A Guide to the Tadpoles of Borneo E-Book

Alexander Haas

• Herausgeber: tredition
• Kategorie: Wissenschaft und neue Technologien
• Sprache: Englisch
• Veröffentlichungsjahr: 2022

Seitenzahl: 345

Beschreibung

The most comprehensive and fully illustrated guide to the tadpoles of Bornean frogs available. The book presents tadpole descriptions for 99 species from the southeast Asian island of Borneo, covering all species commonly found, as well as representatives of the more cryptic ones. Almost all presented species are depicted from life with color photographs, mostly for the first time. The aims of this book are to allow a broad audience an easy access to the tadpole fauna of Borneo, increase awareness of these life stages, document their diversity, and provide insights into their fascinating biology.

Leseprobe

Photo courtesy of © Lars Fehlandt

Haas, Das, Hertwig, Bublies, Schulz-Schaeffer

A Guide to the Tadpoles of Borneo

Danum Valley canopy.

Alexander Haas, Indraneil Das, Stefan T. Hertwig,

Pia Bublies, Reinhard Schulz-Schaeffer

A GUIDE TO THE

TADPOLES

OF

BORNEO

IMPRESSUM

© 2022 Alexander Haas, Indraneil Das, Stefan T. Hertwig, Pia Bublies, Reinhard Schulz-Schaeffer

ISBN Softcover: 978-3-347-64345-1

ISBN E-Book: 978-3-347-64346-8

Printed and distributed in behalf of the authors by tredition GmbH, Halenreie 40-44, 22359 Hamburg.

The authors are responsible for the contents. Publication and distribution in behalf of the authors by tredition, to be reached at: "Impressumservice", Halenreie 40-44, 22359 Hamburg, Germany.

Printed Version 1.0

This book is published under a creative commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) license. You are free to copy and redistribute the material in any medium or format. You must give appropriate credit, provide a link to the license, and indicate if changes were made. You may do so in any reasonable manner, but not in any way that suggests the licensor endorses you or your use. You may not use the material for commercial purposes. If you remix, transform, or build upon the material, you may under no circumstances distribute the modified material. You may not apply legal terms or technological measures that legally restrict others from doing anything the license permits.

Photographs and illustrations remain under copyright © 2022 by the authors or as credited.

The views expressed in this book are those of the authors, and not necessarily those of the supporting publisher institutions and sponsors.

Cover: Microhyla malang

Cover Design: Reinhard Schulz-Schaeffer

Project and book creation sponsored by

CONTENTS

1 PREFACE

ACKNOWLEDGMENTS

2 INTRODUCTION

General scope

Bornean frog species

Taxonomy

Who should use this book?

How to use this book?

3 AMPHIBIAN STUDIES ON BORNEO

Brief history of studies

Biogeography

4 NATURAL HISTORY

Natural history

Tadpole diets

Reproductive modes & larval habitat

Tadpole microhabitats

5 ETHNOBIOLOGY

6 METHODS TO STUDY TADPOLES

Finding & observing tadpoles

Describing & illustrating tadpoles

Tadpole photography

Measurements

DNA Barcoding

Vouchers and tissue preservation

7 MORPHOLOGY

Tadpole morphology

Variability in tadpoles

8 SPECIES ACCOUNTS

Tadpole descriptions

Flowing water bodies

Bufonidae

Ansonia

Ingerophrynus

Leptophryne

Phrynoidis

Rentapia

Dicroglossidae

Limnonectes

Megophryidae

Leptobrachella

Leptobrachium

Megophrys

Pelobatrachus

Ranidae

Huia

Meristogenys

Odorrana

Staurois

Rhacophoridae

Feihyla

Leptomantis

Stagnant water bodies

Bufonidae

Duttaphrynus

Ingerophrynus

Pelophryne

Dicroglossidae

Fejervarya

Hoplobatrachus

Limnonectes

Occidozyga

Microhylidae

Glyphoglossus

Chaperina

Kaloula

Metaphrynella

Microhyla

Nanohyla

Kalophrynus

Ranidae

Abavorana

Chalcorana

Hylarana

Indosylvirana

Pulchrana

Rhacophoridae

Feihyla

Kurixalus

Leptomantis

Nyctixalus

Philautus

Polypedates

Rhacophorus

Zhangixalus

Terrestrial sites

Rhacophoridae

Philautus

9. GLOSSARY

10 AUTHORS

11. INDEX OF SPECIES DESCRIPTIONS

Phrynoidis juxtasper

Ulu Temburong National Park, Brunei.Photo courtesy of © Hanyrol H. Ahmad Sah.

1 PREFACE

WE WILL NEVER FORGET …

our first trip together in 2001 to the interior of Sarawak and the kind Kelabit people of the Bario Highlands. It was a joyful productive exploration of the beautiful forests of Bario. The morale was high, discussions on shared scientific interests were productive and soon showed that we should try doing a project together. Soon after, we applied to Volkswagen Foundation for a four-year project on an inventory of East Malaysian tadpoles. In the consecutive years, we conducted many field trips together and amassed data far beyond tadpoles. The idea of writing a book on tadpoles always lingered in our heads, fascinating and intimidating us at the same time. It was only after Stefan T. Hertwig, Pia Bublies, and Reinhard Schulz-Schaeffer had later strengthened our team that we started the book writing journey. The time was ripe for a summary of what had been achieved.

When thinking about writing a book on the tadpoles of Borneo, we found us confronted with some tricky questions. How can a book be written about a fauna that is incompletely known at the time of writing? How can we dare writing about the tadpoles of Borneo when many tadpoles have either not been discovered or not been described scientifically? Why would we try to assemble a book if current knowledge is so patchy? And why risk the publication of a book that might be outdated by new discoveries and progress in taxonomy and systematics at the time of its release? These are only the biological and scientific questions raised by such a project. Many more questions concern the format: printed book, e-book, app for tablet PC? What would be the most useful and appealing format of such a publication in times of major changes in the markets. Who would use the book and how would it be used? What value in usability could we deliver?

The excellent previous work of colleagues certainly humbled us, for example Wen-hao Chou and Jun-yi Lin’s Tadpoles of Taiwan and Marion Anstis’ Tadpoles and Frogs of Australia, and Tsi Ming Leong’s publications on Peninsular Malaysia tadpoles. At the same time, books such as Frogs of Borneo by Robert F. Inger, Robert B. Stuebing, T. Ulmar Grafe, and T. Maximilian Dehling inspired us with their book on frogs. The work and high standards of all theses authors encouraged us to fill a gap and experiment with our own ways to approach a publication on a localized tadpole fauna.

Author information p. 276

Many years of field work in the beautiful rainforests of Sarawak and Sabah have enriched us with insights that we want to share. Many students, with their keen enthusiasm have convinced us that producing a publications that facilitates access to the exceptional and fascinating amphibian fauna of Borneo is an effort well spent. The faith of our major financial sponsor for this research project, the Volkswagen Foundation, certainly encouraged us to take this challenge. Last but not least, the numbers of visitors to our website on the frogs of Borneo ( www.frogsofborneo.org) surprised us; we had not expected that attention. On this site, a few clicks lead the user to most of the Bornean species. Although incomplete in coverage and information for each species rather minimalistic, it has proven useful for many users. University students and general naturalists downloaded our imagery to build their personal pocket field guides. It convinced us that there is a need for simplicity among users.

 www.frogsofborneo.org

Knowledge on amphibians and the tools of the trade are in constant change. That should not keep us from communicating the current status in the field in an accessible form. Our team of authors has proposed some new avenues in this book. For us it has been a joyful learning experience.

— Alexander Haas & Indraneil Das —

ACKNOWLEDGMENTS

Over the years, numerous colleagues, friends, students, technicians, and field companions assisted in one way or another in our project to document the tadpoles of Borneo either by making the book a reality, working with us in the field, processing specimens in the laboratory, or just discussing Bornean amphibians with us. Needless to say that our endeavor was substantially motivated by previous groundbreaking scientific work on tadpoles by Robert F. Inger, Wen-hao Chou, Marion Anstis, and Tzi Ming Leong. Their wonderful work provided many inspirations for the present book.

First and foremost, we would like to thank the Volkswagen Foundation for enabling us with a grant to initiate our research on Bornean tadpoles, organize a symposium at Universiti Malaysia Sarawak in 2009, and produce this book. Furthermore, we would like to express our sincere gratitude to our scientific institutions for providing us with the possibility to conduct this research, namely the Institute for Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak; the Center for Natural History, Universität Hamburg, Leibniz-Institute for the Analysis of Biodiversity Change, and the Natural History Museum Bern. The Burgergemeinde Bern and German Academic Exchange Program (DAAD) generously provided funds for field assistants and travel expenses. We also gratefully acknowledge the generous support of our collaborating partners at the Universiti Sabah Malaysia, Charles Vairapppan and Kueh Boon-Hee.

Our research in protected areas of Sarawak and Sabah was only possible with the support and endorsement of the responsible authorities. We are indebted to the Economic Planning Unit, the Prime Minister’s Department, Malaysia, and especially Munirah Abd. Manan. Sarawak Forest Department and Sarawak Forestry Corporation, especially (Datuk) Cheong Ek Choon, Engkamat Lading, Oswald Braken Tisen, Haji Azahari bin Omar, Zolkipli bin Mohamad Aton, Arabi Abang Aimran, (Datu) Haji Ali bin Yusop, Bolhan Budeng, Azahari bin Omar, Mohd. Shabudin Sabki, Nur Afiza Binti Umar, Dayang Nuriza binti Abang Abdillah, Mohamad bin Kohdi. We gratefully acknowledge the support of Sabah Biodiversity Center and Council, Abdul Fatah Amir, C.Y. Chung. Sabah Parks with our contact persons Jamili Nais, Maklarin Lakim, Paul Yambun, Nelly Majuakim. Yayasan Foundation and Maliau Management Committee, particularly Waidi Sinun, Rondy Milin, and Grace Pounsin supported our work at Maliau Conservation Area. Finally, we thank all local park managements and staff that we had the privilege to work with.

Many people contributed to our project. We needed support and assistance in the field, specimens had to be processed, tadpoles had to be barcoded, phylogenetically analyzed, and described. Some students produced Bachelor’s or Master’s Theses on tadpoles and frogs of Sarawak and Sabah as part of our project and moved on to make their own careers. First of all, our gratitude goes to Pui Yong Min who was our reliable, knowledgeable and kind partner and friend in many field trips. We thank him for his sustained support, his inter-cultural assistance, tremendous field work and endless enthusiasm.

Furthermore, we would like to thank our former students, field assistants, and technical staff for their participation in a multitude of different ways and for their good work, in no particular order: Elyas Eric Huil, Laurence Etter, Erina Balmer, Nathalie Reichen, Jana Flury, Hannes Baur, Beatrice Blöchlinger, Chris Sherry, Karin Eva Lilje, Toralf Keilholz, Tobias Einecke, Maximilian Dehling, André Jankowski, Jeet Sukumaran, Daniela Haarmeier, Melitta Wunderskirchner, Cindy Hefenbrock, Wencke Krings, Maria Grimm, Jana Pohlmeyer, Thorben Riehl, Johanna Wolter, Enzo Braskamp, Despina Chaluppa, Stine Griep, Helena Dobbeck, Stephan Senne, Julia Juchheim, Felix Meyer, Sandra James Tinggom, Castro Michael, Lily Sir, Mohd. Iqbal Makmor, Khairul Anuar bin Omar, Yolande Direp ak Michael Direp, Hairi bin Hedeir, Siti Shuhada bt Mustaffa, S. J. Tingsom, C. Michael, Mona Octavia Sulai, Lea Waser, Evelyne Oberhummer, Dario Neokleous, Catherin Barten, Dimitrij Trofimov, Anna Maria Vogt, Monika Hähnel, Angelika Taebel-Hellwig, Reto Hagmann, Masliadi bin Asri, Alvinus Joseph, and Elyas Eric Huil. Finally many thanks go to Jörg Hofmann, good friend and excellent partner in the field.

Ledlenser kindly provided some samples of their LED torches for field testing. Yeo Siew Teck (Cat City Holidays) provided valuable logistics support over the years. Nele Johannsen skillfully developed and contributed a sketched rainforest scenery (p. 46f) that shows where tadpoles live .

The authors hold copyrights for all photos in this book, except for several photos that were kindly provided by other photographers and are marked alongside with the photo. Especially Chien Lee, Hanyrol H. Ahmad, Lars Fehlandt, Pui Yong Min, Nikolay A. Poyarkov, Arne Schulze, and Wencke Krings. Marion Beeck gave some time-saving InDesign tips. We very much appreciate all their contributions!

Our colleagues Robert F. Inger, Ulmar Grafe, Julian Glos, Chan Kin Onn, Umilaela Arifin, Rafe Brown, Manuel Schweizer, Tzi Ming Leong, and Quah Evan have always been open for our questions and supported us when needed. We are grateful for all the discussions, interactions, and sharing of information we had with them and the help we received!

Many thanks to our friends and nature photographers Hanyrol H. Ahmad Sah, and Lars Fehlandt who joined us in field work, provided great images, connected us many times with people, helped us with logistics, and gave us valuable advice during expedition planning. We are grateful to Nadja Schilling for proof reading earlier versions and feedback. AH takes full responsibility for all remaining errors. Finally, AH wants to thank Roisin Murphy for her album Róisín Machine. Its steaming and stumping beats kept him going in this project and boosted his morale.

Two species of Abavorana have been described, A. luctuosa and, recently, A. decorata. At present, the limited genetic data available does not allow a definitive identification of this remarkable specimen from Lambir Hills National Park.

2 INTRODUCTION

GENERAL SCOPE

Biodiversity research aims to uncover and understand the full biological richness of a given area. Southeast Asia includes several hotspots of biodiversity that are paralleled in species richness only by the Amazon river basin and adjacent regions in South America. One of the Asian hotspots is Sundaland, a shallow continental shelf on which Borneo, Sumatra, and Peninsula Malaysia are located (p. 26). Today’s islands of Sundaland have been interconnected repeatedly during periods of low sea levels at former times.

The biodiversity of Southeast Asia has been vastly underestimated in the past and researchers are only beginning to comprehend the true richness of this region. Borneo is the largest island of Sundaland and plays a crucial role in the recording and understanding of the evolution of biodiversity in this region. In the past 20 years many species of frogs have been discovered on the island of Borneo. Some of these new species have been split from known taxa, acknowledging that known species had been complexes of several, closely related and morphologically similar, but genetically and ecologically distinct species. Progress is fast. A text like this can become outdated shortly after publication.

In this book we focus on species that we encountered in our own work in Sarawak and Sabah. For many known species, however, tadpoles have not been documented. The current list of Bornean frog species follows below (p. 18). Many more are likely to be described in the decades to come. It is unavoidable that the scientific information available for species and species’ tadpoles (imagery, ecology) differs significantly. Some species are well known, widespread, and commonly found, others are restricted to certain areas, sometimes known only from their respective type localities and rarely seen. Our species accounts necessarily reflect that and are snapshots in an evolving field.

Feihyla kajau

While adults frogs live in numerous terrestrial habitats and niches, tadpoles are the larval aquatic stage in the biphasic life-cycle of frogs. The body shape, anatomy, and ecological requirements are completely different from the terrestrial frog. The tadpole eventually undergoes a metamorphosis to transform into a froglet. Metamorphosis is the process of physical transition from the aquatic larva to the terrestrial adult. The biology of tadpoles is just as fascinating as the biology of frogs and has been central in our own research. We believe that rather few publications have given tadpoles the attention they deserve. Clearly, understanding the ecology of tadpoles is essential for any conservation efforts. If an area does not provide proper habitats for tadpoles, there will be no frogs either! For the naturalist, ecologist or surveyor, tadpoles are an important indicator of the presence of a reproductively active population of that species.

After metamorphosis, the froglets leave the water and move to their different species-specific terrestrial habitats. Frogs occupy a large number of ecological niches, ranging from burrows in the forest floor to the canopy of the rainforests. This variety of living conditions is reflected by the adaptations of their body. Species that perch on shrubs or trees have slender bodies and long legs, while ground-dwellers often show a stocky body and short but strong legs.

All amphibian species from Borneo (and indeed from all over the world) have been described largely, if not entirely, on the basis of adult specimens, because frogs are found more often in the field than their larval stages. Tradition in herpetological research is another reason for the focus on adults and the neglect in tadpole research. Knowledge of tadpole descriptions has thus seriously lagged behind. Although many larval descriptions of species occurring on the island of Borneo have been published, we still lack information on the larval forms of many species. Larval descriptions currently available are sometimes derived from non-Bornean populations that may eventually prove to be non-conspecifics. Several familiar species have been shown in recent years to include morphologically similar albeit biologically distinct species.

Tawau Hills National Park, Sungai Gelas Waterfall.

Data quality is another problem, as a significant proportion of traditional larval descriptions lack voucher specimen information. Voucher specimens are specimens deposited in accessible museum collections for future reference. Many previously published larval descriptions have neglected DNA barcoding techniques for unambiguous matching of tadpoles and frogs. Assigning an unknown tadpole to a frog is no easy task; it may require rearing the tadpole through metamorphosis. Even then, in studies that have done so, wrong assignments have occurred. The froglet may look very unlike the adult frog—the famous Wallace’s Flying Frog Rhacophorus nigropalmatus is one example. With the advent of DNA barcoding techniques it is now possible to match any tadpole with a frog from the same region, stream, or pond with a high reliability. This technique is far superior, less time consuming and less error-prone than rearing experiments. The only drawback is the access to a lab and the need to collect, handle and preserve tissue properly. Once the match and correct assignment has been established by DNA barcoding, morphological features can be re-examined to extract features that might allow to identify a tadpole without DNA barcoding.

In this book, we present pertinent morphological information for common species (if their tadpole is known to science) as a tool for field identification of tadpoles. With the help of this book, tadpoles should be identifiable to the species or at least to the generic level. The continuing discovery of new species and their tadpoles makes the development of reliable, classical dichotomous identification keys very difficult. New discoveries can overthrow existing keys easily. Keys, that where valid at the time of their publication, are included in some of the literature mentioned in this book, most notably in Inger (1985).

LITERATURE

Inger, R.F. (1985) Tadpoles of the forested regions of Borneo. Fieldiana Zoology new series 26: 1-89.

BORNEAN FROG SPECIES

Taxonomy is in constant flux. The list below gives the 200 recognized species of Borneo by the end of 2021. Please refer to Amphibian Species of the World (ASW) database for taxonomic details and updates. Currently, dozens of genetically distinct lineages have been recognized in the genera Limnonectes, Occidozyga and Nyctixalus. They represent potential candidate species. Therefore, the following list is a conservative estimate of Borneo’s true frog diversity. More discoveries are expected in the future, especially from the still little know areas of Kalimantan.

taxonomic reference: http://research.amnh.org/vz/herpetology/amphibia/index.php

BOMBINATORIDAE: 1

Barbourula kalimantanensis Iskandar, 1978

BUFONIDAE: 35

Ansonia albomaculata Inger, 1960

Ansonia echinata Inger and Stuebing, 2009

Ansonia fuliginea (Mocquard, 1890)

Ansonia guibei Inger, 1966

Ansonia hanitschi Inger, 1960

Ansonia kanak Matsui, Nishikawa, Eto, and Hossman, 2020

Ansonia kelabitensis Matsui, Nishikawa, Eto, and Hossman, 2020

Ansonia latidisca Inger, 1966

Ansonia leptopus (Günther, 1872)

Ansonia longidigita Inger, 1960

Ansonia minuta Inger, 1960

Ansonia platysoma Inger, 1960

Ansonia spinulifer (Mocquard, 1890)

Ansonia teneritas Waser, Schweizer, Haas, Das, Jankowski, Min, and Hertwig, 2017

Ansonia torrentis Dring, 1983

Ansonia vidua Hertwig, Min, Haas, and Das, 2014

Duttaphrynus melanostictus (Schneider, 1799)

Ingerophrynus divergens (Peters, 1871)

Ingerophrynus quadriporcatus (Boulenger, 1887)

Leptophryne borbonica (Tschudi, 1838)

Pelophryne api Dring, 1983

Pelophryne guentheri (Boulenger, 1882)

Pelophryne linanitensis Das, 2008

Pelophryne misera (Mocquard, 1890)

Pelophryne murudensis Das, 2008

Pelophryne penrissenensis Matsui, Nishikawa, Eto, and Hossman, 2017

Pelophryne rhopophilia Inger and Stuebing, 1996

Pelophryne saravacensis Inger and Stuebing, 2009

Pelophryne signata (Boulenger, 1895)

Phrynoidis asper (Gravenhorst, 1829)

Phrynoidis juxtasper (Inger, 1964)

Pseudobufo subasper Tschudi, 1838

Rentapia everetti (Boulenger, 1896)

Rentapia hosii (Boulenger, 1892)

Sabahphrynus maculatus (Mocquard, 1890)

CERATOBATRACHIDAE: 3

Alcalus baluensis (Boulenger, 1896)

Alcalus rajae (Iskandar, Bickford, and Arifin, 2011)

Alcalus sariba (Shelford, 1905)

DICROGLOSSIDAE: 23

Fejervarya cancrivora (Gravenhorst, 1829)

Fejervarya limnocharis (Gravenhorst, 1829)

Hoplobatrachus rugulosus (Wiegmann, 1834)

Limnonectes asperatus (Inger, Boeadi, and Taufik, 1996)

Limnonectes cintalubang Matsui, Nishikawa, and Eto, 2014

Limnonectes conspicillatus (Günther, 1872)

Limnonectes finchi (Inger, 1966)

Limnonectes hikidai Matsui and Nishikawa, 2014

Limnonectes ibanorum (Inger, 1964)

Limnonectes ingeri (Kiew, 1978)

Limnonectes kenepaiensis (Inger, 1966)

Limnonectes kong Dehling and Dehling, 2017

Limnonectes leporinus (Andersson, 1923)

Limnonectes malesianus (Kiew, 1984)

Limnonectes moquardi (Mocquard, 1890)

Limnonectes palavanensis (Boulenger, 1894)

Limnonectes paramacrodon (Inger, 1966)

Limnonectes rhacodus (Inger, Boeadi, and Taufik, 1996)

Limnonectes sinuatodorsalis Matsui, 2015 Occidozyga baluensis (Boulenger, 1896)

Occidozyga laevis (Günther, 1858)

Occidozyga berbeza Matsui, Nishikawa, Eto, Hamidi, Hossman, and Fukuyama, 2021

Occidozyga sumatrana (Peters, 1877)

MEGOPHRYIDAE: 32

Leptobrachella arayai (Matsui, 1997)

Leptobrachella baluensis Smith, 1931

Leptobrachella bondangensis Eto, Matsui, Hamidy, Munir, and Iskandar, 2018

Leptobrachella brevicrus Dring, 1983

Leptobrachella dringi (Dubois, 1987)

Leptobrachella fritinniens (Dehling and Matsui, 2013)

Leptobrachella fusca Eto, Matsui, Hamidy, Munir, and Iskandar, 2018

Leptobrachella gracilis (Günther, 1872)

Leptobrachella hamidi (Matsui, 1997)

Leptobrachella itiokat Eto, Matsui, and Nishikawa, 2016

Leptobrachella juliandringi Eto, Matsui, and Nishikawa, 2015

Leptobrachella marmoratus (Matsui, Zainudin, and Nishikawa, 2014)

Leptobrachella maurus (Inger, Lakim, Biun, and Yambun, 1997)

Leptobrachella mjobergi Smith, 1925 Leptobrachella palmata Inger and Stuebing, 1992

Leptobrachella parva Dring, 1983

Leptobrachella pictus (Malkmus, 1992)

Leptobrachella sabahmontanus (Matsui, Nishikawa, and Yambun, 2014)

Leptobrachella serasanae Dring, 1983

Leptobrachium abbotti (Cochran, 1926)

Leptobrachium gunungense Malkmus, 1996

Leptobrachium hendricksoni Taylor, 1962

Leptobrachium ingeri Hamidy, Matsui, Nishikawa, and Belabut, 2012

Leptobrachium kanowitense Hamidy, Matsui, Nishikawa, and Belabut, 2012

Leptobrachium kantonishikawai Hamidy and Matsui, 2014

Leptobrachium montanum Fischer, 1885

Megophrys dringi Inger, Stuebing, and Tan, 1995

Pelobatrachus baluensis (Boulenger, 1899)

Pelobatrachus edwardinae (Inger, 1989)

Pelobatrachus kalimantanensis (Munir, Hamidy, Matsui, Iskandar, Sidik, and Shimada, 2019)

Pelobatrachus kobayashii (Malkmus and Matsui, 1997)

Pelobatrachus nasutus (Schlegel, 1858)

MICROHYLIDAE: 28

Chaperina fusca Mocquard, 1892

Gastrophrynoides borneensis (Boulenger, 1897)

Glyphoglossus brooksii (Boulenger, 1904)

Glyphoglossus capsus (Das, Pui, Hsu, Hertwig, and Haas, 2014)

Glyphoglossus flava (Kiew, 1984)

Glyphoglossus smithi (Barbour and Noble, 1916)

Kalophrynus baluensis Kiew, 1984

Kalophrynus barioensis Matsui and Nishikawa, 2011

Kalophrynus calciphilus Dehling, 2011

Kalophrynus dringi Fukuyama, Matsui, Eto, Hossman, and Nishikawa, 2021

Kalophrynus eok Das and Haas, 2003

Kalophrynus heterochirus Boulenger, 1900

Kalophrynus intermedius Inger, 1966

Kalophrynus meizon Zug, 2015

Kalophrynus nubicola Dring, 1983

Kalophrynus punctatus Peters, 1871

Kalophrynus puncak Fukuyama, Matsui, Eto, Hossman, and Nishikawa, 2021

Kalophrynus subterrestris Inger, 1966

Kaloula baleata (Müller, 1836)

Kaloula pulchra Gray, 1831

Metaphrynella sundana (Peters, 1867)

Microhyla berdmorei (Blyth, 1856)

Microhyla borneensis Parker, 1928

Microhyla maculifera Inger, 1989 Microhyla malang Matsui, 2011

Microhyla nepenthicola Das and Haas, 2010

Nanohyla perparva (Inger and Frogner, 1979)

Nanohyla petrigena (Inger and Frogner, 1979)

RANIDAE: 30

Abavorana luctuosa (Peters, 1871)

Abavorana decorata (Moquard, 1821)

Chalcorana megalonesa (Inger, Stuart, and Iskandar, 2009)

Chalcorana raniceps (Peters, 1871)

Huia cavitympanum (Boulenger, 1893)

Hylarana erythraea (Schlegel, 1837)

Indosylvirana nicobariensis (Stoliczka, 1870)

Meristogenys amoropalamus (Matsui, 1986)

Meristogenys dyscritus Shimada, Matsui, Yambun, and Sudin, 2011

Meristogenys jerboa (Günther, 1872)

Meristogenys kinabaluensis (Inger, 1966)

Meristogenys macrophthalmus (Matsui, 1986)

Meristogenys maryatiae Matsui, Shimada, and Sudin, 2010

Meristogenys orphnocnemis (Matsui, 1986)

Meristogenys penrissenensis Matsui, Nishikawa, Eto, and Hossman, 2017

Meristogenys phaeomerus (Inger and Gritis, 1983)

Meristogenys poecilus (Inger and Gritis, 1983)

Meristogenys stenocephalus Shimada, Matsui, Yambun, and Sudin, 2011

Meristogenys stigmachilus Shimada, Matsui, Yambun, and Sudin, 2011

Meristogenys whiteheadi (Boulenger, 1887)

Odorrana hosii (Boulenger, 1891)

Pulchrana baramica (Boettger, 1900)

Pulchrana glandulosa (Boulenger, 1882)

Pulchrana laterimaculata (Barbour and Noble, 1916)

Pulchrana picturata (Boulenger, 1920)

Pulchrana signata (Günther, 1872)

Staurois guttatus (Günther, 1858)

Staurois latopalmatus (Boulenger, 1887)

Staurois parvus Inger and Haile, 1959

Staurois tuberilinguis Boulenger, 1918

RHACOPHORIDAE: 48

Feihyla inexpectata (Matsui, Shimada, and Sudin, 2014)

Feihyla kajau (Dring, 1983)

Kurixalus absconditus Mediyansyah, Hamidy, Munir, and Matsui, 2019

Kurixalus chaseni (Smith, 1924)

Leptomantis angulirostris (Ahl, 1927)

Leptomantis belalongensis (Dehling and Grafe, 2008)

Leptomantis cyanopunctatus (Manthey and Steiof, 1998)

Leptomantis fasciatus (Boulenger, 1895)

Leptomantis gadingensis (Das and Haas, 2005)

Leptomantis gauni (Inger, 1966)

Leptomantis harrissoni (Inger and Haile, 1959)

Leptomantis malkmusi (Dehling, 2015)

Leptomantis penanorum (Dehling, 2008)

Leptomantis rufipes (Inger, 1966)

Nyctixalus pictus (Peters, 1871)

Philautus acutus Dring, 1987

Philautus amoenus Smith, 1931

Philautus aurantium Inger, 1989

Philautus bunitus Inger, Stuebing, and Tan, 1995

Philautus davidlabangi Matsui, 2009

Philautus disgregus Inger, 1989

Philautus erythrophthalmus Stuebing and Wong, 2000

Philautus gunungensis Malkmus and Riede, 1996

Philautus hosii (Boulenger, 1895)

Philautus ingeri Dring, 1987

Philautus juliandringi Dehling, 2010

Philautus kakipanjang Dehling and Dehling, 2013

Philautus kerangae Dring, 1987

Philautus larutensis (Boulenger, 1900)

Philautus macroscelis (Boulenger, 1896)

Philautus mjobergi Smith, 1925

Philautus nepenthophilus Etter, Haas, Lee, Pui, Das. Hertwig 2020

Philautus nephophilus Dehling, Matsui, and Yambun Imbun, 2016

Philautus refugii Inger and Stuebing, 1996

Philautus saueri Malkmus and Riede, 1996

Philautus tectus Dring, 1987

Philautus umbra Dring, 1987

Polypedates colletti (Boulenger, 1890)

Polypedates leucomystax (Gravenhorst, 1829)

Polypedates macrotis (Boulenger, 1891)

Polypedates otilophus (Boulenger, 1893)

Rhacophorus baluensis Inger, 1954

Rhacophorus borneensis Matsui, Shimada, and Sudin, 2013

Rhacophorus nigropalmatus Boulenger, 1895

Rhacophorus pardalis Günther, 1858

Theloderma horridum (Boulenger, 1903)

Theloderma licin McLeod and Ahmad, 2007

Zhangixalus dulitensis (Boulenger, 1892)

LITERATURE

Frost, D.R. (2021) Amphibian Species of the World: an Online Reference. Version 6.0. At https://amphibiansoftheworld.amnh.org/index.php.

McLeod, D.S. (2010) Of Least Concern? Systematics of a cryptic species complex: Limnonectes kuhlii (Amphibia: Anura: Dicroglossidae). Molecular Phylogenetics and Evolution 56: 991–1000.

Flury, J.M., Haas, A., Brown, R.M., Das, I., Pui, Y.M., Boon-Hee, K., Scheidt, U., Iskandar, D.T., Jankowski, A., Hertwig, S.T. (2021) Unexpectedly high levels of lineage diversity in Sundaland puddle frogs (Dicroglossidae: Occidozyga Kuhl and van Hasselt, 1822). Molecular Phylogenetics and Evolution 163: 107210.

TAXONOMY

taxonomic reference: http://research.amnh.org/vz/herpetology/amphibia/index.php

Taxonomy is the science of describing and naming species and classifying them within the comprehensive scientific system of all living creatures on earth. Because of the ongoing discovery of new organisms, especially in the tropical realm, and the availability of new methods to study them, taxonomy is a highly dynamic field of research. From our point of view, a well justified hypothesis on phylogeny is the only acceptable way to order, describe, and name organisms. New insights on the evolution and phylogenetic relationships (relatedness by common descent) lead to new arrangement in the classification systems.

As science progresses, many scientific names of Bornean frogs have changed in recent times. What used to be Rana malesiana is now Limnonectes malesianus, for example. Such changes are necessary and document new research insights. For the naturalist or student in the field, however, changes in names can be very confusing, especially when using various books and articles to learn about the fauna; some sources may use old names, some more recent names. This is particularly true when researching Bornean taxa. Furthermore, if species have been split up into two or more, it is often difficult to assign previous tadpole descriptions to one of the new species, especially if DNA barcodes are not available. In order to avoid misunderstandings with names, it is a common procedure to cite the authors and year of first description of a species after its name. We provide this information in the individual species accounts. Comprehensive treatment on the taxonomic history of a species, including previous names (=synonyms) can be retrieved from the web site Amphibian Species of the World. We adopt the taxonomy of ASW herein (p. 18).

A crucial question in taxonomy is the understanding of the term ‘species’. There is no universally accepted definition of a species, rather, there is a number of species concepts. Moreover, the criteria used for recognition and delimiting of species of a certain group of organisms are still hotly debated. Many understand species as independently evolving lineages or potentially reproducing meta-populations. Genetic, behavioral, ecological or morphological characters can be indicators of evolutionary independence or reproductive isolation from other such groups. Cryptic species can confound true diversity even more. In this book, we will deal with species pragmatically and consider all species that have been published according to the international rules of taxonomy.

WHO SHOULD USE THIS BOOK?

Be fascinated by the tadpoles and frogs of Borneo!

Our target audience include people with a genuine interest in going to the field and experience frogs in their natural environment. Therefore, a comprehensive expert textbook is not our goal. This may disappoint the expectations of some professionals and specialists. This book is meant to be an introductory guide to Bornean tadpoles for a broad audience: researchers, naturalists, biology students, amateur herpetologists, protected area staff, forestry staff, and travelers. Structure, appeal, look, style and usability are just as important to us as the scientific facts. Form must follow function. Visual representations

(image knowledge) in some cases can transmit information better than text and may even render text superfluous; old traditions of scientific field guide books and textbooks need to be questioned, sometimes broken. The behavior of the readership also changes in times of social media and tablet PCs. Brevity and precision of information as well as fast and non-linear navigation through information seems key and defines usability. Reduction of jargon and text as well as exploiting the power of illustrations as information transmitters, however, is a challenge. We tried to apply image knowledge whenever feasible.

HOW TO USE THIS BOOK?

Each species of frog has a specific reproductive biology and chooses specific sites for egg deposition and larval development (see Tadpole Microhabitats p. 46). We grouped species in three sections that correspond to three major microhabitat classes of water bodies at which tadpoles or developmental stages (in direct-developing species) can be found: stagnant water bodies, flowing water, and terrestrial sites. We consider these categories most relevant for the field naturalist, who will most likely find herself or himself at a site that falls in one of these classes and wants to know, which kinds of tadpoles to expect. Sorting species according to microhabitat classes will facilitate getting familiar with specific faunas.

Terrestrial sites are used by species with direct development (lack of a free-swimming larvae; some Philautus). There are some species, however, which deposit eggs on land but still have free-swimming larvae later on; Guardian Frogs (Limnonectes palavanensis and L. finchi) are an example. In our scheme, the latter belong to the water body categories (stagnant or flowing) and not to the terrestrial category.

Phytotelma breeders lay their eggs into water bodies that are usually provided by plant cavities such as Nepenthes pitchers, bamboo internodes, tree holes or water in fallen log cavities. These situations are technically stagnant water bodies and phytotelma breeders shall be categorized as such in that section of the book.

For most species, these classes defined by the body of water are non-overlapping and clearly separate. Stagnant versus flowing water categories work reliably in tadpoles for the vast majority of species. A few exceptions exist in which case tadpoles of a particular species can be found in more than one of the four microhabitat classes. In adult frogs, things may be a bit more fuzzy, because some frogs can be encountered at a stream, yet lay their eggs into a water body that qualifies as stagnant (for example, an isolated side-pool of that stream). This must be considered in field situations, when using the book. Surprisingly few species can actually develop as tadpoles in either (slightly) flowing or (fully) stagnant water bodies, among them are mostly riparian species. If a species’ tadpole can be found in more than one of the three microhabitat categories, appropriate comments will be made on the respective species’ pages. Within the major categories, we present the species alphabetically, first by family name, then by scientific genus and species names.

The tadpoles of a given species are presented on a double page. Essential information (size, shape, color) is given immediately by photographs and graphic drawings, so that this information is available even before reading more details. We developed a reduced style of abstraction for mouthparts and body contours. In the field, size and body shape have proven very helpful as first clues for identification; both are essential to quickly recognize a tadpole, often to the genus level. More details in the text and from color photographs will allow, in many cases, for determination to the species level. The text repeats and deepens the information content of the photographs and drawings. Text is broken up into small blocks that cover specific topics. It makes non-linear reading and finding details more easy. Pictograms help to find the pertinent text block. Photographs vary in quality because they where taken over a long time period, when digital photography (and our skills) improved substantially.

In a common situation a naturalist will be in the field and will try to determine a tadpole right at the site where the tadpole is encountered. It is the priority to supply information that serves immediate identification to the best level; often genus level, sometimes species level. Similar species that could likely be confused with the given species under study will be mentioned and distinguishing features will be given if current knowledge allows that.

A complete literature survey is not the goal of this book. We suggest readings in appropriate places to guide the reader to pertinent or potentially interesting literature. Following the literature cited in those works will allow deeper research of the topic.

LITERATURE

This icon introduces publications for further reading that could be relevant to the respective section of the book or species in question..

3 AMPHIBIAN STUDIES ON BORNEO

A BRIEF HISTORY OF STUDIES

Map of Borneo and adjacent regions by Jodocus Hondius in Gerard Mercator’s atlas (1613).

Borneo was not well known to western navigators before the 19th Century, being far from the trading routes of European naval powers. Perhaps the earliest accurately executed map of the island was prepared by Jodocus Hondius (Latinized version, Joost de Hondt) (1563–1612), a Flemish/Dutch engraver and cartographer. His maps in Gerard Mercator’s (1613) atlas helped establish Amsterdam as the center of cartography in Europe in the 17th century. To the left: Hondius’ hand colored ‘Insulae Indiae Orientalis Praecipuae, In quibus Moluccae celeberrime sunt’.

Portrait of botanist-explorer-turned administrator, Hugh Low (1824-1905).

At the time of publication of the 10th edition of Systema Naturae 1758, by Carolus Linneaus (1707–1778), the celebrated Swedish botanist, no frogs were described from Borneo. The earliest amphibian checklist for Borneo was published by the botanist-explorer-turned administrator, Hugh Low (1824–1905). Low was sent out to the East by his father to acquire horticultural specimens for the family business in London, and is perhaps best known for being the namesake for the highest peak on the island (Gunung Kinabalu’s Low’s Peak, at 4,095 m a.s.l.). His 1848 book, entitled: ‘Sarawak. Its inhabitants and productions.’ These notes taken during a residence in that country with His Excellency Mr. Brooke included a checklist that show two frog species, presumably made around the region of modern-day Kuching. The island was therefore terra incognita for herpetological studies during the visit by Odoardo Beccari (1843–1920) from Italy. Beccari’s collection of amphibians was, of course, incidental to botanical collections, and made in collaboration and financial support by Marquis Giacomo Doria of Genoa (1840–1913), a patron of the Civic Museum of Natural History at Genoa, between 1865–1868. Collections were made from Sarawak, Kalimantan and Brunei, including the vicinity of Kuching, Gunung Pueh, Gunung Matang, Batang Lupar, Kapuas, Labuan, and several frog species (such as Kalophrynus punctatus) were described by the Curator of the Berlin Museum, Wilhelm Peters and by Peters and Giacomo Doria.

Italian botanist, Odoardo Beccari (1843-1920).

The next update of the fauna was provided by Edward Bartlett (ca. 1836–1908), Curator of the Sarawak Museum between 1895–1897. He wrote a three page account of the amphibians of Borneo that were represented in the Sarawak Museum or reported in the literature available to him. It lists 44 species (39 using contemporary taxonomy), and included localities, and if available, sizes, elevational distribution, color variations, vernacular names, abundance and habits.

A view of Gunung Kinabalu from John Whitehead’s (1893) ‘The Exploration of Mount Kina Balu’.

By the middle of the 19th century, Enlightenment was sweeping Europe, with scientific discourse unshackled by superstition and especially, the rise of Darwinism and the need for empirical evidence, especially of human origins. At this time, Alfred Hart Everett (1849–1898), arrived in Borneo (in 1869), at the recommendation of the famous British scientist, Sir Charles Lyell, in order to examine cave deposits. For the first few years, he made natural history collecting for museums and collectors back home in England his primary occupation. Everett collected from Gunung Pueh and Gunung Penrissen, his material was worked on by Albert Günther and his successor, George Boulenger at the British Museum (Natural History), London. Outstanding amongst these (using contemporary day names) are Alcalus baluensis and Rentapia everetti. Another resident of Sarawak at the time was colonial administrator, Charles Hose (1863–1929), an amateur naturalist, geographer and anthropologist. Employed as Resident of Baram District by the Sarawak Civil Service, Hose authored a number of popular books that were based on his experiences in Borneo, and sole or donated collections of biological specimens to museums in Europe, North America and Asia. New frog species collected by Everett and Hose were described by Boulenger, and those that bear his name include Odorrana hosii, Rentapia hosii and Philautus hosii. Hose was also the collector of the holotype of arguably the most famous Bornean frog, the Wallace’s Flying Frog, Rhacophorus nigropalmatus, from the ‘Akar River’. Wallace’s own specimen was apparently not preserved.

Plate showing Polypedates otilophus collected by Alfred Everett and Charles Hose in Boulenger (reproduced from Proc. Zool. Soc. London 1893).

The English explorer, John Whitehead (1860–1899), visited the Gunung Kinabalu area in 1887–1888 to make zoological collections, reaching the summit in February 1888. His herpetological material from Kinabalu was reported by Boulenger (1887) at the British Museum London, and Mocquard (1890) at the Muséum National d‘Histoire Naturelle, Paris. Whitehead’s lasting contribution is the magnificent work, ‘The Exploration of Mount Kina Balu’ (1893), whose plates are often reprinted. The frog, Meristogenys whiteheadi, from the upper reaches of Kinabalu, honors Whitehead.

Robert Walter Campbell Shelford (1872–1912) was Curator of the Sarawak Museum between 1898–1905. His amphibian collections were also described by Boulenger. The frog species name, Rhacophorus shelfordi is named for him. Shelford was succeeded by the Swedish naturalist, Eric Georg Mjöberg (1882–1938), between 1922–1924. Mjöberg’s herpetological collections, particularly from Gunung Murud, Gunung Gading, Gunung Penrissen and Gunung Pueh, were written up by the English physician-herpetologist, Malcolm Smith. The collections made from Murud were particularly remarkable. The mountain had been rarely visited. The trip resulted in the discovery of a large number of new species of amphibians and reptiles, and Mjöberg wrote a chapter on his observations on Wallace’s Flying Frog. Mjöberg is the namesake for both Leptobrachella mjobergi and Philautus mjobergi.

Robert Walter Campbell Shelford (1872–1912).

The American field naturalist and philanthropist, William Louis Abbott (1860–1936), described as “…one of the greatest field naturalists that America has produced…”, studied medicine in London, but decided to engage in scientific explorations. Abbott organized a number of expeditions, including to America, Africa, Seychelles, Madagascar, central Asia, the Himalayas, and the Dutch coastal portion of Borneo, from where he collected a frog that bears his name, Leptobrachium abbotti.

In the past half century, several teams contributed to amphibian collections from Borneo. Most notably Robert F. Inger (Field Museum of Natural History) and his collaborators. His and his team’s work led to several book publications on the frogs of Borneo and a key publication on Bornean tadpoles. Major collecting efforts were initiated by Sabah Parks (Maklarin Lakim, Tan Fui Lian and Paul Yambun), the Universities of Kyoto (Masafumi Matsui and colleagues), Bandung Institute of Technology (Djoko Iskandar and colleagues), and finally, members of the Society for the Study of Southeast Asian Herpetology, Germany (particularly, Rudolph Malkmus and Ulrich Manthey).

Wallace’s Flying Frog, Rhacophorus nigropalmatus, an iconic frog species of Borneo.

BIOGEOGRAPHY

With 200 recorded species (p. 18), Borneo boasts an astonishingly high number of frogs. Over 100 species have been recorded in the Gunung Mulu National Park (544 km2) alone. This extraordinarily high species richness makes Borneo one of the global hot spots for amphibian diversity. The island is part of the biogeographical region of Sundaland, a recognized center of biodiversity for numerous groups of animals and plants. Sundaland also includes the Malay Peninsula, Sumatra, Java, Bali, and several smaller islands. Together they constitutes the emerged land masses of the Sunda shelf, which is a tectonically relatively stable extension of the Asian continent. The Sunda shelf consists of an assembly of old Gondwana blocks and subsequently amalgamated parts of the Asian continent. The contemporary shorelines of the Sunda islands, that are separated today by shallow seas less than 200 m deep, are geologically young: Borneo has been separated from the continent for just under five million years. Thus, the evolution of the amphibian diversity of Borneo can only be explained taking into account the biogeography and palaeogeography of the surrounding islands and archipelagos.

Plate tectonics and biogeography