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Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes

  • Stable Isotopes Issue
  • Published:
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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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Authors and Affiliations

  1. Department of Zoology, Stockholm University, 10691, Stockholm, Sweden

    F. Dalerum & A. Angerbjörn

Authors
  1. F. Dalerum
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  2. A. Angerbjörn
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Corresponding author

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

Lavin et al. (2003) Can J Zool 81:1070–1082

2

Red fox (Vulpes vulpes), Coyote (Canis latrans)

Serum, Blood, Hair

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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