Abstract
Maintaining adequate energy and mass balance is necessary to the survival and reproduction of any organism. However, nearly all organisms experience periods of catabolism, when insufficient food is being consumed and endogenous stores must be metabolized to provide the difference. The ubiquity of this phenomenon, perhaps an intuitive understanding of the threat that starvation poses to an individual’s survival, and the fact that many organisms seem to "voluntarily" enter long periods of catabolism (fasting) has caused great interest among physiologists to discover and understand the mechanisms organisms have evolved to survive such periods. In wild animals, merely detecting the existence and duration of periods of fasting or starvation can be difficult and much effort has been devoted toward establishing stable isotope analysis (SIA) as a tool for detecting and understanding the duration of catabolic states in wild animals. However, the results of these studies have been mixed. Increasingly, SIA is also being used to investigate the mechanisms organisms use to cope with periods of catabolism: how nutrients are routed, which are recycled, which are used for energy, and how that differs between different organs and organ systems. This chapter reviews the past and current applications of SIA for understanding fasting and starvation in animals and identifies areas where SIA may yet be applied to increase our understanding of fasting and starvation.
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References
Adams TS, Sterner RW (2000) The effect of dietary nitrogen content on trophic level 15N enrichment. Limnol Oceanogr 45:601–607
Adamscewski JZ (1995) Digestion and body composition in muskoxen. University of Saskatchewan
Alamaru A, Yam R, Shemesh A, Loya Y (2009) Trophic biology of Stylophora pistillata larvae: evidence from stable isotope analysis. Mar Ecol-Progr Ser 383:85–94
Ankney CD, MacInnes CD (1978) Nutrient reserves and reproductive performance of female Lesser Snow Geese. Auk 95:459–471
Ayliffe LK, Cerling TE, Robinson T, West AG, Sponheimer M, Passey BH, Hammer J, Roeder B, Dearing MD, Ehleringer JR (2004) Turnover of carbon isotopes in tail hair and breath CO2 of horses fed an isotopically varied diet. Oecologia 139:11–22
Baker AL, Kotake AN, Schoeller DA (1983) Clinical utility of breath tests for the assessment of hepatic function. Semin Liver Dis 3:318–329
Barboza PS, Parker KL (2006) Body protein stores and isotopic indicators of N balance in female reindeer (Rangifer tarandus) during winter. Physiol Biochem Zool 79:628–644
Battley PF, Dietz MW, Piersma T, Tang S, Hulsman K (2000) Is long-distance bird flight equivalent to a high-energy fast? Body composition changes in migrated and fasted Great Knots. Physiol Biochem Zool 74(3):435–449
Bauchinger U, Kolb H, Afik D, Pinshow B, Biebach H (2009) Blackcap warblers maintain digestive efficiency by increasing digesta retention time on the first day of migratory stopover. Physiol Biochem Zool 82:541–548
Bazar KA, Yun AJ, Lee PY (2005) “Starve a fever and feed a cold: feeding and anorexia may be adaptive behavioral modulators of autonomic and T helper balance”. Med Hypotheses 64:1080–1084
Ben-David M, McColl CJ, Boonstra R, Karels TJ (1999) 15N signatures do not reflect body condition in Arctic ground squirrels. Can J Zool 77:1373–1378
Best PB, Schell DM (1996) Stable isotopes in southern right whale (Eubalaena australis) baleen as indicators of seasonal movements, feeding and growth. Marine Biol 124:483–494
Biebach H (1990) Strategies of trans-Sahara migrants. In: Gwinner E (ed) Bird migration. Springer, Berlin
Boag B, Neilson R, Scrimgeour CM (2006) The effect of starvation on the planarian Arthurdendyus triangulatus (Tricladida:Terricola) as measured by stable isotopes. Biol Fert Soils 43:267–270
Bonnet X, Bradshaw D, Shine R (1998) Capital versus income breeding: an ectothermic perspective. Oikos 83:333–342
Bottitta GE, Nol E, Gilchrist HG (2003) Effects of experimental manipulation of incubation length on behavior and body mass of Common Eiders in the Canadian Arctic. Waterbirds 26:100–107
Browne T, Lalas C, Mattern T, van Heezik Y (2011) Chick starvation in yellow-eyed penguins: evidence for poor diet quality and selective provisioning of chicks from conventional diet analysis and stable isotopes. Austral Ecol 36:99–108
Cahill GF (1970) Starvation in man. J Clin Endocrinol Metab 5:397−415
Castellini MA, Rea LD (1992) The biochemistry of natural fasting at its limits. Experientia 48:575–582
Castillo LP, Hatch KA (2007) Fasting increases δ15N-values in the uric acid of Anolis carolinensis and Uta stansburiana as measured by nondestructive sampling. Rapid Commun Mass Spectrom 21:4125–4128
Chang HR, Bistrian B (1998) The role of cytokines in the catabolic consequences of infection and injury. J Parent Enter Nutr 22:156–166
Cherel Y, Robin J, Le Maho Y (1988) Physiology and biochemistry of long-term fasting in birds. Can J Zool 66:159–166
Cherel Y, Hobson KA, Bailleul F, Groscolas R (2005) Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881–2888
Chow S et al (2010) Japanese eel Anguilla japonica do not assimilate nutrition during the oceanic spawning migration: evidence from stable isotope analysis. Mar Ecol-Progr Ser 402:233–238
Conti-Nibali S, Baldari S, Vitulo F, Sferlazzas C, Russo E, Tedeschi A, Bonanno N, Magazzu G (1990) The 14CO2 urea breath test for Helicobacter pylori infection. J Pediat Gastroenterol Nutr 11:284–285
Darwin C (1859) The origin of species by means of natural selection, 6th edn. Project Gutenberg, London
Delvin EE, Brazier JL, Deslandres C, Alvarez F, Russo P, Seidman E (1999) Accuracy of the (13C)-urea breath test in diagnosing Helicobacter pylori gastritis in pediatric patients. J Pediat Gastroenterol Nutr 28:59–62
Demmelmair H, Sauerwald T, Koletzko B, Richter T (1997) New insights into lipid and fatty acid metabolism via stable isotopes. Eur J Pediat 156(Suppl 1):S70–S74
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506
Doi H, Kikuchi E, Takagi S, Shikano S (2007) Changes in carbon and nitrogen stable isotopes of chironomid larvae during growth, starvation and metamorphosis. Rapid Commun Mass Spectrom 21:997–1002
Doucett RR, Booth RK, Power G, McKinley RS (1999) Effects of the spawning migration on the nutritional status of anadromous Atlantic salmon (Salmo salar): insights from stable-isotope analysis. Can J Fisheries Aquat Sci 56:2172–2180
Drent R, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252
Duchesne J, Lacroix M, Mosora F (1982) Use of the 13C/12C breath test to study sugar metabolism in animals and men. In: Schmidt HL, Forstel H, Heinzinger K (eds) Stable isotopes. Elsevier Scientific Publishing Company, Amsterdam
Focken U (2001) Stable isotopes in animal ecology: the effect of ration size on the trophic shift of C and N isotopes between feed and carcass. Isot Environ Health Stud 37:199–211
Fuller BT, Fuller JL, Sage NE, Harris DA, O’Connell TC, Hedges REM (2004) Nitrogen balance and δ15N: why you’re not what you eat during pregnancy. Rapid Commun Mass Spectrom 18:2889–2896
Fuller BT, Fuller JL, Sage NE, Harris DA, O’Connell TC, Hedges REM (2005) Nitrogen balance and δ15N: why you’re not what you eat during nutritional stress. Rapid Commun Mass Spectrom 19:2497
Gaebler OH, Vitti TG, Vukmirovich R (1966) Isotope effects in metabolism of 14N and 15N from unlabeled dietary proteins. Can J Biochem 44:1249–1257
Gannes LZ, O’Brien D, Martinez del Rio C (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271–1276
Gannes LZ, Martinez del Rio C, Koch P (1998) Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comp Biochem Physiol A 119:725–737
Gauthier G, Bety J, Hobson KA (2003) Are greater snow geese capital breeders? New evidence from a stable-isotope model. Ecology 84:3250–3264
Gaye-Siessegger J, Focken U, Muetzel S, Abel H, Becker K (2004) Feeding level and individual metabolic rate affect δ13C and δ15N values in carp: implications for food web studies. Oecologia 138:175–183
Gaye-Siessegger J, Focken U, Abel H, Becker K (2007) Starvation and low feeding levels result in an enrichment of 13C in lipids and 15N in protein of Nile tilapia Oreochromis niloticus L. J Fish Biol 71:90–100
Gil D, Heim C, Rocha M, Puerta M, Nagiulo M (2004) Negative effects of early developmental stress on yolk testosterone levels in a passerine bird. J Exp Biol 207:2215–2220
Gloutney ML, Alisauskas RT, Afton AD, Slattery SM (2001) Foraging time and dietary intake by breeding Ross’s and Lesser Snow Geese. Oecologia 127:78–86
Gomez-Campos E, Borrell A, Aguilar A (2011) Nitrogen and carbon stable isotopes do not reflect nutritional condition in the striped dolphin. Rapid Commun Mass Spectrom 25:1343–1347
Gorokhova E, Hansson S (1999) An experimental study on variations in stable carbon and nitrogen isotope fractionation during growth of Mysis mixta and Neomysis integer. Can J Fisheries Aquat Sci 56:2203–2210
Gustine DD, Barboza PS, Lawler JP (2010) Dynamics of body protein and the implications for reproduction in captive muskoxen (Ovibos moschatus) during winter. Physiol Biochem Zool 83:687–697
Gustine DO, Barboza PS, Adams LG, Farnell RG, Parker KL (2011) An isotopic approach to measuring nitrogen balance in carbou. J Wildl Manage 75:178–188
Habran S, Debier C, Crocker DE, Houser DS, Lepoint G, Bouquegneau JM, Das K (2010) Assessment of gestation, lactation and fasting on stable isotope ratios in northern elephant seals (Mirounga angustirostris). Mar Mammal Sci 26:880–895
Hare PE, Fogel ML, Stafford TWJ, Mitchell AD, Hoering TC (1991) The isotopic composition of carbon and nitrogen in individual amino acids isolated from modern and fossil proteins. J Archaeol Sci 18:277–292
Hatch KA, Sacksteder KA, Treichel IW, Cook ME, Porter WP (1995) Early detection of catabolic state via change in 13C/12C ratios of blood proteins. Biochem Biophys Res Comm 212:719–726
Hatch KA, Pinshow B, Speakman JR (2002a) Carbon isotope ratios in exhaled CO2 can be used to determine not just present, but also past diets in birds. J Comp Physiol B 172:263–268
Hatch KA, Pinshow B, Speakman JR (2002b) The analysis of 13CO2/12CO2 ratios in exhaled CO2: its advantages and potential application to field research to infer diet, changes in diet over time, and substrate metabolism in birds. Integr Comp Biol 42:21–33
Hatch KA, Crawford MA, Kunz AW, Thomsen SR, Eggett DL, Nelson ST, Roeder BL (2006) An objective means of diagnosing anorexia nervosa and bulimia nervosa using 15N/14N and 13C/12C ratios in hair. Rapid Comm Mass Spectrom 20:3367–3373
Haubert D, Langel R, Scheu S, Ruess L (2005) Effects of food quality, starvation and life stage on stable isotope fractionation in Collembola. Pedobiologia 49:229–237
Hiele M, Ghoos Y, Rutgeerts P, Vantrappen G, de Buyser K (1990) 13CO2 breath test to measure the hydrolysis of various starch formulations. Gut 31:175–178
Hobson KA (2006) Using stable isotopes to quantitatively track endogenous and exogenous nutrient allocations to eggs of birds that travel to breed. Ardea 94:359–369
Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95:388–394
Hobson KA, Thompson JE, Evans MR, Boyd S (2005) Tracing nutrient allocation to reproduction in Barrow’s goldeneye. J Wildlife Manage 69:1221–1228
Hubbs AH, Boonstra R (1997) Population limitation in Arctic ground squirrels: effects of food and predation. J Anim Ecol 66:527–541
Hume ID, Biebach H (1996) Digestive tract function in the long-distance migratory garden warbler, Sylvia borin. J Comp Physiol B 166:388–395
Iverson S (2009) Encyclopedia of mammals. Academic Press, San Diego
Jackson AL, Inger R, Bearhop S, Parnell A (2009) Erroneous behaviour of MixSIR, a recently published Bayesian isotope mixing model: a discussion of Moore, Semmens (2008). Ecol Lett 12:E1–E5
Jenni L, Jenni-Eiermann S (1998) Fuel supply and metabolic constraints in migrating birds. J Avian Biology 29:521–528
Jenni-Eiermann S, Jenni L (1991) metabolic responses to flight and fasting in night-migrating passerines. J Comp Physiol B 161:465–474
Jenni-Eiermann S, Jenni L (1992) High plasma triglyceride levels in small birds during migratory flight: a new pathway for fuel supply during endurance locomotion at very high mass specific metabolic rates. Physiol Zool 65:112–123
Jenni-Eiermann S, Jenni L (1997) Diurnal variation of metabolic responses to short-term fasting in passerine birds during the postbreeding, molting and migratory period. Condor 99:113–122
Katzenberg MA, Lovell NC (1999) Stable isotope variation in pathological bone. Int J Osteoarchaeol 9:316–324
Kempster B, Zanette L, Longstaffe FJ, MacDougall-Shackleton SA, Wingfield JC, Clinchy M (2007) Do stable isotopes reflect nutritional stress? Results from a laboratory experiment on song sparrows. Oecologia 151:365–371
King JR, Murphy ME (1985) Periods of nutritional stress in the annual cycles of endotherms: fact or fiction? A Zool 25:955–964
Kirk KL (1997) Life-history responses to variable environments: starvation and reproduction in planktonic rotifers. Ecology 78:434–441
Klaassen M, Lindström A, Heltofte H, Piersma T (2001) Arctic waders are not capital breeders. Nature 413:794
Koch PI (1997) Nitrogen isotope ecology of carnivores and herbivores. J Vertebr Paleontol 17:57A
Kurle CM, Worthy GAJ (2002) Stable nitrogen and carbon isotope ratios in multiple tissues of the northern fur seal Callorhinus ursinus: implications for dietary and migratory reconstructions. Mar Ecol-Progr Ser 236:289–300
Lacroix M, Pallikarakis N, Mosora F (1982) Comparison of Naturally and artificially labelled glucose utilization to study glucose oxidation by means of 13CO2/12CO2 breath test. In: Schmidt HL, Förstel H, Heinzinger K (eds) Stable Isotopes. Elsevier Scientific Publishing Company, Amsterdam
Le Boeuf BJ, Whiting RJ, Gantt RF (1973) Perinatal behavior of northern elephant seal females and their young. Behaviour 43:121–156
Logan RPH (1998) Urea breath tests in the management of Helicobacter pylori infection. Gut 43(Suppl 1):S47–S50
Malthus T (1798) An essay on the principle of population. J. Johnson, St. Paul’s Church-Yard, London
Macko SA, Lee WY, Parker PL (1982) Nitrogen and carbon isotope fractionation by two species of marine amphipods: laboratory and field studies. J Exp Mar Biol Ecol 63:145–149
Martinez del Rio C, Wolf BO (2005) Mass balance models for animal isotopic ecology. In: Starck MA, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, New Hampshire
Martinez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111
Martins IJ, Redgrave TG (2004) Obesity and post-prandial lipid metabolism. Feast or famine? J Nutr Biochem 15:130–141
McClean P, Harding M, Coward WA, Green MR, Weaver LT (1993) Measurement of fat digestion in early life using a stable isotope breath test. Arch Dis Child 69:366–370
McCue MD (2007a) Western diamondback rattlesnakes demonstrate physiological and biochemical strategies for tolerating prolonged starvation. Physiol Biochem Zool 80:25–34
McCue MD (2007b) Snakes survive starvation by employing supply- and demand-side economic strategies. Zoology 110:318–327
McCue MD (2008) Endogenous and environmental factors influence the dietary fractionation of 13C and 15N in hissing cockroaches Gromphadorhina portentosa. Physiol Biochem Zool 81:14–24
McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol 156:1–18
McCue MD (2011) Tracking the Oxidative and Nonoxidative Fates of Isotopically Labeled Nutrients in Animals. Bioscience 61:217–230
McCue MD, Pollock ED (2008) Stable isotopes may provide evidence for starvation in reptiles. Rapid Commun Mass Spectrom 22:2307–2314
McCue MD, Sivan O, McWilliams SR, Pinshow B (2010) Tracking the oxidative kinetics of carbohydrates, amino acids and fatty acids in the house sparrow using exhaled 13CO2. J Exp Biol 213:782–789
McCue MD, McWilliams SR, Pinshow B (2011) Ontogeny and nutritional status influence oxidative kinetics of nutrients and whole-animal bioenergetics in zebra finches, Taeniopygia guttata: new applications for 13C breath yesting. Physiol Biochem Zool 84:32–42
McWilliams SR, Karasov WH (2001) Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance. Comp Biochem and Physiol A-Mol and Integr Physiol 128:579–593
McWilliams SR, Karasov WH (2005) Migration takes gut: digestive physiology of migratory birds and its ecological significance. In: Mara P, Greenberg R (eds) Birds of two worlds: the ecology and evolution of migration. Johns Hopkins University Press, Baltimore
Meijer T, Drent R (1999) Re-examination of the capital and income dichotomy in breeding birds. Ibis 141:399–414
Miller RF, Orr GL, Fritz P, Downer RGH, Morgan AV (1984) Stable carbon isotope ratios in Periplaneta americana L., the American cockroach. Can J Zool 63:584–589
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between 15N and animal age. Geochimica Cosmochimica Acta 48:1135–1140
Moen J, Anderson R, Illius A (2006) Living in a seasonal environment. In: Danell K, Bergstrom R, Duncan P, Pastor J (eds) Large herbivore ecology, ecosystem dynamics and conservation. Cambridge University Press, Cambridge
Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Let 11:470–480
Mrosovsky N, Sherry DF (1980) Animal anorexias. Science 207:837–842
Newton I (2004) Population limitation in migrants. Ibis 146:197–226
Nowicki S, Searcy WA, Peters S (2002) Brain development, song learning and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”. J Comp Physiol A 188:1003–1014
Oelbermann K, Scheu S (2002) Stable isotope enrichment (δ15N and δ13C) in a generalist predator (Pardosa lugubris, Araneae: Lycosidae): effects of prey quality. Oecologia 130:337–344
Ohlsson T, Smith HG (2001) Early nutrition causes persistent effects on pheasant morphology. Physiol Biochem Zool 74:212–218
Olive PJW, Pinnegar JK, Polunin NVC, Richards G, Welch R (2003) Isotope trophic-step fractionation: a dynamic equilibrium model. J Anim Ecol 72:608–617
Passey BH, Robinson TF, Ayliffe LK, Cerling TE, Sponheimer M, Dearing MD, Roeder BL, Ehleringer JR (2005) Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. J Archaeol Sci 32:1459–1470
Pearson SF, Levey DJ, Greenberg CH, del Rio CM (2003) Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia 135:516–523
Peterson RO, Thomas NJ, Thurber JM, Vucetich JA, Waite TA (1998) Population limitation and the wolves of Isle Royale. J Mammal 79:828–841
Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269
Phillips DL, Koch PL (2002) Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–125
Piniak GA, Lipschultz F (2004) Effects of nutritional history on nitrogen assimilation in congeneric temperate and tropical scleractinian corals. Mar Biol 145:1085–1096
Polischuk SC, Hobson KA, Ramsay MA (2001) Use of stable-carbon and -nitrogen isotopes to assess weaning and fasting in female polar bears and their cubs. Can J Zool 79:499–511
Reynolds PE (2001) Reproductive patterns of female muskoxen in northeastern Alaska. Alces 37:403–410
Rion S, Kawecki TJ (2007) Evolutionary biology of starvation resistance: what we have learned from Drosophila. J Evolution Biol 20:1655–1664
Ryder JP (1970) A possible factor in the evolution of clutch size in Ross Goose. Wilson Bull 82:5–13
Schmidt O, Scrimgeour CM, Curry JP (1999) Carbon and nitrogen stable isotope ratios in body tissue and mucus of feeding and fasting earthworms (Lumbricus festivus). Oecologia 118:9–15
Schoeller DA, Brown C, Nakamura K, Nakagawa A, Mazzeo RS, Brooks BA, Budinger TF (1984) Influence of metabolic fuel on the 13CO2/12CO2 ratio of breath CO2. Biomed Mass Spectrom 11:557–561
Schwilch R, Jenni L, Jenni-Eiermann S (1996) Metabolic responses of homing pigeons to flight and subsequent recovery. J Comp Physiol B 166:77–87
Sears J, Hatch SA, O’Brien DM (2009) Disentangling effects of growth and nutritional status on seabird stable isotope ratios. Oecologia 159:41–48
Semmens BX, Moore JW, Ward EJ (2009) Improving Bayesian isotope mixing models: a response to Jackson et al. (2009). Ecol Lett 12:E6–E8
Senechal E, Bety J, Gilchrist HG, Hobson KA, Jamieson SE (2011) Do purely capital layers exist among flying birds? Evidence of exogenous contribution to arctic-nesting common eider eggs. Oecologia 165:593–604
Sick H, Roos N, Saggau E, Haas K, Meyn V, Walch B, Trugo N (1997) Amino acid utilization and isotope discrimination of amino nitrogen in nitrogen metabolism of rat liver in vivo. Z Ernahrungswiss 36:340–346
Sponheimer M, Robinson TF, Cerling TE, Tegland L, Roeder BL, Ayliffe L, Dearing MD, Ehleringer JR (2006) Turnover of stable carbon isotopes in the muscle, liver, and breath CO2 of alpacas (Lama pacos). Rapid Commun Mass Spectrom 20:1395–1399
Starck JM, Moser P, Werner RA, Linke P (2004) Pythons metabolize prey to fuel the response to feeding. Proc Roy Soc Ser B 271:903–908
Steele KW, Daniel RM (1978) Fractionation of nitrogen isotopes by animals: a further complication to the use of variations in the natural abundance of 15N for tracer studies. J Agr Sci 90:7–9
Stevens RE, Lister AM, Hedges REM (2006) Predicting diet, trophic level and palaeoecology from bone stable isotope analysis: a comparative study of five red deer populations. Oecologia 149:12–21
Sullivan KA (1989) Age-specific mortality in juvenile juncos (Junco phaenotus). J Anim Ecol 58:275–286
Swain SD (1992) Energy substrate profiles during fasting in Horned Larks (Eremophila alpestris). Physiol Zool 65:568–582
Tsukamoto K (2009) Oceanic migration and spawning of anguillid eels. J Fish Biol 74:1833–1852
Ugan A, Coltrain J (2011) Variation in collagen stable nitrogen values in black-tailed jackrabbits (Lepus californicus) in relation to small-scale differences in climate, soil, and topography. J Archaeol Sci 38:1417–1429
Van Dyke JU, Beaupre SJ (2011) Bioenergetic components of reproductive effort in viviparous snakes: costs of vitellogenesis exceed costs of pregnancy. Comp Biochem Physiol 160:504–515
Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182
Wang T, Hung CCY, Randall DJ (2006) The comparative physiology of food deprivation: from feast to famine. Annu Rev Physiol 68:223–251
Warner DA, Bonnet X, Hobson KA, Shine R (2008) Lizards combine stored energy and recently acquired nutrients flexibly to fuel reproduction. J Anim Ecol 77:1242–1249
Waterlow JC (1968) The adaptation of protein metabolism to low protein intake. In: McCance RA, Widdowson EM (eds) Calorie and protein deficiencies. Little, Brown and Company, Boston
Waterlow JC (1986) Metabolic adaptation to low intakes of energy and protein. Annu Rev Nutr 6:495–526
White TCR (1993) The inadequate environment: nitrogen and the abundance of animals. Springer, Berlin
White RG, Rowell JE, Hauer WE (1997) The role of nutrition, body condition and lactation on calving success in muskoxen. J Zool 243:13–20
Williams CT, Buck CL, Sears J, Kitaysky AS (2007) Effects of nutritional restriction on nitrogen and carbon stable isotopes in growing seabirds. Oecologia 153:11–18
Young VR, Scrimshaw NS (1971) The physiology of starvation. Sci Am 225:14–21
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I would like to thank Marshall McCue for giving me the opportunity to contribute this chapter and for reviewing this chapter. His comments and insights were very helpful and his patience greatly appreciated.
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Hatch, K.A. (2012). The Use and Application of Stable Isotope Analysis to the Study of Starvation, Fasting, and Nutritional Stress in Animals. In: McCue, M. (eds) Comparative Physiology of Fasting, Starvation, and Food Limitation. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-29056-5_20
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