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Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes

Abstract

Assessments of temporal variation in diets are important for our understanding of the ecology of many vertebrates. Ratios of naturally occurring stable isotopes in animal tissues are a combination of the source elements and tissue specific fractionation processes, and can thus reveal dietary information. We review three different approaches that have been used to resolve temporal diet variation through analysis of stable isotopes. The most straightforward approach is to compare samples from the same type of tissue that has been sampled over time. This approach is suited to address either long or short-term dietary variation, depending on sample regime and which tissue that is sampled. Second, one can compare tissues with different metabolic rates. Since the elements in a given tissue have been assimilating during time spans specific to its metabolic rate, tissues with different metabolic rates will reflect dietary records over different periods. Third, comparisons of sections from tissues with progressive growth, such as hair, feathers, claws and teeth, will reveal temporal variation since these tissues will retain isotopic values in a chronological order. These latter two approaches are mainly suited to address questions regarding intermediate and short-term dietary variation. Knowledge of tissue specific metabolic rates, which determine the molecular turnover for a specific tissue, is of central importance for all these comparisons. Estimates of isotopic fractionation between source and measured target are important if specific hypotheses regarding the source elements are addressed. Estimates of isotopic fractionation, or at least of differences in fractionation between tissues, are necessary if different tissues are compared. We urge for more laboratory experiments aimed at improving our understanding of differential assimilation of dietary components, isotopic fractionation and metabolic routing. We further encourage more studies on reptiles and amphibians, and generally more studies utilizing multiple tissues with different turnover rates.

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Correspondence to F. Dalerum.

Additional information

Communicated by Jim Ehleringer

Appendix 1

Appendix 1

Studies found to have used stable carbon or nitrogen isotopes to resolve temporal patterns in the diets of wild vertebrates, including species studied and measured tissues

References Typea Species Tissue
Mammals
Ben-David et al. (1997) Oecologia 111:280–291 1 American marten (Martes americana) Blood, Muscle
Ben-David et al. (2001) Alces 37:371–402 1 Moose (Alces alces), Caribou (Rangifer tarandus) Blood Blood, Hair
Ben-David et al. (2004) Oecologia 138:465–474 1 Grizzly bear (Ursus arctos horribilis)  
Cerling et al. (2004) Palaeogeogr Palaeoclim Palaeoecol 206:367–376 1 African elephant (Loxodonta africana) Hair
Drever et al. (2000) Can J Zool 78:2010–2018 1 Keen’s mice (Peromyscus keeni), Townsend’s vole (Microtus townsendii cowani) Muscle, Liver
Felicetti et al. (2003) Can J Zool 81:763–770 1 Grizzly bear (Ursus arctos horribilis) Blood, Hair
Fleming et al. (1993) Oecologia 94:72–75 1 Lesser long-nosed bat (Leptonycteris curasoae), Palla’s long-tongued bat (Glossophaga soricina) Muscle
Herrera et al. (2001) J Mamm 82:352–361 1 Jamaican fruit bat (Artibeus jamaicensis), Palla’s long-tongued bat (Glossophaga soricina) Blood
Hildebrand et al. (1996) Can J Zool 74:2080–2088 1 Grizzly bear (Ursus arctos horribilis) Bone, Blood
Hiron et al. (2001) Oecologia 129:591–601 1 Steller sea lions (Eumetopias jubatus), Northern fur seal (Callorhinus ursinus), Harbour seal (Phoca vitulina) Bone
Kurle and Worthy (2001) Oecologia 126:254–265 1 Northern fur seal (Callorhinus ursinus) Skin
Roth (2002) Oecologia 133:70–77 1 Arctic fox (Alopex lagopus) Hair
Smith et al. (2002) J Arid Env 52:419–430 1 Dipodomys ordii, D. merriami, Chaetodipus beileyi, C. Pencillatus, Reithrodontomys megalotis, Onychomys torridus Bone
Szepanski et al. (1999) Oecologia 120:327–335 1 Grey wolf (Canis lupus) Bone
Walker et al. (1999) Mar Mamm Sci 15:335–350 1 Bottlenose dolphin (Tursiops truncatus) Teeth
Abend et al. (1995) Ices J Mar Sci 52:837–841 2 Long-finned pilot whale (Globichephala melas) Muscle, Blubber, Teeth, Skin
Ben-David et al. (2004) Oecologia 138:465–474 2 Grizzly bear (Ursus arctos horribilis) Blood, Hair
Hobson et al. (1999) J Wildl Manage 63:14–25 2 Norway rat (Rattus norvegicus) Muscle, Liver
Kurle and Worthy (2002) Mar Ecol Prog Ser 236:289–300 2 Northern fur seal (Callorhinus ursinus) Fur, Muscle, Brain, Blubber, Liver, Kidney
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Barnett (1994) MSc, University of Alaska, Fairbanks 3 Caribou (Rangifer tarandus) Hoof, Hair
Best and Schell (1996) Mar Biol 124:483–494 3 Southern right whale (Eubaleana australis) Baleen
Cerling and Viehl (2004) Afr J Ecol 42:88–92 3 Forest hog (Hylochohoerus meinertzhageni) Hair
Cerling et al. (2003) Palaeogeogr Palaeoclim Paeleoecol 206:367–376 3 African elephant (Loxodonta africana) Hair, Teeth
Derimont and Reimchen (2002) Can J Zool 80:1638–1642 3 Grey wolf (Canis lupus) Hair
Hobson and Schell (1998) Can J Fish Aq Sci 55:2601–2607 3 Bowhead whale (Balaena musticetus) Baleen
Hobson and Sease (1998) Mar Mamm Sci 14:116–129 3 Steller sea lions (Eumetopias jubatus) Teeth
Schell (2000) Limn Oceanogr 45:459–462 3 Bowhead whale (Balaena musticetus) Baleen
Schell et al. (1989) Mar Biol 103:433–443 3 Bowhead whale (Balaena musticetus) Baleen
Zazzo et al. (2002) Palaeogeogr Palaeoclim Paleoecol 186:145–161 3 Tragoportax afghanicus Teeth
Birds
Ainley et al. (2003) Condor 105:95–106 1 Adelie penguin (Pygoscelis adeliae) Claws
Bearhop et al. (1999) J Appl Ecol 36:75–84 1 Cormorant (Phalacrocorax carbo) Feathers
Bearhop et al. (2000) Mar Ecol Prog Ser 195:261–268 1 Great skua (Stercorarius skua) Feathers
Bearhop et al. (2001) Condor 103:802–809 1 Great skua (Stercorarius skua) Feathers
Cherel et al. (2002) Mar Ecol Prog Ser 228:283–299 1 Blue petrel (Halobanea caerulea) Feathers
Cherel et al. (2000) Oecologia 122:155–162 1 Black browed albatross (Diomeda melanophrys) Feathers
Forero et al. (2002) Mar Ecol Prog Ser 234:289–299 1 Magellanic penguin (Spheniscus magellanicus) Blood
Graves et al. (2002) PNAS 99:8096–8100 1 Black-throated blue warbler (Dendroica caerulesens) Feathers
Hebert et al. (1999) Can J Fish Aq Sci 56:323–338 1 Herring gull (Larus argentatus) Egg
Hodum and Hobson (2000) Mar Ecol Prog Ser 198:273–281 1 Antarctic fulmar (Fulmarus glacialoides), Antarctic petrel (Thalassoica antarctica), Cape petrel (Daption capense), Snow petrel (Pagodroma nivea) Blood cells
Minami et al. (1995) Condor 97:565–574 1 Sooty sheerwater (Puffinus griseus), Short-tailed sheerwater (P. tennuirostris) Muscle
Mizutani et al. (1990) Auk 107:400–437 1 Great cormorant (Phalacrocorax carbo) Feathers
Nisbeth et al. (2002) Mar Ecol Prog Ser 242:267–274 1 Common tern (Sterna hirundo) Feathers
Sagerup et al. (2002) Ecotoxicology 11:119–125 1 Glaucus gull (Larus hyperboreus)  
Smith et al. (2002) J Arid Env 52:419–430 1 Black-throated sparrow (Amphispiza bilineata), Brewer’s sparrow (Spizella breweri) Bone
Thompson and Furness (1995) Auk 112:493–498 1 Northern fulmar (Lulmarus glacialis) Feathers
Thomson et al. (1995) Mar Ecol Prog Ser 125:3–11 1 Northern fulmar (Lulmarus glacialis) Feathers
Hobson (1993) Mar Ecol Prog Ser 95:7–18 2 Dovekies (Alle alle), Galucous gulls (Larus hyperboreus), Common eider (Somateria mollissima), Black-legged kittiwake (Rissa trdactyla), Thick-billed murres (Uria lomvia), Northern fulmar (Fulmarus glacialis), Black guillemot (Cepphus grylle) Bone, Muscle, Liver
Hobson and Sealy (1991) Auk 108:437–440 2 Northern Saw-whet owl (Aegolius acadicus) Muscle, Bone
Knoff et al. (2001) Iso Env Health Stud 37:67–88 2 Laughing gull (Larus atricilla) Blood, Feather, Muscle
Morrisey et al. (2004) J Appl Ecol 41:502–512 2 American dipper (Cinclus mexicanus) Blood, Feather
Schmutz and Hobson (1998) Condor 100:119–130 2 Glaucus gull (Larus hyperboreus) Muscle, Liver, Blood
Thompson and Furness (1995) Auk 112:493–498 2 Northern fulmar (Lulmarus glacialis) Feathers, Muscle, Bone
Bearhop et al. (2003) Funct Ecol 17:270–275 3 Great tit (Parus major), Blue tit (P. caeruleus), Coal tit (P. ater), Chaffinch (Fingilla coelebs), Robin (Erithacus rubecula) Claw
Knoff et al. (2002) Waterbirds 25:142–148 3 Laughing gull (Larus atricilla) Feather
Fish
Gao et al. (2001) Env Biol Fish 61:445–453 1 Cod (Gadus morhua) Otoliths
Limburg (1998) Can J Fish Aq Sci 55:431–437 1 Alosa aestivalis, A. sapidissima, A. pseudoharengus Whole body
MacAvoy et al. (2001) Can J Fish Aq Sci 58:923–932 1 Blue catfish (Ictalurus furcatus) Muscle
Maruyama et al. (2001) Can J Fish Aq Sci 58:2125–2128 1 Goby (Rhinogobius sp.) Muscle
Murchie and Power (2004) Freshw Biol 49:41–54 1 Yellow perch (Perca flavescens) Whole body
Persic et al. (2004) Est Coast Shelf Sci 60:261–272 1 Atherina boyeri, Gobius niger, Pomathoschistus sp., Gasterosteus aculeatus, Sygnatus acus, Anguilla anguilla, Lepomis gibbosus, Stizostedion lucioperca, Abramis sp., Mugilidae sp. Whole body, Muscle
Persson and Hanson (1999) Can J Fish Aq Sci 56:70–78 1 Roach (Rutilus rutilus), Perch (Perca fluviatilis) Muscle
Pruell et al. (2003) Fish Man Ecol 10:329–336 1 Striped bass (Marone saxatilis) Scales, Muscle
Vizzini and Mazzola (2003) Mar Biol 142:1009–1018 1 Anguilla anguilla, Atherina boyeri, Gobius niger, Lipophrys pavo, Liza aurata, Sungtatus abaster, Zosterisessor ophiocephalus Whole body
Wantzen et al. (2002) Aq Sci 64:239–251 1 Freshwater fish Whole body
Gaston and Suthers (2004) J Exp Mar Biol Ecol 304:17–33 2 Mado (Atuphictus strigatus) Bone, Liver, Muscle
Carpenter et al. (2003) Nature 423:70–74 3 Vohrisia vulpes Otoliths
Gao and Beamish (2002) Fish Res 60:393–404 3 Pacific halibut (Hippoglossus stenolepis) Otoliths
Gao et al. (2001) Can J Fish Aq Sci 58:2113–2120 3 Pacific herring (Clupea pallasi) Otoliths
Weidman and Millner (2000) Fish Res 46:327–342 3 Cod (Gadus morhua) Otoliths
Wurster and Paterson (2003) Paleobiol 29:492–505 3 Freshwater drum (Aplodinotus grunnies) Otoliths
Reptiles
Smith et al. (2002) J Arid Env 52:419–430 1 Holbrookia makulata, Urosaurus ornatus, Cnemidophorus uniparens, Sceloporus virgatus, S. Undulatus Bone
  1. aIndicates type of comparison for temporal analysis; 1 comparison of same tissue, 2 comparisons of tissues with different metabolic growth, 3 comparisons of segments of tissues with progressive growth

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Dalerum, F., Angerbjörn, A. Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144, 647–658 (2005). https://doi.org/10.1007/s00442-005-0118-0

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Keywords

  • δ13C
  • δ15N
  • Ecophysiology
  • Seasonality
  • Feeding ecology