BIODIVERSITY OF PANTEPUI

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BIODIVERSITYOF PANTEPUIThe Pristine “Lost World” of theNeotropical Guiana Highlands

Edited by

VALENTI RULLInstitute of Earth Sciences Jaume Almera (ICTJA-CSIC), Barcelona, Spain

TERESAVEGAS-VILARRUBIADepartment of Evolutionary Biology, Ecology and Environmental Sciences, University of Barcelona, Barcelona, Spain

OTTO HUBERBotanical Institute of Venezuela Foundation, Caracas, Venezuela

CELSA SENARISCenter of Ecology, Venezuelan Institute for Scientific Research (IVIC), Caracas, Venezuela

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Contents

List of contributors ixForeword xiAcknowledgments xiiiIntroduction xv

Part IGENERAL ASPECTS

1. Definition and characterizationof the Pantepui biogeographical

provinceVALENTI RULL, OTTO HUBER, TERESAVEGAS-

VILARRUBIA AND CELSA SENARIS

Introduction 3History of the Pantepui biogeographical

concept 21Phytogeographical Pantepui 24Pantepui floristic subdivisions 26Zoogeographical insights 29Conclusions and final remarks 30Acknowledgments 31References 31

2. Climatic and ecological history ofPantepui and surrounding areas

VALENTI RULL, ENCARNI MONTOYA,

SANDRA NOGUE, ELISABET SAFONT

AND TERESAVEGAS-VILARRUBIA

Introduction 33Regional paleoclimatic trends 37Paleoecology of Pantepui and adjacent areas 39Final remarks 50Acknowledgments 51References 51

3. Pantepui as a dynamicbiogeographical concept

VALENTI RULL AND TERESAVEGAS-VILARRUBIA

Introduction 55Hypotheses and approaches 56The Pantepui components 57The Pantepui oscillator 62The future 64Conclusions and further research 65Acknowledgments 66References 66

4. Origin and evolution of the Pantepuibiota

VALENTI RULL

Introduction 69Evolutionary inferences from biogeography 71Paleoecological contributions and geological

insights 76Molecular phylogenetics and phylogeography 81General conclusions 86Further research 88Acknowledgments 89References 89

Part IITHE PHOTOSYNTHETIC

WORLD

5. AlgaeJAN KAsTOVSKY, KAROLINA FUcIKOVA, JANAVESELA,

CHARLES BREWER CARIAS

AND TERESAVEGAS-VILARRUBIA

Introduction 95Phycological studies on Pantepui 98

v

Tepuis and algal endemics 115Acknowledgements 117References 118

6. Vascular plants and bryophytesRICARDA RIINA, PAUL E. BERRY, OTTO HUBER

AND FABIAN A. MICHELANGELI

Introduction 121Main patterns of diversity in vascular plants 124Pantepui bryophytes 133Current phylogenetic knowledge and biogeographic

implications 134Future perspectives on phylogeography 141Acknowledgments 141References 141

7. Plant communitiesOTTO HUBER AND VALENTI RULL

Introduction 149The table-mountain landscape of the Guiana

Shield 150Vegetation types 152Endemic vegetation types in Pantepui 160Phytosociological studies 162Final remarks 162Acknowledgments 163References 163

Part IIIANIMAL DIVERSITY

8. Aquatic insectsTOMAs DERKA, CARMEN ZAMORA-MUNOZ

AND JOSE MANUEL TIERNO DE FIGUEROA

Introduction 167Mayflies (Ephemeroptera) 171Stoneflies (Plecoptera) 176Caddisflies (Trichoptera) 177Orthopterans (Orthoptera) 181Dragonflies and damselflies (Odonata) 181Dobsonflies (Megaloptera) 182Beetles (Coleoptera) 182True bugs (Heteroptera) 183True flies (Diptera) 183Origin and evolution of Pantepui aquatic

insects 184

Recommendations for conservation of the aquaticinsects of Pantepui and ideas for futureresearch 186

Acknowledgments 187References 187

9. ButterfliesANGEL L. VILORIA AND MAURO COSTA

Introduction 193The biogeographic Pantepui 194Exploration, discovery, and taxonomic studies of

butterflies in the tepuis 197Endemic butterflies of Pantepui 201Biogeographic significance and conclusions 214Acknowledgments 217References 217

10. ScorpionsJOSE A. OCHOA

AND FERNANDO J.M. ROJAS-RUNJAIC

Introduction 223First explorations 226Gonzalez-Sponga’s contributions 228Expeditions in the Guiana region 231Recent years 232Pattern of diversity and endemism of

scorpions 232Endemism 234Distribution patterns 237Acknowledgments 238References 238Appendix 242

11. Land snailsABRAHAM S.H. BREURE

Introduction 247Material and methods 249Systematics 249Species of Pantepui sensu stricto

($1500 m) 250Species of the uplands and lowlands

(below 1500 m) 256Ecology 257Biogeography 259Further avenues for research 260References 261

vi CONTENTS

12. Amphibians and reptilesCELSA SENARIS AND FERNANDO J.M. ROJAS-RUNJAIC

Introduction 263Defining Pantepui for amphibians and

reptiles 264Amphibians and reptiles of the Guiana

Highlands 265Insights on the origin and evolution of the Pantepui

herpetofauna 280Final remarks 283Acknowledgments 284References 284Appendix 291

13. BirdsJORGE L. PEREZ-EMAN, MIGUEL LENTINO

AND ELISA BONACCORSO

Introduction 299A definition of Pantepui 300Patterns of diversity and

endemism 302Historical explanations for diversity and endemism

in Pantepui 310Future prospects and

conservation 317Acknowledgments 318References 318Appendix I 323Appendix II 329Appendix III 331

14. MammalsDANIEL LEWAND BURTON K. LIM

Introduction 333Mammalian richness of the

Guianas 335Elevational occurrence 339Pantepui mammals 340Biogeography 351References 353Appendix 357

15. Vertebrate parasitesRICARDO GUERRERO

Introduction 373Historical expeditions 373Recent collections 374Preliminary conclusions 380Acknowledgements 384References 384

Part IVBIODIVERSITYCONSERVATION

16. Conservation of Pantepui: betweencomplex emergency and climate change

MARIAPIA BEVILACQUA, CELSA SENARIS

AND OTTO HUBER

Introduction 389Antecedents in the conservation of

Pantepui 390Failure of natural resource management

institutions 393Complex crisis 395Climate change 397Final reflection 398References 399

17. Pantepui and global warmingVALENTI RULL, SANDRA NOGUE, ELISABET SAFONT

AND TERESAVEGAS-VILARRUBIA

Introduction 403Current extinction estimates 404Conservation insights 406Weaknesses and future research 411Bureaucratic constraints 413Conclusions and recommendations 414Acknowledgments 414References 415

Taxonomic Index 419Subject Index 445

viiCONTENTS

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List of contributors

Paul E. Berry University of MichiganHerbarium, Department of Ecology andEvolutionary Biology, Ann Arbor, MI,United States

Mariapia Bevilacqua Venezuelan Associationfor the Conservation of Natural Areas -ACOANA, Caracas, Venezuela

Elisa Bonaccorso Institute BIOSFERA andLaboratory of Evolutionary Biology, UniversitySan Francisco de Quito, Quito, Ecuador

Abraham S.H. Breure Naturalis BiodiversityCenter, RA Leiden, The Netherlands; RoyalBelgian Institute of Natural Sciences, Brussels,Belgium

Charles Brewer Carıas Venezuelan Society forNatural Sciences, Caracas, Venezuela

Mauro Costa Museum of the Institute ofAgricultural Zoology (MIZA), Faculty ofAgronomy, Central University of Venezuela,Maracay, Venezuela

Tomas Derka Department of Ecology, Facultyof Natural Sciences, Comenius University,Bratislava, Slovakia

Karolina Fucıkova Assumption College,Worcester, MA, United States

Ricardo Guerrero Institute of TropicalZoology, Faculty of Sciences, CentralUniversity of Venezuela, Caracas, Venezuela

Otto Huber Trauttmansdorff BotanicalGardens, Merano, Italy; Botanical Instituteof Venezuela Foundation, Caracas, Venezuela

Burton K. Lim Department of Natural History,Royal Ontario Museum (ROM), Toronto, ON,Canada

Jan Kastovsky University of South Bohemia,Ceske Budejovice, Czech Republic

Miguel Lentino Phelps OrnithologicalCollection, Caracas, Venezuela

Daniel Lew Biodiversity Unit, VenezuelanInstitute of Scientific Research (IVIC),Caracas, Venezuela

Fabian A. Michelangeli The New YorkBotanical Garden, Bronx, NY, United States

Encarni Montoya Institute of Earth SciencesJaume Almera (ICTJA-CSIC), Barcelona, Spain

Sandra Nogue Department of Geography andEnvironment, University of Southampton,Southampton, United Kingdom

Jose A. Ochoa Faculty of Sciences, Departmentof Biology, National University of SanAntonio Abad del Cusco, Cusco, Peru

Jorge L. Perez-Eman Institute of TropicalZoology and Ecology, Central University ofVenezuela, Caracas, Venezuela; PhelpsOrnithological Collection, Caracas, Venezuela

Ricarda Riina Royal Botanical Garden,RJB-CSIC, Madrid, Spain

Fernando J.M. Rojas-Runjaic La Salle NaturalHistory Museum, La Salle Natural SciencesFoundation, Caracas, Venezuela; Laboratoryof Vertebrate Systematics, ZoologyPostgraduate Program, School of Sciences,Pontifical Catholic University of Rio Grandedo Sul (PUCRS), Porto Alegre, Brazil

Valentı Rull Institute of Earth Sciences JaumeAlmera (ICTJA-CSIC), Barcelona, Spain

Elisabet Safont Department of EvolutionaryBiology, Ecology and Environmental Sciences,Faculty of Biology, University of Barcelona,Barcelona, Spain

Celsa Senaris Laboratory of Population Genetics,Center of Ecology, Venezuelan Institute forScientific Research (IVIC), Caracas, Venezuela

Jose Manuel Tierno de Figueroa Departmentof Zoology, Faculty of Sciences, University ofGranada, Granada, Spain

ix

Teresa Vegas-Vilarrubia Department ofEvolutionary Biology, Ecology andEnvironmental Sciences, Faculty of Biology,University of Barcelona, Barcelona, Spain

Jana Vesela University of South Bohemia,Ceske Budejovice, Czech Republic

Angel L. Viloria Center of Ecology,Venezuelan Institute for Scientific Research(IVIC), Altos de Pipe, Venezuela

Carmen Zamora-Munoz Department ofZoology, Faculty of Sciences, University ofGranada, Granada, Spain

x LIST OF CONTRIBUTORS

Foreword

Eastern tepui chain. Photo: V. Rull.

Having visited tepuis in Venezuela, Guyana, and Brazil, I am fully aware of the biologi-cal importance of the Pantepui region and of the relevance of this book. Each mountainthere is an isolated island where plants and animals are also relatively isolated from theircongeners and so may evolve into separate species. The region is famous for the endemic-ity of many of the species of the organisms that occur there. It has been the joy and privi-lege of many naturalists to discover new species as they explore the tops of thesemountains. On two expeditions to the isolated Brazilian tepui of Araca in 1984 and 1985we discovered 25 new species and one new genus of plants on that mountain, and this hasbeen the experience of many other explorers of Pantepui.

The early biological work that stimulated interest in Pantepui was mainly from birdsand plants. Here we see that now a lot of other disciplines have been involved in biologi-cal research in the region. I am glad that this volume brings together data from a largenumber of different fields and about such a wide range of organisms from algae to mam-mals and higher plants. The published information on the various organisms that inhabitPantepui is very scattered and often hard to access. It is so good summarize all this infor-mation together in a single volume. This book will be a reference volume that unites a lotof scattered information ranging from paleoecology to the most modern phylogenetic andevolutionary concepts. There is a lot of information here, but it is still a fact that the major-ity of the tepuis remain virtually unexplored. I hope that this book will challenge futureresearchers to find out many more of the secrets of this fascinating region. It certainlyserves to show that Pantepui is a dynamic biogeographical concept.

Thankfully the Pantepui region is still relatively pristine, and this book shows its biolog-ical and evolutionary importance. It will certainly help to support the efforts to preservethe region and keep it pristine for future generations, and so I am most happy to see afinal section on the important topic of biodiversity conservation and climate change.

Sir Ghillean T. Prance

xi

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Acknowledgments

Tirepon-tepui (Chimanta massif). Photo: V. Rull.

The editors are very grateful to all the authors who contributed to this book for theirdedication and hard work leading to high-quality chapters. We also wish to thank thereviewers for their time and expertise. They are (in alphabetic order) Alexandre Antonelli,Gerardo Aymard, Paul Berry, Elisa Bonaccorso, Israel Canizares, Jurgen Demarmels, CarlDick, Mark Engstrom, Angel Fernandez, Jose Marıa Fernandez-Palacios, Suzette Flantua,Sherilyn Fritz, Stefan Gorzula, Marinus Hoogmoed, Bruce Host, Carlos Lasso, Daniel Lew,Burton Lim, Celio Magalhaes, Fabian Michelangeli, Shinichi Nakahara, Jorge Perez-Eman,Lorenzo Prendini, Gustavo Romero, Donald Taphorn, Rodrigo Salvador, Luiz RicardoLopes de Simone, Nathan Stansell, Fred Stauffer, and Zicheng Yu. We are also very grate-ful to people who provided photographs for free, especially Javier Mesa, and also StefanGorzula. We greatly acknowledge the invitation of Elsevier/Academic Press for writing/editing the book and the managing editors Kiruthika Govindaraju, Ruby Smith and AnnaValutkevicth for their constant support in editorial and production tasks.

xiii

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Introduction

Valentı Rull1, Teresa Vegas-Vilarrubia2, Otto Huber3

and Celsa Senaris41Institute of Earth Sciences Jaume Almera (ICTJA-CSIC), Barcelona, Spain 2Department of

Evolutionary Biology, Ecology and Environmental Sciences, University of Barcelona, Barcelona,

Spain 3Botanical Institute of Venezuela Foundation, Caracas, Venezuela 4Center of Ecology,

Venezuelan Institute for Scientific Research (IVIC), Caracas, Venezuela

To our knowledge, this is the first attempt to summarize the existing knowledge on thePantepui biota, including most plant and animal groups studied to date. The availableinformation on the biodiversity of Pantepui is dispersed in hundreds of books and articles,including gray literature, and a synthesis of the state of the art in this matter seemed perti-nent. Knowing the extant biodiversity patterns and the potential environmental driversand evolutionary mechanisms involved in their generation and maintenance is essential,not only for the progress of fundamental science but also for biodiversity conservation(Rull, 2019). Unfortunately, such knowledge is still very limited for Pantepui, and only apreliminary assessment can be offered due to incomplete exploration. However, it ishoped that this book will provide a basis to advance the ecological and evolutionary studyof the unique Pantepui biota and will help set the basis for its conservation.

Aims and scope

The main aims of this book are (1) to summarize the present state of knowledge on theextant biodiversity of the Pantepui biogeographical province of the Guiana region, (2) toprovide insights on relevant biogeographical and endemism patterns, (3) to initiate discus-sions on the potential origin and evolution of the unique Pantepui biota as a whole, and(4) to evaluate the main current and potential threats to Pantepui biodiversity and toenvisage some potential conservation actions. The peculiar physiographic features of thesespectacular, remote, and nearly pristine Guiana Highlands and their geological originshave already been highlighted in scientific and popular literature, movies, and websites.Here the emphasis is on the biotic component.

xv

The terms “Pantepui” and “Guiana Highlands” (or Guayana Highlands, to refer specifi-cally to those in the Venezuelan territory) are often used as synonyms in the literature.Although the first is a biogeographical term and the second a physiographical one, bothallude to the summits of the characteristic table mountains (tepuis) above B1500 elevation,which is the lower boundary defined for the highlands of the Guiana region (Huber,1995). The first chapter of this book is more explicit in this respect. For a more extendedaccount on geological, geographical, physiographical, and climatic aspects, we recommendthe first volume of the Flora of the Venezuelan Guayana, edited by Berry et al. (1995). Thelong-term geomorphological evolution of the Pantepui area leading to its present topo-graphical configuration was summarized by Briceno and Schubert (1990) and Huber andGarcıa (2011). The history of scientific exploration of Pantepui is a fascinating subject(Huber, 1995; McDiarmid and Donnelly, 2005) that requires a monography by itself and isbeyond the scope of this book.

The lack of autoecological and synecological studies developed on Pantepuiorganisms and ecosystems prevents us from providing more detailed ecological infor-mation on the unique biological communities of this biogeographical province.Therefore for the time being, a book on Pantepui biota should necessarily be focusedon taxonomic and biogeographic aspects and the eventual evolutionary insightsderived from them. It is hoped that this will change in the near future, and a booklike this could provide the basis for further studies focused on specific ecological andevolutionary topics. The book has been organized into four main parts, namely (1)general aspects, (2) the photosynthetic world, (3) animal biodiversity, and (4) biodiver-sity conservation.

General aspects

The first part of the book presents the general aspects of Pantepui biodiversity and iscomposed of four chapters. The first chapter (Rull et al.) defines explicitly the Pantepuibiogeographical province, mainly on the basis of vascular plant biogeography, andincludes a list of all the tepuis and other highlands falling within the definition ofPantepui, as well as a location map for all of them. To avoid repetitions and eventual geo-graphical inconsistencies, this map is the reference for all the remaining chapters. The sec-ond chapter (Rull et al.) is a summary of paleoecological works developed to date onPantepui in an attempt to understand the ecological state and composition of modernPantepui ecosystems in light of the environmental shifts experienced since the Last GlacialMaximum, which has been recognized worldwide as the resetting point for modern livingcommunities. Chapter 3 (Rull & Vegas-Vilarrubia) attempts to show that Pantepui is not astatic biogeographical concept as it has changed through time, especially during theQuaternary, due to the significant ecological changes caused by the glacial�interglacialrecurrence. The final chapter of this section (Rull) is a an attempt to unravel how thePantepui biota has originated and evolved since the Mesozoic until its present conditions,as well as the geological and environmental drivers that have influenced this process.

xvi INTRODUCTION

The photosynthetic world

The second part is focused on algae and plant diversity and biogeography and consistsof three chapters. The first chapter (Kastovsky et al.) is about Cyanobacteria andEukaryotic algae inhabiting several types of extreme habitats with relatively uniform, yetvery specific, algal floras across all investigated summits. The role of these organisms asfounders and promoters of more complex pioneer communities on rocky substrates ishighlighted. The second chapter (Riina et al.) updates the main patterns of diversity andendemism of the Pantepui flora, including mosses and vascular plants, and discusses theexisting knowledge about the phylogenetics of some plant lineages to provide insights inthe evolution and historical biogeography of the unique Pantepui flora. The third chapter(Huber and Rull) provides an overview of the vegetation cover of Pantepui in terms ofplant communities. Forty vegetation types are described and classified into four forma-tions: forests, shrublands, herbaceous, and pioneer communities. The occurrence of sometypes of vegetation endemic to Pantepui is also highlighted.

Animal diversity

The third part of the book deals with animal biodiversity and includes the major taxo-nomic groups present in Pantepui that have been studied to date. Other groups mayoccur, but they are rare or studies are inexistent or still embryonic. The case of fishes isremarkable, as no highland species have been found and lowland/upland species rarelycross the lower elevational boundary of Pantepui, with very few exceptions (Lasso et al.,1989).

This section has been subdivided into eight chapters organized taxonomically. The firstchapter (Derka et al.) summarizes the available information on the aquatic insect fauna,mainly mayflies, stoneflies, and caddisflies, which are confined to the nutrient-poor watersof the Guiana Shield. The second chapter (Viloria and Costa) is concerned with thePantepui-endemic butterflies relevant for the definition of the Pantepui biogeographicprovince within the Neotropical Amazonian subregion. The next chapter (Ochoa andRojas-Runjaic) summarizes the scorpion fauna of Pantepui and peripheral areas of theGuiana region, which is composed almost exclusively of endemic species, with speciesrichness decreasing with elevation. Noteworthy is the occurrence of four endemic genera.The fourth chapter (Breure) updates knowledge about land snail fauna, mostly from theeastern Pantepui area, which shows a high level of endemism. Some preliminary ecologi-cal and biogeographical insights are provided. It follows a chapter (Senaris and Rojas-Runjaic) on the Pantepui herpetofauna (amphibians and reptiles), a remarkable groupwith many endemisms of very restricted distribution. This chapter updates the richnessand endemism patterns of this group and summarizes the existing molecular phylogeneticstudies, which provide insights on the origin and evolution of the Pantepui herpetofauna.

The next chapter (Perez-Eman et al.) is on birds, one of the better-known groups oforganisms that had provided the basis for the first definition of Pantepui. A review of thenew information on bird distribution furnishes the basis for understanding their current

xviiINTRODUCTION

biogeographical patterns and for inferring the potential processes that have generated theirdiversity and endemism on Pantepui. The chapter on mammals (Lew and Lim) sum-marizes the richness of this group, which in Pantepui is represented mainly by bats androdents. In contrast with other zoological groups, endemism is low, with only one rodentspecies restricted to a tepuian summit (although some opossums and rodents are exclu-sively from tepuian slopes). The final chapter (Guerrero) of the zoological part is a briefpreliminary account of the ectoparasites (mainly insects and acari) and endoparasites(chiefly worms) found on Pantepui vertebrates, especially mammals. The scarce informa-tion available prevents sound inferences on biogegraphy and endemism, but it is believedthat parasites are largely dependent on the geographical patterns of their respective hosts.

Biodiversity conservation

Finally, the fourth part of the book is about the direct and indirect threats to Pantepuibiodiversity and the more suitable conservation actions to avoid or palliate eventualextinction. The first chapter (Bevilacqua et al.) explores why the performance and commit-ments of regional governments towards the practice of conservation in the highlands ofthe Guiana Shield have been insufficient and discusses the complex emergency of climatechange as new threats to Pantepui biodiversity. The final chapter of the book (Rull et al.)reports the GIS-based estimates of potential extinction by habitat loss of the Pantepui vas-cular flora, given the influence of the global warming predicted for the end of this century.Further ecological and genetic studies of the most endangered species needed to refinethese estimates are suggested. This would require national actions and international col-laboration, especially among Guiana Shield countries, including a thorough revision of theprocess for obtaining official field-work permits, which is now the most important handi-cap in terms of scientific study.

References

Berry, P., Holst, B.K., Yaskievych, K., 1995. Flora of the Venezuelan Guayana, Introduction, vol. 1. MissouriBotanical Garden Press, St. Louis.

Briceno, H.O., Schubert, C., 1990. Geomorphology of the Gran Sabana, Guayana Shield, southeastern Venezuela.Geomorphology 3, 125�141.

Huber, O., 1995. Geographical and physical features. In: Berry, P., Holst, B.K., Yaskievych, K. (Eds.), Flora of theVenezuelan Guayana. Introduction, vol. 1. Missouri Botanical Garden Press, St. Louis, pp. 1�61.

Huber, O., Garcıa, P., 2011. The Venezuelan Guayana region and the study areas: geo-ecological characteristics.In: Zinck, J.A., Huber, O. (Eds.), Peatlands of the Western Guayana Highlands, Venezuela, Ecological Studies217. Springer-Verlag, Berlin Heidelberg, pp. 29�89.

Lasso, C., Machado-Allison, C., Perez, R., 1989. Consideraciones zoogeograficas del los peces de la Gran Sabana(Alto Caronı) Venezuela, y sus relaciones con las cuencas vecinas. Mem. Soc. Cien. Nat. 49, 109�129.

McDiarmid, R.W., Donnelly, M.A., 2005. The herpetofauna of the Guayana Highlands: amphibiands and reptilesof the Lost World. In: Donnelly, M.A., Crother, B.I., Guyer, C., Marvalee, H., White, M.E. (Eds.), Ecology andEvolution in the Tropics. University Chicago Press, Chicago, pp. 461�560.

Rull, V., 2019. Neotropical diversification: historical overview and conceptual insightsIn: Rull, V., Carnaval, A.(Eds.), Neotropical Diversification. Springer, Berlin. Peer J Preprints 6: e27294v1. Available from: http://doi.org/10.7287/peerj.preprints.27294v1.

xviii INTRODUCTION