Amphibian diversity in Amazonian flooded forests of Peru Kathleen Anne Upton A thesis submitted for the degree of Doctor of Philosophy from the Durrell Institute of Conservation and Ecology, School of Anthropology and Conservation, University of Kent. December 2015 Word Count: 44,448 Abstract Global biodiversity is currently facing the sixth mass extinction, with extinction rates at least 100 times higher than background levels. The Amazon Basin has the richest amphibian fauna in South America, but there remain significant gaps in our knowledge of the drivers of diversity in this region and how amphibian assemblages are responding to environmental change. Surveys were conducted in the Pacaya-Samiria National Reserve (PSNR) in Amazonian Peru, with a view to (1) comparing assemblage structure on floating meadows and adjacent terrestrial habitats; (2) determining the predictors of diversity in these habitats; and (3) exploring the effects of disturbance and seasonal flooding on diversity measures. Eighty-one species of amphibians have been recorded in these habitats since 1996 representing 11 families and three orders. In 2012-2013 22 anuran species used the floating meadow habitat, of which 10 were floating meadow specialists. These specialists were predominantly hylids which breed on floating meadows all the year round. Floating meadows therefore host an assemblage of species which is different to that found in adjacent terrestrial areas which are subject to seasonal flooding. Floating meadows enhance the amphibian diversity of the region, and rafts of vegetation that break away and disperse frogs downstream may explain the wide distribution of hylids within the Amazon Basin. Fourteen different reproductive modes were represented within the 54 anuran species observed. The number of reproductive modes present was influenced by localised disturbance and seasonal flooding. Diversity increased in the low water period, with hylids breeding in temporary pools. When the forest is inundated most species disperse away from the flood waters. Disturbance, habitat change, emerging diseases and climate change would likely lead to changes in species composition and assemblage structure rather than wholescale extinctions. However, further studies are needed to evaluate long-term consequences of synergistic environmental change. KEY WORDS: Amazonian amphibians; floating meadows; climate change; flooding; reproductive modes i Acknowledgements My PhD began as an idea while undertaking my undergraduate research project in the Amazon; I must thank Peter Bennett who planted this initial thought in my mind! Without this encouragement my PhD would never have taken shape. Of course many others deserve thanks for the constant support and help I have received throughout my research and write up. Firstly my supervisor, Richard Griffiths, who has given support, advice, encouragement and red pen to shape my work and help me grow as a researcher. Richard Bodmer, without whom my fieldwork would not have been possible, for his support and guidance in the field. I am grateful to the organisations that made data collection possible: AmazonEco, the Wildlife Conservation Society (WCS), FundAmazonia and the reserve authority. Also the many students and volunteers from DICE, Operation Wallace and Earthwatch, as well as the many local guides, cooks and biologists who helped with data collection and general jungle life. Financially I am forever grateful to the many alumni of the university who donated to my scholarship and the amazing ladies in the scholarship office who have helped me throughout, and always shown interest in my research and frog photos. Finally special thanks to Hannah & Jess (for all the phone calls), Emma, Elli & Izzy (for their invaluable help), Pip (for the title page drawings), Jamie, Lilly, my wonderful family, parents and especially Sophie for putting up with the third ‘person’ in our relationship for the last four years!! I couldn’t have done it without you all around me. ii Table of Contents Abstract.………………………………………………………………………………………………………………….....i Acknowledgements………………………………………………..…………………………………………………..ii Table of Contents…………………………………………………….………………………………………………..iii List of Figures………………………………………………………………………………………………………….vii List of Tables.…………………………………………………………………………………………………………..ix Chapter 1 - Introduction 1 1.2 Global biodiversity conservation 2 1.3 Global amphibian declines 3 1.4 Amphibian diversity and distribution 6 1.5 South American diversity, distribution and conservation 7 1.6 Thesis overview 10 References 12 Chapter 2 - Study site and general methods 17 2.1 Study site 18 2.2 Floating meadows method 25 2.3 Terrestrial transect method 32 References 34 Chapter 3 - Amphibian species richness in the Pacaya-Samiria National Reserve, Peru 36 3. Abstract 37 3.1 Introduction 38 3.2 Methods 40 3.2.1 Data collection (2003 – 2013) 40 3.2.2 Rarefaction curves 42 3.3 Results 43 3.3.1 Terrestrial vs floating meadow 46 3.3.2 Floating meadow rarefaction 48 3.3.3 Terrestrial rarefaction 51 3.4 Discussion 53 iii 3.5 Conclusions 56 References 57 Chapter 4 - Floating meadows as an amphibian habitat in the Amazon Basin 60 4. Abstract 61 4.1 Introduction 62 4.1.1 Floating meadows 65 4.2 Methods 67 4.2.1 Floating meadow survey 67 4.2.2 Identification 68 4.2.3 Statistical analysis 69 4.3 Results 73 4.3.1 Summary statistics 74 4.3.2 Floating meadow GLMM predictors of abundance 76 4.3.3 Floating meadow GLMM predictors of species richness 79 4.3.4 Water level, macrohabitat and location 80 4.4 Discussion 85 4.4.1 Predictors of anuran abundance 87 4.4.2 Predictors of anuran richness 89 4.4.3 Macrohabitat and site 90 4.4.4 Hylidae distribution 93 4.5 Conclusion 95 References 96 Appendix 4.1 – 4.7 101 Chapter 5 - Comparison of amphibian assemblage structure between floating meadows and terrestrial habitats 108 5. Abstract 109 5.1 Introduction 110 5.2 Methods 112 5.2.1 Floating meadows 112 5.2.2 Terrestrial 112 5.2.3 Survey method differences 113 iv 5.2.4 Bromeliad survey methods 113 5.2.5 Statistical analysis 114 5.2.6 Species diversity 114 5.2.7 Species richness 114 5.2.8 Habitat generalists and specialists 115 5.3 Results 117 5.3.1 Species lists for all sites 117 5.3.2 Individual density 120 5.3.3 Species richness estimates 120 5.3.4 Bromeliad anurans 121 5.3.5 Species diversity 122 5.3.6 Habitat generalist and specialist 123 5.4 Discussion 125 5.5 Conclusion 132 References 133 Chapter 6 - Predictors of anuran reproductive modes in a Peruvian flooded forest 135 6. Abstract 136 6.1 Introduction 137 6.2 Methods 140 6.2.1 Disturbance 140 6.2.2 Reproductive modes 141 6.2.3 Statistical analysis 144 6.3 Results 147 6.3.1 Low water reproductive modes 151 6.3.2 Low water reproductive mode predictors 152 6.3.3 PV2 reproductive modes 153 6.3.4 PV2 reproductive mode predictors 154 6.3.5 Modelling summary 156 6.4 Discussion 157 6.4.1 Reproductive mode predictors 159 6.5 Conclusion 162 v References 163 Chapter 7 - The impacts of seasonal flooding on amphibian diversity in a Peruvian lowland flooded forest 167 7. Abstract 168 7.1 Introduction 169 7.2 Methods 172 7.2.1 Flooding 172 7.2.2 Statistical analysis 173 7.2.3 Species diversity 174 7.2.4 Generalist and specialist 174 7.3 Results 176 7.3.1 Water level impact on diversity and abundance 178 7.3.2 Water level generalist and specialist 180 7.4 Discussion 184 7.4.1 Predictors of amphibian diversity and abundance 187 7.5 Conclusion 189 References 190 Chapter 8 - General Discussion 193 References 201 Appendix 1 – Publications 204 Appendix 2 – Amphibian Phylogenies 205 vi List of figures Figure Description Page Distribution of worldwide amphibian species richness reprinted from the 1.1 6 global amphibian assessment. 2.1 The location of the Pacaya-Samiria National Reserve within Peru. 18 2.2 Pacaya-Samiria Reserve. 19 2.3 The location of PV1 Shiringal at the mouth of the Maranon River 19 The location of PV2 Tacshacocha where the majority of surveys were 2.4 20 undertaken 2.5 Temperature and humidity graph from 7th June 2013 – 5th September 2013. 21 2.6 Temperature and humidity graph from 26th June 2013 – 4th July 2013. 22 Water level of the Maranon River recorded at Nauta from January to 2.7 22 December 2012 and 2013. 2.8 A small patch of floating meadow within a bend of the channel at PV2. 27 2.9 Floating vegetation in the low water in the channel at PV2. 27 2.10 Continuous floating meadow vegetation around the lake edge at PV2. 28 Dense floating meadow vegetation on the south facing edge of the lake. In 2.11 28 places this extended by over 50 m from the tree line into the lake. A floating raft of vegetation which would have broken away from a section 2.12 29 of floating meadow upriver. The main river, channel and lake at PV2. Although not to scale, this 2.13 31 highlights the differences in availability of floating meadows. Estimated species richness for the floating meadow and terrestrial habitats 3.1 46 at both 1000 and 5500 individuals. Extrapolated rarefaction curves for the floating meadow and terrestrial 3.2 47 habitat estimated by number of individuals. 3.3 Estimated species richness for the three water level periods. 48 Extrapolated rarefaction curves for the three water periods estimated by 3.4 49 number of surveys. Extrapolated rarefaction curves for the three water periods estimated by 3.5 49 number of individuals. Extrapolated rarefaction curves for the three macrohabitats, estimated by 3.6 50 number of individuals. Extrapolated rarefaction curves for the three main sites surveyed, estimated 3.7 50 by number of individual.