Diet and body temperature in mammals and birds

Aim We test the hypothesis that endotherm body temperature varies with diet. Location Global terrestrial ecosystems. Methods We compile data from the literature on diet and body temperature in mammals and birds. We analyse these and demonstrate global macrophysiological patterns. Results In mammals, carnivores overall have a lower mean body temperature (Tb) than either herbivores or omnivores. However, within carnivores, those taking vertebrate prey have a higher mean Tb than predators of invertebrates. Among herbivores, species eating grass, leaves or seeds have the highest mean Tb, those taking fruit an intermediate mean Tb and those taking flowers or nectar the lowest mean Tb. These patterns are robust to the influence of body mass and phylogenetic non-independence. In birds the relationship between Tb and diet is complicated by a significant inverse relationship between body mass and Tb and strong dietary niche conservation within lineages. After allowing for body mass, herbivores show an identical qualitative pattern to mammals, whereas carnivores show the opposite trend to mammals: those taking invertebrate prey have a higher mean Tb than those taking vertebrates. Main conclusions There is a significant relationship between diet and Tb in mammals. Birds show a qualitatively similar but non-significant pattern. Published studies show that in reptiles and fish herbivory is largely confined to species that can maintain a relatively high Tb either by living in warm environments or through behavioural thermoregulation. We therefore propose a general relationship for all vertebrates: herbivory requires a warmer body than carnivory. The basal metabolic rate (BMR) will then be higher in herbivores because of the universal relationship between BMR and Tb, together with the higher maintenance costs of their longer guts. We suggest that the evolution of endothermy was a key factor in the widespread incidence of herbivory in mammals.

[1]  G. Gunnell,et al.  Giant lizards occupied herbivorous mammalian ecospace during the Paleogene greenhouse in Southeast Asia , 2013, Proceedings of the Royal Society B: Biological Sciences.

[2]  W. Jetz,et al.  The global diversity of birds in space and time , 2012, Nature.

[3]  R. Marquis,et al.  Herbivore pressure increases toward the equator , 2012, Proceedings of the National Academy of Sciences.

[4]  B. G. Lovegrove,et al.  The evolution of mammalian body temperature: the Cenozoic supraendothermic pulses , 2012, Journal of Comparative Physiology B.

[5]  D. Ellerby,et al.  Leeches run cold, then hot , 2011, Biology Letters.

[6]  J. Eiler,et al.  Dinosaur Body Temperatures Determined from Isotopic (13C-18O) Ordering in Fossil Biominerals , 2011, Science.

[7]  W. Karasov,et al.  Ecological physiology of diet and digestive systems. , 2011, Annual review of physiology.

[8]  H. Pörtner,et al.  Temperature, metabolic power and the evolution of endothermy , 2010, Biological reviews of the Cambridge Philosophical Society.

[9]  C. Labandeira,et al.  Fossil insect folivory tracks paleotemperature for six million years , 2010 .

[10]  J. D. Hoyo,et al.  Handbook of the Birds of the World , 2010 .

[11]  N. Isaac,et al.  Scaling of basal metabolic rate with body mass and temperature in mammals. , 2010, The Journal of animal ecology.

[12]  Kevin J. Gaston,et al.  Macrophysiology: A Conceptual Reunification , 2009, The American Naturalist.

[13]  Kate E. Jones,et al.  PanTHERIA: a species‐level database of life history, ecology, and geography of extant and recently extinct mammals , 2009 .

[14]  R. Freckleton The seven deadly sins of comparative analysis , 2009, Journal of evolutionary biology.

[15]  Susanne A. Fritz,et al.  Geographical variation in predictors of mammalian extinction risk: big is bad, but only in the tropics. , 2009, Ecology letters.

[16]  K. Clements,et al.  Nutritional ecology of marine herbivorous fishes: ten years on , 2009 .

[17]  B. McNab An analysis of the factors that influence the level and scaling of mammalian BMR. , 2008, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[18]  D. Royer,et al.  Sharply increased insect herbivory during the Paleocene–Eocene Thermal Maximum , 2008, Proceedings of the National Academy of Sciences.

[19]  P. Withers,et al.  Comprar Ecological and Environmental Physiology of Amphibians | Stanley S. Hillman | 9780198570318 | Oxford University Press , 2008 .

[20]  P. Rothery,et al.  Scaling of body temperature in mammals and birds , 2007 .

[21]  R. Baker,et al.  Squirrels: the animal answer guide , 2007 .

[22]  Ron B. H. Wills,et al.  Effects of temperature. , 2007 .

[23]  H. R. D. Silva,et al.  How much fruit do fruit‐eating frogs eat? An investigation on the diet of Xenohyla truncata (Lissamphibia: Anura: Hylidae) , 2006 .

[24]  C. R. White,et al.  The scaling and temperature dependence of vertebrate metabolism , 2006, Biology Letters.

[25]  C. R. White,et al.  Sample size and mass range effects on the allometric exponent of basal metabolic rate. , 2005, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[26]  D. S. Glazier,et al.  Beyond the ‘3/4‐power law’: variation in the intra‐and interspecific scaling of metabolic rate in animals , 2005, Biological reviews of the Cambridge Philosophical Society.

[27]  M. Horn,et al.  Geographical gradients of marine herbivorous fishes: patterns and processes , 2005 .

[28]  C. Tracy,et al.  Recurrent evolution of herbivory in small, cold-climate lizards: breaking the ecophysiological rules of reptilian herbivory. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  B. G. Lovegrove,et al.  Locomotor Mode, Maximum Running Speed, and Basal Metabolic Rate in Placental Mammals , 2004, Physiological and Biochemical Zoology.

[30]  C. R. White,et al.  Does Basal Metabolic Rate Contain a Useful Signal? Mammalian BMR Allometry and Correlations with a Selection of Physiological, Ecological, and Life‐History Variables , 2004, Physiological and Biochemical Zoology.

[31]  C. R. White,et al.  Mammalian basal metabolic rate is proportional to body mass2/3 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[32]  B. G. Lovegrove,et al.  The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum , 2003, Journal of Comparative Physiology B.

[33]  Tobias Wang,et al.  Effects of temperature on the metabolic response to feeding in Python molurus. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[34]  W. Cooper,et al.  Distribution, extent, and evolution of plant consumption by lizards , 2002 .

[35]  K. Clements,et al.  Hindgut Fermentation in Three Species of Marine Herbivorous Fish , 2002, Applied and Environmental Microbiology.

[36]  L. Fuiman,et al.  A killer appetite: metabolic consequences of carnivory in marine mammals. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[37]  P. Coley,et al.  Insect herbivory, plant defense, and early Cenozoic climate change , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Barry G Lovegrove,et al.  The Zoogeography of Mammalian Basal Metabolic Rate , 2000, The American Naturalist.

[39]  M. Pagel Inferring the historical patterns of biological evolution , 1999, Nature.

[40]  M. O’connor,et al.  Biophysical constraints on the thermal ecology of dinosaurs , 1999, Paleobiology.

[41]  C. Labandeira,et al.  Response of plant-insect associations to paleocene-eocene warming , 1999, Science.

[42]  J. Speakman The Cost of Living: Field Metabolic Rates of Small Mammals , 1999 .

[43]  Daryl E. Wilson,et al.  Mammal Species of the World: A Taxonomic and Geographic Reference , 1993 .

[44]  D. Penny The comparative method in evolutionary biology , 1992 .

[45]  B. McNab A statistical analysis of mammalian rates of metabolism , 1992 .

[46]  C. Tracy,et al.  Interactions between the Environment and Ectothermy and Herbivory in Reptiles , 1989, Physiological Zoology.

[47]  M. Horn Biology of marine herbivorous fishes , 1989 .

[48]  W. Wiebe,et al.  Fermentative microbial digestion in herbivorous fishes , 1987 .

[49]  A. Heusner,et al.  Body size and energy metabolism. , 1985, Annual review of nutrition.

[50]  J. Lubchenco,et al.  A UNIFIED APPROACH TO MARINE PLANT-HERBIVORE INTERACTIONS. II. BIOGEOGRAPHY , 1982 .

[51]  D. Chivers,et al.  Morphology of the gastrointestinal tract in primates: Comparisons with other mammals in relation to diet , 1980, Journal of morphology.

[52]  J. W. Lang Thermophilic Response of the American Alligator and the American Crocodile to Feeding , 1979 .

[53]  F. H. Pough,et al.  Lizard Energetics and Diet , 1973 .

[54]  B. McNab An Analysis of the Body Temperatures of Birds , 1966 .