JOURNAL TRANSCRIPT
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
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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
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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 is not as straightforward as one would expect. Although 'carnivore' literally means 'meat eater', not all species can be as easily regarded as just 'eating meat'. One of the most pronounced examples is the giant panda (Ailuropoda melanoleuca) that is taxonomically regarded as a carnivore but thrives on a bamboo-dominated diet, i.e. a completely herbivorous diet (Krause et al., 2008; Xue et al., 2015). Numerous other carnivores rely on an omnivorous (e.g. brown bear, Ursus arctos) (Elfström et al., 2014), insectivorous (e.g. aardwolf, Proteles cristatus) (Wilman et al., 2014) or even frugivorous diet (e.g. kinkajou, Potos flavus) (Julien-Laferrière, 1999). Only members of the felid family and some species of the mustelid family (e.g. least weasel, M. nivalis) (King, 1980) are considered strictly carnivorous although recent evidence suggests that wolves (Canis lupus, Canidae), that are often referred to as omnivores, are of a true carnivorous kind with only negligible consumption of plant material (Bosch et al., 2015). However, a specific dietary composition can be affected by food availability which in turn can be impacted by seasonal and geographical conditions (Fuller and Sievert, 2001; Hill and Dunbar, 2002). The yellow-throated marten (Martes flavigula) e.g. is known to become an opportunistic frugivore when fruit abundance reaches its temporal maximum
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in contrast to an otherwise rodent-dominated diet (Zhou et al., 2011). European wildcats (Felis silvestris) exhibit greater diet diversity at lower latitudes (i.e., mediterranean climates) where there is greater prey richness (Lozano et al., 2006). It must be clear that only from considering dietary habits of carnivores, great variation originates at an interspecific as well as intraspecific level, contributing to the great diversity that characterizes the Mammalian order of Carnivora. Table 1 Family subdivision of the Mammalian order of Carnivora Carnivore family Number of Species example species Ailuridae Canidae Eupleridae Felidae Herpestidae Hyaenidae Mephitidae Mustelidae Nandiniidae Odobenidae Otariidae Phocidae Prionodontidae Procyonidae Ursidae Viverridae
1 35 8 37 34 4 12 57 1 1 16 19 2 12 8 34
Red panda (Ailurus fulgens) Gray wolf (Canis lupus) Fossa (Cryptoprocta ferox) Lion (Panthera leo) Water mongoose (Atilax paludinosus) Spotted hyaena (Crocuta crocuta) Striped hog-nosed skunk (Conepatus semistriatus) Pine marten (Martes martes) African palm civet (Nandinia binotata) Walrus (Odobenus rosmarus) Antarctic fur seal (Arctocephalus gazella) Common seal (Phoca vitulina) Banded linsang (Prionodon linsang) Common raccoon (Procyon lotor) Brown bear (Ursus arctos) Common genet (Genetta genetta)
1.2 Digestive physiology of terrestrial carnivores Current knowledge on carnivore digestive physiology stems from an extensive amount of research conducted with captive non-domestic and domestic carnivores (i.e. domestic dog (Canis familiaris) and cat (Felis catus)) (e.g. NRC (2006), Stevens and Hume (1995)). Carnivores are typically referred to as having a simple digestive tract because of a highly digestible natural diet compared to other feeding types (Fig. 1) (Stevens and Hume, 1995) and different taxonomic groups seem to share similarities in nutrient digestibility (Clauss et al., 2010). Although carnivore species share certain digestive characteristics, it appears hard to put forward one carnivore digestive prototype since diversity still occurs among carnivores at different levels of digestive physiology.
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Fig. 1 Gastrointestinal tract of a carnivorous, omnivorous and herbivorous feeder Left figure: carnivorous feeder, the domestic dog (Canis familiaris) with bodylength 90 cm; middle figure: omnivorous feeder, the black bear (Ursus americanus) with bodylength 125 cm; right figure: herbivorous feeder, sheep (Ovis aries) with bodylength 110 cm (From Stevens and Hume (1995))
1.2.1 Morphometry, allometry and transit in the gastrointestinal tract The carnivore stomach is of a simple nature without any diverticula (Stevens and Hume, 1995; Hume, 2002) and with the potential in some species, e.g. the dog (C. familiaris), to expand considerably (Hume, 2002; Bosch et al., 2015). The latter probably originated in wild counterparts in order to accumulate excessive amounts of prey (Hume, 2002). Wolves (C. lupus) are able to ingest up to 22 % of their own body weight (Stahler et al., 2006). Tigers (Panthera tigris) and lions (Panthera leo) can eat up to one fifth of their own bodyweight in a very short period of time (Schaller, 1967; Bertram, 1975). Spotted hyenas (Crocuta crocuta) are able to eat one third of their bodyweight in one eating session (Kruuk, 1972). Such large meals require enough gastric capacity and extension and indeed, Bertram (1975) noticed the swollen abdomen of lions after ingesting large amounts of food in a few hours and classified this gastric extension on a scale from
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one to five. A similar scaling (belly depth to body length ratio) exists for African wild dogs to assess meat consumed (Potgieter and Davies-Mostert, 2012). The intestinal tract of carnivores is relatively short with the longest relative lengths measured in mustelids (McGrosky et al., 2016). The small intestine or midgut is short but is perceived as the dominant feature of the carnivore gut where most of the enzymatic digestion takes place (Hume, 2002). The large intestine or hindgut (i.e., colon, caecum and rectum) is comparatively short and simple (Stevens and Hume, 1995). The colon tends to be wide and unsacculated (Hume, 2002). As for the caecum, not all carnivore species possess a caecum which even further simplifies the intestinal tract (Fig. 2) (Mitchell, 1903-6; Kostanecki, 1926; McGrosky et al., 2016). Typically, ursids, mustelids and procyonids and species such as the binturong (Arctictis binturong) lack a caecum (McGrosky et al., 2016). For those that possess a caecum, morphological outturn can differ from e.g. a coiled appendage in the dog (C. familiaris) to not as coiled in the domestic cat (F. catus) (Stevens and Hume, 1995). Omnivorous and herbivorous feeders within the Order of Carnivora show similarities with strict carnivorous feeders, although again some diversity exists. The aardwolf for instance (P. cristatus; insectivorous feeder) has a similar digestive tract as the domestic cat and dog (Anderson et al., 1992; Stevens and Hume, 1995) with a caecum that resembles the dog's caecum but is relatively small compared to hyaenids (Anderson et al., 1992). The omnivorous raccoon (Procyon lotor) has a relatively longer small intestine than dogs and cats but has a shorter hindgut without caecum (Stevens and Hume, 1995). A complete herbivorous carnivore such as the giant panda (A. melanoleuca) has similarly a simple hindgut with no caecum (Dierenfeld et al., 1982; Stevens and Hume, 1995) which infers that a caecum might not be a prerequisite for omnivorous or herbivorous feeders (McGrosky et al., 2016).
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Fig. 2 Gastrointestinal tracts of carnivore species with and without caeca Figure a: the Mongolian wolf (Canis lupus chango); figure b: the Canadian lynx (Lynx canadensis); figure c: the ferret (Mustela putorius); figure d: the brown bear (Ursus arctos); black arrows indicate the caecum (Adapted from McGrosky et al. (2016))
Studying the movement of digesta through the gastrointestinal tract connects physiological gut motility and the type of diet (physical and nutritional) provided to the animal (Clemens and Stevens, 1980; Warner, 1981). Typically, the rate at which digesta move through the gastrointestinal tract will be optimal when it matches the rate of feeding, digestion and absorption. The latter is necessary to ensure maximal conversion of the ingested food in as short as possible period and small as possible gut volume (Clemens and Stevens, 1980; Penry and Jumars, 1987; Stevens and Hume, 1995). In general, if one assumes the highly digestible 'meat diet' of carnivores, i.e. high quality foods, this implies a high digestion rate and consequently short digesta retention times compared to other feeding types (Sibly, 1981; Hume, 1989). However, there is no such thing as one typical retention time in carnivores and comparison between species or between different feeding types are constrained by different physical and nutritional characteristics of the diet (Hogan and Weston, 1969; Hintz et al., 1971). For instance, large dietary volumes are known to slow down gastric emptying in dogs (Gupta and Robinson, 1995; Lin, 1996). Meals with a high energy density or with a high fat content can similarly slow down gastric emptying (Meyer et al., 1994; Wyse et al., 2001). Again, in dogs, the inclusion of plant-derived insoluble fibre in the diet can affect transit time: the inclusion of cellulose in a canine diet decreases total transit time
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(Burrows et al., 1982) and the addition of 10 % insoluble fibre (sugarcane fibre) in a dog’s diet can delay gastric emptying and colonic filling time (Pedreira et al., 2013). Additionally, digesta retention time as measured by the fecal excretion of marker substances is particularly constrained in its validity in carnivores: the highly digestible diet results in a comparatively low amount of faeces that the animal can afford to not defecate instantaneously, but carry around in its rectum until a behaviourally suitable situation, e.g. for scent marking, presents itself (Parker, 2010). This is in contrast to herbivores that mostly have a more continuous flow of digesta through and hence of faeces out of their digestive tract (Penry and Jumars, 1987).
1.2.2 Digestion of nutrients and metabolic adaptations in obligate carnivores After a diet is ingested it will go through a series of mechanical, chemical and microbial events which can be simply summarized as the process of enzymatic digestion in the upper gut, fermentation of enzymatically undigested components in the lower gut and the absorption of processed dietary components after which they are metabolised in the animal's body (Stevens and Hume, 1995; McDonald et al., 2011). The principal nutrients found in animal diets that are to be digested are carbohydrates, lipids, proteins and nucleic acids (McDonald et al., 2011). The archetype of a carnivorous diet, i.e. animal tissue, is protein-rich and low in carbohydrates, which has led to certain metabolic adaptations in some obligate carnivores (Hume, 2002). The wildcat (F. silvestris) is known as a strict, obligate carnivore consuming whole prey, which has led to metabolic adaptations (= idiosyncrasies) still present in domestic cats (MacDonald et al., 1984; Morris, 2002). A summation of metabolic adaptations in domestic cats is given in Table 2. Some mustelids, i.e. the mink (Mustela lutreola) and ferret (Mustela putorius), which are also perceived as strictly carnivorous, share the same pecularities in enzyme activity for de novo synthesis of arginine (Leoschke and Elvehjem, 1959; Deshmukh and Shope, 1983). Lions (P. leo) are similarly incapable of synthesising arachidonic acid from linoleic acid (Rivers et al., 1976). Domestic dogs on the contrary do not share the same metabolic adaptations as seen in domestic cats. They are capable of synthesising essentiel nutrients such as arginine, taurine, niacin and arachidonic acid and to down-regulate catabolic amino acid enzymes on low dietary protein diets (MacDonald et al., 1984; Legrand-Defretin, 1994). Therefore, dogs seem to resemble omnivorous species such as pigs (Baker and Speer, 1983) and rats (Harper, 1965). However, recent evidence suggests that the dog is not to be perceived as an omnivore but is of a carnivorous kind as is his wild ancestor the
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wolf (Axelsson et al., 2013; Bosch et al., 2015). Bosch et al. (2015) launched the idea that the metabolic differences observed between carnivore species might be caused by differences in feeding strategies in the wild. The typical feast and famine regime (i.e. periods of prey, hence food abundance alternated with periods of famine) to which wolves are often submitted contrasts with the frequent feeding style with regular nutrient intake of cats. Famine periods might have caused a necessity to decrease metabolic losses and preserve the ability to synthesise essentiel nutrients whereas the regular feeding style might have relaxed selection pressure against certain metabolic pathways (see section 2.4). In addition, recent evidence shows that during the domestication of dogs, three genes involved in starch digestion and glucose uptake were subject to selective pressure, suggesting that the domestic dog adapted to starch-rich diets that were common during domestication (see below) (Axelsson et al., 2013). Hence, the ability of dogs to thrive on starchrich diets does not stem from the so thought omnivorous nature of the wolf but from digestive adaptations that occurred during domestication.
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Table 2 Digestive and metabolic adaptations of domestic cats Metabolic adaptation
Enzymes/Receptor
Reference
Inability to down-regulate catabolic amino acid enzymes when dietary protein is low Inability for de novo arginine synthesis due to reduced activity of enzymes involved in the intestinal citrulline pathway Low activity of enzymes involved in endogenous taurine synthesis Inability to synthesise retinol from carotenoids Inability to synthesise vitamine D3 due to high activity of enzymes that catabolyse the precursor Inability to syntesise niacin from tryptophan due to high degradative enzyme activity Limited capacity to produce arachidonate from linoleate due to low desaturase activity Adaptations in sugar and starch metabolism associated with absent or low activity of degradative enzymes Inability to taste the sweetness of sugar due to the absence of a receptor
Aminotransferases
MacDonald et al. (1984) Morris (2002)
Pyrroline-5-carboxylate synthase Ornithine aminotransferase
MacDonald et al. (1984) Morris (2002)
Cystein dioxygenase Cysteinsulfinic acid decarboxylase Carotene dioxygenase
MacDonald et al. (1984) Morris (2002)
7-dehydrocholesterol
MacDonald et al. (1984) Morris (2002) Morris (2002)
Picolinic carboxylase
MacDonald et al. (1984) Morris (2002)
∆6-desaturase ∆8-desaturase
MacDonald et al. (1984) Morris (2002)
Salivary, pancreatic and intestinal amylase Hepatic glucokinase Hepatic fructokinase Tas1R2 receptor
Kienzle (1993a) Kienzle(1993b) Kienzle (1994) Washizu et al. (1999) Li et al. (2005)
1.2.3 Fermentation Although characterized by highly digestible diets and a simple large intestine, carnivores do harbour microbial populations in the hindgut in order to ferment nutrients that were enzymatically indigestible or escaped digestion and absorption in the upper tract (Stevens and Hume, 1995; NRC, 2006). Fermentation is commonly defined as the anaerobic breakdown of carbohydrates and proteins (dietary or endogenous) in the large intestine which renders energy for microbial growth and maintenance (Macfarlane and Gibson, 1995; Wong et al., 2006). Fermentation of dietary carbohydrates such as starch, sugars and fibre (indigestible plant-derived fibre) renders the production of
short-chain fatty acids (SCFA) together with the gases CO2, H2 and CH4
(Cummings et al., 1987). Protein fermentation similarly renders SCFA and the branched-chain
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General introduction
fraction (BCFA) of SCFA are typically associated with protein fermentation (Rasmussen et al., 1988; Macfarlane et al., 1992). Next to the production of SCFA, protein fermentation is also associated with the production of putrefactive compounds such as ammonia (NH3), phenols, indoles, aliphatic amines and sulphur-rich compounds (Cummings and Macfarlane, 1991). Typically SCFA are associated with beneficial gastrointestinal and (after absorption) metabolic effects (e.g. energy for gut epithelial cells and important role in water and Na absorption) (Stevens and Hume, 1998; Wong et al., 2006). Putrefactive compounds, associated with protein fermentation, are known to be detrimental for the health of the host although mainly studied in humans (e.g. association with inflammatory bowel disease in humans) (Matsui et al., 1995; Pedersen et al., 2002; Tuohy et al., 2006). However, some biogenic amines (putrescine, spermidine and spermine) are considered beneficial for cell growth and function in low concentrations (Delzenne et al., 2000). Typically in herbivorous carnivores (i.e. the giant panda) fermentation will depend on carbohydrate substrates (Xue et al., 2015), in omnivorous carnivores (e.g. the raccoon) on a mixture of carbohydrates and proteins (Clemens and Stevens, 1979), whereas in strict obligate carnivores it is likely that fermentation will depend largely upon proteins. The fermentation of proteins in carnivores has received attention since protein fermentation is perceived as partly detrimental for gut health as explained before, although strict carnivores seem to have adapted to this process. When ingesting whole prey, proteins entering the large intestine can originate from the actual meat and organs (highly enzymatically digestible), since there is always a small fraction that escapes enzymatic digestion, and from compounds such as connective tissues (e.g. collagen), bones, hairs or feathers that are known to be barely enzymatically digestible (Asghar and Henrickson, 1982). The latter compounds will enter the hindgut in a rather unmodified way and can serve as substrates for fermentation (Banta et al., 1978; Macfarlane and Allison, 1986; Depauw et al., 2012; Depauw et al., 2013). This low to non-digestible (glyco)protein-rich matter, such as raw bones, tendons, cartilage, skin, hair or feathers was recently called 'animal fibre' by Depauw et al. (2012, 2013). The authors pointed out the analogies with plant-derived fibre in terms of fermentation potential and fermentative differences between different types of fibre. In their studies with cheetahs (Depauw et al., 2013), the faecal propionic acid, butyric acid, BCFA and putrefactive compounds were higher in cheetahs fed supplemented beef in comparison with cheetahs fed whole rabbit, suggesting more protein fermentation in supplemented beef. Therefore,
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it was suggested that differences in fermentation between animal substrates (more fermentable substances such as collagen vs less fermentable compounds such as hair and bones) exist, which was also seen with the in vitro fermentation of animal substrates with cheetah faecal inoculum (Depauw et al., 2012). It is possible that indigestible material such as hair and bones acts as a possible bulking agent, forming a physical barrier between substrates and bacteria and filling the large intestine, tempering protein fermentation. The microbial population and the intestinal production of fermentation metabolites have been studied in several carnivore species, e.g. domestic dogs (Bosch et al., 2008; Bosch et al., 2009; Beloshapka et al., 2012; Panasevich et al., 2015), cheetahs (Acinonyx jubatus) (Depauw et al., 2012; Depauw et al., 2013; Becker et al., 2014), domestic cats (Sunvold et al., 1995; Brosey et al., 2000; Ritchie et al., 2008; Kerr et al., 2014a), raccoons (Clemens and Stevens, 1979), the giant panda (Xue et al., 2015), bobcats (Lynx rufus), jaguar (Panthera onca), tiger (P. tigris) (Vester et al., 2008), African wildcat (Felis lybica) (Vester et al., 2010b). In general, the gut microbiota within the mammalian order of Carnivora are dominated by the facultative anaerobes Enterobacteriaceae and Enterococcus (Schwab et al., 2011; Schwab and Gänzle, 2011). The microbial composition in the mammalian gut is mainly, next to gut physiology, shaped by the diet (Ley et al., 2008; Muegge et al., 2011). For instance, when the protein level in diets was varied in domestic cats, the micriobiota profile in cats fed the high protein diet (after eight weeks of adaptation) only showed 40% similarity with the profile of cats fed a moderate protein diet (Lubbs et al., 2009). Similarly, when the comparison between wild ancestors and domestic descendants is made (i.e. the wolf and domestic dog; the wild cat and domestic cat), it is questionable whether the 'domestic' microbiome is still representative for wild counterparts. Today, many carnivorous diets (e.g. canine and feline petfood), but also diets of wild carnivores maintained in captivity, are enriched with plant-derived fibre for its beneficial effects on food intake, appetite and intestinal health (Fahey et al., 2004). However, an obligate carnivore’s natural diet barely includes plant fibre. The natural diet of wildcats is characterised by its high protein and low carbohydrate level and thus barely includes plant fibre, whereas the diet of the domestic cat changed substantially to high protein and carbohydrate levels (traditional kibble diets and canned meats) (Plantinga et al., 2011). Similarly, the commercial diets typically fed to dogs have higher carbohydrate (mainly starches) fractions than the natural diet of wolves (Bosch et al., 2015). It seems likely that the inclusion of plant-derived fibre has induced adaptations in the microbiome of domestic carnivores.
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Indeed, when studying the microbiome of captive cheetahs fed whole prey, it seemed that significant compositional differences occurred with the microbiome of domestic cats on commercial diets (the latter often being used as a model for exotic felids) (Becker et al., 2014). However, apart from the strong adaptive capacity of microbiota to dietary changes, some evolutionary adaptations have remained preserved in some carnivores. For instance, a new genus of bacteria, Novospingobium spp, was recently identified in the hindgut of the domestic cat. This genus is known to use indoles and phenols as fermentation substrate which are typically perceived as detrimental fermentation metabolites from protein fermentation (see above) (Lubbs et al., 2009). The presence of this genus might therefore be an evolutionary adaptation to a natural high protein diet that has preserved throughout domestication. Additionally, the giant panda, which is known to rely on a completely herbivorous diet, has not evolved a gut microbiota adapted to its highly fibrous diet; instead, it shows a typical carnivore-like gut microbiome which contradicts the assumption that adaptation of microbiota to the diet is always obligatory (Xue et al., 2015).
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2. The implications of carnivore body size Within the mammalian order of Carnivora, diversity occurs in all aspects of ecology, behaviour and morphology. The questions "Why are carnivores so diverse?", "How can a certain characteristic be explained?" or "Why is a species as it is?" do not lend themselves to simple answers. In this light, a conversation quoted in Karasov and Diamond (1988) between physiologists and ecologists Martin Cody, Robert MacArthur and Jared M. Diamond while going for a bird walk might offer more perspective in this matter: "Near a stream they saw a black phoebe (Sayornis nigricans), a species of flycatcher confined to the vicinity of water. To MacArthur's question, "Why do you suppose the black phoebe lives only near water?", Diamond and Cody gave opposite dogmatic responses. Diamond insisted "There must be physiological reasons, like low renal concentrating ability resulting in high water requirements. Physiological factors often determine an animal's ecology." Cody replied equally firmly, "Nonsense. Natural selection makes an animal's physiology adapt to the animal's ecological niche, so that physiology provides nothing more than proximate causes. The ultimate causes must be ecological ones, like food availability near streams or else competition with flycatcher species of drier habitats."" Many years later, authors agreed that the question "Does physiology constrain ecology?" or vice versa is complex and both can occur, with the time scale at which physiological adaptations take place being a central element. Although explaining carnivore physiological characteristics and their relation with ecology is a complex issue, one can only try to find regularities in order to elucidate or predict certain biological phenomena. Body size is one of the most obvious features of an animal and can be used in studying the interplay between physiology and ecology, and size-driven diversification (Peters, 1983; Cohen et al., 1993; Cohen, 1994; Carbone et al., 1999; Woodward et al., 2005).
2.1 The basics of body size relationships Body size relationships typically try to empirically relate body size with biological phenomena, i.e. the animal's characteristics in order to unravel constraints or implications for ecology (Peters, 1983). The latter has been used in paleontology (Gould, 1966; Sander and Clauss, 2008), physiology (Pedley, 1977; Hernot et al., 2005; Blueweiss et al., 2010; Müller et al., 2013; Wilson
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et al., 2015), morphology (Thompson, 1961), ecology (Kendeigh et al., 1977; Carbone et al., 2014) and behaviour (Clutton-Brock and Harvey, 1977). Body size relationships are mostly formulated as a power function: Y = aMb with Y being the animal's characteristic that is to be predicted, M being the body mass, and a and b being empirically deducted constants. Initially, data are typically converted to their logarithms in order to simplify and improve graphic and statistical reasoning. Since the variable that is to be predicted (i.e., Y) and M change with different magnitudes or rates, body size power relations are often referred to as allometric relations or as Y scaling to body size (Peters, 1983).
2.2 Body size versus animal physiology 2.2.1 Metabolic rate and food intake/ingestion versus body size in endothermic mammals As simply stated by Peters (1983), what goes into an animal (be it energy or mass) must come out: Ingestion = somatic or individual growth + reproductive growth + respiration + egestion + excretion The latter formula is referred to as the balanced growth equation with growth factors, respiration, egestion and excretion expressing the rate of energy expenditure per unit time by endothermic animals, i.e. the metabolic rate. Typically, metabolic rate is expressed as a rate of carbon or energy or energy flux (e.g. watt (joules/sec)). The standard metabolic rate expresses the metabolic rate under standard laboratory conditions in animals that are awake, inactive, unexcited, healthy, nonreproductive adults and are in a fasting or postabsorptive state under neutral temperatures. Maximum metabolic rates are measured in trained animals that move at maximum speed. The expension of energy in an animal will occur at a rate somewhere between the standard and maximum metabolic rate and is called the daily energy expenditure or the average daily metabolic rate (Peters, 1983; McNab, 1997).
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Metabolic rate has long been recognized as scaling to body size as metabolic rate = aMb (Kleiber, 1932; Peters, 1983; Nagy et al., 1999; White and Seymour, 2003). For many years, there has been a lot of debate on the constant b, whether the value lies around 2/3 or rather 3/4 (White and Seymour, 2005). The scaling exponent of 2/3 stems from the early work of a.o. Rubner (1883) and is based on the 'surface law' of metabolism. Basically the surface law says that the basal metabolism of animals that differ in size is almost proportional to their body surface. The heat that originates from metabolic processes must be dissipated through the body surface, hence, the rate of heat production should be matched to the surface area over which it is released. Knowing that body surface A
M2/3, it is plausible that the
etabolic rate
2/3
(White and Seymour, 2005;
Hudson et al., 2013). However, later on, empirical work of Kleiber (1932) showed that the metabolic rate did not scale in proportion to body surface area (b = 2/3), but with an exponent significantly greater (b = 3/4). This was further supported by the work of Brody (1945) who found the same exponent for almost the entire body size spectrum of terrestrial mammals and published the well-known mouse-to-elephant curve (Fig. 3). Until today, no consensus is reached on the use of an exponent of 2/3 or 3/4 (White and Seymour, 2003; White and Seymour, 2005) although the use of b = 3/4 has been commonly accepted in comparative physiology for over seven decades and is currently still used. Opponents of the exponent 3/4 (White and Seymour, 2005) have indicated that the increase from a 2/3 to 3/4 exponent simply stems from the inclusion of larger herbivores in empirical datasets since their metabolic rate cannot be measured in a post-absorptive state due to the microbiota inhabiting the gut, even not after a period of fasting. Apart from the discussion on scaling exponents, the fact that a scaling effect exists with body size means that small-bodied animals require more energy and nutrients per day and per unit of bodymass than do large animals (Geist, 1974). However, the scaling of one single measure (here metabolic rate) in itself has no explanatory power. Only when this scaling is compared to the scaling of another factor to body size (such as gut capacity), deductions on size driven diversification can be made (Clauss et al., 2013).
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Fig. 3 The mouse-to-elephant curve Metabolic rate is scaled to body mass for several mammals and birds with a scaling exponent of ~ 0.74 (From West (2014); Adapted from Brody (1945))
In the previous discussion on scaling of metabolic rate to body mass, the metabolic rate used always concerns the standard metabolic rate (McNab, 1997; Hudson et al., 2013). However, these metabolic rates are originating from animals that are kept under standardized laboratory conditions (see above). When considering free-ranging mammals, e.g. free-living carnivores, the use of standard metabolic rates is less desirable since one would want to use a direct estimate of energy consumption in nature. The use of field metabolic rates (FMR) has made such an estimation possible and is typically assessed through the doubly labelled water technique (Speakman, 1997). Field metabolic rates are suggested to be more ecologically relevant (Hudson et al., 2013). The FMR of e.g. African wild dogs is known to be 5.2 x the standard metabolic rate during its normal activities (Gorman et al., 1998). Field metabolic rates have been scaled to body size (e.g. Nagy et al. (1999)). However, in general for mammals, the FMR scales to M0.73 which is close to exponent 3/4 typically found for standard metabolic rates. For the mammalian order of Carnivora FMR scales to M0.87 and the dietary group of carnivorous mammals scales to M0.85. The latter is significantly different from and has a higher slope than other dietary groups such as insectivores and herbivores. However, this difference in scaling between dietary groups might be confounded
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by taxonomic affiliation since these differences disappear within taxonomic affiliations (Nagy et al., 1999). Food intake or ingestion is perceived to be directly related to energetic requirements or metabolic rate (see above, balanced growth equation) (Peters (1983); herbivores: Demment and Soest (1985); Illius and Gordon (1992)), which in turn, as explained before, scales to M3/4. Empirical data sets indeed confirm that food intake scales similarly, also for carnivores. In 12 carnivorous species e.g., the absolute dry matter intake per day scaled to M0.72 (Bourlière, 1975). The energy intake of 120 zoo animals, including ursids, viverrids, mustelids, felids, canids, procyonids scaled to M0.75 (Evans and Miller, 1968). Farlow (1976) similarly reported energy intake to scale to M0.70 for 100 carnivorous mammals.
2.2.2 Gut capacity, food intake and retention times scaled to body size: herbivore insights Three major digestive variables, i.e. gut capacity, food intake and retention time and their interplay, are considered important digestive efficiency determinators as shown and extensively studied in herbivore species (Clauss et al., 2007b; Clauss et al., 2013). If gut capacity would be fixed, than an increase in food intake would lead to shorter retention times. If retention time would be fixed, than an increase in food intake would lead to an increase in gut capacity. The difference in allometric scaling to body mass between all three variables appeals to clarify species diversification and niche separation along a certain body mass range in mammalian herbivores, e.g. "How can herbivores of larger body size sustain themselves on lower quality diets?" (Müller et al., 2013). As gut capacity is known to scale almost isometrically to M1.0 (Parra, 1978; Demment and Soest, 1985) and food intake to M0.75 (cf supra), it implies that these different scalings result in a larger gut fill per unit food intake for increasing M. The latter has led to deductions concerning mean retention time (MRT) and digestibility in several ecological studies: the larger gut fill per unit food intake with increasing M implies an elongation of the retention time with increasing body mass (Demment and Soest, 1985; Illius and Gordon, 1992). Therefore the MRT should scale to M0.25 (M1.0-0.75) in mammalian herbivores. Since MRT is positively related to digestive efficiency in herbivores (Foose, 1982; Udén and Van Soest, 1982; Clauss et al., 2007b) this would imply that larger herbivores are more efficient at digestion, hence can tolerate lower quality diets (Demment and Soest, 1985; Illius and Gordon, 1992). However,
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empirical data have shown that the scaling MRT ~ M0.25 does not exist (Clauss et al., 2007a; Müller et al., 2011; Müller et al., 2013). Moreover, several deficits in the previous reasoning were adressed by Clauss et al. (2013) concerning the forage quality, the relation between digestibility and retention times and the overall digestive efficiency. Without going into detail, the authors pointed out that the gut capacity scaling higher than requirements, might allow larger herbivores to subsist on lower quality diets by just ingesting disproportionately more of them. As for the explanation why larger herbivores ingest low quality diets, this would result from ecological scenarios rather than physiological ones (Clauss et al., 2013; Müller et al., 2013). Empirical datasets on gut capacity, food intake, retention times and additionally digestibility in carnivores have not been combined and analyzed so far. Considering the allometric relation with body size of each parameter might further establish regularities in order to explain species diversification in terms of physiology.
2.3 Body size versus animal ecology: the case of predator-prey interactions Food webs are essential elements of ecosystems. This interconnection of food chains is established by consumer prey interactions that link different species in every food web (Estes, 1996). Consumer-prey interactions from a carnivore point of view are of a topdown-control, i.e. high level consumers such as carnivores depress the trophic level on which they feed (their prey) with an indirect increase in the next lower trophic level (Hunter and Price, 1992; Estes, 1996). Terrestrial carnivores are accordingly fundamental shapers of ecosystems and community structures through predation and intraguild interactions (Terborgh, 1992; McLaren and Peterson, 1994; Palomares and Caro, 1999; Ritchie and Johnson, 2009). Predator-prey interactions are considered indispensible when studying carnivores in terrestrial ecosystems (Cohen et al., 1993; Cohen, 1994; Woodward et al., 2005) and can be approached by the construction of empirical relations between predator size to the size of prey predated on (Rosenzweig, 1966; Paine, 1976; Woodward et al., 2005). Carnivore body size appears to be a driving factor in the choice for a specific prey size (Peters, 1983; Carbone et al., 1999; Carbone et al., 2014; Gervasi et al., 2014). Several allometric scalings have been established based on different empirical datasets in the form prey size = a predator sizeb (Vézina, 1985; Carbone et al., 2014). These relationships are not,
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however, concentrated on terrestrial mammalian carnivores solely but exceed the carnivore order level with datasets including predators within amphibians, snakes, birds and mammals (Vézina, 1985) and terrestrial mammals (Carbone et al., 2014). Scaling exponents obtained from general predator datasets are typically close to 1 (e.g. b = 1.05 for terrestrial mammals (Carbone et al., 2014)) (Fig. 4). However, Vézina (1985) obtained a scaling exponent of 1.18 for carnivorous feeders (including amphibians, snakes, birds and mammals) which exceeds a slope of 1. Overall, a slope close to 1 implies that prey size almost isometrically increases with predator size. A slope exceeding 1, as is the case for carnivorous feeders, implies that large predators take relatively larger prey compared to small predators. This is an effect that e.g. Carbone et al. (1999) observed, but rather than interpreting it as an ever-increasing ratio of prey:predator size, these authors introduced a cutoff at about 20 kg, below which carnivores typically consume prey much smaller than themselves, and above which carnivores take prey of a similar size as themselves. Large carnivores (> 20 kg) are more specialised in hunting and feeding on large vertebrate prey, i.e. prey of about or larger than their own bodymass whereas small carnivores (< 20 kg) tend to specialize in prey with a lower mass than their own body weight (including vertebrate and invertebrate prey) (Carbone et al., 1999; Carbone et al., 2007).
Fig. 4 Predator-prey size relationship for terrestrial mammals The scaling exponent of the linear relationship is 1.05 (Adapted from Carbone et al. (2014))
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The underlying driver of prey size differences can be sought in mass related energetic requirements: small carnivores can subsist on a small vertebrate/invertebrate diet because of their lower absolute energetic requirements. However, these diets seem to be unsustainable for larger carnivores. A mass of ca. 20 kg is the maximum that can be sustained on small prey (Carbone et al., 1999), most likely due to a lacking availability of sufficiently dense stacks of small prey that could meet the high absolute requirements of large carnivores. Therefore, two functional groups within carnivores can be distinguished (small vs large carnivores), both representing distinct groups with own ecological and possibly physiological characteristics.
2.4 How body size could link carnivore feeding ecology with digestive physiology The choice for a specific prey size is strongly determined by the body size and concomitantly by the energetic requirements of the carnivore (see 2.3) (Carbone et al., 1999), and the availability of a sufficient amount of available prey packages. In the study of predator-prey interactions, other fundamental elements related to body size such as the frequency at which carnivores consume prey (x kills/predator/unit time) (Holling, 1959; Vucetich et al., 2011) may yield important information on carnivore ecology. Apart from a scarce amount of field kill frequency data available in literature, efforts have been made to estimate predator kill frequency based on prey size and energetic requirements (Peters, 1983; Vézina, 1985). In order to do so, simply stated, data on predator daily food intake (or ingestion rate) are divided by the average prey size of the predator. Typically, these kill frequency estimates predict a decrease in kill frequency with (i) predator body size and (ii) prey size for a range of mammalian and avian carnivores with kill frequency (prey/day) = 28.8 M-0.427 (Vézina, 1985). Larger carnivores are suggested to have less hunting obligations than do smaller carnivores. The latter shows how ecological features such as kill frequency might find their origins in physiological traits of the animal (i.e. body size hence energetic requirements) and point out the interplay between animal physiology and ecology. The approaches used in the kill frequency modeling of Peters (1983) and Vézina (1985), however, do not take into account an important consequence from the predator-prey-size relationship: predators taking prey whose mass exceeds their intake capacity (i.e. larger predators) can feed selectively on their prey and will consume highly digestible body parts such as muscles and organs
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(Hornocker, 1967; Bowland and Bowland, 1991; Stahler et al., 2006; Gidna et al., 2014; Bosch et al., 2015), while predators that kill comparatively small prey will consume their prey entirely (Mills, 1996; Bothma and Coertze, 2004; Anwar et al., 2011). Indeed, in literature it has been reported that large body-sized carnivores (focussed on vertebrate feeders), often sustain themselves on a 'feast-and-famine' regime associated with hunting on large prey. Large, highly digestible meals are alternated with periods of famine. A feast and famine regime may apply to short-term changes (i.e. having a hunting and eating day followed by a fasting and digestion day) and long-term changes such as extended periods of low prey availability (i.e. famine) alternating with periods of prey abundance (i.e. feast) (Bosch et al., 2015). This in contrast to small bodysized carnivores with their small prey, who adopt a more frequent feeding pattern with a regular food intake and a complete utilization of prey (e.g. the wildcat (Bradshaw, 2006)). The implications that prey size has on the maintained feeding strategy of a predator might be an overlooked principle when emperically looking at the scaling relationship of body size with ecological and physiological characteristics and their interplay, and requires further attention. The differences in carnivore feeding strategies have been suggested to explain physiological differences observed between carnivore species (Bosch et al., 2015). The feeding strategy of obligate carnivores that have to hunt frequently during the day with a constant food intake (e.g. wildcat), might have enabled them to lose certain enzymatic pathways that facilitate synthethizing essential nutrients from endogenous stores during evolution (MacDonald et al., 1984; Morris, 2002). Similarly, other species with frequent-prey intake have been reported with adaptations in enzyme activity (i.e. mustelids, de novo synthesis of arginine; see section 1.2.2) (Leoschke and Elvehjem, 1959; Deshmukh and Shope, 1983) although lions (i.e. large carnivores with a typically feast and famine lifestyle) are not able to synthesise arachidonic acid from linoleic acid (Rivers et al., 1976). On the other hand, carnivores that can gorge themselves and hence adopt a 'feast-andfamine-regime' such as the wolf might have benefitted from maintaining such enzymatic pathways to cover essential nutrient production during days without prey intake (Kreeger, 2003; Bosch et al., 2015). The protein sparing capacity e.g., as seen in wolves, has also been described for other carnivores that have to cope with periods of famine (e.g. polar bear (Ursus maritimus) (Derocher et al., 1990)).
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Next to metabolic adaptations to carnivore feeding strategies, the discrepancy in feeding strategies might also be reflected in morphometric characteristics such as gastric extension. Large prey enables predators to gorge themselves, i.e. ingest large quantities of prey which has been observed for several large mammalian carnivores (see above). Similarly, the choice for a specific feeding strategy might have implications for carnivore gut retention times when considering the close interplay between gut capacity, retention times and food intake (see 2.2.2). Given the assumption that a certain feeding strategy has implications for the nature of the digesta and the frequency at which the carnivore consumes prey (i.e. frequent feeding: complete prey ingestion at high frequency vs feast-and-famine: high quantity of highly digestible prey material at low frequency), this might lead to differences reflected in the gut retention time. Empirically studying retention times in relation to carnivore body size might further unravel adaptations to carnivore feeding strategy. Gastrointestinal passage or retention time has been studied in carnivores in captivity and domestic carnivores (Bruce et al., 1999; Wyse et al., 2003; Boillat et al., 2010a; Elfström et al., 2013). Studying gastrointestinal transit in wild carnivores in captivity is useful when studying dietary composition based on faecal analysis in the wild, where incorporating gut retention time facilitates combining feeding habits with spatio-temporal behaviour (Elfström et al., 2013). An extensive amount of literature covers gastrointestinal passage in domestic carnivores, with the majority of studies concerning the domestic dog (C. familiaris) (e.g. Wyse et al., 2001; Rolfe et al., 2002). Such transit studies are often performed in order to establish reference standars for healthy individuals which should improve the diagnosis of gastrointestinal transit disorders (Bruce et al., 1999; Washabau, 2003; Wyse et al., 2003; Boillat et al., 2010a; Boillat et al., 2010b). Typically, gastric residence time or gastric emptying time is considered an important part of gastrointestinal passage and has been studied in dogs for species specific purposes (Boillat et al., 2010a), or as an animal model for human gastric motility in physiological and pharmaceutical studies (Wyse et al., 2003). Currently, several methods are available to assess total digesta transit time in animals and even the transit through the different compartments of the gastrointestinal tract (e.g. gastric emptying time). The most simple way to assess total gut retention time is the application of a particle marker (be it powder or beads) to the diet, where the pattern of faecal marker concentrations makes it possible
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to assess overall gut retention times (Thielemans et al., 1978). This method has been used predominantly in herbivore species (Steuer et al., 2010) but also in carnivore species (Tsuji et al., 2015). Given the need to study passage through different gut compartiments, several techniques have been developed and/or used in domestic carnivores such as diagnostic imaging techniques (e.g. radioscintigraphy), electric resistance techniques and tracer techniques (including gastric tracers, plasma tracers and breath tracers) (Wyse et al., 2003). Compiling data on the relation body size vs retention time might therefore not be as straightforward as is the case in herbivores where most retention time studies are restricted to a single method (see above). In carnivores, methodologies are widespread. However, apart from these methodology differences, one major constraint in the emperical study of body size and retention time, from an evolutionary perspective, is the dramatic shift in 'diet type'. Not only did domestic carnivores switch from a high protein, low carbohydrate to a high protein, high carbohydrate diet (Plantinga et al., 2011; Bosch et al., 2015), a switch from a high level of physical structure present in whole prey (presence of hairs, bones, tendons, feathers, i.e. animal fibre; Depauw et al., 2013) to a less structured pelleted or canned diet should not be neglected. Evidently, current transit studies are mostly performed with commercial diets (kibble and canned diets) (Itoh et al., 1986; Peachey et al., 2000; Wyse et al., 2003; Boillat et al., 2010b). The physical structure of a diet can affect transit parameters, e.g. plant fibre particle size and dietary particle size can affect transit in herbivores, birds and humans (Vincent et al., 1995; Ferguson and Harris, 1997; Carré, 2000). Although the dietary physical structure effect has not been studied in carnivores, it might be that whole prey acts differently than the average commercial petfood diet and that different transit even occurs between different body parts present in whole prey. Hence, it is important to unravel how gastrointestinal passage is affected by whole prey feeding if one wants to study evolutionary adaptations to carnivore feeding strategies. Carnivore body size might therefore be a determining driver of feeding strategies in the wild to which carnivores might have physiologically adapted. Digestive physiology diversity and the corresponding feeding strategy in the wild has extensively been studied in herbivorous mammals (Clauss et al., 2007a; Clauss et al., 2013; Müller et al., 2013) but is rather new in carnivore digestive physiology. The latter would offer more insight in digestive physiology of carnivores and lessons from the wild might be a key part in the management of carnivores in captivity and
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domestic carnivores. The use of domestic carnivores as a model for wild carnivores or vice versa should not impose major drawbacks (see section 3.).
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3. Domestic carnivores: the preservation of evolutionary adaptations The most extensively studied domestic carnivores are the domestic dog and cat. Dogs were domesticated ca. 14.000 years ago and diverged from their wild ancestor, the wolf (C.lupus), when man shifted from a hunter-gatherer to a sedentary lifestyle (Vilà et al., 1999; Bradshaw, 2006; Galibert et al., 2011; Axelsson et al., 2013; Frantz et al., 2013). Cats were domesticated approximately 9000-10.000 years ago and diverged from a least five subspecies of the wildcat (F. silvestris), similarly as the dog, during the transition of man from hunter-gatherer to an agricultural lifestyle (Driscoll et al., 2007). The domestic dogs' and cats' genome seems to be strongly preserved compared to their wild ancestors (O’Brien and Yuhki, 1999;
urphy et al.,
2000). Although breeding practices have led to a great morphological diversity among dogs and cats (Driscoll et al., 2009; Driscoll and Macdonald, 2010), this will not have affected certain physiological and metabolic traits in certain breeds since the breed-specific morphological traits are dominated by simple genetics (Lipinski et al., 2008; Boyko et al., 2010). The ability to synthesise essential nutrients and slow down the protein catabolism in wolves, e.g., is still present in domestic dogs (Legrand-Defretin, 1994; Kreeger, 2003; Bosch et al., 2015). Additionally, it would be very unlikely that dogs evolved certain physiological and metabolic traits that strongly differ from wolves (Meyer and Stadtfeld, 1980). However, dogs compared to wolves have evolved certain genetic mutations associated with starch digestion and glucose uptake which adapted them to the starch-rich diets commonly fed during domestication (Axelsson et al., 2013). Current knowledge on the digestive physiology of the wild ancestors stems mostly from studies in the domestic descendants. Knowledge on the wolf's digestive physiology e.g. has been largely deducted from studies of the domestic dog (Peterson and Ciucci, 2003). Although one has to be careful with drawing parallels between wild ancestors and domestic descendants because of dramatic shifts in diets between the wild and domestic species (see above; Axelsson et al. (2013)), studying the digestive physiology in domestic descendants might expose evolutionary adaptations also present in wild counterparts. Challenging domestic species with natural-like diets (i.e. whole prey diets) has not been common practice so far. The digestion and metabolism of domestic cats, e.g, has been studied on raw meat diets (commercially available) and whole prey in order to model
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digestive physiology of captive exotic felids (Vester et al., 2010a; Kerr et al., 2013; Kerr et al., 2014b). Similar studies might be of interest to expose any digestive physiological features on (preferably) whole prey diets. Additionally, unconventional diets such as whole prey feeding and raw meat feeding (e.g. bone and raw food (BARF)) are gaining more and more popularity in domestic carnivores (Schlesinger and Joffe, 2011; Freeman et al., 2013). Research concerning whole prey feeding is therefore imposing to unravel possible advantages and disadvantages where a knowledge on the whole prey associated digestive physiology is crucial.
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Vilà, C., J. E. Maldonado, and R. K. Wayne. 1999. Phylogenetic relationships, evolution, and genetic diversity of the domestic dog. J. Hered. 90:71–77. Vincent, R., A. Roberts, M. Frier, A. C. Perkins, I. A. MacDonald, and R. C. Spiller. 1995. Effect of bran particle size on gastric emptying and small bowel transit in humans: a scintigraphic study. Gut 37:216–219. Vucetich, J. A., M. Hebblewhite, D. W. Smith, and R. O. Peterson. 2011. Predicting prey population dynamics from kill rate, predation rate and predator–prey ratios in three wolf-ungulate systems. J. Anim. Ecol. 80:1236–1245. Warner, A. 1981. Rate of passage of digesta through the gut of mammals and birds. Nutr. Abstr. Rev. Ser. 51:789–820. Washabau, R. J. 2003. Gastrointestinal motility disorders and gastrointestinal prokinetic therapy. Vet. Clin. North Am. - Small Anim. Pract. 33:1007–1028. Washizu, T., A. Tanaka, T. Sako, M. Washizu, and T. Arai. 1999. Comparison of the activities of enzymes related to glycolysis and gluconeogenesis in the liver of dogs and cats. Res. Vet. Sci. 67:205–206. West, B. 2014. A fractional probability calculus view of allometry. Systems 2:89–118. White, C. R., and R. S. Seymour. 2003. Mammalian basal metabolic rate is proportional to body mass2/3. Proc. Natl. Acad. Sci. U. S. A. 100:4046–4049. White, C. R., and R. S. Seymour. 2005. Allometric scaling of mammalian metabolism. J. Exp. Biol. 208:1611–1619. Wilman, H., J. Belmaker, S. Jennifer, C. de la Rosa, M. M. Rivadeneira, and W. Jetz. 2014. EltonTraits 1.0: Species-level foraging attributes of the world’s birds and a als. Ecology 95:2027. Wilson, D. E., and D. M. Reeder, eds. 2005. Mammal species of the world: a taxonomic and geographic reference. 3rd edition. Johns Hopkins University Press, Baltimore, Maryland. Wilson, R. P., I. W. Griffiths, M. G. Mills, C. Carbone, J. W. Wilson, and D. M. Scantlebury. 2015. Mass enhances speed but diminishes turn capacity in terrestrial pursuit predators. Elife 4:e06487. Wong, J. M. W., R. de Souza, C. W. C. Kendall, A. Emam, and D. J. A. Jenkins. 2006. Colonic health: Fermentation and short-chain fatty acids. J. Clin. Gastroenterol. 40:235–243. Woodward, G., B. Ebenman, M. Emmerson, J. M. Montoya, J. M. Olesen, A. Valido, and P. H. Warren. 2005. Body size in ecological networks. TRENDS Ecol. Evol. 20:402–409. Wyse, C. A., J. McLellan, A. M. Dickie, D. G. M. Sutton, T. Preston, and P. S. Yam. 2003. A review of methods for assessment of the rate of gastric emptying in the dog and cat: 1898 – 2002. J. Vet. Intern. Med. 17:609–621.
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Wyse, C. A., T. Preston, S. Love, D. J. Morrison, J. M. Cooper, and P. S. Yam. 2001. Use of the 13 C-octanoic acid breath test for assessment of solid-phase gastric emptying in dogs. Am. J. Vet. Res. 62: 1939–1944. Xue, Z., W. Zhang, L. Wang, R. Hou, M. Zhang, L. Fei, X. Zhang, H. Huang, L. C. Bridgewater, Y. Jiang, C. Jiang, L. Zhao, X. Pang, and Z. Zhang. 2015. The bamboo-eating giant panda harbors a carnivore-like gut microbiota, with excessive seasonal variations. MBio 6:e00022. Zhou, Y., C. Newman, C. D. Buesching, A. Zalewski, Y. Kaneko, D. W. Macdonald, and Z.-Q. Xie. 2011. Diet of an opportunistically frugivorous carnivore, Martes flavigula, in subtropical forest. J. Mammal. 92:611–619.
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Scientific aims
Scientific aims
The digestive physiology of terrestrial carnivorous mammals is characterised by a notable diversity among species. The occurrence of peculiar physiological and metabolic traits might find their origin in body size driven feeding strategies in the wild (Bosch et al., 2015). It has been well established that carnivore body size is a determining factor in the choice for a specific prey size with a switch from small to large prey feeding at a body mass treshold of ca. 20 kg (Carbone et al., 1999). Carnivore body size and the associated average prey size could further dictate a carnivore's feeding strategy. Reports in the literature describe large carnivores hunting prey larger than or similar to their own mass, typically ingesting large amounts of highly digestible food alternated with periods of famine (feast-and-famine adherents) (e.g. the wolf (Stahler et al., 2006; Bosch et al., 2015)); and, small carnivores that tend to specialize in prey with a lower mass than their own body weight that will typically ingest small, frequent meals in a non-selective way (e.g. wildcat (Bradshaw, 2006)). As such, it seems that carnivore body size drives a whole feeding strategy. However, the functional existence of both feeding strategies and their relation to carnivore body size has not been studied for a broad carnivore size spectrum (i.e. vertebrate-prey feeders) and could offer more insight in species diversification. Given the apparent difference in food intake, kill frequency and dietary composition between both feeding strategies, a difference in gut retention time can be expected. However, since gut retention can be affected by the physical structure of the diet (Ferguson and Harris, 1997; Carré, 2000) and since the majority of gastrointestinal passage studies in domestic carnivores and carnivores in captivity are conducted on traditional kibble diets or processed meats (Wyse et al., 2003; Boillat et al., 2010), gut retention time should be studied on whole prey diets (presence of physical structure) as a first step for future empirical relations of gut retention time and carnivore body size. Whole prey is characterised by more heterogeneity and structure and might affect gastrointestinal passage in ways that hitherto have been left unstudied. In general, this dissertation aims to elucidate how carnivore feeding strategies have co-evolved with carnivore digestive physiology: Does carnivore body size drive the choice for the 'frequentfeeding' strategy and 'feast-and-famine' strategy? How does digestive processing (focussed on gastrointestinal transit) occur on a whole prey diet? First, the feature kill frequency, considered an important part of a feeding strategy, will be modelled and scaled to carnivore body size. Kill frequency modelling will
Scientific aims
account for several carnivore as well as prey characteristics: carnivore size, prey size, pack size, energetic requirements of carnivores, energy content in prey, gut capacity and selective feeding. Carnivores will be labelled feast-and-famine or frequent-feeding adherent based on the relationship prey size and gut capacity. The focus will be on vertebrate-prey feeding species given the different foraging strategies maintained by insectivorous and omnivorous species. The scaling of kill frequency with carnivore body size for both feeding strategies will render new information on the body size driven theory. The second part of this dissertation aims to study
passage through the carnivore
gastrointestinal tract on a whole prey diet (varied in structure). The domestic dog (Canis familiaris) will be studied as a carnivore species in order to unravel all components of gastrointestinal passage (gastric emptying time, small bowel transit time, colonic transit time and total transit time) and faecal characteristics (consistency and fermentation profiles) on whole prey diets.
Scientific aims
References Boillat, C. S., F. P. Gaschen, L. Gaschen, R. W. Stout, and G. L. Hosgood. 2010a. Variability associated with repeated measurements of gastrointestinal tract motility in dogs obtained by use of a wireless motility capsule system and scintigraphy. Am. J. Vet. Res. 71:903–908. Bosch, G., E. A. Hagen-Plantinga, and W. H. Hendriks. 2015. Dietary nutrient profiles of wild wolves: insights for optimal dog nutrition? Br. J. Nutr. 113:S40–S54. Bradshaw, J. W. S. 2006. The evolutionary basis for the feeding behavior of domestic dogs (Canis familiaris) and cats (Felis catus). J. Nutr. 136:S1927–S1931. Carbone, C., G. M. Mace, S. C. Roberts, and D. W. Macdonald. 1999. Energetic constraints on the diet of terrestrial carnivores. Lett. to Nat. 402:286–288. Carré, B. 2000. Effets de la taille des particules alimentaires sur les processus digestifs chez les oiseaux d’élevage. Prod. Ani . - Paris - Inst. Natl. la Rech. Agron. 13:131–136. Ferguson, L. R., and P. J. Harris. 1997. Particle size of wheat bran in relation to colonic function in rats. LWT - Food Sci. Technol. 30:735–742. Stahler, D. R., D. W. Smith, and D. S. Guernsey. 2006. Foraging and feeding ecology of the gray wolf (Canis lupus): Lessons from Yellowstone National Park, Wyoming, USA. J. Nutr. 136:S1923–S1926. Wyse, C. A., J. McLellan, A. M. Dickie, D. G. M. Sutton, T. Preston, and P. S. Yam. 2003. A review of methods for assessment of the rate of gastric emptying in the dog and cat: 1898 – 2002. J. Vet. Intern. Med. 17:609–621.
.
Research chapters
1. Predator-prey size ratios determine kill frequency and carcass surplus production in terrestrial carnivorous mammals
Adapted from De Cuyper A1, Clauss M2, Carbone C3, Codron D4,5,6, Cools A1, Hesta M1 and Janssens GPJ1. Predator-prey size ratios determine kill frequency in carnivores and carcass provision for scavengers. Submitted 18th of August 2017, Oecologia (Under review) 1
Laboratory of Animal Nutrition, Department of Nutrition, Genetics and Ethology, Faculty of Veterinary Medicine, Ghent University, Heidestraat 19 9820 Merelbeke, Belgium 2
Clinic for Zoo Animals, Exotic Pets and Wildlife, University of Zurich, Winterthurerstrasse 260 CH-8057 Zürich, Switzerland 3
Institute of Zoology, Zoological Society of London, Regent's Park, London NW 1 4RY, United Kingdom 4
Institut für Geowissenschaften, AG für Angewandte und Analytische Paläontologie, Johannes Gutenberg-Universität Mainz, 55128 Mainz, Germany 5
Florisbad Quaternary Research Department, National Museum, PO Box 266, Bloemfontein, 9300, South Africa 6
Centre for Environmental Management, University of the Free State, PO Box 339, Bloemfontein, 9300, South Africa
Chapter 1
1.1 Abstract Carnivore kill frequency is a fundamental part of predator-prey interactions which are important ecosystem shapers. Current field kill frequency data are lacking and existing models are insufficiently adapted to carnivore functional groups. We developed a kill frequency model accounting for carnivore mass, prey mass, carnivore specific maintenance energy requirements and metabolisable energy in prey, hunting pack size, selective feeding and carnivore gut capacity. Two main carnivore functional groups, small prey-feeders vs large prey-feeders, were established based on the relationship gut capacity (C) and pack corrected prey mass (iMprey); both groups have a linear scaling of the predator-prey size relationship, and although the majority of small prey-feeders is below, and of large prey-feeders above a body mass of 10-20 kg, both occur across the whole body size spectrum. Generally, kill frequency models predict an overall negative relationship between predator size and kill frequency, which we confirmed for large prey-feeders. However for small prey-feeders, this negative relationship was absent. When comparing carnivore prey requirements to estimated stomach capacity, small carnivores may have to eat to their full capacity repeatedly per day, requiring fast digestion and gut clearance. Large carnivores do not necessarily have to consume until they reach their maximal gastric capacity per day, or do not need to eat every day, which in turn reduces kill frequencies or drives other ecological processes such as scavenging, kleptoparasitism, and selective (incomplete) carcass consumption. The large prey-feeding strategy therefore appears particularly attractive for large carnivores, which can thus reduce activities related to hunting.
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1.2 Introduction Terrestrial carnivores are important drivers of the top-down control of ecosystems and the shaping of community structure, through both predation and intraguild interactions (Terborgh, 1992; McLaren and Peterson, 1994; Ritchie and Johnson, 2009). Predator-prey relationships are considered fundamental for studying terrestrial and marine ecosystems (Cohen et al., 1993; Heithaus, 2001; Carbone et al., 2014). Relating predator size to prey size is a commonly used approach to describe community interactions and feeding relationships at an interspecific level (Rosenzweig, 1966; Holling et al., 1976; Paine, 1976; Carbone et al., 1999). It is known that carnivore body size drives the choice for a specific prey size (Peters, 1983; Carbone et al., 1999; Carbone et al., 2014): a switch from small to large prey feeding occurs at a body mass threshold of about 20 kg (Carbone et al., 1999; Carbone et al., 2007). Small carnivores (20kg) will opt for large vertebrates equal to or exceeding their own mass (Carbone et al., 2007). Other important elements in predator-prey interactions, which are also related to body size, include the frequency at which carnivores consume prey (kills/predator/time) (Holling, 1959; Vézina, 1985; Vucetich et al., 2011), carnivore energetics (Carbone et al., 1999; Pawar et al., 2012; Carbone et al., 2014) and community structure (Nilsen et al., 2009; Vucetich et al., 2011). However, literature on field kill frequency data is rather scarce and almost exclusively available for large carnivores because of the labour intensive field methods and the fact that small prey items are mostly consumed entirely and therefore missed by field methods. Some papers report kill frequencies for small carnivores (e.g. van Aarde (1980); feral cat) but base the kill frequency on annual caloric requirement estimations rather than on direct observations. Others only consider preyspecific kill frequencies (e.g. the number of moose killed by wolves) and do not consider all prey species hunted by the carnivore (e.g. Zimmermann et al. (2015)). Apart from field kill frequency data, efforts have been made to estimate carnivore kill frequency for a broad carnivore range based on carnivore prey size and energetic requirements (Peters, 1983; Vézina, 1985). Estimates show a decrease in kill frequency with (i) increasing carnivore body size and (ii) increasing prey size, which implies that smaller carnivores have more hunting obligations than do larger carnivores. For example, small cats need to kill multiple times per day (Bradshaw, 2006). Considering kill frequencies alongside prey size, prey energy content and energy requirements shows that smaller carnivores need to invest a significant portion of their day hunting (Jeschke, 2007). Larger carnivores can afford 66
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to be 'lazy' since they can produce prey surplus on top of their energetic maintenance requirements. The approaches used in previous modeling, however, do not explicitly account for a very important consequence of the predator-prey-mass relationship within vertebrate-prey feeders: predators taking prey whose mass exceeds their intake capacity can feed selectively on their prey, using only parts of increased energy density (Hornocker, 1967; Bowland and Bowland, 1991; Stahler et al., 2006; Gidna et al., 2014; Bosch et al., 2015), whereas predators that kill comparatively small prey will consume their prey entirely (Mills, 1996; Bothma and Coertze, 2004; Anwar et al., 2011). On the other hand, predators might not be able to fully consume their comparatively large prey, due to the limitation of their own intake capacity and the problem of preventing kleptoparasitism (scavenging) by other predators over an extended period of time (Carbone et al., 1997). Not considering predators separately whose prey does or does not exceed intake capacity may lead, for example, to estimates of kill frequencies for a 4 kg cat of 0.8 (Vézina, 1985) or 1.6 (Peters, 1983) times per day, rather than the 'multiple times' considered realistic for cats (Bradshaw, 2006). Therefore, we wanted to explore the relationship between kill frequency and carnivore body size and elucidate whether this varies across functional carnivore groups within the group of vertebrate-prey feeders (considering prey size in relation to intake capacity). In doing so, we develop a kill frequency model based on carnivore mass, the average of most common prey mass per carnivore, carnivore specific maintenance energy requirements and metabolisable energy in prey, hunting pack size, gut capacity, and the opportunity for selective feeding. Our working hypothesis was that if the mean prey mass available for the individual predator at a kill scaled lower than, or similar to, energy requirements, then no reduction in kill frequency and hunting obligation would occur with increasing predator mass; in contrast, if the prey mass available for the individual predator scaled higher than energy requirements, then a reduction in kill frequency would occur with increasing predator mass. We hypothesized that these results would be modified depending on the difference between prey mass and gut capacity.
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1.3 Material and methods 1.3.1 Data set A literature review was performed using Web of Knowledge, Pubmed and Google scholar to identify potentially eligible studies reporting feeding habits of wild carnivores. The literature search was conducted following Leenaars et al. (2012) by using two search terms, one based on the order of the Carnivora and the second on feeding habit associated factors. Aquatic carnivores or carnivores that depend on aquatic foraging strategies as well as carnivores of which the diet consists
ainly (≥ 50 %) of vegetation and/or invertebrates were excluded
from the database (based on the quantitative dataset on mammalian diets of Wilman et al. (2014)). The latter was done given the difference in foraging strategies between terrestrial vertebrate-prey feeders and insectivorous or omnivorous carnivores, and aquatic carnivores. Clearly, these foraging strategies differ in terms of search and feeding time (e.g. the difference in dispersal of terrestrial vertebrate and invertebrate prey; in the marine environment several small prey can be 'subdued' in the same hunting bout (swarms of fish) whereas this is not seen in terrestrial environments). The following data were extracted from each publication: carnivore species, study location, methods used for diet analysis, number of samples, carnivore sex, most frequent prey based on frequency or relative frequency of occurrence (FO= frequency of occurrence= identified prey items of a certain species/total number of scats (%); rFO= relative frequency of occurrence= identified prey items of a certain species/total number of prey items (%)), pack size (number of animals) (Npack), kill frequency (1 kill/x days) (the 'real' kill frequency rKF) and maximal gut capacity (kg/carnivore/feeding event) (C). For the lion (Panthera leo), the spotted hyena (Crocuta crocuta), the tiger (Panthera tigris), the leopard (Panthera pardus), the cheetah (Acinonyx jubatus) and the African wild dog (Lycaon pictus), we included the reviews of Hayward and collaborators (Hayward and Kerley, 2005; Hayward, 2006; Hayward et al., 2006a; Hayward et al., 2006b; Hayward et al., 2006c; Hayward et al., 2012). Therefore, publications used in these reviews were excluded from the dataset. For pack size, maximal gut capacity and kill frequency data, additional literature searches were conducted. Predator and prey mass (kg) (female and male average or range average) (Mpred, Mprey) were obtained from publications itself when authors were able to give typical carnivore and/or prey masses from the study area. Other carnivore and prey masses were mainly obtained from Nowak's Walker's Mammals of the world (Nowak, 1999), the panTHERIA database (Jones et
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al., 2009) and the internet as a last reference. Other small dietary items were estimated at 0.001 kg for insects, 0.005 kg for aquatic invertebrates, 0.1 kg for small unidentified rodents and birds (Carbone et al., 1999). If studies expressed the most frequent prey as a group, class or order (e.g. small mammals, rodents), the average mass of that group (when given by publication) or all species included in that group, class or order was taken as mass of the most frequent prey. Whenever studies reported juveniles of a prey species as being the most frequent prey, juvenile prey mass given by the authors was used. If no juvenile prey mass was available, juvenile mass found in Nowak's Walker's mammals (Nowak, 1999) were used, or 10 % of the maternal prey mass was taken as representative of juvenile prey mass (Blueweiss et al., 2010). If the most frequent prey was confirmed to be carrion, the data point was omitted. If, for a certain carnivore species, the study gave the most frequent prey per location and/or per season/year/period, then prey was inserted per location and/or per season/year/period unless a total of all localities and/or periods was given. Whenever it occured that the frequency of occurrence of prey species A was lower than the frequency of occurrence of prey order B and prey order B had no species specification, then the frequency of occurrence of the prey order of species A was used to compare with the frequency of occurrence of prey order B. Whenever a study had two most frequent prey species that showed identical frequencies of occurrence, both were included in the database. If the study did not report frequency (FO) or relative frequency (rFO) of occurrence to point out the most frequent prey of a predator (e.g. indexes, consumed biomass,% of dry matter of scats) and/or FO and rFO could not be calculated from present measures (e.g. from consumed biomass), the study was excluded. Whenever the study itself mentioned that too few scats were analysed to determine the diet of a certain carnivore species, that part of the study was excluded. Per carnivore species, 10 publications (or less if no more than 10 were available), focussing on reviews, were added to the database. Observed kill frequency data (rKF) were corrected for the pack size of the carnivore species, obtained from the publication itself (i.e., dividing the reported frequency with pack size). Kill frequencies that apply only to a specific prey species (e.g., the number of moose killed by wolves, irrespective of other prey taken in the same time period) were not taken into account since these estimates did not consider all prey species hunted by the carnivore (Kroshko et al., 2016). Per carnivore species, the average of most common prey mass (Mprey), the average NPack and the average rKF were calculated.
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1.3.2 Kill frequency modelling A theoretical kill frequency (KF) model was developed based on Mpred, Mprey, carnivore specific maintenance energy requirements (Qpred) and metabolisable energy in prey (Eprey). For each species, KF is calculated as Qpred / Eprey. Based on the scaling relationships of Mprey ~ Mpredp Qpred ~ Mpredq and the assumption that the energy content of prey is directly proportional to prey mass, we would expect KF ~ Mpred(q-p) However, given the occurrence of pack hunting, and our considerations about feeding selectivity and gut capacity, several modifications to this simple concept need to be applied. Under the assumption that pack size scales with predator mass Npack ~ Mpredn the amount of prey available for the individual predator (iMprey) scales to iMprey ~ Mpred(p-n) and therefore KF ~ Mpred(q-p+n) Note that a scaling of pack size with body mass may not be expected, but data for individual species must be corrected for pack size nevertheless. The relationship of Mprey ~ Mpredp needs to be established for several groups of predators, in relation to their gut capacity C. We divided predators into those where iMprey < 1% of C (i.e., predators mainly preying on insects), those where 1% of C < iMprey < C (or 'small prey pedators'), and those where C < iMprey (or 'large prey predators' who cannot consume their average prey in one meal). The metabolisable energy of whole prey was estimated at 5348 kJ/kg fresh weight calculated from data given by Plantinga et al. (2011), and prey items < 5 kg were considered to be completely edible whereas prey items of > 5 kg were considered 95% edible. For selective feeding, prey was considered to be consumed as 70% (Mills, 1990; Stander, 1992; Caro, 1994), at a metabolisable energy content of 8048 kJ/kg fresh weight (the
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average value given by Bosch et al. (2015) taking into account the selective feeding of wolves (Canis lupus)). Large prey predators were assumed to only consume the equivalent of their gut capacity C per day. For this group, KF estimates were either based on a single-day feeding on their prey (in a selective mode, i.e. eating the amount of C at 8048 kJ/kg) or a complete consumption of their prey (in a non-selective mode, i.e. with 95% consumption at 5348 kJ/kg), to outline theoretical minimum and maximum kill frequencies. Following Nagy et al. (1999), we parameterize the relationship of Qpred = b Mpredq as Qpred = 791kJ Mpred0.85 d-1. Evaluations of scaling relationships were performed using linear regressions for logtransformed data in ordinary least squares (OLS) in R using the package nlme (Pinheiro et al., 2011). To account for the phylogenetic structure of the dataset, data were linked to a phylogenetic tree (Fritz et al., 2009), and also analysed in phylogenetic generalized least squares (PGLS) with the phylogenetic signal λ esti ated by
axi u
likelihood, using the
package caper (Orme et al., 2010). Extrapolation to other species (for C) was based on OLS scaling, because PGLS scalings are based on phylogenies that do not include the species to which the extrapolation is to be applied. Because we considered the polar bear (Ursus maritimus) as an extreme example of a predator that might switch between comparatively small prey (fish) and large prey (seals), we excluded this species from scaling analyses, and used it as an example for the range of kill frequencies available to large carnivores with the option of such a large prey range. For comparison, the KF models of Peters (1983) and Vézina (1985) were included in the graphs representing our KF.
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1.4 Results 1.4.1 Carnivore characteristics A total of 456 studies, 513 prey size datapoints, 182 pack size datapoints, 56 kill frequency datapoints and 22 gastric capacity datapoints were incorporated in the database. Seventy eight carnivore species were included in the prey size database. Pack size data could only be obtained for 75 carnivore species. Real kill frequency data were obtained for 11 carnivore species. Carnivore weight ranged from 0.1375 to 387.5 kg. Data on the maximal gastric capacity (C) were available for 9 species ranging from 0.19 kg to 150.0 kg; these data were used to determine the allometric function [with 95% CI] of C = 0.09 [0.06;0.14] Mpred1.19 [1.07;1.30]
, which was used to calculate the C for all carnivore species. A compilation of the
carnivore families and species included in the dataset for KF modelling can be found in Appendix 1. Of the 75 carnivore species for which pack data were available, 12 species were pack hunters and 63 species were solitary hunters. Pack size scaled nominally to 1 [1;1] Mpred0.14 [0.05;0.24]. Of the 12 pack hunting species, 7 species had a C < iMprey, i.e. the pack could not consume the whole prey animal in one day. Five pack hunting species had larger C than iMprey, i.e. were supposedly sharing prey that each individual could have eaten more of - the yellow throated marten (Martes flavigula, 2 pack members), the golden/asian jackal (Canis aureus, 2.5 pack members), red wolf (Canis rufus, 2.4 pack members), Ethiopian wolf or simien jackal (Canis simensis, 5.7 pack members), and bush dog (Speothos venaticus, 11 pack members). Of these, only the bush dog had a higher Mprey than C (i.e. the pack was killing prey that would have been too large to be consumed by an individual member). Therefore, the bush dog appeared as an outlier in the graph displaying the Mpred-Mprey relationship (Fig. 1a), but not in the graph linking Mpred to iMprey (Fig. 1b).
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(a)
(b)
Fig. 1 Relationship between individual predator species mass and (a) average prey mass or (b) average prey mass divided by the number of pack members (iMprey) The dotted line represents y=x (prey mass = predator mass). Predators are groups according to their iMprey relative to their stomach capacity C. The linked diamonds indicate the two ecotypes of the polar bear (Ursus maritimus, see text). Note that due to its comparatively large prey and large pack size, the bushdog (Speothos venaticus) is an outlier in (a) but not in (b). For statistics, see Table 1.
Real kill frequency data were found for 11 species weighing between 11.2 kg and 175.5 kg. Using species averages, the real kill frequency scaled to 1.11 [0.20;6.18] Mpred-0.48 [-0.91;-0.04], and did not show a phylogenetic signal (λ not significantly different from 0).
1.4.2 Predator-prey mass scaling Across all carnivore species, prey mass scaled to predator mass with a scaling exponent larger than 1.0, also exceeding linearity in the 95% confidence interval (Table 1). In contrast, when considering carnivore groups individually based on relative prey size, linear scaling was included in the 95% confidence interval of both small and large prey predators and hence also overlapped between these groups (Table 1). However, there was a large difference in the scaling factor (intercept), which was 0.05 for small prey predators and 0.5 for large prey predators, with no overlap in the 95% confidence intervals (Table 1).
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Table 1 Scaling relationships of prey mass (Mprey) or prey mass available for the individual predator (iMprey) with predator mass (Mpred) according to a Mpredb in different datasets (depending on the relationship between stomach capacity C and iM prey) using ordinary least squares (OLS) or phylogenetic generalized least squares (PGLS) Dependent
Dataset
n
Statistic
λ
a (95%CI)
p
b (95%CI)
p
whole
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OLS
(0)
0.03 (0.01;0.07)