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1 Using Feeding Ecology to Influence Captive Slow 1 USING FEEDING ECOLOGY TO INFLUENCE CAPTIVE SLOW LORIS (NYCTICEBUS SPP.) NUTRITION AND HUSBANDRY FRANCIS CABANA 2016 2 USING FEEDING ECOLOGY TO INFLUENCE CAPTIVE SLOW LORIS (NYCTICEBUS SPP.) NUTRITION AND HUSBANDRY AUTHOR: Francis Cabana SUPERVISION TEAM: Director of Studies: Prof K.A.I. Nekaris Co-Supervisor: Dr Giuseppe Donati Advisor: Dr. Ellen S Dierenfeld Thesis is submitted in partial fulfillment of the requirements of the award of Doctor of Philosophy September 2016 3 ABSTRACT Despite the advancement of science within the animal nutrition field, specifically production and domestic animals, exotic animal nutrition is very little studied. Some species are so understudied or shrouded in routine and anecdotes that both zoos and rescue centres manage them the same way, the wrong way. The slow lorises Nycticebus spp. are one of these species. I aimed to investigate the diet of wild Javan slow lorises, in order to create an appropriate captive diet for them. My objectives were to assess the current state of captive slow loris diets, calculate the nutrient intake rates and energy expenditure in wild individuals, assess the importance of natural food items within their diet, and finally, to trial a new diet and assess its long term impacts on health. From June 2014 to June 2015 I collected behavioural and feeding data on 17 radio-collared wild Javan slow lorises near Cipaganti, Indonesia. Food samples were collected and analysed for proximate and fibre analyses. Our diet trials were conducted in a rescue centre where we introduced gum into their diets and recorded food passage time. We collecte faecal samples of wild and captive individuals and analysed them for chitinolytic activity. We developed a new diet and compared nutrient intake, digestion and passage rate of the old and new diets. Wild diet was gum, insects and plant parts with seasonal variations in intake. Average intake was high in protein and fibre, low in sugars. They are able to vary their behavior to adjust energy expenditure. Captive animals increased passage rates when fed gum and potentially can digest chitin. Our new diet of gum, insects and vegetables had similar physiological effects than wild diets: slower and more efficient digestion and more appropriate nutrient intake. It was conducive to optimum weight and health. 4 ACKNOWLEDGEMENTS I can pinpoint the moment when my career was born. When Dr Amy Plowman offered me an internship in animal nutrition following my masters when her dedicated student dropped out. Things have a funny way of happening and working out for me. Always giving me the benefit of the doubt and supporting me in whatever situation I was in all while remaining perfectly British. I will always remain deeply loyal to you. You have my eternal gratitude. I never would have looked into slow lorises this intently if it wasn't for Matthew Webb. His exact sentence was "You should look into slow lorises; they have loads of issues". Following his wise advice, I started to look into slow loris nutrition. For sending me on this path Matt, I am very thankful. This led to a short paper with a sample size of two which happened to catch the eye of my supervisor to be, Prof Anna Nekaris. She saw the potential for an entire PhD which I accepted. You have been a constant source of patience and advice throughout this journey. Coupled with the counsel and effort from Dr Giuseppe Donati and Dr Ellen Dierenfeld, I felt like I was in safe hands. I can never repay the time and energy you have all spent on me, I am humbled. You have showed me how important it is to be selfless and to nurture the next generation of researchers who can make a difference and solve the issues of tomorrow, even if this problem is properly feeding small nocturnal primates. I hope you do not regret the time spent on me. My fieldwork was the most significant time of my life. Never have I, nor will I be forever changed by a period of my life like this, that I would never want to forget, yet never want to repeat. I had both the best and worst moments of my life. I learned a lot about myself, found a different version of myself I didn't know existed and I met both the best people I will ever meet but I also met the worst. To my trackers, I literally owe you my life as I would surely have perished without you. Thank you Dendi Rustandi Pondiana, Adin Sopian, Dede Ahmad Aconk and Yiyi Muhamed. Saya sangat menghargaii pekerjaan kalian. Terimah Kasih. Thank you 5 to my field assistants for your time and effort: Katie Reinhardt, Katy Elsom, Katherine Kling, Josh Hill, Taylor Tench, Lewis Castle, Nita Listiyani, Bagus Sumpamutra, Rifqi Leonyl and the volunteer Jess Wise who refuses to be called my research assistant. Thank you to Charlotte York, Johanna Rode-Margono and Richad Moore for understanding me and keeping me on the right path. I also need to acknowledge and thank the Indonesian authorities of the Riset and Teknology (Ristek) and Ibu Wirdateti from the Indonesian Institute of Science for granting me my research visa and seeing the potential in my research. As well as Dr Christoph Schwitzer and Prof Vincent Nijman on their comments during my viva. Maman et papa, je vous remercie de m'avoir appris c'est quoi aimer inconditionnellement et de mettre les autre avant vous même. Vous êtes les deux personnes les plus généreuse que je connais et c'est vous qui me donne le courage le dédié ma vie à protéger les animaux qui ne peuvent pas se défendre eux même. Je vous aime et je m'ennuis de vous a chaque jour. David, merci de m'avoir écouté quand j'ai eu peur, quand j'ai été fâcher et quand j'ai juste besoin d'un petit boost. Jean-François, merci de m'avoir appris de prendre ça une journée a la fois, et de persévérer contre mes démons. Je vous aime mes frères, merci de me protéger. Victoria et Gloria, merci de m'avoir appris qu'on est tous nées innocent et bon. Juju, tu est mon ange gardien, j'aurai aimer que tu soient la pour m'appeler "docteur". Vous êtes ma famille et je suis fier d'être un Cabana. We would like to acknowledge the following funders for believing in this project: Longleat Safari and Adventure Park, Whitley Wildlife Conservation Trust, Primate Society of Great Britain, and International Primatological Society Captive Care Working party, Nacey Maggioncalda Foundation, University’s Federation for Animal Welfare, Disney Worldwide Conservation Fund, Colombus Zoo, Phoenix Zoo, Cleveland Zoo and Zoo Society, Shaldon Wildlife Trust, Shepreth Wildlife Park, Sophie Danforth Foundation, Conservation International Primate Action Fund, and Mazuri Zoo Feeds for their funding support with various elements of this ongoing research. 6 And last but not least, thank you to the slow lorises. I have seen many devastating scenes at animal markets and rescue centres, where the only release for these poor animals would be death. We are used to hearing about the strength of an elephant and the speed of the cheetah and the prowess of the lion. No one speaks about the will to live of a slow loris. No one knows how strong they are, how much they can suffer through and what they can come back from. No one sees their struggles hidden behind their clown-like faces. I saw you little ones, and I hope I can help some of you have a second chance. This was all for you. 7 TABLE OF CONTENTS TITLE PAGE...............................................................................................PAGE 2 ABSTRACT...................................................................................... ...........PAGE 3 ACKNOWLEDGEMENTS........................................................................PAGE 4 TABLE OF CONTENTS...........................................................................PAGE 7 LIST OF TABLES............................................................... ……………..PAGE 8 LIST OF FIGURES.........................................,….............. ……………PAGE 10 ABBREVIATIONS...............................................................................….PAGE 11 PREFACE…………………………………….………………………….PAGE 12 CHAPTER 1..............................Introduction........................... …...…...PAGE 13 STRUCTURE OF THESIS……………………………………....……..PAGE 32 CHAPTER 2.............................General Methods................................... PAGE 34 CHAPTER 3................Captive Slow Loris Questionnaire Study......…PAGE 49 CHAPTER 4.............................Wild Feeding Ecology........................... PAGE 66 CHAPTER 5.............................Free-Ranging Energetics…….............. PAGE 90 CHAPTER 6.................Food Passage Rate Comparison ………..…....PAGE 108 CHAPTER 7.............................Chitin Digestion....................................PAGE 126 CHAPTER 8.............New Diet Creation and Trial............. ………….PAGE 143 CHAPTER 9.............................Synthesis............................................... PAGE 167 CHAPTER 10...NUTRITION GUIDELINES……………………...…PAGE 172 LITERATURE CITED................................. …………………..……...PAGE 174 APPENDIX I………………….Zoo Questionnaire………………….. PAGE 221 APPENDIX II…………………Ethical Approval Letter……………..PAGE 223 APPENDIX III………………..Publications List…………………......PAGE 224 APPENDIX IV……………...Javan Slow Loris Intake Raw Data…..PAGE 225 APPENDIX V……………Greater Slow Loris Intake Raw Data…...PAGE 232 APPENDIX VI……..Philippine Slow Loris Intake Raw Data……....PAGE 239 APPENDIX VII..….. …………Zoo Biology Publication …………….PAGE 245 APPENDIX VIII………………AJPA Publication……….......………PAGE 252 8 LIST OF TABLES Table 1.1 Mammal species which have been identified
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