Whitworth, Andrew William (2016) Conservation value, biodiversity value and methods of assessment in regenerating and human disturbed tropical forest. PhD thesis. http://theses.gla.ac.uk/7426/ Copyright and moral rights for this thesis are retained by the author A copy can be downloaded for personal non-commercial research or study This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the Author The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the Author When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given Glasgow Theses Service http://theses.gla.ac.uk/ [email protected] Conservation Value, Biodiversity Value and Methods of Assessment in Regenerating and Human Disturbed Tropical Forest Andrew William Whitworth MSc Conservation Biology (distinction) – Manchester Metropolitan University BSc Zoology (Hons) – The University of Leeds A thesis submitted in partial fulfilment of the requirements for the degree of doctor of philosophy. The Institute of Biodiversity, Animal Health and Comparative Medicine, The College of Medical, Veterinary & Life Sciences, The University of Glasgow. Supervisors: Dr Ross MacLeod and Prof. Roger Downie June 2016 1 ―Uniformity is not nature’s way; diversity is nature’s way.‖ Vandana Shiva 2 Thesis Abstract Although the value of primary forests for biodiversity conservation is well known, the potential biodiversity and conservation value of regenerating forests remains controversial. Many factors likely contribute to this, including: 1. the variable ages of regenerating forests being studied (often dominated by relatively young regenerating forests); 2. the potential for confounding on-going human disturbance (such as logging and hunting); 3. the relatively low number of multi-taxa studies; 4. the lack of studies that directly compare different historic disturbances within the same location; 5. contrasting patterns from different survey methodologies and the paucity of knowledge on the impacts across different vertical levels of rainforest biodiversity (often due to a lack of suitable methodologies available to assess them). We also know relatively little as to how biodiversity is affected by major current impacts, such as unmarked rainforest roads, which contribute to this degradation of habitat and fragmentation. This thesis explores the potential biodiversity value of regenerating rainforests under the best of scenarios and seeks to understand more about the impact of current human disturbance to biodiversity; data comes from case studies from the Manu and Sumaco Biosphere Reserves in the Western Amazon. Specifically, I compare overall biodiversity and conservation value of a best case regenerating rainforest site with a selection of well-studied primary forest sites and with predicted species lists for the region; including a focus on species of key conservation concern. I then investigate the biodiversity of the same study site in reference to different types of historic anthropogenic disturbance. Following this I investigate the impacts to biodiversity from an unmarked rainforest road. In order to understand more about the differential effects of habitat disturbance on arboreal diversity I directly assess how patterns of butterfly biodiversity vary between three vertical strata. Although assessments within the canopy have been made for birds, invertebrates and bats, very few studies have successfully targeted arboreal mammals. I therefore investigate the potential of camera traps for inventorying arboreal mammal species in comparison with traditional methodologies. Finally, in order to investigate the possibility that different survey methodologies might identify different biodiversity patterns in habitat disturbance assessments, I investigate whether two different but commonly used survey methodologies used to assess 3 amphibians, indicate the same or different responses of amphibian biodiversity to historic habitat change by people. The regenerating rainforest study site contained high levels of species richness; both in terms of alpha diversity found in nearby primary forest areas (87% ±3.5) and in terms of predicted primary forest diversity from the region (83% ±6.7). This included 89% (39 out of 44) of the species of high conservation concern predicted for the Manu region. Faunal species richness in once completely cleared regenerating forest was on average 13% (±9.8) lower than historically selectively logged forest. The presence of the small unmarked road significantly altered levels of faunal biodiversity for three taxa, up to and potentially beyond 350m into the forest interior. Most notably, the impact on biodiversity extended to at least 32% of the whole reserve area. The assessment of butterflies across strata showed that different vertical zones within the same rainforest responded differently in areas with different historic human disturbance. A comparison between forest regenerating after selective logging and forest regenerating after complete clearance, showed that there was a 17% greater reduction in canopy species richness in the historically cleared forest compared with the terrestrial community. Comparing arboreal camera traps with traditional ground-based techniques suggests that camera traps are an effective tool for inventorying secretive arboreal rainforest mammal communities and detect a higher number of cryptic species. Finally, the two survey methodologies used to assess amphibian communities identified contrasting biodiversity patterns in a human modified rainforest; one indicated biodiversity differences between forests with different human disturbance histories, whereas the other suggested no differences between forest disturbance types. Overall, in this thesis I find that the conservation and biodiversity value of regenerating and human disturbed tropical forest can potentially contribute to rainforest biodiversity conservation, particularly in the best of circumstances. I also highlight the importance of utilising appropriate study methodologies that to investigate these three-dimensional habitats, and contribute to the development of methodologies to do so. However, care should be taken when using different survey methodologies, which can provide contrasting biodiversity patterns in response to human disturbance. 4 Contents Thesis Abstract ................................................................................................................................. 2 Thesis Organisation .......................................................................................................................... 7 List of Figures .................................................................................................................................. 9 List of Tables ................................................................................................................................. 13 Acknowledgements ........................................................................................................................ 15 General Introduction ..................................................................................................................... 18 What is biodiversity?..................................................................................................................... 18 Outside of conservation, why does biodiversity matter to people? ............................................ 18 How fast is biodiversity being lost, and why? ............................................................................... 20 Why are tropical forests so important for biodiversity? and how fast are they being lost and degraded? ..................................................................................................................................... 22 What are the greatest threats to tropical forest biodiversity? ..................................................... 23 Regenerating landscapes and their biodiversity and conservation value .................................... 25 Roads a major cause of degradation to tropical forests ............................................................... 27 Understanding the canopy............................................................................................................ 28 The importance of understanding the results of different survey methodologies ...................... 28 Thesis study areas ......................................................................................................................... 29 The importance but lack of multi-taxa research ........................................................................... 30 Survey groups within this study .................................................................................................... 31 Chapter 1 - How much potential biodiversity and conservation value can a regenerating rainforest provide? A site-level, comparative species list approach to infer the value of local reserves for conservation. .................................................................................................. 34 Authors and contributions ............................................................................................................ 34 Abstract ......................................................................................................................................... 35 Introduction .................................................................................................................................. 36 Methods ........................................................................................................................................ 40 Results ........................................................................................................................................... 48 Discussion...................................................................................................................................... 52 5 Chapter 2 - Long lasting impressions: After decades of regeneration, rainforest biodiversity remains differentially affected following varied human disturbances; but has high potential conservation value. ...................................................................................... 59 Authors and contributions ............................................................................................................ 59 Abstract ......................................................................................................................................... 60 Introduction .................................................................................................................................. 61 Methods ........................................................................................................................................ 64 Results ........................................................................................................................................... 76 Discussion...................................................................................................................................... 91 Chapter 3 – The response of faunal biodiversity to an unmarked road in the Western Amazon. ........................................................................................................................................... 96 Authors and contributions ............................................................................................................ 96 Abstract ......................................................................................................................................... 97 Introduction .................................................................................................................................. 98 Methods ...................................................................................................................................... 100 Results ......................................................................................................................................... 104 Discussion.................................................................................................................................... 109 Chapter 4 - Past human disturbance effects upon biodiversity are greatest in the canopy; a case study on rainforest butterflies. ...................................................................... 113 Authors and contributions .......................................................................................................... 113 Abstract ....................................................................................................................................... 114 Introduction ................................................................................................................................ 115 Methods ...................................................................................................................................... 118 Results ......................................................................................................................................... 127 Discussion.................................................................................................................................... 141 6 Chapter 5 - Out on a limb: Arboreal camera traps as an emerging methodology for inventorying elusive rainforest mammals. .............................................................................. 147 Authors and contributions .......................................................................................................... 147 Abstract ....................................................................................................................................... 148 Introduction ................................................................................................................................ 149 Methods ...................................................................................................................................... 151 Results ......................................................................................................................................... 155 Discussion.................................................................................................................................... 161 Chapter 6 - Methods matter: Different biodiversity survey methodologies identify contrasting biodiversity patterns in a human modified rainforest. .................................... 164 Authors and contributions .......................................................................................................... 164 Abstract ....................................................................................................................................... 165 Introduction ................................................................................................................................ 166 Methods ...................................................................................................................................... 168 Results ......................................................................................................................................... 175 Discussion.................................................................................................................................... 182 Thesis Discussion .......................................................................................................................... 187 References – main data chapters .............................................................................................. 195 Appendix manuscript 1 - Herpetofaunal responses to anthropogenic habitat change within a small forest reserve in Eastern Ecuador. ................................................................. 289 Appendix manuscript 2 – A first test of the thread bobbin tracking technique as a method for studying the ecology of herpetofauna in a tropical rainforest. ..................... 314 Appendix manuscript 3 - Bamboo traps as refugia for Pristimantis olivaceus (Anura: Craugastoridae) and as breeding site for Osteocephalus castaneicola (Anura: Hylidae) ........................................................................................................................................................ 338 Appendix manuscript 4 - Osteocephalus mimeticus (Melin, 1941) (Amphibia: Anura: Hylidae): New locality, range extension and notes on distribution. .................................. 346 Appendix manuscript 5 - Doryfera johannae (Bourcier, 1847) (Aves: Apodiformes: Trochilidae): New locality, range extension and notes on distribution. ............................ 354 7 Thesis Organisation This thesis is presented in the form of six main chapters, each of which has been prepared for publication in the style of a stand-alone manuscript (including introduction and discussion) suitable for submission to scientific journals in the fields of ecology and conservation. Presentation as manuscripts does mean that some information, particularly in methods, is repeated more than once, but this should make each chapter of the thesis more readable without a constant need to refer back to other chapters. 1) Chapter one assesses the overall biodiversity and conservation value of a regenerating rainforest site from the Amazon region of SE Peru. The chapter compares the values of this regenerating study site with the biodiversity found at a selection of well-studied primary forest sites and the predicted species list for the region. In addition it focuses upon key indicator species and species of key conservation concern. 2) The second chapter investigates the biodiversity within a regenerating forest once subjected to different types of historic anthropogenic disturbance. This is achieved through a multi-taxa analysis including data on amphibians, butterflies, birds and mammals. 3) Chapter three assesses the ecological disruption to faunal biodiversity of the presence of a small, unmarked Amazonian road; from the eastern Amazon region of Ecuador. The study is multi-taxa, including an assessment of amphibians, birds and butterflies. 4) Chapter four examines terrestrial and arboreal patterns of biodiversity within a regenerating rainforest, focussing upon butterflies. Measures include species richness, species diversity, community structure and abundance. 5) The fifth chapter examines the efficiency and potential for the use of arboreal camera traps in generating rapid inventories of arboreal rainforest mammals; in comparison with traditional survey techniques. The comparison includes both the effectiveness of data gathering and a financial cost-benefit comparison. 8 6) This final data chapter examines patterns of amphibian biodiversity, with the aim to directly assess whether different survey methodologies provide the same or contrasting patterns of biodiversity in response to different forms of historic human disturbance; a potentially contributing factor towards the controversy about the biodiversity value of regenerating rainforest. In addition to these six chapters, the thesis begins with a general introduction on biodiversity and finishes with a short final discussion which brings together the major findings and conclusions of the main chapters and assesses their overall significance; with suggestions for future progression of research in this field. Appendices that provide supporting materials for the data chapters are all located at the very end of the thesis. In addition to the appendices for each of the main chapters, the appendices contain five additional published or accepted supporting papers on regenerating rainforest biodiversity and survey methods. These demonstrate my ability to produce publication quality research on these subjects. These relate to: 1. the effects of human habitat disturbance on amphibian and reptile communities; 2. trialling bobbin tracking methodologies for amphibians and reptiles, for the first time in a tropical rainforest; 3. the use of bamboo traps as refugia for two poorly known species of rainforest amphibians; 4. the first distribution map and range extension for a species of frog of the genus, Osteocephalus; and 5. the first distribution map and range extension of a species of hummingbird. These supporting papers were co- authored, initiated and overseen by myself and their inclusion follows university thesis guidelines. In the appendix I explain what my specific role and involvement was for each paper, explain their relevance to the thesis and provide the full citation for published versions. They are added into this section to separate them from the papers/manuscripts on which I am the first author.