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Dietary Modulation of Intestinal Fermentation in Raptors

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Dietary Modulation of Intestinal Fermentation in Raptors Dietary modulation of intestinal fermentation in Raptors. Word count: 26 020 Anika Daneel Student number: 01110677 Supervisor: Prof. dr. Geert Janssens Supervisor: Dr. Katherine Whitehouse-Tedd A dissertation submitted to Ghent University in partial fulfillment of the requirements for the degree of Master of Veterinary Medicine Academic year: 2017 - 2018 Ghent University, its employees and/or students, give no warranty that the information provided in this thesis is accurate or exhaustive, nor that the content of this thesis will not constitute or result in any infringement of third- party rights. Ghent University, its employees and/or students do not accept any liability or responsibility for any use which may be made of the content or information given in the thesis, nor for any reliance which may be placed on any advice or information provided in this thesis. Foreword I would like to thank Professor Geert Janssens and Dr Katherine Whitehouse-Tedd for their excellent guidance, countless revisions and support throughout my thesis. I also wish to thank Herman De Rycke, Katja Van Nieuland and all the people that assisted with the measurements, Donna Vanhauteghem and Gerry Whitehouse-Tedd, without whose cooperation I would not have been able to collect and analyse all the data. I would also like to thank my friends and family for their moral support. To my mother who deserves a particular note of thanks: thank you for assisting with the revision and your wise counsel. I hope you enjoy your reading. Index 1. Abstract and Summary…………………………………………………………………………………………………………………………………………………. 1 2. Literature study…………………………………………………………………………………………………………………….…....................................... 2 2.1. Introduction………………………………………………………………………………………………………………….…………………………………….. 2 2.2. Anatomy and physiology of the raptor digestive system………………………………………….…………………………………..…… 3 2.2.1. Esophagus………………………………………………………………………………………………………………………………………………… 4 2.2.2. Ingluvies………………………………………………………………………………………………………………..…………………………………..….4 2.2.3. Proventriculus………………………………………………………………….…………………………………………………………………….... 5 2.2.4. Ventriculus………………………………………………………………………………...…………………………………………………………….....5 2.2.5. Small intestine (duodenum loop, jejunum and ileum)………………………………………………………………………….….. 7 2.2.6. Large intestine (colon)………………………………………………………………….……………………….………………………………….. 7 2.2.7. Caeca………………………………………………………………………………………………………………………………….…………………..…..8. 2.2.8. Cloaca…………………………………………………………………………………………………………………………..……………………………. 9 2.3. Intestinal separation mechanism (SM)………………………………………………………………………….…..................................... 9 2.4. Microbiota of the digestive tract………………………………………………………………………………………………………………………….10 2.4.1. Bacteria in the different parts of the digestive tract………………………………..……………….……………………………….. 12 2.4.2. Bacterial phyla found in the digestive tract of birds……………………………………………….….................................... 12 2.5. Nutrient content of prey…………………………………………………………………..……………………………..…………………………………. 16 2.6. Protein catabolism………………………………………………………………………………................................……………………………….. 19 2.7. Microbial fermentation………………………………………………………………………….………………………….................................... 22 2.7.1. Short chain fatty acids (SCFA) ……………………………………………………….………………………….................................... 23 2.7.2. Microbial fermentation……………………………………………………………….………………………….......................................25 2.8. Fermentation of uric acid………………………………………………………………………………………………….……………………………….. 25 2.9. Digesta passage rate…………………………………………………………………..………………………………………..……………………………. 26 2.10. Mean retention time (MRT)…………………………………………..………………………………………..………………………………………… 26 2.10.1. Influence of quantity and type of diet……………………………………………………………………………………………………….26 2.10.2. Influence of body temperature…………………………………………………………………..………………………………………..…..26 2.10.3. Influence by length of digestive tract………………………………………………………………………………………………………….27 2.11. Inert markers………………………………………………………………..……….…….…………………………………………………………………….. 27 2.11.1. C isotopes…………………………………………………………………..……………………………………………………………………….. 28 2.11.2. N isotopes………………………………………………………………...……………………………………………………………………………..28 2.11.3. S isotopes………………………………………………………………..……........................................................................... 29 2.11.4. H isotopes………………………………………………………………………………………………………….…………………………………….29 3. Hypothesis…………………………………………………………………………………………………………….……………………………………………………… 29 3.1. Function of vestigial caeca………………………………………………………………………………………………………….……….….……………29 3.2. Efficiency of digestion…………………………………………………………………………………………………………….………………………………29 3.3. Speed of excretion………………………………………………………………….………………………………………………………………………………30 4. Aim…………………………………………………………………………………………….………………………………………………………………………………… 30 4.1. Objective 1: Food intake and excretion pattern………………………………………………………………………………………………………30 4.2. Objective 2: Efficiency of diet utilization……………………………………………………………………………………………………………. 30 4.3. Objective 3: Passage rate and mean retention time (MRT)…………………………………………………………………………………….31 5. Material and methods………………………………………………………………………….………………………………..………………………………………31 5.1. Food intake and excretion pattern…………………………………………………….……………………………………………………………….. 31 5.2. Efficiency of diet utilization…………………………………………..…………………………………………........................................... 33 5.3. Passage rate…………………………………………………………………………………..……………………………………...................................34 6. Results………………………………………………………………………………………………..………………………………………………………………………… 36 6.1. Food intake and excretion pattern……………………………………………………………………………………………………………………….36 6.2. Efficiency diet utilization……………………………………………………………….…….....................................................................39 6.3. Passage rate…………………………………………………………………………………..……………………………………………………………………….41 7. Discussion…………………………………………………………………………………………………………….………………………………………………………. 43 7.1. Food intake and excretion pattern…………………………………………………………………………………………………………….…………43 7.2. Efficiency of diet utilization…………………………………………………………………………………………………………….…………………… 45 7.3. Passage rate……………………………………………………………………………………………………………………………………………………….. 46 8. Conclusion……………………………………………………………………………………………………………………………………………………………………..46 9. Reference list…………………………………………………………………………………………………………………………………………………………………..47 10. Attachments…………………………………………………………………………………………………………………………………………………………………. 56 1. Abstract Birds of prey also known as raptors are carnivore birds that feed on other animals, which can be categorized into 7 families. Strigidae, Tytonidae and Falconidae are the only families that do not belong to Accipitriformes. When considering their digestive tracts Strigiformes is the only order that has a different digestive tract: they have appendicular caeca, while the rest of the raptors have vestigial caeca. This is of importance since all raptors live on the same high proportion of animal tissues. In this study two vulture species were used to determine how they accommodate these differences, how efficient they digest food and what are their passage rates. The actual collection period lasted four days. During the first three days the efficiency of digestion was studied by measuring the change in stable isotopes from food to excreta. The last day a bolus of titanium dioxide (TiO2) was given to each vulture, which was used to determine the passage rate. Variance analysis was applied to evaluate effects of vulture species. Lappet-faced vultures (Torgos tracheliotos) ingested significantly more than griffon vultures (Gyps fulvus) despite similar body weights, produced significantly more brown fecal samples than green fecal samples compared to griffon vultures. Although the stable isotope analysis showed no difference in digestive efficiency, the excreta C and N analysis still suggested that the lappet-faced vultures digested and absorbed protein more efficiently than griffon vultures. The high amount of leftover pieces collected from griffon vultures indicate that nutritional values based on whole prey is not entirely adequate for raptors and can lead to shifted dietary nutrient profiles. Although only numerical, griffon vultures appeared to have a faster passage rate than lappet-faced vultures. The consistency of fecal samples and mean retention time (MRT) were not different between vulture species. The results demonstrate that the differences in digestive anatomy between lappet-faced vultures and griffon vultures is associated with higher food intake and a higher digestive capacity, in particular for diets with high amounts of animal fiber. 1. Samenvatting Roofvogels zijn vogels wiens dieet voornamelijk bestaat uit andere dieren. Ze kunnen in 7 verschillende families ingedeeld worden. Strigidae, Tytonidae en Falconidae zijn de enige families die niet tot Accipitriformes behoren. Wanneer wordt gekeken naar het spijsverteringsstelsel van Strigiformes, zijn ze de enige groep roofvogels die een appendiculair caeca heeft, terwijl de andere roofvogels een rudimentair caeca hebben. Dit is van belang aangezien alle roofvogels van dezelfde hoge proportie dierlijk weefsels afhangen. Tijdens deze studie zijn twee type gieren gebruikt om te evalueren hoe ze met deze verschillen omgaan, hoe efficiënt ze hun eten verteren en wat de passagesnelheid is voor de twee type gieren. De eigenlijke collectieperiode duurde vier dagen. De eerste drie dagen werd de verteringsefficiëntie door middel de verandering in stabiele isotopen profiel van voer tot excreta. Tijdens de laatste
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