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Prey Selection and Digestive Processing in Terrestrial Carnivorous Mammals

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Prey Selection and Digestive Processing in Terrestrial Carnivorous Mammals Prey selection and digestive processing in terrestrial carnivorous mammals Annelies De Cuyper A dissertation submitted to Ghent University in fulfilment of the requirements for the degree of Doctor of Veterinary Sciences 2017 Supervisors Prof. dr. ir. Geert P.J. Janssens Prof. dr. Marcus Clauss Prof. dr. Myriam Hesta Department of Nutrition, Genetics and Ethology Table of contents List of abbreviations………………………………………………………………………………...9 General introduction ........................................................................................................................ 13 1. What makes a carnivore? ......................................................................................................... 15 1.1 Carnivore diversity: a dietary perspective ......................................................................... 15 1.2 Digestive physiology of terrestrial carnivores ................................................................... 16 2. The implications of carnivore body size .................................................................................. 26 2.1 The basics of body size relationships ................................................................................ 26 2.2 Body size versus animal physiology .................................................................................. 27 2.3 Body size versus animal ecology: the case of predator-prey interactions ......................... 31 2.4 How body size could link carnivore feeding ecology with digestive physiology ............. 33 3. Domestic carnivores: the preservation of evolutionary adaptations ........................................ 38 Scientific aims .................................................................................................................................. 55 Research chapters ............................................................................................................................ 61 1. Predator-prey size ratios determine kill frequency and carcass surplus production in terrestrial carnivorous mammals .................................................................................................................. 63 1.1 Abstract .............................................................................................................................. 65 1.2 Introduction ........................................................................................................................ 66 1.3 Material and methods ......................................................................................................... 68 1.4 Results ................................................................................................................................ 72 1.5 Discussion .......................................................................................................................... 78 2. How does dietary particle size affect canine gastrointestinal transit: A comparison of dietary markers ......................................................................................................................................... 91 2.1 Abstract .............................................................................................................................. 93 2.2 Introduction ........................................................................................................................ 94 2.3 Materials and methods ....................................................................................................... 96 2.4 Results .............................................................................................................................. 102 2.5 Discussion ........................................................................................................................ 105 3. Are carnivore digestive separation mechanisms revealed on structure-rich diets?: Faecal inconsistency in dogs (Canis familiaris) fed day-old-chicks ..................................................... 115 3.1 Abstract ............................................................................................................................ 117 3.2 Introduction ...................................................................................................................... 118 3.3 Material and methods ....................................................................................................... 120 3.4 Results .............................................................................................................................. 124 3.5 Discussion ........................................................................................................................ 132 General discussion ......................................................................................................................... 145 1. Introduction ............................................................................................................................ 147 2. Is carnivore kill frequency a body size driven feature? ......................................................... 149 2.1 Model building: a path to generalisation ......................................................................... 149 2.2 The variable small prey-feeders and body size driven large-prey feeders....................... 154 2.3 Carnivore functional group dichotomy: the body size driven theory under siege ........... 161 3. Challenging domestic carnivore digestive physiology with 'ancestral' diets ......................... 163 3.1 Whole prey diets: a matter of structure ............................................................................ 163 3.2 Passage of whole prey diets through the canine gastrointestinal tract ............................. 169 4. Conclusions and implications for current feeding practices in zoos and domestic carnivores ................................................................................................................................................... 182 5. Future perspectives ................................................................................................................ 184 Summary ........................................................................................................................................ 199 Samenvatting ................................................................................................................................. 205 Appendices ..................................................................................................................................... 213 Acknowledgements ........................................................................................................................ 227 Curriculum Vitae ........................................................................................................................... 235 Bibliography .................................................................................................................................. 239 List of abbreviations Ace = acetic acid ADF = acid detergent fibre BARF = bone and raw food BCFA = branched-chain fatty acids But = butyric acid C = gut capacity CF = crude fibre CI = confidence interval CTT = colonic transit time DM = dry matter Eprey = metabolisable energy in prey FMR = field metabolic rate FO = frequency of occurrence GET = gastric emptying time GMC = giant migrating complexes GRT = gastric residence time IMMC = interdigestive migratory myoelectric complex iMprey = pack corrected prey mass isoBut = iso-butyric acid isoVal = iso-valeric acid KF = kill frequency M = body mass MaxRT = maximum retention time 9 ME = metabolisable energy MER = maintenance energy requirements Mpred = predator body mass Mprey = prey mass MRT = mean retention time NfE = nitrogen free extract Npack = pack size OLS = ordinary least squares PGLS = phylogenetic generalized least squares Pro = propionic acid Qpred = carnivore specific maintenance requirements rFO = relative frequency of occurrence SBTT = small bowel transit time SCFA = short-chain fatty acids SD = standard deviation SEM = standard error of the mean T1/2-GET = gastric half emptying-time TDF = total dietary fibre TTT = total transit time Val = valeric acid 10 General introduction General introduction 1. What makes a carnivore? 1.1 Carnivore diversity: a dietary perspective The mammalian order of Carnivora harbours a great diversity of species. Taxonomic classification renders 281 species included in 128 genera and 16 families (Wilson and Reeder, 2005) (Table 1). The order is characterised by a significant variation in terms of morphology, ecology and behaviour (Gittleman, 1989). Body size can range from a species as small as the least weasel (Mustela nivalis) that weighs ca. 50 grams to a gigantic southern elephant seal (Mirounga leonina) of more than 3500 kg (Nowak, 1999). Carnivores inhabit various habitats from aquatic terrains to terrestrial environments such as grasslands (e.g. Indian fox, Vulpes bengalensis) (Vanak and Gompper, 2007), deserts (e.g. fennec fox, Vulpes zerda) (Gittleman, 1989), forests (e.g. pine marten, Martes martes) (Storch et al., 1990) and many more. If we ought to give one example of behavioural differences between carnivores, carnivore species can be generally subdivided in solitary (e.g. Eurasian lynx, Lynx lynx) (Ratkiewicz et al., 2014) versus social predators (e.g. African wild dog, Lycaon pictus) (Creel and Creel, 1995). When it comes to feeding or dietary habits, classification
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