig. 4. (A) Mortality rate of different test groups until

metamorphosis. (B) Average growth rate of the different test

groups. (C) Number of tadpoles metamorphosed per day after

hatching (O = osmosis water, P = pond water, number indicates

individuals per container).

ed all frogs were relocated into their regular terrarium.

Males continued calling infrequently, females showed no

further reproductive behavior.

About three weeks after relocating the toads into their

regular terrarium at least one female toad spawned again.

Several egg clumps were found in the water, the spawn

was attached to moss and leaves. As before, these eggs

were relocated into an aquarium measuring 30 x 30 x 30

cm and raised in this tank at a temperature of 22-25 °C

and a water depth of about 20 cm.

Development

Development of eggs and M. klappenbachi tadpoles

have not been documented in the wild and development

mostly correlated the records of Kurth et al. (2013) and

Bland (2015). Tadpoles hatched within two to four days

after spawning. There was no difference in hatching rate

between eggs deposited in clumps and those deposited

individually. After giving a few drops of the food mixture

into water tadpoles seemed to actively seek for food on

the ground. Larvae did also feed by rasping algae from

the object slide. The first tadpoles metamorphosed af¬

ter 19 days, whereas the last tadpoles of the test groups

needed much more time to complete their development

and left the water after 36 days. However, there were still

a few tadpoles left in the bigger aquarium (30 x 30 x

30 cm), which did not metamorphose by this time. They

were still fully aquatic and did only grow hind legs or no

legs at all. After 83 days the last two of these remaining

larvae metamorphosed, being the same size as the earlier

metamorphed toadlets.

Just after reabsorbing the tail the small toadlets mea¬

sured 6-7 mm (snout-vent-length). At this stage their col¬

oration was dark grey to black without the conspicuous

yellow markings (see Fig. 3 A). Typical patterns devel¬

oped after one to two weeks (see Fig. 3 B). However,

all bred toadlets did not develop any red coloration on

their ventral surface, unlike the wild caught adults which

showed ventral flash markings colored yellow. The first

three weeks young toads were fed tropical springtails

(<Collembola sp.) once a day, so that food was always

available. Afterwards they were fed every second day.

Mortality

All larvae kept in water with the lowest pH value (pH

5.5-5.8) survived for at least two days, but then died

within the following four days. Tadpoles raised in wa¬

ter with the highest pH value (pH 7.7-8.0) had a total

mortality rate of 30.56% (11 out of 36); the singly kept

larvae had a mortality of 50.00% (3 out of 6). Those kept

in groups of five had a mortality of 26.67% (8 out of 30).

Those larvae which were kept in osmosis water with a

pH value of 6.5-7.0 had a total mortality rate of 25.00%

(9 out of 36). Single tadpoles had a mortality of 33.33%

(2 out of 6) and larvae raised in groups of five showed a

mortality of 23.33% (7 out of 30) (Fig. 4 A).

In the first eight days after hatching the total number

of deceased tadpoles was at the highest level. After this

period there were only occasional losses in the different

test groups. In the test group of single tadpoles kept in

pond water (P-l) there were no losses of larvae after day

six.

Growth rate

Tadpoles in water with the lowest pH value of 5.5-5.8

did not show any sign of growth before they died. The

group size did not show an influence on the growth of

the tadpoles in the more alkaline pond water (P-l, single

tadpole, and P-5, five tadpoles per box). In osmosis wa¬

ter the single-kept tadpoles (O-l) grew slower than tad¬

poles in groups of five larvae per box (0-5). Aside from

these results, tadpoles grew faster in pond water than in

Amphib. Reptile Conserv.

May 2018 | Volume 12 | Number 1 | el 53

Behr and Rodder

2.5 -r

2.0

1.5 -

1.0

0.5

0 -L

2.5 -r

2.0

1.5 -

1.0

0.5 -

0-1

■x

Day 1 Day 6 Day 13

P-1

Day 1 Day 6 Day 13

2.5 -r

2.0

1.5 -

1.0

0.5

0 -L

0-5

Day 1 Day 6 Day 13

2.5 -r

2.0

1.5 -

1.0

0.5 -

P-5

Day 1 Day 6 Day 13

Fig. 5. Body size of different test groups. (A) Single tadpole, 0-1, and (B) five tadpoles per box, 0-5, in osmosis water. (C) Single

tadpole, P-1, and (D) five tadpoles per box, P-5, in pond water.

osmosis water (compare Fig. 4 B).

Single kept tadpoles raised in osmosis water (0-1)

showed the slowest growth of the test groups, with a

mean body size of 0.773 cm 2 on day 13 after hatching

and the biggest larva measuring 1.347 cm 2 (Fig. 5 A).

Tadpoles in groups of five (0-5) grew faster and had a

mean body size of 1.206 cm 2 on day 13. The largest tad¬

pole of the test groups was in the prior group and mea¬

sured 2.281 cm 2 on the third measurement (Fig. 5 B). The

growth rate of tadpoles raised in pond water was quite

similar in both test groups. On day 13, single kept larvae

(P-1) had a mean body size of 1.537 cm 2 and a maxi¬

mum size of 2.102 cm 2 (Fig. 5 C), while tadpoles reared

in groups (P-5) showed a mean body size of 1.441 cm 2

with the largest tadpole measuring 2.183 cm 2 (Fig. 5 D).

Metamorphosis

On day 19 after hatching the first tadpoles of three test

groups (P-1, P-5, and 0-5) metamorphosed. The number

of tadpoles metamorphosing per day reached its highest

level on this day: in total seven larvae metamorphosed,

four out of these seven tadpoles were in group P-5. The

first tadpoles of the fourth group (0-1) metamorphosed

on day 23. The last two larvae metamorphosed on day 36

(Fig. 4 C).

Discussion

Based on our husbandry experiences, the keeping, breed¬

ing, and rearing of Melanophryniscus klappenbachi in

captivity is rather easily achieved. Most noticeable in the

lifecycle of Klappenbach’s Red-bellied Frog is of course

the rapid larval development with the first tadpoles

completing metamorphosis after 19 days at pH values

between 6.5 and 7.9. This fast development represents

an adaptation to the climate in their natural habitat. Af¬

ter heavy rainfalls adults start breeding in the emerging

small temporal water bodies, which have a high desicca¬

tion risk due to drying up of these small puddles. Thus,

the fact that a few tadpoles did not metamorphose after

80 days is rather surprising and has never been reported.

Amphib. Reptile Conserv.

May 2018 | Volume 12 | Number 1 | el 53

Klappenbach’s Red-bellied Frog, Melanophryniscus klappenbachi

Table 2. Husbandry parameters for adult breeding groups of Melanophryniscus klappenbachi according to Kurth et al. (2013),

Bland (2015), and data from this study.

Kurth etal. (2013)

Bland (2015)

own data

Breeding group

12 adults

3 adults (2 males + 1 female)

8 adults

Terrarium size (L x W x H)

80 x 40 x 40 cm

46 x 39 x 30 cm

120 x 50 x 50 cm

Water part (L x W)

30 x 10 cm

shallow water dish

120 x 12 cm

Water depth

10 cm

—

2 cm

Temperature

—

22-26 °C

Hibernation: duration;

temperature

3 weeks; 8 °C

4 days; 5-8 °C (only the

female)

not applied

Rainy season: duration;

temperatures

—

—; 20-25 °C

11 days; 22-26 °C

Rain chamber (L x w x H)

40 x 50 x 40 cm

60 x 45 x 45 cm

60 x 50 x 70 cm

Water part (L x W)

1/4 of the terrarium (500 cm 2 )

60 x 45 cm (only floating

cork bark as land areas)

60 x 50 cm (only xaxim, a

root and plants as land areas)

Water depth

5 cm

10 cm

6 cm

Nourishment

—

Hatchling crickets,

Drosophila sp., Siera sp.;

supplemented with Repashy

Calcium Plus

Hatchling crickets,

Drosophila melanogaster ,

D. hydei ; supplemented with

herpetal powder (Amphib,

Mineral + Vitamin D3,

Complete Terrarium)

It was not known that tadpoles of M. klappenbachi might

stay in the larval stage for a longer time before metamor¬

phosing. This behavior was only observed in the tadpoles

which were kept in the bigger aquarium with a water level

of at least 20 cm, whereas none of the test animals in the

small boxes (10 x 10 x 10 cm) showed this long-time lar¬

val stage. A possible reason for this might be intraspecific

competition amongst tadpoles. The availability of food

and other resources could directly influence length of the

larval stage as well. It could also be possible that tadpoles

might be able to sense water levels of their surrounding

environment so larvae could metamorphose before water

levels decrease. Perhaps it is an adaptation, which allows

a few tadpoles to survive in deeper water pools increas¬

ing overall species survivorship as a “backup.” If the ma¬

jority of the first, fast metamorphosing froglets die due

to unstable environmental conditions, these “backup”

tadpoles could increase the persistence of the species.

Richter-Boix et al. (2011) investigated the influence of

drying conditions on larval development in anurans and

found plasticity of development across different taxa.

Therefore, it would be an interesting approach for future

studies on M. klappenbachi to investigate the influence

of desiccation stress on the duration of tadpole develop¬

ment and growth rates.

For the last steps of metamorphosing, growing legs,

and reabsorbing the tail, tadpoles did not require more

time than larvae metamorphosing earlier, these steps

were accomplished in only two to three days. The pres¬

ence of long-tenn tadpoles under natural conditions

might provide a steady supply of metamorphosed toads

to their environment. However, this is currently not

known from wild populations of M. klappenbachi and

further field studies are suggested.

Water with a low pH value of 5.5-5.8 had a lethal ef¬

fect on tadpoles within a few days and tadpoles which

survived for five or six days in this water did not show

any sign of growth. As M. klappenbachi deposits its eggs

into small ephemeral ponds produced by rainwater, the

pH value of these breeding sites is directly dependent on

the characteristics of rainwater and soil. Therefore, the

ground in Klappenbach’s Red-bellied Frog’s native envi¬

ronment has most likely neutral or even alkaline charac¬

teristics. Hence acid rain, which for example could occur

due to air pollution, might be a possible future threat to

tadpoles of M. klappenbachi. The burning of woodland

is a common procedure in slash-and-burn agriculture to

establish land for agricultural cultivation and can lead to

a higher amount of acidity in regional rainfall (Tinker et

al. 1996).

In the groups of five tadpoles it was often the case that

there were three or four big tadpoles which grew faster

than the remaining one or two. These remaining tadpoles

showed slower growth, stayed smaller for a longer time,

and metamorphosed a few days later than the larger tad¬

poles in the group. Additionally, these smaller specimens

showed a higher mortality rate. Though live cannibal¬

ism was not observed, the deceased tadpoles were often

partly or even completely eaten by their kin. Intraspe¬

cific competition for resources, mostly food and space,

is a likely explanation for this observation. However in

the single kept tadpoles there were a few slow-growing

specimens (compare growth rate, Fig. 4 B). Since these

tadpoles were not influenced by conspecifics and intra-

Amphib. Reptile Conserv.

May 2018 | Volume 12 | Number 1 | el 53

Behr and Rodder

specific competition for food, the difference in growth

might be at least partly genetically controlled. Small and

weaker tadpoles might be predestined to be cannibalized

by conspecifics and thus make up an important source

of food, as there could be a lack of other food options

in ephemeral breeding sites. A similar case is the can¬

nibal morph of some Ambystoma tigrinum larvae, which

have the genetic capacity to develop distinct characters

adapted to feeding on conspecifics and other salamanders

(Rose and Armentrout 1976).

Breeding of Klappenbach’s Red-bellied Frog is often

stimulated by a brumation period followed by the simu¬

lation of a rainy season (Kurth et al. 2013; Bland 2015;

see also Table 2). However, our data indicates that a bru¬

mation is not a crucial factor for the successful mating

and breeding of M. klappenbachi. After a long dry sea¬

son of five to six months we relocated toads into the rain

chamber (without hibernating at low temperatures) and

males began to call almost immediately. This method is

less stressful for the toads, thus it is recommended to use

a mild brumation period as described by Bland (2015), if

females do not deposit eggs after one to two weeks in the

rain chamber.

Klappenbach’s Red-bellied Frogs rely on the avail¬

ability of very small prey items. Anything larger than a

large Drosophila sp. was observed to not be eaten. Fruit

flies, pinhead crickets, small isopods (e.g., Trichorhina

tomentosa ), and springtails are easily accepted food

items, which can be purchased in pet stores and online

shops, and are consumed willingly by adult toads. One

interesting observation made while feeding breeding

groups was that fully grown adult toads preferred small¬

er prey items to those larger in size. It was noticed that

while feeding fruit flies and springtails at the same time

springtails were favored over fruit flies.

One problem in rearing young metamorphosed toad-

lets was the need to have the smallest food items avail¬

able. We fed these toadlets only springtails, as these are

the smallest available food insects which can be pur¬

chased in most pet stores. It is most probable as well that

small toads would feed on mites, tiny ground-dwelling

insects, and other invertebrates. Drosophila hydei were

fed to toadlets after two to three months though only the

larger toads managed to catch these fruit flies successful¬

ly. Smaller toads tried to eat these flies, too, but showed

problems swallowing them. None-the-less, larger toad¬

lets preferred to feed on springtails.

To prevent high mortality, toadlets need to be kept on

humid ground with high air humidity. For that purpose a

few layers of the artificial material Hygrolon® were used

and worked well keeping humidity high in containers.

The Hygrolon® layers soaked up water, thus ensuring a

high humidity in rearing boxes. However, with advanc¬

ing age the froglets prefer dryer areas in their rearing

containers and seem to suffer from ground humidity that

was too high, especially in combination with insufficient

air ventilation. Thus, toads must be observed carefully

in the first few weeks and months to recognize the right

time to decrease humidity or to relocate toadlets into a

dryer box. The right humidity turned out to be a crucial

factor in the husbandry of Klappenbach’s Red-bellied

Frogs, especially in rearing young toads.

Introducing captive breeding programs and maintain¬

ing reserve populations in captivity might be one basic

requirement for adequate ex situ conservation arrange¬

ments. Together with natural history studies the husband¬

ry and captive breeding of endangered species give an in¬

sight into behavior and leads to a better understanding of

amphibians, the most endangered group of vertebrates.

Currently, M. klappenbachi is fisted as Least Concern by

the IUCN Red List of Threatened Species due to its rela¬

tively wide distribution, large and stable populations, and

its occurrence in several protected areas in both Paraguay

and Argentina (Aquino et al. 2004). Nevertheless Aqui¬

no et al. (2004) have stated that more research on the

species’ distribution and the effects of the pet trade are

necessary. Furthermore the explosive breeding behavior

of this species makes it more vulnerable to diseases, as

many adults gather in small vernal pools for mating and

spawning. As Bland (2015) has noted, Batrachochytrium

dendrobatidis or other infectious diseases could become

a serious threat for Klappenbach’s Red-bellied Frog and

could lead to severe population declines or extinction.

According to the IUCN Red List many other species of

the genus Melanophryniscus are listed as Near Threat¬

ened or Threatened, with three species listed as Critically

Endangered (i.e., M. admirabilis , M. langonei, and M.

peritus) and for some species sufficient data is missing

suggesting further field studies are necessary (Acquino

et al. 2004). These endangered species might benefit

from detailed knowledge about the husbandry and repro¬

duction in captivity of a closely related species like M

klappenbachi, as the methods described herein may be

applicable to them as well. This knowledge can be used

to build up reserve populations and to set up breeding

programs to returning captive produced specimens to the

wild, if necessary.

Acknowledgements. —We are grateful for financial

support from Alexander-Koenig-Gesellschaft, Bonn.

Thomas Ziegler and an anonymous referee provided

helpful comments to an early version of the manuscript.

Timo Hartmann and David Hornes helped with the cap¬

tive management of the species.

Literature Cited

Aquino L, Kwet A, Baldo D, Cespedez J. 2004. Mela¬

nophryniscus klappenbachi. The IUCN Red List

of Threatened Species 2004: e.T54822Al 1209703.

Available: http://dx.doi.org/10.2305/IUCN.UK.2004.

RLTS.T54822A11209703.en [Accessed: 21 August

2016],

Bland AW. 2015. A record of captive reproduction in

Amphib. Reptile Conserv.

May 2018 | Volume 12 | Number 1 | el 53

Klappenbach’s Red-bellied Frog, Melanophryniscus klappenbachi

the Red bellied toad Melanophryniscus klappenbachi

with notes on the use of a short-term brumation pe¬

riod. The Herpetological Bulletin 131: 15-18.

Cruz CAG, Caramaschi U. 2003. Taxonomic status

of Melanophryniscus stelzneri dorsalis (Mertens,

1933) and Melanophryniscus stelzneri fulvoguttatus

(Mertens, 1937) (Amphibia, Anura, Bufonidae). Bo-

letim do Museu Nacional Nova Serie, Zoologia 500:

1 - 11 .

Frost DR. 2016. Amphibian Species of the World: An

online reference. Version 6.0 (17 January 2014). Elec¬

tronic database. American Museum of Natural His¬

tory, New York, New York, USA. Available: http://

research.amnh.org/herpetology/amphibia/index.html

[Accessed: 21 August 2016],

Gawor A, van der Straeten K, Karbe D, Manthey U,

Ziegler T. 2011. Reproduction and development of

the dark-sided frog Hylarana nigrovittata sensu lato

at the Cologne Zoo. Salamandra 47: 1-8.

Hoffmann M. 2010. The impact of conservation on the

status of the world’s vertebrates. Science 330: 1,503-

1,509.

Kurth M, Hornes D, Esser S, Rodder D. 2013. Notes on

the acoustic repertoire of Melanophryniscus klappen¬

bachi Prigioni & Langone, 2000. Zootaxa 3626(4):

597-600.

Pereyra LC, Lescano JN, Leynaud GC. 2011. Breeding-

site selection by red-belly toads, Melanophryniscus

stelzneri (Anura: Bufonidae), in Sierras of Cordoba,

Argentina. Amphibia-Reptilia 32: 105-112.

Richter-Boix A, Tejedo M, Rezende EL. 2011. Evolu¬

tion and plasticity of anuran larval development in re¬

sponse to desiccation: A comparative analysis. Ecol¬

ogy and Evolution 1: 15-25.

Rose FL, Armentrout D. 1976. Adaptive strategies of

Ambystoma tigrinum Green inhabiting the Llano Es-

tacado of west Texas. Journal of Animal Ecology 45:

713-729.

Stuart S, Chanson JS, Cox NA, Young BE, Rodrigues

ASL, Fishman DL, Waller RW. 2004. Status and

trends of amphibian declines and extinctions world¬

wide. Science 306: 1,783-1,786.

Tinker PB, Ingram JSI, Struwe S. 1996. Effects of slash-

and-burn agriculture and deforestation on climate

change. Agin culture Ecosystems & Environment 58:

13-22.

Nils Behr is a master’s student studying organismic biology, evolutionary biology, and palaeobiology

at the University of Bonn, Germany. In 2016 he joined the working group of the herpetological section

of the Zoological Research Museum Alexander Koenig in Bonn, where he is currently working as a

scientific research assistant. His main focus lies on breeding amphibians to investigate their ecology

and larval development.

Dennis Rodder is Curator of Herpetology at the Zoological Research Museum Alexander Koenig, Bonn.

His scientific interests include the taxonomy, faunistics, diversity, aut-/synecology, and conservation

of amphibians and reptiles. Next to more traditional methods (morphology/anatomy, bioacoustics,

empirical field studies, and experiments), he combines genetics and natural history information with

recently developed collection based macroecological approaches (species distribution modeling,

environmental niche modeling). These techniques allow him to analyze the structure and evolution of

species’ environmental niches through space and time in a phylogenetic context as well as assessments

of species’ likely responses to anthropogenic climate change.

Amphib. Reptile Conserv.

May 2018 | Volume 12 | Number 1 | el 53

Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

12(1) [General Section]: 27-34 (el54).

Rediscovery of the rare Star Mountai ns Worm-eating

Snake, Toxicocalamus ernstmayri O’Shea etal., 2015

(Serpentes: Elapidae: Hydrophiinae) with the description

of its coloration in life

^ark O’Shea, 1 2 Brian Herlihy, 3 Blaise Paivu, 4 Fred Parker, 5 Stephen J. Richards,

and 6 Hinrich Kaiser

1 Faculty of Science and Engineering, University of Wolverhampton, West Midlands WV1 1LY, UNITED KINGDOM; West Midland Safari

Park, Bewdley, Worcestershire DY 12 ILF, UNITED KINGDOM, and Australian Venom Research Unit, University of Melbourne, Victoria 3010,

AUSTRALIA 23 Ok Tedi Mining Limited, P.O. Box 1, Tabubil, Western Province 332, PAPUA NEW GUINEA 4 / J . O. Box 5623, Townsville, Queensland

4810, AUSTRALIA 5 Herpetology* Department, South Australian Museum, North Terrace, Adelaide, South Australia 5000, AUSTRALIA 6 Department

of Biology, Victor Valley College, 18422 Bear Valley Road, Victorville, California 92395, U.S. A.; and Department of Vertebrate Zoology, National

Museum of Natural History, Smithsonian Institution, Washington, DC 20013, U.S. A.

Abstract. —Aseries of photographs of the recently described Star Mountains Worm-eating Snake, Toxicocalamus

ernstmayri O’Shea et al., 2015, taken at the 0k Tedi Mine in the Star Mountains, North Fly District, Western

Province, Papua New Guinea, represents only the second record of this poorly-known species. Toxicocalamus

ernstmayri was hitherto only known from its holotype, collected in December 1969 at the village of Wangbin

approximately 13.2 km ESE of the photo locality. The Ok Tedi snake was observed and photographed during the

day in October 2015 as it moved across a section of active mine workings, before retreating into dense montane

rainforest. This series of photographs constitutes the first sighting of this snake in 45 years and the first

sighting of a living animal, providing evidence of the species’ continued existence in an area of considerable

environmental and demographic changes brought about by human development. These images also provide

evidence of its startling coloration in life.

Keywords. Elapidae, Toxicocalamus ernstmayri , snake, Star Mountains, Western Province, Papua New Guinea

Citation: O’Shea M, Herlihy B, Paivu B, Parker F, Richards SJ, Kaiser H. 2018. Rediscovery of the rare Star Mountains Worm-eating Snake,

Toxicocalamus ernstmayri O’Shea et al., 2015 (Serpentes: Elapidae: Hydrophiinae) with the description of its coloration in life. Amphibian & Reptile

Conservation 12(1) [General Section]: 27-34 (el 54).

NoDerivatives 4.0 International License, which permits unrestricted use for non-commercial and education purposes only, in any medium, provided

the original author and the official and authorized publication sources are recognized and properly 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-

reptiie-conservation.org>.

Received: 07 November 2017; Accepted: 07 March 2018; Published: 18 June 2018

The genus Toxicocalamus Boulenger, 1896 currently

comprises fifteen taxa (fourteen species and one subspe¬

cies) of diurnal, semi-fossorial to terrestrial, secretive,

vermivorous elapid snakes that are endemic to the island

of New Guinea and nearby islands. Several species are

poorly represented in museum collections, and the most

recently described species, Toxicocalamus ernstmayri

O’Shea et al., 2015, is one of four species known only

from their holotypes, the others being T. grandis (Bou¬

lenger, 1914), T. mintoni Kraus, 2009, T. pachysomus

Kraus, 2009, and T. cratermontanus Kraus 2017. The

holotype of T. ernstmayri (Museum of Comparative Zo¬

ology, Harvard University, accession number R-145946)

is also the largest specimen so far recorded for the genus,

with a snout-vent length (SVL) of 1,100 mm, and a total

length of 1,200 mm (O’Shea et al. 2015).

The holotype of Toxicocalamus ernstmayri , an adult

female, was collected by one of us (FP) at Wangbin Village

in the Star Mountains (5°14’26.72”S, 141°15’31.92”E,

elev. 1,468 m). North Fly District, Western Province,

Papua New Guinea, on 23 December 1969. The snake

had been killed by a villager and handed to FP, a kiap x

patrolling the area. It was originally accessioned into

the museum collection as Micropechis ikaheka Lesson,

1830, due to its superficial resemblance to that taxon.

We here report on the second individual of T. ernst¬

mayri, the first seen and photographed in life. The snake

was sighted by one of us (BP) at 0750 hrs on 9 October

1 Kiap is a pidgin word derived from the German word Kapitan , which

was applied to Australian pre-independence government patrol officers.

Fred Parker served as a kiap from 1960-73, being based in Western

Province from 1968-73.

Correspondence. 1 m.oshea@wlv.ac.uk (Corresponding author); 2 brian.herlihy@bigpond.com; 3 blaise.paivu@oktedi.com;

A fred_pl@bigpond.com ; 5 Steve.richards@samuseum.sa.gov.air . 6 hinrich.kaiser@vvc.edu

Amphib. Reptile Conserv.

June 2018 | Volume 12 | Number 1 | el 54

O’Shea et al.

Fig. 1. Satellite map (derived from Google Earth) of the southern Star Mountains, North Fly District, Western Province, Papua New

Guinea, with yellow dots on the larger map indicating two localities (Wangbin and Ok Tedi Mine), approximately 13 km apart,

where Toxicocalamus ernstmayri has been recorded. The main town is Tabubil at the confluence of the Ok Tedi and Ok Mani, which

flow into the Fly River. Scale = 5 km. The inset map illustrates the location of the larger map in relationship to the rest of New

Guinea.

2015, as it crawled across an area of active mine workings

along the west wall at the Ok Tedi Mine (5°12 , 53.77”S,

141°08 , 38.57 ,, E, elev. 1,670 m) approximately 13.2 km

WNW of Wangbin, in the North Fly District where the

holotype was collected (Fig. 1). It was observed for ap¬

proximately 20 min and photographed several times.

The snake was not captured and measured, but as it

can be seen completely spanning a 747 mm tire track

(Fig. 2A) its total length is certainly >750 mm (estimated

as ca. 850 mm). It was observed and photographed as it

crossed open ground (Fig. 2B), rubble piles (Fig. 2C),

and passed underneath a stationary digger (Fig. 2D), until

it disappeared into the vegetation on the steep slope at the

top left of Fig. 3.

The snake can be identified as a member of the genus

Toxicocalamus by the presence of six supralabials and

the lack of the temporolabial scale (Fig. 4B’). The only

other terrestrial Papuan elapid genus to lack a temporo¬

labial scale is Pseudonaja. An anterior body dorsal scale

count of eight, from the vertebral scale row to the lowest

dorsal scale row, can also be discerned from the images

(Fig. 4C’, D’), indicating an anterior dorsal scale count

of 15. There does not appear to be any head scute fusion

although this is harder to discern with certainty from the

images. The patterning of this snake in life can be seen

clearly: it has a yellow body with large grey basal spots

on each dorsal scale, and a grey cap to the head. This

description agrees very closely with that given by Parker

(1982: 55) for the aberrant Micropechis ikaheka , which

would become the holotype of Toxicocalamus ernst¬

mayri:

“One snake taken at Wangbin (1500 m above sea

level) in the Star Mountains differed so much in co¬

louring from those at Kiunga and Ningerum that it

may well represent another species. It was brought

in already dead by a Wangbin villager People there

agreed with him that it was extremely rare in the area.

The head was black, the lips bright yellow. The body

scales were a deep yellow, each having a grey ante¬

rior tip. The amount of pigmentation on each scale de¬

creasedfrom the vertebral row towards the outermost

laterals, and increased evenly along the body, with the

tail darkest. There were no indications of any bars on

the body. The ventral surfaces were uniform yellow. ”

The characters observed in the photographs of the

newly observed individual are clearly diagnostic of T.

ernstmayri and allow us to make an unequivocal species

determination. The only other genus with which this

snake can be confused is Micropechis, which exhibits

a temporolabial scale (Fig. 5). Although entirely yellow

specimens of M. ikaheka are known, they are confined

to the Vogelkop Peninsula, West Papua Province,

western New Guinea; all specimens of M. ikaheka

known from PNG are strongly banded on the posterior

Amphib. Reptile Conserv.

June 2018 | Volume 12 | Number 1 | e154

Rediscovery of the rare Star Mountains Worm-eating Snake

Fig. 2. The first live individual of Toxicocalamus ernstmayri, observed and photographed in broad daylight at the Ok Tedi Mine,

North Fly District, Western Province, Papua New Guinea. (A) The individual’s serendipitous crossing of a 747 mm wide tire track

allowed an approximation of its total length as near 850 mm. (B) The snake moves in a straight line across open ground. (C) Slower

movement across a rubble pile allowed a more detailed examination of head and body scales (see Fig. 4). (D) The individual moving

under the tracks of a stationary digger. Photos by Blaise Paivu.

body. At an SVL > 750 mm total length this individual

of T. ernstmayri would appear to be a subadult, as it is

considerably shorter than the holotype (SVL 1,200 mm).

The encounter with an unusual, “golden” snake at the Ok

Tedi Mine was sufficiently noteworthy, even in Papua

New Guinea where snake encounters are commonplace,

that it was presented in the mine’s own magazine {Ok

Tedi Weng magazine, Issue 1, 2017, p. 6).

Topography

The source of the Ok Tedi 2 lies at approximately 2,900

m elevation in the central Star Mountains (Hyndman and

Menzies 1990), just north of the provincial border be¬

tween Western and Sandaun (formerly West Sepik) Prov¬

inces of PNG, and approximately 28 km east of the in¬

ternational border with Papua Province, Indonesian New

Guinea. From its source the Upper Ok Tedi flows rapidly

south through extremely rugged mountainous terrain to

2 Ok = river, in the local Wopkaimin language (Keig 2001), the river

is therefore known as the Ok Tedi, not the Ok Tedi River. In 1876 the

Italian naturalist-explorer Luigi Maria d’Albertis (1841-1901) was the

first foreigner to discover and navigate the lower reaches of the Ok

Tedi, which he named the Alice River (d’ Albertis 1879, 1880), in honor

of an acquaintance, Miss Alice Hargrave.

meet the Ok Mani, flowing in from the southern slopes of

Mount Fubilan, at an elevation of 400 m, just to the west

of Tabubil. The distance travelled from the source of the

Ok Tedi to the Ok Mani confluence is only ca. 28.5 river

kilometers (23 km in a direct line), but the river has al¬

ready lost 2,500 m in elevation. The distance from Tabu¬

bil to the confluence of the Ok Tedi with the Fly River

at d’Albertis Junction 3 is a further 170 river kilometers

(100 km in a direct line) with a further drop in elevation

to 70 m, from where the Fly meanders first southwest,

then southeast to the Gulf of Papua. The town of Kiunga

on the Fly River, (upstream by 45 river kilometers, 20

km in a direct line) east of d’Albertis Junction, lies at an

elevation of only 20 m, yet it is approximately 375 km

from the Fly delta, while the actual distance is closer to

800 river kilometers due to its meandering course across

the low-lying flood plains (Halse et al. 1996).

The Ok Tedi Mine is located on the slopes of Mount

Fubilan (2,084 m), “a copper mountain with a gold cap”

(Knox 2013), at an elevation of approximately 1,700 m.

It is approximately 12 km northwest of the nearest popu-

3 D’Albertis originally called the confluence of the Alice River (Ok

Tedi) with the Fly “Snake Junction” because he captured a python there

(d’Albertis 1880) but today it is named in his honor.

Amphib. Reptile Conserv.

June 2018 | Volume 12 | Number 1 | e154

O’Shea et al.

Fig. 3. View of an actively worked area of the Ok Tedi

Mine. The observed individual of Toxicocalamus ernstmayri

eventually disappeared into the vegetation on the slope in the

top left of the photograph. Photo by Blaise Paivu.

lation center, the town of Tabubil which was established

to support the mine, yet the mine lies over 1.2 km higher.

Tabubil, located at only 457 m elevation, is approximate¬

ly 450 km from the coast. The steepness of the southern

Star Mountains, rising by 1,200 m in elevation over only

12 km in horizontal distance, contrasts with the almost

imperceptible south-north increase in elevation (< 500 m

over 450 km) of the Trans-Fly Region as a whole.

At 1,700 m elevation, the Ok Tedi Mine is approxi¬

mately 230 m higher than Wangbin Village (1,468 m ele¬

vation), the type locality of T. ernstmayri , suggesting that

this snake is probably confined to mid-montane eleva¬

tions in the Star Mountains. It is unlikely that it occurs

as low as Tabubil (elevation < 500 m), given the com¬

plete lack of any specimens from there despite the large-

scale development and burgeoning human population

(see below). Even within its known range, this relatively

large, diurnally-active snake would seem to be rare, as

this region has been fairly thoroughly investigated by bi¬

ologists, including by one of us (SJR), yet no specimens

have been collected or reported.

The Vegetation and Climate

Ok Tedi Mine’s elevation is close to the boundary be¬

tween Lower Montane Rainforest (1,000-1,800 m el¬

evation), and Low-altitude Midmontane Rainforest

(1,800-2,200 m elevation), Zones 2 and 3 respectively of

Hyndman and Menzies (1990). Lower Montane Rainfor¬

est comprises mixed evergreen forest with a 20-30 m tall

canopy, dominated by emergent white oak ( Castanopsis

acuminatissima) at tree height of up to 40 m, whereas

Low-altitude Midmontane Rainforest is dominated by

moss-covered Myrtle (Syzygium) and Screw Palm (Pun¬

ci anus) with a 25-30 m canopy height.

Rainfall is high in the Upper Ok Tedi-Mount Fubilan

region, with as much as 10,000 mm being recorded annu¬

ally at the mine (Hearn 1995), with little seasonal varia¬

tion, the lowest rainfall averaging 433 mm in Novem¬

ber, and the highest averaging 576 mm in June (Merkel

2017). The area lies in a belt known as the “midaltitude

fringe high rainfall zone” (Hyndman and Menzies 1990),

which experiences continual heavy rain, defined as over

50 mm per week (Brookfield and Hart 1971), although

the previous figures amount to 100-140 mm of rainfall

per week. Sometimes rainfall is excessive, and on at least

four days a year there will be over 100 mm of rainfall

over a 24-hour period, and once every 1-3 years rain¬

fall will exceed 150 mm in a single day (McAlpine et

al. 1983). The Upper Ok Tedi-Mount Fubilan region is

one of the wettest places, not only on the island of New

Guinea but in the world 4 .

The almost constant rainfall, and accompanying

heavy cloud cover, results in lowered ambient tempera¬

tures. Temperatures recorded at several sites, at differ¬

ent elevations from Tabubil to Mount Fubilan, are lower

than those expected for central New Guinea (Hyndman

and Menzies 1990). Maximum daily temperatures range

from 23.0-24.7 °C, while minimums at night range from

13.8-14.6 °C (Merkel 2017). The nights above 2,200

m are even colder with lows of 6.4 °C being recorded

at Finimterr (2,300 m) (Hyndman and Menzies 1990),

which means temperatures fall by 1 °C with every 200

m increase in elevation. This combination of relatively

cold nighttime temperatures, almost continual rain, and

dense cloud cover could in part account for the diurnal

activity cycle of a relatively large snake species such as

T. ernstmayri.

Human Development

Until the late 1960s Tabubil did not exist as a settlement.

Shortly after the holotype of T. ernstmayri was collected

by FP (late 1969) a small mining camp was established

besides an airstrip (O’Shea et al. 2015: Fig. 9H) by the

Kennecott Copper Corporation, who were engaged in the

exploratory drilling on Mount Fubilan. Wangbin was a

small neighboring hamlet on the edge of Lake Wangbin

(O’Shea et al. 2015: Figs. 9A-C). During 1976-1980 the

Anglo-Australian mining company BHP Billiton negoti¬

ated with the Government of Papua New Guinea to es¬

tablish the mining town of Tabubil and they subsequently

established Ok Tedi Mining Limited to operate the gold

and copper mine.

The population of the Star Mountains Tabubil “census

division” increased by 201%, from 556 to 1,676, in the

decade 1980-1990 (Keig 2001), directly as a result of the

establishment of the Ok Tedi Mine and the development

of Tabubil. Over the same period Keig (2001) reported

that the population of Western Province increased from

64,623 to 74,834, which amounts to only a 15.8% popu-

4 The annual rainfall at the Ok Tedi Mine is close to that received by the

wettest places on Earth, listed as Mawsynram, Meghalaya (11,873 mm)

and Cherrapunji, Meghalaya (11,430 mm), both in northeastern India

(Anonymous 2017).

Amphib. Reptile Conserv.

June 2018 | Volume 12 | Number 1 | e154

Rediscovery of the rare Star Mountains Worm-eating Snake

Fig. 4. Confirming the individual’s identification as Toxicocalamus ernstmayri. (A) Close-up of the snake shown in Fig. 2C with

insets B, C, and D indicated. (B, B ) Head and neck in extreme close-up. Color coding of head scalation includes six supralabials

(orange), one anterior temporal (yellow), and two posterior temporals (blue), but no temporolabial (see Fig. 5). The head scutes

appear to comply with the colubrid-elapid nine dorsal scute arrangement (i.e., two intemasals, two prefrontals, one frontal, two

supraoculars, and two panetals; therefore lacking any head scute fusion, although this is difficult to discern from the magnified

image with accuracy. (C, C’) Based on the visible dorsal scales, the dorsal scale count on the anterior body is 15. The count is

achieved by locating the vertebral scale row and counting down to the lowest dorsal scale row (eight scales), doubling the count,

and subtracting one scale to account for the single vertebral scale row. (D, D’) The dorsal scale count at midbody, performed as

described for the previous panel, is also 15.

lation increase overall. Western Province is vast, cov¬

ering 96,218 km 2 (37,150 sq mi; Blake 1972), and it is

PNG’s largest province (by land area), and while a report

by the IUCN (1995) gave the population of the province

as 110,000, with a very low overall population density

of 1.14/km 2 , the same report provided a population of

12,000 for Tabubil. This indicates a 716% increase in

population size during the years 1990-1995, making

Tabubil the largest urban population in the province, ex¬

ceeding even the 8,490 population of Daru, the provin¬

cial capital in the south of the province. The 2011 census

(National Statistical Office of Papua New Guinea 2014)

Amphib. Reptile Conserv.

June 2018 | Volume 12 | Number 1 | e154

O’Shea et al.

Fig. 5. Distinguishing Toxicocalamus from Micropechis. (A, A’) Holotype of T. ernstmayri (MCZ R-145946) from Wangbin, Western

Province, PNG. (B, B’) Holotype of T. grandis (BMNH 1946.1.18.34) from Setakwa River, Papua Province, Indonesian New

Guinea. (C, C’) Yellow phase of Micropechis ikaheka (BMNH 1909.4.30.12) from the FakFalc Peninsula, West Papua Province,

Indonesian New Guinea. Color-coding of head scalation includes six supralabials (orange), a single anterior temporal (yellow), two

posterior temporals (blue), and a temporolabial (red). The individual we report here clearly has the same head scute arrangement

as T. ernstmayri.

provided a provincial population of 201,351 with 10,270

for Tabubil, 631 for Wangbin, and 15,142 for Dam, sug¬

gesting a reversal in the relative populations sizes of

Tabubil and Dam. Regardless of this apparent decline

the population size and development of the Tabubil area

during the last 4.5 decades has been substantial. The de¬

mographics of the Tabubil population are eclectic with

company employees from around the world. However,

the population of the Ok Tedi Mine remains relatively

small, with employees concentrated within the actual

mine compound. The surrounding midmontane rainfor¬

est remains thinly populated and under-explored.

extremely rare in the area.” That it is also a diurnal spe¬

cies, of moderately large size, and seemingly relatively

slow moving, would suggest that this species could be

more vulnerable to persecution than some other taxa. It is

therefore especially heartening that this snake was at no

time hindered or molested as it crossed the mine work¬

ings, and that it was thought interesting and newswor¬

thy enough to be photographed, the images then being

circulated to specialists for an identification, and then

finally the sighting was featured as a full-page article in

the company’s seven-page in-house publication, which

finishes with this plea to its readers:

Conservation

The incursion of roads into remote rainforest areas could

lead to the persecution and disappearance of vulnerable

and misunderstood species like snakes. Toxicocalamus

ernstmayri has always been an infrequently encoun¬

tered species, as exemplified by Parker’s (1982) com¬

ment above: “ People there agreed with him that it was

“So should yon he fortunate enough to see one of

these snakes in the wild, please observe it from a dis¬

tance and let it go on its way. They are very rare and

recorded sightings are even rarer. Like all the wild life

in our foot print we should appreciate its diversity,

this snake and perhaps there are other animals out

there are unique to this part of PNG and the world

and should be appreciated and not killed. ”

Amphib. Reptile Conserv.

June 2018 | Volume 12 | Number 1 | e154

Rediscovery of the rare Star Mountains Worm-eating Snake

Acknowledgements. —The authors would like to

thank Ok Tedi Mining Limited for granting pennission

for this specimen to be reported and for images of the

location to be published.

Literature Cited

Anonymous. 2017. Highest rainfall annually. Guinness

World Records Limited, London, England. Avail¬

able: http://www.guinnessworldrecords.com/world-

records/highest-rainfall-annually/ [Accessed: 23 Sep¬

tember 2017],

Blake DH. 1972. Western District. Pp. 1,187-1,193 In:

Encyclopedia of Papua and New Guinea. Volume

2 L-Z. Ryan R, editor. Melbourne University Press,

Melbourne, Victoria, Australia. 1,231 p.

Boulenger GA. 1896. Description of a new genus of

elapine snakes from Woodlark Island, British New

Guinea. Annals and Magazine of Natural History

18(104): 152.

Boulenger GA. 1914. An annotated list of the batrachi-

ans and reptiles collected by the British Ornitholo¬

gists’ Union Expedition and the Wollaston Expedition

in Dutch New Guinea. Transactions of the Zoological

Society of London 20(5): 247-274.

Brookfield H, Hart D. 1971. Melanesia: A Geographical

Interpretation of an Island World. Methuen, London,

United Kingdom. 464 p.

d’Albertis LM. 1879. Journeys up the Fly River and in

other parts of New Guinea. Proceedings of the Royal

Geographical Society 1(1): 4-16.

d’Albertis LM. 1880. New Guinea: What I Did and What

I Saw (2 Volumes). Sampson Low, Marston, Searle, &

Rivington, London, England. X+406 p.

Halse SA, Pearson GB, Jaensh RP, Kulmoi P, Gregory

P, Kay WR, Storey AW. 1996. Waterbirds surveys of

the Middle Fly River floodplain, Papua New Guinea.

Wildlife Research 23: 557-569.

Hearn GJ. 1995. Landslide and erosion hazard mapping

at Ok Tedi copper mine, Papua New Guinea. Quar¬

terly Journal of Engineering Geology and Hydrogeol¬

ogy 28(1): 47-60.

Hyndman DC, Menzies JI. 1990. Rain forests of the Ok

Tedi headwaters, New Guinea: An ecological analy¬

sis. Journal of Biogeography 17: 241-273.

IUCN. 1995. The Fly River Catchment, Papua New

Guinea: A Regional Environmental Assessment.

IUCN, Gland, Switzerland. X+86 p.

Keig G. 2001. Rural population growth in Papua New

Guinea between 1980 and 1990. Asia Pacific View¬

point 42(2-3): 255-268.

KnoxM. 2013. Boom: The Underground History of Aus¬

tralia, from Gold Rush to GFC. Penguin, Melbourne,

Victoria, Australia. 416 p.

Kraus F. 2009. New species of Toxicocalamus (Squa-

mata: Elapidae) from Papua New Guinea. Journal of

Herpetology 65(4): 460-467.

McAlpine JR., Keig G, Falls R. 1983. Climate of Papua

New Guinea. Australian National University Press,

Canberra, Australian Capital Territory, Australia.

Xii+200 p.

Merkel A. 2017. CLIMATE-DATA.ORG. Available:

https://en.climate-data.org/location/19240/ AM On¬

line Projects, Oedheim, Germany [Accessed: 03 July

2017],

National Statistical Office of Papua New Guinea. 2014.

2011 National Population & Housing Census: Ward

Population Profile: Southern Region. National Statis¬

tical Office, Waigani, National Capital District, Papua

New Guinea. 33 p.

O’Shea M, Parker F, Kaiser H. 2015. A new species of

New Guinea wonn-eating snake, genus Toxicocala¬

mus (Serpentes: Elapidae), from the Star Mountains

of Western Province, Papua New Guinea, with a re¬

vised dichotomous key to the genus. Bulletin of the

Museum of Comparative Zoology 161(6): 241-264.

Parker F. 1982. Snakes of Western Province. Division of

Wildlife, Department of Lands and Environment, Port

Moresby, Papua New Guinea. 78 p.

I Mark O’Shea is a British herpetologist with a specialist interest in the snakes of New Guinea. He wrote A

I Guide to the Snakes of Papua New Guinea (1996) and is currently working on the second edition, expanded to

encompass the entire New Guinea region, and he is also the author of four other books. Since 1986 he has made ten

expeditions to New Guinea to conduct herpetological fieldwork, capture medically important elapids for snakebite

research, or made films for Animal Planet or the BBC. He has worked in PNG for a variety of organizations

from Operation Raleigh to Oxford University’s Department of Clinical Medicine, Liverpool School of Tropical

Medicine, and the Australian Venom Research Unit, University of Melbourne. O’Shea has considerable field

experience in other countries in Asia, Africa, and South America, and has been engaged in fieldwork projects since

the 1980s. He presented four seasons of the herpetological television series O’Shea’s Big Adventure, for Animal

Planet and Discovery Channel, and has made films with other companies and broadcasters. Mark was awarded

the Millennium Award for Services to Zoology by the British Chapter of the Explorers’ Club in 2000, and in 2001

was awarded an honorary Doctor of Sciences degree by his alma mater, the University of Wolverhampton, for

services to herpetology. He is now Professor of Herpetology at the University of Wolverhampton and teaches the

“Animal Behaviour and Wildlife Conservation and Evolution” and “Origins of Life” courses at the University. He

also holds the post as Consultant Curator of Reptiles at West Midland Safari Park, in the United Kingdom. O’Shea

and Kaiser (below) are the leaders of the first comprehensive survey of the herpetofauna of Timor-Leste, Asia’s

newest country. With ten phases of the project completed since 2009, the team has recorded upwards of 70 species,

with more than twenty of these new to science. O’Shea, Kaiser, and Fred Parker (also below) are the describers of

Toxicocalamus emstmayri , the subject species of this paper.

Amphib. Reptile Conserv.

June 2018 | Volume 12 | Number 1 | e154

O’Shea et al.

Brian Herlihy is a New Zealander, and a Senior Safety Advisor for Ok Tedi Mines Limited (OTML). He holds

an MBA in Technology Management from Deakin University/APESMA (Association of Professional Engineers,

Scientists and Managers, Australia). He has worked for OTML since 2016.

Blaise Paivu is a Papua New Guinean citizen, and a Senior Mining Engineer for Ok Tedi Mines Limited (OTML).

He has been employed by OTML from 1995 to 2010, and from 2013 until the present. He holds a Bachelor in

Mining Engineering from University of Technology, Lae, Papua New Guinea.

Fred Parker was born in India and migrated to Australia in 1949. While working at the Healesville Sanctuary

in the late 1950s he met the herpetologist Charles Tanner and became interested in herpetology. From 1960

until 1973 he worked as a kiap on Bougainville, in the Central Highlands, and Western District, Papua New

Guinea. Derived from the German word kapitan , it is the tokpisin name for a Government Patrol Officer, usually

an Australian, in Pre-Independence Papua New Guinea. During this time Parker collected many herpetological

specimens for Ernest Williams, at the Museum of Comparative Zoology (MCZ), Harvard, and Richard Zweifel, at

the American Museum of Natural History (AMNH), New York. He also collected a large number of death adders

for venom research and antivenom production by Tanner at the Commonwealth Serum Laboratories (CSL),

Melbourne, Australia. From 1973 he worked for the Wildlife Division in Port Moresby, on projects as diverse as

crocodiles and butterflies, and rose to the position of Head of the Division, before returning to Australia in 1979.

He has authored and coauthored numerous papers on the herpetofauna of PNG, including the original description

of Toxicocalamus ernstmayri. Two frogs ( Cornufer parkeri and Xenorhina parkerorum ), one turtle ( Chelodina

parkeri ), a skink ( Tribolonotusparkeri ), and three snakes ( Bothrochilus fredparkeri , Gerrhopilusfredparkeri , and

Tropidonophis parkeri ) are named in his honor.

Stephen J. Richards is an Honorary Research Associate at the South Australian Museum in Adelaide, Australia

with a special interest in the herpetofauna of New Guinea. Since 1991 he has made approximately 50 expeditions

to New Guinea to conduct herpetological fieldwork, and he has co-authored more than 130 publications about

frogs and reptiles of that region, including the formal descriptions of nearly 100 new species discovered during

these expeditions. He has published three field guides to frogs of local regions in New Guinea and the Solomon

Islands. Stephen is the Regional Chair for Melanesia of the IUCN’s Amphibian Specialist Group and a member of

the Papua New Guinea Government’s Biodiversity Expert Group. Richards has two frogs ( Hylophorbus richardsi

and Litoria richardsi) and a skink ( Ctyptoblepharus richardsi) named in his honor.

Hinrich Kaiser is a German-American herpetologist and educator with a research focus on biodiversity and

conservation of tropical environments. A passion for scuba diving with experiences in the arctic and the tropics

led Hinrich to study marine biology at McGill University and the University of Victoria in Canada. After an

inspiring semester learning about amphibians and reptiles in David Green’s herpetology class in the Redpath

Museum, Kaiser found his true calling and earned his Ph D. at McGill with a dissertation on the systematics and

biogeography of Lesser Antillean frogs. After a Boehringer Ingelheim postdoctoral fellowship at the University

of Wurzburg, Germany, he spent five years as Professor of Biology at La Sierra University, Riverside, California,

USA, before accepting his current position in the Department of Biology at Victor Valley College in Victorville,

California, USA. Kaiser holds an appointment as Research Associate with the United States National Museum

of Natural History, Smithsonian Institution, Washington, D.C., USA. He currently serves as an Editor-in-Chief

of Herpetology Notes , but his interests in international affairs and music also led him to memberships on the

International Advisory Board of the Foundation for Post-Conflict Development, New York, and on the Advisory

Council of the Baltimore Symphony Youth Orchestras. Kaiser serves as a member of the Executive Committee

of the World Congress of Herpetology. His most recent publications have focused on the herpetofauna of Timor-

Leste and nearby areas of Wallacea, as well as on the defense of herpetological taxonomy against taxonomic

vandalism. He was also a coauthor on the original description of Toxicocalamus ernstmayri. His educational

specialty is to expose community college students to biological, cultural, and historical experiences overseas,

including canopy walks in Brunei, cooking classes in Bah, tracking Komodo dragons on Rinca Island, homestays

in Cuba, and surveying Pacific atolls.

Amphib. Reptile Conserv.

June 2018 | Volume 12 | Number 1 | el 54

Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

12(1) [General Section]: 35-48 (el55).

Amphibians and reptiles of Parsa National Park, Nepal

^antosh Bhattarai, 12 Chiranjibi Prasad Pokheral, ^abu Ram Lamichhane, 3 Uba Raj Regmi,

3 Ashok Kumar Ram, and 4 Naresh Subedi

1 National Trust for Nature Conservation - Biodiversity Conservation Center, Ratnanagar-6, Sauraha, Chitwan-44204, NEPAL 2 National Trust for

Nature Conseryation-Central Zoo, Jawalakhel, Lalitpur, NEPAL 3 Department of National Parks and Wildlife Conservation, Parsa National Park,

NEPAL 4 National Trust for Nature Conservation-Khumaltar, Lalitpur, NEPAL

Abstract. —We report the results of a herpetofaunal inventory between July, 2014 and March, 2017 of Parsa

National Park that detected 51 herpetofaunal species. Three amphibians (Microhyla nilphamariensis,

Sphaerotheca breviceps, and Uperodon taprobanicus), two Gecko species (Hemidactylus flaviviridis and

H. frenatus), one Agamid (Sitana fusca), two Skinks (Eutropis carinata and Sphenomorphus maculatus), 13

snakes ( Ahaetulla nasuta, Bungarus lividus, Coelognathus helena, Coelognathus radiatus, Chrysopelea ornata,

Dendrelaphis tristis, Lycodon aulicus, Lycodon jara, Oligodon arnensis, Psammodynastes pulverulentus, Ptyas

mucosa, Rhabdophis subminiatus, and Trimeresurus albolabris), and one crocodile ( Crocodylus palustris) are

new records to Parsa National Park. This paper aims to highlight the understanding of amphibians and reptiles

of Parsa National Park and will be a reference for herpetofaunal management in the park.

Keywords. Herpetofauna, biodiversity, conservation, protected area, Terai-Arc Landscape, new records

Citation: Bhattarai S, Pokheral CP, Lamichhane BR, Regmi UR, Ram AK, Subedi N. 2018. Amphibians and reptiles of Parsa National Park, Nepal.

Amphibian & Reptile Conservation 12(1) [General Section]: 35-48 (el 55).

NoDerivatives 4.0 International License, which permits unrestricted use for non-commercial and education purposes only, in any medium, provided

the original author and the official and authorized publication sources are recognized and properly credited. The official and authorized publication

credit sources, which will be duly enforced, are as follows: official journal title Amphibian & Reptile Conservation ; official journal website <amphibian-

reptile-conservation.org>.

Received: 23 January 2018; Accepted: 20 February 2018; Published: 17 July 2018

Introduction

Globally, amphibians and reptiles are among the least

studied vertebrate taxa (Fazey et al. 2005). The amphib¬

ians and reptiles of Nepal have a wide range of both ver¬

tical and horizontal distribution. However, the field of

herpetology has always received less priority than other

vertebrates (Bhattarai et al. 2017). Among herpetofaunal

species, only the gharial ( Govialis gangeticus ) subjected

to long term monitoring and conservation efforts (Acha-

rya et al. 2017). Information on species richness and

distribution of amphibians and reptiles in management

plans of many Protected Areas of Nepal including Parsa

National Park (PNP) are poorly documented. Past stud¬

ies by Schleich and Kastle (2002) and Shah and Tiwari

(2004) recorded 37 species from the PNP and lack de¬

tailed locality information. Since then, several taxonomic

revisions of the species have been done. In addition to

this, Kastle et al. (2013) listed eight species of herpeto¬

fauna which underestimates the species richness of the

PNP. Here, we provide the comprehensive checklist on

species richness with natural history data to highlight un¬

derstanding of the amphibian and reptile fauna of Parsa

National Park.

Study Area

Parsa National Park (PNP), the youngest National Park

in the country, was established in 1984 as Wildlife Re¬

serve and upgraded to National Park in 2017. It is geo¬

graphically located within 27° 15’ to 27°33’N, 84°4r to

84°58 , E. The unique sub-tropical dry ecosystem was

established to protect habitat mainly for the resident

population of wild Asian elephant (Elephas maximus).

However, it also provides a habitat for migratory wild¬

life species and a dispersal site for spill-over popula¬

tion of Chitwan National Park to which it is connected

at its western boundary and Valmaki Tiger Reserve of

India to the South. Examples are the Asian one-homed

Rhinoceros (Rhinoceros unicornis ), Royal Bengal tiger

(Panthera tigris) and Gaur (Bos gaums). Understanding

the potential to conserve many charismatic species, the

Government of Nepal extended the area of the PNP in

2015 and the current area is 627 km 2 (Fig. 1). Besides its

biodiversity conservation value, the PNP is also serving

the vital needs of the large human population living south

of the park by conserving water sources in the Siwalik

hill and has reduced the soil erosion in the hill. The PNP

includes mainly sub-tropical forests of the Siwalik and

Correspondence. 1 santosh.bhattarai@hotmail.com (Corresponding author)

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 55

Bhattarai et al.

84°45'E

84°50'E

84°55'E

85°0'E

85°5'E

85°10'E

Fig. 1. Study location, Parsa National Park.

Bhabar physiographic regions of Parsa, Makwanpur and

Bara districts. The vegetation is mainly dominated by Sal

(,Shorea robusta ) forest, and riverbeds and flood plains

are covered by Saccharum spontaneum and Imperata cy-

lindrica (Chhetri 2003). Although the PNP is connected

with Chitwan National Park (Nepal) and Valmiki Tiger

Reserve (India), very little information on species rich¬

ness and diversity is available (Lamichhane et al. 2017).

We concentrated our search effort near permanent water

bodies and artificially created ponds inside the park. Field

investigations were conducted at Rambhori-Bhata, Halk-

horia Daha, Amlekhganj-Hattisar, Adhabhar, Ghodema-

san, Mahadev Khola, Gaduwa-line, and Nirmalbasti,

Ramaul i-Pratappur.

Field Methods

We conducted surveys in both the dry and wet seasons.

We used the visual encounter survey protocol (Heyer

et al. 1994) and active searches from 10-20 July, 2014,

15-27 March, 2015, 18-21 June, 2015, 04-10 February,

2016, 17-25 July, 2016, and 03-09 March, 2017. We

covered all major sites within the park. Our search effort

focused on recording the diverse herpetological commu¬

nity as efficiently as possible. On each expedition, we

spent three hours of intensive search combined with op¬

portunistic records. During the survey, on detection of an

animal, we recorded the location, date, time, and micro¬

habitat. We did not use dogs or chemicals or any auditory

cues for species detection. However, we included op¬

portunistic records of various herpetofauna encountered

elsewhere within the PNP in our results. Photographs of

detected animals were taken whenever possible and used

as visual evidence for verifying species identifications.

We used keys described in Smith (1935), Schleich and

Kastle (2002), and Shah and Tiwari (2004) for identifica¬

tion. We followed Frost (2017) for nomenclature of am¬

phibians and Uetz et al. (2017) for reptiles.

Results

We recorded 12 species of amphibians in eight genera

and four families of anurans (Table 1), and 39 species of

reptiles which consisted of five species of skinks, three

species of Geckonids, two species of Agamids, two spe¬

cies of monitor lizards, 25 snake species, and one tortoise

and crocodile each (Table 1). We recorded 22 additional

species in the area which accounted for 51 species of the

herpetofauna in the PNP. These additional species consist

of three species of anurans, two species of gecko, two

species of skinks, 13 snake species, and one crocodile

species.

Species Accounts

AMPHIBIANS

Bufonidae (Gray 1825)

Duttaphrynus melanostictus (Schneider 1799): Recorded

from Amlekhganj-Hattisar, Adhabhar, Rambhori-Bhata,

Halkhoria Daha, Nirmalbasti, and Ramauli-Pratapur.

This was commonly seen in and around human settle¬

ments during monsoon. Road-killed individuals of this

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | e155

Amphibians and Reptiles of Parsa National Park, Nepal

Table 1. Amphibians and Reptiles of Parsa National Park, Nepal. An asterisk (*) denotes new records to the area.

S.N. Species IUCN Status

AMPHIBIANS

Bufonidae Gray, 1825

1. Duttaplvynus melanostictus (Schneider 1799) LC

2. D. stomaticus (Liitken 1864) LC

Dicroglossidae Anderson, 1871

3. Euphlyctis cyanophlyctis (Schneider 1799) LC

4. Fejarvarya syhadrensis (Annandale 1919) LC

5. Fejarvaiya teraiensis ( Dubois 1984) LC

6. Hoplobatrachus crassus (Jerdon 1853) LC

7. Hoplobatrachus tigerinus (Daudin 1802) LC

8. * Sphaerotheca breviceps (Schneider 1799) LC

Microhylidae Gunther, 1858

9. *Microhyla cf. nilphamariensis (Howlader, Nair, Gopalan, and Merila 2015) LC

10. Uperodon globulosus (Gunther 1864) LC

11. * Uperodon taprobanicus (Parker 1934) LC

Rhacophoridae Hoffman, 1932 (1858)

12. Polypedates macn/atiis (Gray 1830) LC

REPTILES

Gekkonidae Gray, 1825

13. Hemidactylus cf. brookii Gray, 1845 NA

14. * Hemidactylus flaviviridis Rtippell, 1835 LC

15. * Hemidactylus frenatus Dumeril and Bibron, 1836 LC

Agamidae Gray, 1827

16. Ca/oles versicolor (Daudin 1802) NA

17. * Sitana fusca Schleich and Kastle, 1998 NA

Scincidae Gray, 1825

18. * Eutropis carinata (Schneider 1801) LC

19. Eutropis dissimilis (Hallowell 1857) NA

20. Eutropis macularia (Blyth 1853) NA

21. Lygosoma punctata (Gmelin 1799) NA

22. *Sphenomorphus maculalns (Blyth 1853) NA

Varanidae Merrem, 1820

23. Varanns bengalensis (Daudin 1802) LC

24. Varanus flavescens (Hardwicke and Gray 1827) NA

Typhlopidae Merrem, 1820

25. hidotyphlops braminus (Daudin 1803) NA

Boidae Gray, 1825

26. Eryx conicus (Schneider 1801) NA

Pythonidae Fitzinger, 1826

27. Python bivitlaliis Kuhl. 1820 VU

Colubridae Oppel, 1811

28. *AhaetuIIa nasuta (Bonnaterre 1790) NA

29. Boiga tiigonata (Schneider 1802) LC

30. *CoeIognathus helenam (Daudin 1803) NA

31. *Coelognathus radiatus ( Boie 1827) LC

32. *ChiysopeIea ornata (Shaw 1802) NA

33. *DendreIaphis tristis (Daudin 1803) NA

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 55

Bhattarai et al.

Table 1. Amphibians and Reptiles of Parsa National Park, Nepal. An asterisk (*) denotes new records to the area.

S.N.

Species

IUCN Status

Colubridae Oppel, 1811

34.

*Lycodon aulicus (Linnaeus 1758)

35.

*Lycodonjara (Shaw 1802)

36.

* Ol igodon amen sis (Shaw 1802)

37.

*Psammodynastes pulverulentus (Boie 1827)

38.

*Ptyas mucosa (Linnaeus 1758)

39.

Sibynophis Sagittarius (Cantor 1839)

Elapidae F. Boie, 1827

40.

Bungarus caeruleus (Schneider 1801)

41.

Bungarus fasciatus (Schneider 1801)

42.

* Bungarus lividus Cantor, 1839

43.

Naja naja (Linnaeus 1758)

44.

Ophiophagus hannah (Cantor 1836)

Natricidae Bonaparte, 1838

45.

Amphiesma stolatum (Linnaeus 1758)

46.

Xenochropis piscator (Schneider 1799)

47.

*Rhabdophis subminiatus (Schlegel 1837)

Viperidae Oppel, 1811

48.

Daboia russelii (Shaw and Nodder 1797)

49.

* Trimeresurus albolabris Gray, 1842

Testudinidae Batsch, 1788

50.

Indotestudo el on gat a (Blyth 1854)

Crocodylidae Cuvier, 1806

51.

* Crocody/us palustris Lesson, 1831

species were frequently observed in the east-west nation¬

al highway between Amlekhgunj and Adhabhar segment.

This is the most common bufonid in Terai, Nepal (Fig.

2 ).

Fig. 2. Duttaphrymis melanostictus. Photograph by Kapil

Pokharel/NTNC-BCC.

Duttaphrymis stomaticus (Lutken 1864): This was fre¬

quently encountered at NTNC-Parsa Conservation Pro¬

gram Office complex, Hattisar, Amlekhganj, Adhabhar,

Ramauli-Pratappur, Bhata, and Nirmalbasti (Fig. 3). The

individuals can be distinguished from D. melanostictus

by absence of canthal black ridge and smaller tympanum.

Fig. 3. Duttaphrymis stomaticus. Photograph by Santosh Bhat¬

tarai.

Dicroglossidae (Anderson 1871)

Euphlyctis cyanophlyctis (Schneider 1799): The most

common frog of Terai Nepal within and outside protected

areas commonly encountered in water pools (Fig. 4).

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | e155

Amphibians and Reptiles of Parsa National Park, Nepal

Fig. 4. Euphlyctis cyanophlyctis. Photograph by Santosh Bhat-

tarai.

Fejarvarya syhadrensis (Annandale 1919): The indi¬

viduals we recorded had no mid dorsal line with reddish

orange patches which is characteristic of this species

(Schleich and Kastle 2002). We recorded this species

along marshy lands in the ponds inside the park.

Fejervarya teraiensis (Dubois 1984): The calling males

were recorded at puddles in Amlekhgunj, Adhabar, and

Bhata. The individuals had a cream colored mid dorsal

line with dorsolateral fold. According to Schleich and

Kastle (2002), this species is well distributed in the entire

Terai from 71 to 400 m.

Hoplobatrachus crassas (Jerdon 1853): We found an in¬

dividual of this species at an anny post in Gaduwaline

inside the park. Shah and Tiwari (2004) also recorded

this species from Parsa.

Hoplobatrachus tigerinus (Daudin 1802): This is the

largest frog of Terai region. Yellow colored breeding

males were frequently observed in puddles during mon¬

soon (Fig. 5).

Fig. 5. Hoplobatrachus tigerinus. Photograph by Santosh

Bhattarai.

Sphaerotheca breviceps (Schneider 1799): Almost toad¬

like, stocky with distinct supratympanal fold. We found

some specimens in Halkhoria Daha and Amlekhgunj-

Hattisar area during June and July and calling males were

also observed. This is the first record to Parsa National

Park.

Fig. 6. Sphaerotheca breviceps. Photograph by Santosh Bhat¬

tarai.

Microhylidae (Gunther 1843,1858)

Microhyla cf. nilphamariensis (Howlader, Nair, Gopa-

lan, and Merila 2015): The type locality of this frog is

Koya Golahut, Saidpur, Nilphamari, Bangladesh. Re¬

cently, Khatiwada et al. (2017) recorded it from central

and eastern Nepal and proposed the Chitwan population

to be M. nilphamarariensis based on molecular and call

records. We believe the Parsa population to be M. nil¬

phamariensis (Fig. 7). However, only detailed molecular

study will resolve its taxonomy.

Fig. 7. Microhyla cf. nilphamariensis. Photograph by Santosh

Bhattarai.

Uperodon globulosus (Gunther 1864): This bulky globu¬

lar frog is frequently seen during monsoon, when calling

males were seen during the night in Bhata area. Shah and

Tiwari (2004) also reported the occurrence of this species

from Parsa National Park (Fig. 8).

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 55

Bhattarai et al.

Fig. 8. Uperodon globulosus. Photograph by Santosh Bhatta¬

rai.

Fig. 10. Polypedates maculatus. Photograph by Santosh Bhat¬

tarai.

Uperodon taprobanicus (Parker 1934): This frog is gray¬

ish black, and individuals have reddish-orange dorsolat¬

eral irregular bands. Individuals with a mid-dorsal line

from snout to vent and with mid-dorsal line were record¬

ed (Fig. 9). Males have folded black vocal sacs and were

observed in amplexus. According to Schleich and Kastle

(2002), this species is distributed from central to eastern

Nepal between 100 and 300 m elevation. Bhattarai et al.

(2017a) also recorded this species from Beeshazar and

associated lakes, a Ramsar site.

Fig. 9. Uperodon taprobanicus. Photograph by Santosh Bhat¬

tarai.

Rhacophoridae (Hoffman 1932)

Polypedates maculatus (Gray 1830): Calling males were

frequently observed at NTNC-Parsa Conservation Pro¬

gram office complex during the monsoon. This species

was frequently observed on the office window and in the

bathroom (Fig. 10).

REPTILES

Gekkonidae (Gray 1825)

Hemidactylus cf. brookii (Gray 1845): Individuals with

strongly keeled dorsal tubercles and tails with spines

were recorded. Schleich and Kastle (2002) recorded H.

brookii on buildings in Chitwan National Park. However,

we recorded them in dead logs inside the park in Parsa

National Park (Fig. 11). This species is regarded as a spe¬

cies complex and has been proposed for detailed molecu¬

lar studies to solve taxonomy of Nepalese populations

(Rosier and Glaw 2010; Kathriner et al. 2014).

\ I

Fig. 11. Hemidactylus brookii. Photograph by Santosh Bhat¬

tarai.

Hemidactylus flaviviridis (Ruppell 1835): This is a com¬

mon house gecko in the study area. Frequently seen at

houses, park guard posts and army posts, and the temple

inside the park, as well as villages nearby the park. This

is the first record from the Parsa National Park.

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 55

Amphibians and Reptiles of Parsa National Park, Nepal

Hemidactylus frenatus (Dumeril and Bibron 1836): We

reported two individuals of this species, photographed

at Bhata-Hattisar and Gaduwa. This is the first record of

this species from Parsa National Park.

Agamidae (Gray 1827)

Calotes versicolor (Daudin 1802): This is the most

common diurnal agamid distributed from below 100 m

to 3,200 m in Nepal (Schleich and Kastle 2002). The

species was frequently observed in and out of the park

boundary (Fig. 12).

Fig. 12. Calotes versicolor. Photograph by Santosh Bhattarai.

Sitana fusca (Schleich and Kastle 1998): This species

was described from Bardibas, Mahottari district, Nepal

ca. 100 km east of Parsa National Park. This is the first

record of Sitana from Parsa National Park. This species

was frequently observed at NTNC-Parsa Conservation

Program office complex, Bhedaha Khola, and Darau

Khola. In June 2016, a gravid female was observed nest¬

ing in the office complex, and two hatchlings of same

species were encountered in August 2016 (Fig. 13).

Fig. 13. Nesting female of Sitana fusca. Photograph by Santosh

Bhattarai.

Scincidae (Gray 1825)

Eutropis carinata (Schneider 1801): Commonly ob¬

served inside the park basking in open grassland and on

rocky substrates. Observed at Kamini Daha, Bhata, Ma-

hadev Khola, Halkhoria Daha, Ghode Masan, Ramauli-

Pratappur, Sikaribasb Bhedaha Khola, and Darau Khola.

This is one of the most commonly observed skinks in

Nepal. However, earlier researchers did not report it from

Parsa National Park (Fig. 14).

Fig. 14. Eutropis carinata. Photograph by Kapil Pokharel/

NTNC-BCC.

Eutropis dissimilis (Hallowell 1857): Recorded from

Amlekhgunj-Hattisar, Sikaribaas basking during winter.

This species is rarely seen compared to its congenerics in

Parsa National Park (Fig. 15).

Fig. 15. Eutropis dissimillis. Photograph by Kapil Pokharel/

NTNC-BCC.

Eutropis macularia (Blyth 1853): Observed from Ka¬

mini Daha, Amlekhgunj-Hattisar, Bhata, Nirmalbasti,

Ramauli Pratappur, Mahadev Khola, and Ghode Masan

(Fig. 16).

Fig. 16. Eutropis macularia. Photograph by Binod Darai/

NTNC-BCC.

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 55

Bhattarai et al.

Lygosomapunctata (Gmelin 1799): Observed from Bha-

ta, Adhabhar, Sikaribaas, and Shitalpur (Fig. 17).

Fig. 17. Lygosoma punctata. Photograph by Binod Darai/

NTNC-BCC.

Sphenomorphus maculatus (Blyth 1853): This species

was frequently observed in the foothills of Siwaliks in¬

side the park and found basking on the rocks of dry river

beds (Fig. 18). This is the first record for Parsa National

Park.

Fig. 18. Sphenomorphus maculatus. Photograph by Santosh

Bhattarai.

Varanidae (Merrem 1820)

Varanus bengalensis (Daudin 1802): Individuals were

observed at Kamini Daha, Masine area, Bhata, Adhab-

har-PNP office, Bhedaha Khola, Shitalpur, and Ramauli-

Pratapur. They were frequently observed at human habi¬

tations at Amlekhgunj, and one adult was rescued from

the Nepal Oil Corporation’s office complex. The species

is frequently seen in holes of the Sal ( Shore a robusta )

trees lying on the ground and on standing trees (Fig. 19).

Fig. 19. Varanus bengalensis. Photograph by Kapil Pokharel/

NTNC-BCC.

Varanus Jiavescens (Hardwicke and Gray 1827): This

species was frequently encountered in the buffer zone

around the PNP and in agricultural lands outside the

park boundary. It is a legally protected varanid of Nepal

which has been accorded the highest degree of protection

in Schedule-I under the National Parks and Wildlife Con¬

servation Act, 1973. The species is facing severe threat

due to illegal hunting for its flesh and skin. The skin of

varanids is used for making musical instruments by local

communities.

Typhlopidae (Merrem 1820)

Indotyphlops braminus (Daudin, 1803): The species was

observed from Kamini Daha living inside leaf litter.

Boidae (Gray 1825)

Eryx conicus (Schneider 1801): This species was en¬

countered at Amlekhgunj-Hattisar (Fig. 20).

Fig. 20. Eryx conicus. Photograph by Kapil Pokharel/NTNC-

BCC.

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 55

Amphibians and Reptiles of Parsa National Park, Nepal

Pythonidae (Fitzinger 1826)

Python bivittatus (Kuhl 1820): The python is the largest

snake species in Nepal and it is distributed from Nep¬

alese Terai up to 2,800 m elevation in Nepal (Bhattarai

et al. 2017). In the PNP, the species was observed from

Bhata, Amlekhgunj-Hattisar, Halkhoria Daha, and Ra-

mauli Pratapur (Fig. 21). The PNP has dry sub-tropical

habitat and gets incidental fire. One injured python was

found with wounds inside the park at Kamini Daha.

Fig. 21. Python bivittatus. Photograph by Om P. Chaudhaiy/

NTNC-BCC.

Colubridae (Oppel 1811)

Ahaetulla nasuta (Bonnaterre 1790): An individual of

this species was observed at Mahadev Khola basking

on grasses and flew to the bush when approached. An¬

other individual was observed at Shitalpur on a Mallotus

philippensis tree approximately 3.5 m from ground level.

We report this species for the first time from the park.

Fig. 22. Boiga trigonata. Photograph by Kapil Pokharel/

NTNC-BCC.

Chrysopelea ornata (Shaw 1802): A juvenile individual

was observed at Shikaribas Khola, and a dead specimen

was found at Amlekhgunj-Hattisar (Fig. 23). This is the

first record from Parsa National Park.

Fig. 23. Chrysopelea ornata. Photograph by Kapil Pokharel/

NTNC-BCC

Dendrelaphis tristis (Daudin 1803): The basking indi¬

viduals were encountered at Amlekhgunj-Hattisar, Bha-

ta-Hattisar, and Ghodemasan (Fig. 24). This is the first

record from Parsa National Park.

Boiga trigonata (Schneider 1802): Many killed speci¬

mens were found in the buffer villages and highway be¬

tween Amlekhgunj and Pathlaiya section of the National

Park (Fig. 22).

Coelognathns helena (Daudin 1803): Observed from

Amlekhgunj-Hattisar, Adhabhar-PNP office complex,

and Ramauli Pratapur. This is the first record from Parsa

National Park.

Coelognathns radiatus (Boie 1827): Dead specimens

were found near human habitation, and an individual was

recorded at Kamini Daha. In May and June, the species

is frequently observed in buffer villages of the park, and

people kill the snakes when they encounter them.

Fig. 24. Dendrelaphis tristis. Photograph by Om P. Chaudhaiy/

NTNC-BCC

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | e155

Bhattarai et al.

Lycodon aulicus (Linnaeus 1758): Observed at NTNC-

Parsa Conservation Program Office complex, and dead

individuals were found at Amlekhgunj-Hattisar. A bask¬

ing individual was frequently observed in a crevice of

a cemented water tank (Fig. 25). This is the first record

from Parsa National Park.

Fig. 25. Lycodon aulicus. Photograph by Santosh Bhattarai.

Lycodon jar a (Shaw 1802): Observed at Amlekhgunj-

Hattisar. According to Schleich and Kastle (2002), it is

a rarely found species from Terai Nepal. However, there

are published reports of it in bordering states of India as

well. This is the first record from Parsa National Park

(Fig. 26).

r . J HIM P 'J _• ‘-V ’Jaw. v V

Fig. 26. Lycodon jar a. Photograph by Santosh Bhattarai.

Oligodon arnensis (Shaw 1802): Observed from Amle¬

khgunj-Hattisar and NTNC-Parsa Conservation Office

Complex (Fig. 27). This species is also frequently ob¬

served in Chitwan National Park.

Fig. 27. Oligodon arnensis. Photograph by Kapil Pokharel/

NTNC-BCC.

Psammodynastes pulvernlentus (Boie 1827): According

to Schleich and Kastle (2002), the records of the species

were from Butwal, western Nepal, and Khotang, Uday-

pur, and Ilam from eastern Nepal. Recently, Bhattarai et

al. (2017) reported it from Ratomate-Harda Khola, Chit-

wan National Park. Later the species was also observed

at Triveni area of Chitwan National Park. In the PNP, the

species was observed at Ghodemasan area, being the first

record from the PNP (Fig. 28).

Fig. 28. Psammodynastes pulvernlentus. Photograph by Tirtha

Lama/NTNC-BCC, photograph taken at Triveni, Chitwan Na¬

tional Park.

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 55

Amphibians and Reptiles of Parsa National Park, Nepal

Ptyas mucosa (Linnaeus 1758): Animals in combat were

observed on 7 June, 2016. A road-killed specimen in the

segment between Amlekhgunj and Adhabhar was record¬

ed. Individuals were frequently observed at NTNC-Parsa

Conservation Office complex (Fig. 29). This report is the

first record for Parsa National Park.

Fig. 29. Ptyas mucosa. Photograph by Santosh Bhattarai.

Sibynophis Sagittarius (Cantor 1839): A specimen was

found at Ghodemasan area basking on a riverbed (Fig.

30).

Fig. 30. Sibynophis Sagittarius. Photograph by Kapil Pokharel.

Elapidae (F. Boie 1827)

Bungarus caeruleus (Schneider 1801): Specimens ob¬

served at Amlekhgunj-Hattisar. Killed specimens were

found near human habitation (Fig. 31).

Fig. 31. Bungarus caeruleus. Photograph by Kapil Pokharel/

NTNC-BCC.

Bungarus fasciatus (Schneider 1801): One individual

was found crawling inside Amlekhgunj-Hattisar in July

2016.

Bungarus lividus (Cantor 1839): An individual was ob¬

served at Bhata-Hattisar on forest trail towards Bhata-

temple. The second individual was found killed in Amle¬

khgunj. This is the first record from Parsa National Park.

Naja naja (Linnaeus 1758): An individual was found

basking in the riverbed of Bhedah Khola. Two individu¬

als were found killed at human habitation at Amlekhgunj

(Fig. 32).

Fig. 32. Naja naja. Photograph by Kapil Pokharel/NTNC-BCC.

Ophiophagus hannah (Cantor 1836): A dead specimen

was recorded at Amlekhgunj-Hattisar. Another individ¬

ual was observed at Shitalpur camp in November 2016.

(Fig. 33).

Fig. 33. Ophiophagus hannah. Photograph by Kapil Pokharel/

NTNC-BCC

Natricidae (Bonaparte 1838)

Amphiesma stolatum (Linnaeus 1758): Frequently ob¬

served at Amlekhgunj-Hattisar, Bhata-Hattisar, and Ad-

habhar-PNP office complex. An individual was observed

feeding on Duttaphrynus melanostictus at NTNC-Parsa

Conservation Office complex. Road kills observed in the

segment between Amlekhgunj and Adhabhar (Fig. 34).

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 55

Bhattarai et al.

Fig. 34. Amphiesma stolatum. Photograph by Kapil Pokharel/

NTNC-BCC.

Xenochrophis piscator (Schneider 1799): The species

was frequently observed in human habitation and a speci¬

men was seen in the Bhata wetland (Fig. 35).

Fig. 35. Xenochropis piscator. Photograph by Kapil Pokharel/

NTNC-BCC.

Rhabdophis subminiatus (Schlegel 1837): Record of

this species was previously not reported from the PNR

Schleich and Kastle (2002) reported it from the Chitwan

National Park. The specimen was recorded at Ghodema-

san area basking on a rock (Fig. 36) in November 2016.

Fig. 36. Rhabdophis subminiatus. Photograph by Dip Prasad

Chaudhary/NTNC-BCC.

Viperidae (Oppel 1811)

Daboia russelii (Shaw and Nodder 1797): A single indi¬

vidual was observed from Bhata on the way to Rambhori

grassland. The individual was basking near a gabion wall

(Fig. 37).

Fig. 37. Daboia russelii. Photograph by San tosh Bhattarai.

Trimeresurus albolabris (Gray 1842): Two individuals

were observed at Kamini Daha in March 2014 and June

2015. The third individual was observed from Ramauli-

Pratapur in December 2016 (Fig. 38).

Fig. 38. Trimeresurus albolabris. Photograph by Kapil

Pokharel/NTNC-BCC

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 55

Amphibians and Reptiles of Parsa National Park, Nepal

Testudinidae (Batsch 1788)

Indotestudo elongata (Blyth 1854): An individual was

observed at Ghodemasan. Two rescued individuals were

kept at Amlekhgunj-Hattisar. Later, they were released

inside the park. Local people, especially business people,

like to keep turtles and tortoises in captivity believing

they are a sign of good luck for their business (Fig. 39).

Fig. 39. Indotestudo elongata. Photograph by Santosh Bhat-

tarai.

Crocodylidae (Cuvier 1806)

Crocodylus palustris (Lesson 1831): An individual was

kept in an enclosure in Amlekhjung-Hattisar. Later, it

was released in a wetland inside the park at Bhata.

Discussion

Our short expeditions resulted in 22 new species records

for the PNP, including three species of frog, two geckos,

one Agamid, two skink species, 13 snake species, and

one crocodile. The details of new species recorded for the

PNP are in Table 1.

The record of Traschischium tenuiceps by Kastle et

al. (2013) from the PNP needs to be verified as the el-

evational range of the species in Nepal is 1,500-2,400 m

(Schleich and Kastle 2002). We presume that the species

was mistakenly reported from the PNP.

Our survey mainly focused on daytime searches due

to logistics. It is highly likely that many other amphibians

and reptiles remain to be added to the list, especially fos-

sorial and arboreal species. During our survey we failed

to document Eryx johnii (Russell 1801) as this species is

frequently observed in nearby areas.

Among the species we recorded, Varamis flavescens

and Python sp. are legally protected species in Nepal.

The pythons are the only legally protected snake species

of Nepal which has been accorded the highest degree of

protection under the National Parks and Wildlife Con¬

servation Act, 1973. The Act has included the python in

the Schedule-I as Python molurus. In 2009 Python bivit-

tatus was elevated to specific status, and the occurrence

of Python molurus in Nepal is doubtful (Bhattarai 2014).

Therefore, we suggest P. bivittatus be listed in the Act

instead of P. molurus.

The IUCN has evaluated the tortoise Indotestudo

elongata as an endangered species. Similarly, Crocody¬

lus palustris , Ophiophagus hannah, and Python bivit¬

tatus have been categorized as vulnerable species. The

rampant killing of snake species in the buffer zone of the

PNP is an observed threat. Buffer communities perceive

all snakes to be venomous despite the fact that only 17%

of Nepalese snakes are venomous (Bhattarai et al. 2017;

Sharma et al. 2013).

The national east-west highway bisects the park in the

Amlekhganj-Pathlaiya section where many wild species

are frequently observed trampled by the vehicular move¬

ment. The regular monitoring of this section will reveal

the extent of wildlife loss due to vehicles.

The PNP shares its western boundary with Chitwan

National Park, and the Siwalik hill in the North might

have unique species as this park has comparatively drier

habitats. We believe detailed inventory will further in¬

crease the species richness and diversity of the park.

Acknowledgements. —Amphibians and reptiles

were recorded during field implementation of two proj¬

ects: 1. Community Based Human-Elephant Conflict

Management in Chitwan-Parsa Complex ( Grant no#

F15AP00340 ), 2. Mitigating Human-Tiger Conflict en¬

gaging local community in Parsa National Park {Grant

no# F15AP00781 ). We would like to thank US Fish and

Wildlife Service for these two funds to NTNC-BCC. We

extend our gratitude to Department of National Parks

and Wildlife Conservation, Chitwan and Parsa Nation¬

al Parks for endorsing these projects. We thank Kapil

Pokharel, Harka Man Lama, Om Prakash Chaudhary,

Ashish Gurung, Dip Prasad Chaudhary, Binod Darai, Ra-

mesh Darai, Tirtha Lama, and team NTNC-BCC for their

assistance in the field. We also acknowledge ZSL Nepal

office for funding support to carryout camera trap sur¬

vey in Parsa National Park. We would also like to thank

Mark O’Shea and Peter Uetz for their comments on the

draft manuscript. We would also acknowledge Abhijit

Das and two other reviewers for their comments on the

manuscript.

Literature Cited

Acharya KP, Khadka BK, Jnawali SR, Mafia S, Bhatta¬

rai S, Wikramanayake E, Kohl M. 2017. Conservation

and population recovery of Gharials ( Gavialis gange-

ticus) in Nepal. Herpetologica 73(2): 129-135.

Bhattarai S, Gurung A, Chalise L, Pokheral CP. 2017.

Geographic Distribution: Psammodynastes pulvern-

lentus (Mock Viper). Herpetological Review 48(1):

129.

Bhattarai S, Pokheral CP, Lamicchane BR. 2017. Death-

feigning behavior in Burmese Python Python bivit¬

tatus Kuhl, 1820 in Chitwan National Park. Russian

Journal of Herpetology 24(4): 323-326.

Bhattarai S, Pokheral CP, Lamichhane BR, Subedi N.

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 55

Bhattarai et al.

Herpetofauna of a Ramsar Site: Beeshazar and As¬

sociated Lakes, Chitwan National Park Nepal. IRCF

Reptiles & Amphibians 24(1): 17-29.

Bhattarai S, Thapa KB, Chalise L, Gurung A, Pokheral

CP, Subedi N, Thapa TB, Shah KB. 2017. On the dis¬

tribution of the Himalayan Stripe-necked Snake Lio-

peltis rappi (Gunther, 1860) (Serpentes: Colubridae)

in Nepal. Amphibian & Reptile Conservation 11(1)

[General Section]: 88-92 (el39).

Bhattarai S. 2014. Population of Python bivittatus in Bar-

dia National Park, Nepal. M.Sc. Dissertation Report,

Department of Wildlife Science, University of Kota,

Rajasthan, India. 64 p.

Chetri M. 2003. Food habits of gaur Bos gaums gaums

Smith, 1827 and livestock (cows and buffaloes) in

Parsa Wildlife Reserve, Central Nepal. Himalayan

Journal of Sciences 1(1): 31-36.

Fazey I, Fischer J, Lindenmayer DB. 2005. What do con¬

servation biologists publish? Biological Conservation

124: 63-73.

Frost DR. 2017. Amphibian Species of the World: An

Online Reference. Version 6.0. American Museum of

Natural History, New York, New York, USA. Avail¬

able: http ://research. amnh. org/vz/herpetology/am¬

phibia/ [Accessed: 25 November 2017],

Heyer WR, Donnelly MA, McDiarmid RW, Hayek LC,

Foster MS. 1994. Measuring and Monitoring Bio¬

logical Diversity: Standard Methods for Amphibians.

Smithsonian Institution Press. Washington, DC, USA.

364 p.

Kastle W, Rai K, Schleich HH. 2013. Field Guide to

Amphibians and Reptiles of Nepal. ARCO-Nepal e.V.

Munich, Germany. 625 p.

Kathriner A, O’Shea M, Kaiser H. 2014. Re-examination

of Hemidactylus tenkatei van Lidth de Jeude, 1895:

Populations from Timor provide insight into the tax¬

onomy of the H. brookii Gray, 1845 complex (Squa-

mata: Gekkonidae). Zootaxa 3887(5): 583-599.

Khatiwada JR, Guo CH, Wang SH, Thapa A, Wang B,

Jiang J. 2017. A new species of Microhyla (Anura:

Microhylidae) from Eastern Nepal. Zootaxa 4254(2):

221-239.

Lamichhane BR, Pokheral CP, Poudel S, Adhikari D,

Giri SR, Bhattarai S, Bhatta TR, Pickles R, Amin R,

Acharya KP, Dhakal M, Regmi UR, Ram AK, Sub¬

edi N. 2017. Rapid recovery of tigers Panthera tigris

in Parsa Wildlife Reserve, Nepal. Oryx 52(1): 16-24.

doi: 10.1017/S0030605317000886.

Rosier H, Glaw F. 2010. Morphological variation and

taxonomy of Hemidactylus brookii Gray, 1845, Hemi¬

dactylus angulatus Hallowell, 1854, and similar taxa

(Squamata, Sauria, Gekkonidae). Spixiana 33: 139—

160.

Schleich HH, Kastle W. 2002. Amphibians and Reptiles

of Nepal. Koenigstein: Koeltz Scientific Books, Ger¬

many. 1,200 p.

Shah KB, Tiwari S. 2004. Herpetofauna of Nepal: A

Conservation Companion - Kathmandu. IUCN Ne¬

pal, Kathmandu, Nepal. 237 p.

Sharma SK, Pandey DP, Shah KB, Tillack F, Chappuis F,

Thapa CL, Elirol E, Kuch U. 2013. Venomous Snakes

of Nepal: A Photographic Guide. B.P Koirala Insti¬

tute of Health Sciences, Dharan, Nepal. 86 p.

Smith, MA. 1935. The Fauna of British India, Including

Ceylon and Burma. Reptilia and Amphibia, Volume 2:

Sauria. Taylor and Francis, London, England. 440 p.

Uetz P, Freed P, Hosek J, editors. 2017. The Reptile Data¬

base. Available: htpp://www.reptile-database.org [Ac¬

cessed: 17 December 2017],

Santosh Bhattarai currently works as Conservation Officer at National Trust for Nature Conservation- Biodiversity

Conservation Center (NTNC-BCC), Sauraha, Chitwan, Nepal. He is particularly interested to understand evolutionary

and ecological drivers of amphibians and reptiles by which species diversify and accumulate through time and space.

Chiranjibi Prasad Pokheral currently works as Program Manager at National Trust for Nature Conservation-

Central Zoo, Lalitpur, Nepal. He completed his Ph.D. in 2012 and has more than two decades of experience in species

conservation and management in Nepal. He is focused on tiger conservation in Nepal.

Babu Ram Lamichhane currently works as Research Officer at NTNC-BCC, He is interested in Human-Carnivore

interactions and is pursuing his doctoral study in the same topic.

Uba Raj Regmi works at Department of National Parks and Wildlife Conservation. He has more than 25 years of

experience of managing Protected Areas in Nepal. He currently works as Chief Conservation Officer at Langtang

National Park, Nepal.

Ashok Kumar Ram works at Department of National Parks and Wildlife Conservation. Currently, he is working

as Assistant Conservation Officer at Parsa National Park. He is focused on Human-Elephant conflict management

issues.

Naresh Subedi completed his Ph.D. in 2012 and is currently based at NTNC-central office, Kathamandu, and works

in the capacity of Conservation Program Manager. His earlier studies focsed on impact of invasive species on native

wild animals and their conservation measures.

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 55

Official journal website:

amphibian-reptile-conservation.org

Amphibian & Reptile Conservation

12(1) [General Section]: 49-51 (el56).

Range extension of Cyrtopodion himalayanus Duda and Sahi,

1978 (Reptilia: Sauria) in Jammu Province of State Jammu

and Kashmir from District Doda, Northern India

^mit Man has, 2 Rajni Raina, and 3 Ashwani Wanganeo

1 Research Scholar, Department of Environmental Sciences and Limnology>, Barkatullah University’ Bhopal, Madhya Pradesh, INDIA 2 Professor,

Department of Zoology), Govt. Science and commerce (Benazir) college, Bhopal, Madhya Pradesh, INDIA 3 Professor, Department of Environmental

Sciences and Limnology, Barkatullah University Bhopal, Madhya Pradesh, INDIA

Abstract. —Documented are new distributional records of the poorly-known Gekkonidae Cyrtopodion

himalayanus from the Doda region of Jammu and Kashmir State (India) based on specimens collected in three

localities of the Doda region (Village Nai-Bhallara, Village Chagsoo, and Village Zazinda). Presented are notes

on the morphology and coloration of the species in Doda, as well as photographs and a map indicating the

known localities of Cyrtopodion himalayanus. This record represents an extension range of 60-80 km from

the earlier reported locality of the species. The species Cyrtopodion himalayanus is the sole representative of

the group Cyrtopodion, documented four decades ago from Kishtwar town of District Kishtwar (formally under

District Doda) in the state of Jammu and Kashmir.

Keywords. Gekkonidae, new distribution, Kishtwar, reptiles, visual encounter survey, morphology

Citation: Manhas A, Raina R, Wanganeo A. 2018. Range extension of Cyrtopodion himalayanus Duda and Sahi, 1978 (Reptilia: Sauria) in Jammu

Province of State Jammu and Kashmir from District Doda, Northern India. Amphibian & Reptile Conservation 12(1) [General Section]: 48-51 (el 56).

NoDerivatives 4.0 International License, which permits unrestricted use for non-commercial and education purposes only, in any medium, provided

the original author and the official and authorized publication sources are recognized and properly 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-

reptiie-conservation.org>.

Received: 18 March 2017; Accepted: 05 July 2017; Published: 17 July 2018

Introduction

The state of Jammu and Kashmir includes three main ar¬

eas: Jammu, Kashmir, and Ladakh, which are different

from one another in terms of topography, altitude, and

climate. District Doda geographically falls in the outer

Himalayan ranges and comes under the Jammu province

of the state Jammu and Kashmir. District Doda also falls

under seismic zone-V as per IS 1893 (Part I): 2002 and

situated between 33°08'N, 75°32'E at an average eleva¬

tion of 1,107 m asl. The studies associated with other

faunal components of the state have been increasing over

the past years, whereas the study associated with reptil¬

ian fauna of the region is very scant. Fenton (1910) was

a pioneer in ophidian studies in the state of Jammu and

Kashmir. Since the publication of The Fauna of British

India by Boulenger (1890) and Smith (1935), very little

attention has been given to its reptilian fauna. The work

of Das et al. (1964), Duda and Koul (1974), Murthy and

Sharma (1976), and Murthy et al. (1979) enlisted some

records of reptiles, but their studies focused on only two

regions of the state (Jammu and Kashmir), Kashmir and

Ladakh.

There was no information regarding reptilians from

Jammu province until Sahi (1979), who has conducted

an extensive survey of Jammu and Kashmir state for

the herptiles and reported 76 species. He stated that the

Jammu province of the state is the richest of the two re¬

gions of the state in terms of reptilian diversity. The dis¬

tinguishing oversight of references to the Doda region of

Jammu province (Jammu and Kashmir state) on herptiles

of the state undoubtedly indicates the lack of any faunis-

tic survey ever having been conducted in this part of the

state since Sahi (1979).

Methodology

We have conducted surveys during the years 2014-2015

following the visual encounter surveying method (Camp¬

bell and Christman 1982). The survey was conducted

from March to mid-June for both years (2014 and 2015).

We have photographed the specimens using a digital

camera (Sony HX300), and geo-coordinates were re¬

corded using GPS (GPS test). Morphological measure¬

ments of the specimens collected were recorded by using

a digital caliper (Precision 150). The specimens sighted

Correspondence. 1 amitmanhasl986@gmail.com (Corresponding author)

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 56

Manhas et al.

&}[#&! led

^ Earlier record

j/y*

A Present record

Fig. 1. Depicting the localities of distribution (Earlier and Present).

were identified with the help of descriptions and keys

given by Sahi (1978).

Results and Discussion

Cyrtopodion is a complex group of Asian geckos com¬

prising of 37 species at present (Uetz and Hosek 2015).

While surveying the herptiles of the state (Jammu and

Kashmir), Duda and Sahi (1978) had collected eight

specimens of Cyrtopodion himalayanus (75.7E, 3.3N;

1,700 m) at an elevation of 1,700 m from a house in

Kishtwar town on 8 May and 24 October, 1978 in District

Kishtwar (formerly under District Doda) and described it

as a new species of Cyrtopodion (earlier = Cyrtodacty-

1ns (Duda and Sahi 1978)) (Fig. 2). During an investiga¬

tion (2014-2015) of reptilian fauna in District Doda, we

sighted individuals of the species from three localities

different from the earlier record (Fig. 1). The stations are

Nai-Bhallara (33°05’20.69”N, 75°42’30.24 ,, E; 1,808 m

asl), Village Chagsoo (33°07 , 33.27 ,, N, 75°40 , 11.50 ,, E;

1,743 m asl), and Village Zazinda (33°5’34.48”N,

75°38 , 19.74”E; 2,157 m asl). The stations Nai-Bhallara

and Village Chagsoo fall under Tehsil Thathri of District

Doda, whereas the latter falls under Tehsil Bhaderwah.

The stations are about 60-80 km away from the Kisht¬

war town. The specimens were sighted near human set¬

tlements (inhabited debris and house wall crevices). The

specimens were studied alive and released at the same

place after ensuring their morphological and physiologi¬

cal characteristics.

The morphological and physiological characteristics

of Cyrtopodion himalayanus sighted during the present

investigation are given in Table 1. Various distinguish-

Amphib. Reptile Conserv.

ing features of every individual were observed, such as:

greyish body with dark brown reticulation; brown head

with a distinct streak from nape to snout passing through

eye on each side; inverted snout; small nostrils placed

dorsolaterally; ten upper-labials; eight lower-labials;

snout longer than the distance between the eye and ear

opening; ear opening sub-oval; clawed digits; claws em¬

bedded between two large shields.

Duda and Sahi (1978) analyzed and documented the

body length of the specimens to be between 125 mm

and 140 mm during their study, whereas morphological

characteristics of Cyrtopodion himalayanus of the cur¬

rent study reveal specimens with lengths from 115 mm

to 136 mm.

Literature Cited

Boulenger GA. 1890. The Fauna of British India: Rep-

tilia and Batrachia. Taylor and Francis, Fondon, Eng¬

land. 570 p.

Campbell HW, Christman SP. 1982. Field techniques for

herpetofaunal community analysis. In: Herpetologi-

cal Communities. Editor, Scott Jr. NJ. Washington,

USA. 239 p.

Das SM, Malhotra YR, Duda PE. 1964. The Palearctic

elements in the fauna of Kashmir. Kashmir Science

1 / 2 : 100 - 111 .

Duda PE, Sahi DN. 1978. Cyrtodactylus himalayanus'. A

new Gekkonid species from Jammu, India. Journal of

Herpetology 12(3): 351-354.

Duda PL, Koul O. 1974. Seasonal changes in the histo-

morphology of the gonads of Agama tuberculata , an

oviparous, and Lygosoma himalayanus , an ovovivipa-

July 2018 | Volume 12 | Number 1 | el 56

Range extension of Cyrtopodion himalayanus

Fig. 2. Cyrtopodion himalayanus (A) Enlarged lateral view of

head. (B) Full lateral view of the body.

rous lizard from Kashmir. Kashmir University. 234 p.

Fenton LL. 1910. The snakes of Kashmir. Journal of the

Bombay Natural History Society 29: 1,002-1,004.

Murthy TSN, Sharma BD, Sharma T. 1979. Second re¬

port on the herpetofauna of Jammu and Kashmir. The

Snake 11: 234-538.

Murthy TSN, Sharma BD. 1976. A contribution to the

herpetology of Jammu and Kashmir. British Journal

of Herpetology 5: 533-538.

Table 1 . Variations in various characteristics of specimens of

species Cyrtopodion himalayanum.

Characteristics

Range

Full body length

115 mm-136 mm

Snout-vent length

61.89 mm-68.79 mm

Tail length

53.11 mm-67.21 mm

Head width

11.75 mm-14.91 mm

Head length

16.35 mm-21.38 mm

Snout to mouth length

12.13 mm-14.58 mm

Intra-orbital distance

1.86 mm-3.10 mm

Eye diameter

5.22 mm-5.45 mm

Nostril to eye length

5.35 mm-6.16 mm

Ear diameter

1.89 mm-2.80 mm

Nostril to ear length

13.86 mm-15.79 mm

Forearm length

17.80 mm-20.81 mm

Hind arm length

14.97 mm-17.87 mm

Supralabial scales

10/10

Infralabial scales

8/8

Sahi DN. 1979. A contribution to the herpetology of

Jammu and Kashmir State. Ph.D. Thesis, University

of Jammu, Jammu and Kashmir, India.

Smith MA. 1935. The Fauna of British India. Volume II.

Sauria. Taylor and Francis, London, England. 440 p.

Uetz P, Hosek J. 2015. The Reptile Database. Available:

http://www.reptile-database.org [Accessed: 22 De¬

cember 2015],

Amit Manhas is an independent researcher. He completed his Ph.D. in zoology in 2017 from

Barkatullah University, Bhopal, India. He has keen interest in studying reptilian diversity,

ecology, and distribution. Presently his research studies are focused on reptilian diversity of

Jammu and Kashmir state of India. He has a keen interest in exploring living and spiritual forms

of ecosystems, and publishing his findings on the Internet (www.personalife.org).

Dr. Rajni Raina is a professor of zoology at Government Science and Commerce College,

Benazir, in Bhopal, Madhya Pradesh, India. She is enthusiastically contributing in the field of

research. Professor Raina is actively supervising new researchers in different aspects of zoology.

Dr. Ashwani Wanganeo is a professor in the Environmental Sciences and Fimnology Department

of Barkatullah University, Bhopal, India. He has made significant contributions in the field of

Fimnology and Ecology. He has also been active in guiding many new researchers fascinated in

various fields of limnology and ecology.

Amphib. Reptile Conserv.

July 2018 | Volume 12 | Number 1 | el 56