Using stable carbon (δ 13 C) and nitrogen (δ 15 N) isotopes to infer trophic relationships among...

Using stable carbon (δ13C) and nitrogen (δ15N)isotopes to infer trophic relationships amongblack and grizzly bears in the upper ColumbiaRiver basin, British Columbia

Keith A. Hobson, Bruce N. McLellan, and John G. Woods

Abstract: Ecological segregation of species is difficult to determine using conventional dietary analysis techniques.However, stable-isotope analysis may provide a convenient means of establishing trophic segregation of species and ofgroups of animals within a species in the same area. We measured stable carbon (δ13C) and nitrogen (δ15N) isotope val-ues in hair of black bears (Ursus americanus) and grizzly bears (Ursus arctos) inhabiting the upper Columbia Riverbasin in southeastern British Columbia, together with samples of potential foods ranging from plant material throughinvertebrates and ungulate meat. We found extensive overlap in bothδ15N and δ13C values of hair from male grizzlybears and black bears of both sexes. Female grizzly bears, however, had lowerδ15N values in their hair than the othergroups of bears, indicating either less animal protein in their diet or a reliance on foods more depleted in15N, possiblyrelated to altitude. Our isotopic model generally confirmed a herbivorous diet for both bear species (a mean estimatedplant contribution of 91%). Bears showing the highestδ15N values were those captured because they posed a manage-ment problem. We suggest that the slope of the relationship between tissueδ15N and δ13C values might provide a con-venient means of evaluating the occurrence of consumption of animal protein in populations, regardless of localisotopic end-points for dietary samples. We examined three black bear cubs from dens and found them to be about atrophic level higher than adult females, reflecting their dependence on mother’s milk, a result generally confirmed byan analysis of eight mother–cub pairs from Minnesota. Our study demonstrates how stable-isotope analysis of bear tis-sue can be used to monitor the feeding habits of populations, as well as provide dietary histories that may reveal di-etary specializations among individuals.

Résumé: La ségrégation écologique entre les espèces est difficile à déterminer au moyen des techniques convention-nelles d’analyse des aliments, mais l’analyse des isotopes stables peut être un moyen pratique d’établir la ségrégationtrophique entre espèces et entre groupes d’animaux de la même espèce vivant dans la même région. Nous avons me-suré les isotopes stables de carbone (*13C) et d’azote*15N) dans le poil d’Ours noirs (Ursus americanus) et de Grizzlis(Ursus arctos) du bassin supérieur du Columbia, dans le sud-est de la Colombie-Britannique, de même que des échan-tillons de nourriture potentielle, plantes, invertébrés ou viande d’ongulés. Nous avons observé un chevauchement impor-tant des valeurs de*15N et de*13C dans les poils de grizzlis mâles et d’ours noirs des deux sexes. Les grizzlisfemelles avaient cependant des valeurs de*15N plus faibles dans leurs poils que dans les poils des autres groupes exa-minés, ce qui révèle que ces animaux consomment moins de protéines animales dans leur régime ou alors comptent surdes aliments appauvris en*15N, peut-être à cause de l’altitude. De façon générale, notre modèle isotopique a confirméle recours à un régime alimentaire herbivore chez les deux espèces (la contribution moyenne des plantes au régimeétait de 91 %). Les ours qui avaient les valeurs de*15N les plus élevées représentaient les cas problèmesd’aménagement. La pente de la relation entre les isotopes*15N et *13C dans un tissu est sans doute un bon indice dela consommation de protéines animales chez les populations, sans tenir compte des valeurs isotopiques locales extrêmesdans les échantillons de nourriture. Nous avons examiné trois oursons de l’Ours noir dans leurs terriers et avons cons-taté qu’ils étaient de niveau trophique supérieur à celui des femelles adultes à cause de leur recours au lait maternel,une constatation généralement confirmée par l’analyse de huit paires mère–ourson du Minnesota. Notre étude démontrecomment l’analyse des isotopes stables dans les tissus des ours peut servir à évaluer les habitudes alimentaires des po-pulations, tout en mettant en lumière des aspects historiques de leur alimentation qui peuvent démontrer les spécialisa-tions alimentaires de certains individus.

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Can. J. Zool.78: 1332–1339 (2000) © 2000 NRC Canada

1332

Received August 9, 1999. Accepted March 30, 2000.

K.A. Hobson.1 Canadian Wildlife Service, 115 Perimeter Road, Saskatoon, SK S7N 0X4, Canada.B.N. McLellan. British Columbia Ministry of Forests, Box 9156, R.P.O. 3, Revelstoke, BC V0E 3K0, Canada.J.G. Woods.Mount Revelstoke and Glacier National Parks, Box 350, Revelstoke, BC V0E 2SO, Canada.

1Author to whom all correspondence should be addressed (e-mail: [email protected]).

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Hobson et al.Introduction

Two bear species, the black bear (Ursus americanus) andgrizzly bear (Ursus arctos), occur sympatrically throughoutmuch of British Columbia (McLellan 1993). The black bearand its ancestors have been in North America for >3 millionyears and, being omnivores, they have filled a generalistniche (Kurten and Anderson 1980). The grizzly bear, anotheromnivorous ursid, radiated across most of North America asrecently as 13 000 BP (Kurten and Anderson 1980). Themorphological and ecological similarity between these spe-cies has stimulated interest in the mechanisms of resourcepartitioning (McLellan 1993; Aune and Kasworm 1994).

Fundamental to understanding resource partitioning is doc-umenting the dietary overlap of sympatric black and brownbears. However, our investigation of the diets of wild bearshas been hampered by limitations inherent in conventionalmethods such as scat analysis (Mattson et al. 1991; Mattsonand Reinhart 1995; McLellan and Hovey 1995; Jacoby et al.1999). Unequal digestibility of foods and unequal detectabilityin the field complicate traditional methods, and without DNAanalysis, it is often difficult to determine which individual,or even species, deposited a scat (McLellan and Hovey1995).Recently, stable-isotope analysis has been used to infer rela-tive trophic positions of black and grizzly bears and, moreparticularly, their use of plants, terrestrial meat, and anadro-mous salmon in C-3 (C3 plant) dominated biomes of west-ern North America (Hilderbrand et al. 1996, 1999; Jacobyet al. 1999). Although limited to determining trophic level,this approach has advantages over conventional approachesand has been used successfully in previous ecological inves-tigations (reviewed by Peterson and Fry 1987; Hobson 1999).

The stable-isotope approach is based on the fact that natu-rally occurring stable-isotope ratios in consumer tissues canbe related to those in consumers’ diets (DeNiro and Epstein1978, 1981). Changes in, or fractionation of, stable nitrogenisotope ratios (15N/14N) occur with trophic level and are ofthe order of 3–4‰ (Peterson and Fry 1987; Hobson andWelch 1992). Thus, isotopic measurement of consumers’ tis-sues can reveal information about their ingested foods andabout trophic level in systems that are relatively simple anddo not involve multiple isotopic inputs. One such simple ap-plication involves determining the relative dependence ofomnivores on plants and vertebrate or invertebrate tissues insystems in which stable nitrogen isotope values of diet plantsare similar and do not overlap those in the tissues of localherbivores. Here we expect stable-isotope values in consum-ers’ tissues to be a reliable indicator of trophic level duringthe period of tissue growth in the case of metabolically inertstructures such as hair or nail and during the period of di-etary integration in the case of metabolically active tissuessuch as blood and muscle (Hobson 1999).

We measured stable carbon and nitrogen isotope ratios inthe hair of black and grizzly bears from the upper ColumbiaRiver basin in British Columbia, Canada. Our own experi-ence had indicated that bears’ hair grows predominantly dur-ing summer and fall (May–October) and, hence, represents adietary average during that period. However, we are awarethat hair growth can show significant individual variationdue to differences in nutrition (Jacoby et al. 1999). We were

particularly interested in the effect of species and sex on thelevel of carnivory.

Methods

Study site and field collectionThe study area in the upper Columbia River basin of British Co-

lumbia was previously described by Woods et al. (1999). Hair sam-ples came from 123 bears captured for research purposes between1994 and 1998 as part of a radio-tracking project. To reduce possi-ble sampling biases, bears were captured using both vehicle- andhelicopter-based trapping plus free-darting from a helicopter to en-sure thorough coverage of the study area. In 10 cases we sampledthe same individuals in successive years but considered these to beindependent in our analyses. Hair samples were also obtained from21 bears that were captured because they posed a managementproblem, i.e., they were feeding in garbage dumps or close to hu-man habitation. The age of “research” and “management” bearsranged from 1.4 to 26.7 years, based on tooth-cementum analysis;for comparisons we used only bears >2 years of age, to ensure thattheir mother’s milk was insignificant in their diet.

We also obtained hair samples from three black bear cubs andtheir mothers in our study area and from eight black bear mothersand their cubs while in dens in northern Minnesota in 1998–1999.These samples were collected to confirm isotopic patterns expectedin nursing cubs versus adults in general. Other tissue samples weresalvaged from mammals found dead within the study area. Tissuesamples were collected from plant species known to be eaten bybears in this area. These samples were collected primarily fromtwo mid-elevation locations (1000–1600 m) and pooled for analysis.Animal handling and specimen collecting were conducted underpermits issued by Parks Canada and the B.C. Ministry of Environ-ment, Lands and Parks. All statistical analyses were performedwith an assumed significance level ofp < 0.05.

Stable-isotope analysesHair was cleaned of surface oils using repeated rinses of a 2:1

chloroform:methanol solution and then air-dried for 24 h. Plant andinsect material and meat were cleaned in distilled water, freeze-dried, and then ground to a powder using a dental-amalgam mill.Approximately 1 mg of each sample was loaded into tin cups forisotopic measurement. Our mass spectrometer consisted of a EuropaRobo Prep combustion system interfaced with a Europa Tracermatcontinuous-flow isotope-ratio mass spectrometer. Samples were an-alyzed as five unknowns separated by two albumin standards. Basedon thousands of standard measurements, we estimate our analyticalerror to be ±0.1‰ for13C measurements and ±0.3‰ for15N mea-surements. We present our stable-isotope results inδ notation asthe deviation from parts per thousand (‰) according to the follow-ing relationship:

[1] δX = [(Rsample/ Rstandard) – 1] × 1000

whereX is 13C or 15N andR is the corresponding ratio13C/12C or15N/14N. Rstandardfor 13C and15N corresponds to the Pee Dee Bel-emnite (PDB) standard and AIR, respectively.

When animals feed on two food types that differ isotopically, asimple two-source mixing model can be used to ascertain the relativedependence of a consumer on each dietary source. Here the aver-age isotopic values of dietary alternatives are referred to as isotopicend-points. In the case of inland terrestrial bears with no access tomarine protein (i.e., salmon), we were interested in the relative de-pendence of individuals on meat and plant material. The relativecontributions of animal and plant protein assimilated in the tissuesof bears can be derived as follows:

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[2] δ15Ndiet = Pa (δ15Na) + Pp (δ15Np)

whereδ15Ndiet is the isotopic value of the diet,δ15Na is the isotopicvalue of animal tissue (including invertebrate prey),δ15Np is theisotopic value of plant foods,Pa is the proportion of the assimilateddiet derived from animal sources, andPp is the proportion of theassimilated diet consisting of plant foods. Using the relationshipPp = 1 – Pa and solving forPa, eq. 2 becomes

[3] Pa = (δ15Ndiet – δ15Np) / (δ15Na – δ15Np)

Hilderbrand et al. (1996) raised black bears in captivity on dietsranging from pure plant material (apples) to pure animal tissue(mule deer and salmon). They derived a linear relationship betweenδ15Ndiet andδ15N values of bear plasma that is probably appropriatefor all bear tissues except adipose tissue. Generalizing the relation-ship derived by Hilderbrand et al. (1996) for plasma to bear hair,we substituted the assumed relationship

[4] δ15Nhair = 4.76 + 0.91 (δ15Ndiet)

into eq. 3 to obtain

[5] Pa = [(δ15Nhair – 4.76) / 0.91 –δ15Np] / (δ15Na – δ15Np)

Results

Both bear species showed a considerable range in theirstable-isotope values for hair (Table 1, Fig. 1). For blackbears there was no relationship betweenδ15N and δ13C val-ues (r2 = 0.03), whereas for grizzly bears a strong positiverelationship was found (r2 = 0.63,p < 0.01) that was drivenlargely by highδ15N and δ13C values for the hair of a fewmanagement bears (Fig. 1).

The δ15N and δ13C values from research bears showed asignificant interaction between species and sex (MANOVA,Wilk’s λ = 0.873,F[2,124] = 9.04,p < 0.001). Using multiplecomparisons of means withα adjusted according to theBonferroni criterion, we determined that male grizzly bearsand black bears of both sexes had similarδ15N values butthat female grizzly bears had lowerδ15N values (Table 1).The δ13C values differed only between female grizzly bearsand female black bears (Table 1).

Of the management bears, only samples of female grizzly(n = 7) and male black (n = 9) bears were large enough to beincluded with research bears of the same species and sex ina MANOVA based on the reason for capture (managementor research). There was a significant interaction between rea-son for capture and sex–species group (female grizzly bears,male black bears; Wilk’sλ = 0.847,F[2,89] = 8.06,p = 0.001).Multiple comparisons of means suggested thatδ15N valuesfor management bears of the two species were equal, butwere higher than those for female grizzly or male black re-search bears. Once again, research male black bears hadhigherδ15N values than research female grizzly bears. Therewas no difference inδ13C values between management andresearch bears.

Our small sample of hair from black bear cubs from densin the upper Columbia River basin was more enriched in15Nand tended to be more depleted in13C than samples fromadults of this species (Table 1). We confirmed that this rela-tionship generally held forδ15N values for hair from mother–cub groups sampled in dens in northern Minnesota (Table 2).In all the family groups, hairδ15N was enriched in cubs rela-tive to their mothers (average of mean enrichment values per

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Sample n

δ13C (‰) δ15N (‰)

Mean ± SD Range Mean ± SD Range

Research bearsMale black 61 –23.2±0.5 –24.4 to –21.9 3.1±0.7 1.3 to 4.8Female black 25 –22.9±0.5 –24.1 to –21.7 3.4±1.0 1.4 to 5.6Male grizzly 26 –23.1±0.4 –24.1 to –22.2 3.1±0.8 1.9 to 4.7Female grizzly 17 –23.3±0.5 –24.1 to –22.4 2.1±1.1 0.2 to 4.3

Management bearsMale black 9 –23.0±0.5 –23.9 to –22.1 3.8±1.0 2.0 to 5.0Female black 1 –22.6 3.6Female grizzly 7 –22.7±1.06 –23.9 to –21.0 5.0±1.9 2.8 to 7.7

Cubs in den 3 –24.5±0.5 –24.0 to –24.9 6.6±0.3 6.4 to 6.8Potential prey

Spring beauty 7 –27.7±1.1 –29.5 to –26.4 –3.9±0.6 –2.7 to –4.5Fireweed (Epilobium angustifolium) 5 –28.8±1.3 –30.8 to –27.5 –1.1±2.0 –3.2 to 1.4Soapberry 7 –28.1±0.9 –29.4 to –26.7 0.1±0.6 –0.8 to 1.9Glacier lily (Erythronium montanum) 7 –26.4±0.6 –27.2 to –25.8 –3.4±0.3 –4.6 to –2.2Elk (Cervus elaphus) 1 –25.5 3.1Moose (Alces alces) 2 –25.7 –25.8 to –25.5 2.9 2.9 to 2.9Mountain goat 2 –23.7 –24.1 to –23.3 1.7 1.6 to 1.8Mule deer (Odocoileus hemionus) 1 –26.8 3.8White-tailed deer 1 –25.9 4.6Ants (Formicidae) 4 –25.5±0.3 –25.8 to –25.1 3.8±0.3 3.5 to 4.2

Note: Bear samples include replicates of some individuals taken at least 1 year apart. Ant samples are separate bulk samplesrepresenting several individuals. Ungulate samples are all meat. Plant samples correspond to portions of the plant consumed bybears.

Table 1. Stable-isotope values for bear hair and samples of potential bear foods in the upper Columbia River basin,British Columbia, 1994–1996.



group = 2.5 ± 1.2‰,n = 8). In six of eight mother–cubgroups, hairδ13C was also enriched in cubs over that of theirmothers (average of mean enrichment values per group =1.4 ± 0.9‰,n = 6); however, in the other two groups, hairδ13C was depleted in cubs relative to their mothers (averageof mean depletion values per group = –0.8‰,n = 2). Whilethere was considerable between-group variance in mother–cub enrichment for both isotopes, within-group variance wasremarkably low (Table 2).

Potential foods of bears ranged widely in stable-isotopevalues (Table 1). In general, plant foods were more depletedin both 15N and 13C than herbivore tissues. Ants were moreenriched in15N than mountain goat, moose, and elk, likely

reflecting their more omnivorous diets. However, white-taileddeer were the most enriched. Meanδ15N values for plants(δ15Np) and meat (δ15Na) can be used to solve eq. 5. Basedon the potential food values listed in Table 1, we estimated(unweighted) average values forδ15Na and δ15Np to be 3.3and –2.1‰, respectively. Assuming further that negative es-timates ofPa indicated no animal tissue in the diet and valuesexceeding 1 indicated 100% animal tissue (e.g., Hilderbrandet al. 1996; Jacoby et al. 1999), vertebrate or invertebratefoods contributed detectable amounts to the diet of 62% ofthe research male black bears, 72% of the research femaleblack bears, and 46% of the research male grizzly bears, butonly 18% of the research female grizzly bears. Using data

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Fig. 1. Distribution of δ15N and δ13C values for hair of black and grizzly bears inhabiting the upper Columbia River basin, BritishColumbia, 1994–1996.



based on individual bears (i.e., not averages as presented inTable 1), the average contribution of meat and (or) inverte-brates to the diet was 8.3% for research male black bears,15.0% for research female black bears, 9.9% for researchmale grizzly bears, and only 3.0% for research female griz-zly bears. Our analyses suggested that 82% of the man-agement bears had a detectable amount of meat and (or) in-vertebrates in their diet, the average contribution being 31%.

The isotope-mixing model used here is obviously sensitiveto choice of isotopic plant and animal dietary end-points.The above calculations are appropriately based on unweightedmean values for a number of species that we felt were poten-tial dietary components in our study area. However, to dem-onstrate the sensitivity of the mixing model to choice oflocal end-point values, we present the extreme example ofresearch male grizzly bears consuming exclusively (i) plantsand meat with the highest meanδ15N values (i.e., soapberry(Shepherdia canadensis) and white-tailed deer (Odocoileusvirginianus)), (ii ) plants and meat with the lowest meanδ15Nvalues (i.e., spring beauty (Claytonia lanceolata) and moun-tain goat (Oreamnos americanus)), (iii ) plants with high andmeat with low meanδ15N values (i.e., soapberry and moun-tain goat), and (iv) plants with low and meat with high meanδ15N values (i.e., spring beauty and white-tailed deer). Forthese four scenarios, the mean percent animal contribution tothe diet (based on data from individual bears) was 0, 37.5, 0,and 24.7%, respectively.

Discussion

Our isotope investigation indicates trophic segregation be-tween female grizzly bears and all other bears of both spe-cies inhabiting the upper Columbia River basin. Few femalegrizzly bears consumed meat or invertebrates in amountssufficient to be detected using our isotopic model. In ourstudy area, female grizzly bears were found most often inremote, higher elevation habitats (B.N. McLellan and J.G.

Woods, unpublished data). Although the abundance of allmammals in the study area has not been documented, largemammals appeared to be relatively rare at higher elevations.There is some evidence that soilδ15N may become depletedwith altitude (Mariotti et al. 1980) and that these patternscan be reflected in local food webs (Gröcke et al. 1997). Wedo not know if this is the case in our study area, but if it is,greater depletion ofδ15N in female grizzly bears would notnecessarily mean lower consumption of animal protein rela-tive to bears inhabiting lower altitudes. Smaller mammals,such as marmots (Marmota caligata) and ground squirrels(Spermophilus columbianus) were common in these higherbasins, and female bears have often been seen digging forthem. Male grizzly bears, with their larger ranges (Woodset al. 1999), not only travel more but also are found at lowerelevations more often than female grizzly bears (B.N.McLellan and J.G. Woods, unpublished data) and thus malesmay encounter large mammals more often. Isotopic mea-surements from ground squirrels at high altitudes, as well asfrom soils or plants along an altitudinal gradient, are re-quired to fully resolve the question of whether female grizzlybears actually consume less animal protein, as is suggestedby our isotopic approach.

Ants are a major food for many black bear populations(Hatler 1972; MacHutchon 1989; Holcroft and Herrero 1991;Noyce et al. 1997), and adjacent to our study area they werethe main food item during June and July (Raine and Kansas1990). Grizzly bears also consume ants (Hamer and Herrero1987; Mattson et al. 1991; McLellan and Hovey 1995), butthese were not the dominant food during any season. Be-cause a higher proportion of black bears had detectableamounts of animal protein in their diet than male or femalegrizzly bears, it is probable that ants, which are more ubiqui-tous than large mammals, made up a higher portion of theblack bears’ diet in our study area and that consumption ofants is reflected in theδ15N values of black bear hair. As ex-pected, management bears had more animal protein in their

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Group

δ13C (‰) δ15N (‰)

Mother Cub ∆δ13C (‰) Mother Cub ∆δ15N (‰)

1 –22.5 –20.6 +1.9 3.9 7.7 +3.82 –22.8 –20.9 +1.9 3.7 7.6 +3.9

–20.3 +2.5 7.5 +3.83 –22.4 –21.9 +0.5 4.6 5.0 +0.4

–22.0 +0.4 4.8 +0.24 –22.7 –21.5 +1.2 4.6 7.7 +3.1

–21.7 +1.0 7.6 +3.0–21.7 +1.0 7.5 +2.9

5 –22.7 –22.5 +0.2 5.2 7.6 +2.4–22.0 +0.7 7.5 +2.3–22.4 +0.3 7.4 +2.2

6 –23.9 –24.2 –0.3 4.8 7.2 +2.4–24.2 –0.3 7.1 +2.3

7 –22.8 –24.1 –1.3 3.8 5.2 +1.4–23.9 –1.1 5.2 +1.4

8 –22.5 –20.3 +2.2 4.2 7.3 +3.1–21.0 +1.5 7.5 +3.3

Table 2. Stable-isotope values for hair of black bear mother–cub groups sampled from dens inMinnesota in 1998–1999 and their relative differences.



diet than research bears. These bears risked a close associa-tion with people to gain access to these high-quality foods.

Recently, Jacoby et al. (1999) used stable carbon and ni-trogen isotope analysis of hair and bone to investigate trophicrelationships among populations of black and grizzly bearsin several areas in the western United States and Alaska.Much of Glacier National Park and all of the Cabinet/Yaakof Montana are, like our study area, in the Columbia Riverdrainage. Like the bears in our study, recent (post 1996)samples of subadult male and female grizzly (n = 13), adultfemale grizzly (n = 2), and black (n = 13) bears from thesesites had low meanδ15N values (2.6–3.9‰; Jacoby et al.1999; Table 1). However, adult males at these sites (n = 9)had higher meanδ15N values (4.5–5.2‰), and contemporarysamples from adult males in the Greater Yellowstone andBlackfeet and Flathead Indian Reservations (n = 26) hadconsiderably higherδ15N values (7.4–7.6‰). This indicatesthat adult males sampled by Jacoby et al. (1999), particu-larly those in Glacier National Park, had higher levels of ani-mal protein in their diet than the bears in our sample.

The isotopic model used by Jacoby et al. (1999) differedfrom ours in that they estimated plant isotope dietary end-points based on herbivores in the area. Our investigationsuggests that this may be inappropriate because ungulatesmay have fed on foods that differed isotopically from thosepreferred by bears. For example, while we found plant foodsof bears with an average (unweighted)δ15N value of –2.1‰,our estimate, if it were based solely on herbivores in ourarea, would have suggested a value of –0.8‰. Using ourvalue of δ15Np (–2.1‰) and theδ15Na value of 3.4‰ mea-sured by Jacoby et al. (1999) for ungulate meat in their area,our isotope model provides generally higher estimates of animal-protein input for the Glacier National Park and Cabinet/Yaak samples. Without a detailed isotopic survey of plantfoods of bears from these areas, it is currently impossible toknow which estimates of animal-protein input into the dietsof these bears are correct. Importantly, our comparison sim-ply serves to suggest that the isotopic models used are quitesensitive to the choice of isotopic end-point values, and it isclearly more appropriate to use estimates based on knownbear foods than those based on more indirect methods. Cer-tainly, estimates of the contribution of meat to the diets ofbears across their range, as recently provided by Hilderbrandet al. (1999) and based on local herbivore end-points, shouldbe interpreted cautiously. While such studies are useful inproviding general trends, they may not provide useful abso-lute dietary estimates. This is a general problem in applyingthe stable-isotope technique to the reconstruction of animaldiets in cases where individuals may have access to prey thatvaries considerably in isotope values within so-called dietaryend-points. We have provided an example of research malegrizzly bears from our study area involving four scenarios ofpopulations feeding exclusively on components of plant andanimal diets that represented combinations of high and lowstable isotope values. This exercise, although representing aworst case scenario, illustrates the sensitivity of the modelsto field sampling of appropriate dietary items and our ulti-mate knowledge of how best to estimate dietary end-pointvalues (Schwarcz 1991; Hobson 1993). The overlap betweenants and ungulate meat in theδ15N values that we measured

further underlines the need to interpret isotopic models withcare. For example, currently we cannot distinguish isotopi-cally between those bears that feed heavily on ants and thosethat feed heavily on ungulates, despite the obvious ramifica-tions for ecological interpretation.

The above discussion underlines the need for caution whenusing stable-isotope models in ecological research. In thecase of bears that have access to both plant and animalfoods, there is the additional problem of interpreting isotopedata because nutritional pathways involving proteins andcarbohydrates may be different (Ambrose and Norr 1993;Tieszen and Fagre 1993; Hobson and Stirling 1997).Hilderbrand et al. (1996) provided valuable evidence that theδ15N andδ13C values for blood plasma correspond closely tothose for bear diets ranging in composition from 100% plant(i.e., apples) to 100% meat, and this has provided a firm em-pirical basis for the isotope models used here and in otherstudies. However, in cases where plant carbon derived fromcarbohydrates is used largely in the manufacture of lipids in-stead of carbon from plant proteins contributing to bear pro-tein (e.g., plasma, hair, muscle),δ13C values in bear tissueswill depend on tissue type (i.e., protein versus lipid) and theδ13C value of the plant macronutrient contributing to that tis-sue. Our isotopic analysis of bear hair provides informationon the relative contributions of protein sources, rather thancarbohydrate or lipid sources, to bears. Thus, we need torealize that estimates of meat in the diet may be overrated,depending on whether, nutritionally, the bear is primarilyacquiring protein or storing fat. As with other applications ofthe stable-isotope technique, understanding animal nutritionalecology is crucial to interpreting isotope data (e.g., Hobsonand Stirling 1997).

If plant protein and carbohydrate differ in theirδ13C val-ues, then the overall plantδ13C value would depend on plantcarbohydrate content, resulting in a broad distribution ofplant δ13C values even though the range of plantδ15N valuesremained fairly narrow. In our study, we found a weak cou-pling betweenδ15N and δ13C values for a bear populationthat was consuming largely plant material. Including the bearsthat consumed animal protein created trophic enrichment inboth15N and13C that drove the positive relationship for griz-zly bears, probably because both carbon and nitrogen showpositive isotopic fractionation with trophic level, althoughthe effect is weaker with carbon. Interestingly, in their exam-ination of stable isotope ratios across bear populations repre-senting a broad range of dependence on meat, Hilderbrand etal. (1999) present a figure that shows much higher variancein δ13C andδ15N values for bear populations that are largelydependent on plants than for populations dependent on meat.

We suggest that the strong positive correlation betweenδ15N andδ13C values in bear tissues indicates that the nutri-tional pathways of carbon and nitrogen are coupled (i.e.,dietary δ13C values correspond closely to those for dietaryprotein) and that this is much more likely in populationsconsuming primarily meat than in those consuming primar-ily plant foods. Rather than relying heavily on isotopic mod-els to infer meat consumption by bears within populationshaving access to both plants and meat, an examination of thedispersion ofδ15N andδ13C values in bear tissues should re-veal those individuals that rely to a greater extent on meat in

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Hobson et al. 1337



their diet. In our study, the grizzly bears shown in the upperright quadrant of the lower panel of Fig. 1 likely consumedsubstantial animal protein, probably meat.

Nursing black bear cubs in dens generally showed isoto-pic enrichment in their hair compared with the hair of theirmothers. This was expected, especially for15N, because cubsdepend exclusively on their mother’s milk for protein de-rived from parental tissues, which thus constitutes a trophicenrichment step. While few other studies have included aninvestigation of such effects in mother–offspring pairs, thereis some evidence that maternal transfer of nutrients leads toisotopic enrichment in offspring. For example, theδ15N valuesin the muscle tissue of nursing northern fur seal (Callorhinusursinus) pups were 1.9‰ higher than those of their mothers(Hobson et al. 1997), and theδ15N values of tooth annulifrom Steller sea lions (Eumetopias jubatus) were higher dur-ing their first year of life (Hobson and Sease 1998). Finger-nails from human infants were also found to be enriched in15N by 2.4‰ over those of their mothers (Fogel et al. 1989).Bocherens et al. (1994) inferred a nursing effect in decidualteeth of extinct cave bears (Ursus spelaeus) and, more re-cently, Nelson et al. (1998) speculated that enrichedδ15Nand depletedδ13C in the bone collagen of young versus adultcave bears was related in part to their dependence on mother’smilk. In the case of our analysis of hair from black bearmothers and cubs, it is possible that some decoupling of theparent–offspring isotopic-enrichment effect occurred for somegroups because the isotope values for hair from the mothersonly represent the diet during the period of hair growth andmay not always correspond to the diet when nutrients arestored for transfer to cubs during nursing. In addition, bearmilk consists primarily of protein and lipids, and the relativemobilization of these two sources of carbon to bear hair isexpected to strongly influence theδ13C values of cub hair,since lipids are typically more depleted in13C than proteins(Gearing 1991). More research into the factors determiningisotopic relationships between the tissues of mothers andtheir nursing cubs would be extremely useful.

Acknowledgements

Stable-isotope analyses were provided by G. Parry of theSoil Science Stable Isotope Facility at the University of Sas-katchewan. Additional assistance in the preparation of stable-isotope samples was provided by S. van Wilgenburg andP. Healy. Funding was provided by K.A.H. and the CanadianWildlife Service. Bear hair was collected as part of the WestSlopes Bear Research Project, jointly supported by the Brit-ish Columbia Ministry of Environment, Lands, and Parks(Grizzly Bear Conservation Strategy); the British ColumbiaMinistry of Forests; the Columbia Basin Fish and WildlifeCompensation Program; Forest Renewal British Columbia;the Friends of Mount Revelstoke and Glacier National Parks;Parks Canada (Glacier, Kootenay, Mount Revelstoke, Yoho,Ottawa); the Southern British Columbia Guides and GuideOutfitters Association; the University of Alberta; and TheUniversity of British Columbia. In addition, we thank the in-dividuals who assisted us in capturing research bears, andthe Conservation Officers of the Ministry of Environment,Lands, and Parks who made our study of management bearspossible. Roger Ramcharita assisted with the collection of

bear food samples and Kelly Stalker with hair sampling.Conan Phelan assisted with data-base management. Blackbear hair samples from Minnesota were provided by KarenNoyce of the Minnesota Department of Natural Resources.

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