International Association for Ecology

Consumption of Salmon by Alaskan Brown Bears: A Trade-off between Nutritional Requirements and the Risk of Infanticide? Author(s): Merav Ben-David, Kimberly Titus, LaVern R. Beier Source: Oecologia, Vol. 138, No. 3 (Feb., 2004), pp. 465-474 Published by: Springer in cooperation with International Association for Ecology Stable URL: http://www.jstor.org/stable/40005854 Accessed: 10/02/2010 09:23

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http://www.jstor.org Oecologia (2004) 138: 465-474 DOT10.1007/s00442-003-1442-x

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Merav Ben-David • Kimberly Titus • LaVern R. Beier Consumption of salmon by Alaskan brown bears: a trade-off between nutritional requirements and the risk of infanticide?

Received: 27 February2003 / Accepted: 27 October2003 / Publishedonline: 13 December 2003 © Springer-Verlag 2003

Abstract The risk of infanticide may alter foraging accompanied by young than when mated, while 6 did decisions made by females, which otherwise would have not. Radiotelemetrydata indicated that females with spring been based on nutritionalrequirements and forage quality cubs were found, on average, further away from streams and availability. In systems where meat resources are during the spawning season compared with females with spatially aggregated in late summer and fall, female brown no young, but both did not differ from males and females bears (Ursus arctos) would be faced with a trade-off with yearlings and 2-year-olds. Females with young that situation. The need of reproductive females to accumulate avoided salmon streams were significantly lighter indicat- adequate fat stores would likely result in a decision to ing that female choice to avoid consumption of salmon frequent salmon streams and consume the protein- and carries a cost that may translate to lower female or cub lipid-rich spawning salmon. In contrast, aggregations of survivorship. The role of the social hierarchyof males and bears along salmon streams would create conditions of females, mating history, and paternity in affecting the risk high risk of infanticide. We investigated consumption of of infanticide and foraging decisions of female brown salmon by brown bears on Admiralty and Chichagof bears merit further investigation. Islands in Southeast Alaska from 1982 to 2000 using • stable isotope analysis and radiotelemetry.While nearly all Keywords Alaska Cubs • Diet • Dominance hierarchy • males (22 of 23) consumed relatively large amounts of Stable isotope ratios salmon (i.e., >10% relative contribution to seasonal diet), not all females (n =56) did so. Five of 26 females for which we had reproductive data, occupied home ranges Introduction that had no access to salmon and thus did not consume salmon when they were mated or accompanied by young. The risk of predation may alter foraging decisions made Of females that had access to salmon streams (n =21), all by individuals (Cowlishaw 1997; Diehl et al. 2000; Grand mated individuals (n =16) had 615N values indicative of 2002; Kie 1999; Lima 1998; Luttbeg and Schmitz 2000; salmon consumption. In contrast, 4 out of 16 females with Sweitzer 1996). Such alterationin foraging strategies may cubs avoided consuming salmon altogether, and of the be most pronounced for reproductive females faced with a other 12, 3 consumed less salmon than they did when they trade-off between meeting nutritional requirements and were mated. For 11 of 21 females with access to salmon avoiding the risk of predation, in an attempt to maximize streams we had data encompassing both reproductive lifetime reproductive success (Stearns 1992). In many states. Five of those altered foraging strategies and species, females accompanied by young select habitats of exhibited significantly lower values of 615N when lower quality, where the risk of predation may be lower or escape terrainmore accessible (Barten et al. 2001; Bowyer M. Ben-David (121) et al. 1998; Cowlishaw 1997; Lima 1998; Rachlow and Departmentof Zoology and Physiology, University of Bowyer 1998). Although superficially similar to condi- Wyoming, tions of under the risk of P.O. Box 3166 USA foraging predation risk, avoiding Laramie,WY, 82071, infanticide is further on e-mail: [email protected] complicated by dependency Tel: +1-307-7665307 intraspecific social conditions. While animals foraging Fax: +1-307-7665625 under predation risk are likely to experience predation related to densities and habitat K. Titus • L. R. Beier pressures predator characters Lima and Dill infanticide Division of Wildlife Conservation,Alaska Departmentof Fish (Grand 2002; 1990), and Game, may also depend on male social hierarchy (Weilgus and Douglas, AK, 99824, USA Bunnel 1995, 2000), male coalition size (Packer and Pusey 466

1984), or male-female mating history (Bartos and offspring are derived from energy-stores accumulated Madlafousek 1994). Thus, foraging decisions made by prior to denning (Barboza et al. 1997; Farley and Robbins females in species experiencing risk of infanticide may 1995). Thus, the ability of females to obtain meat have evolved under fluctuating pressures, which may lead resources and accumulate adequate fat stores in late to high variability in individual responses and have large summer and early fall has a large influence on gestation consequences for the dynamics of populations and and lactation through the winter dormancy and the ecosystem processes. associated fast (Barboza et al. 1997; Farley and Robbins Although rarely observed, infanticide in brown bears 1995). Indeed, several studies documented that reproduc- {Ursus arctos), black bears (U. americanus), and polar tive success in bears is directly related to body mass in the bears {U. maritimus) is a well-documented phenomenon fall (Atkinson and Ramsey 1995; Rogers 1987; Samson (Craigheadet al. 1995a; Derocher and Wiig 1999; Wielgus and Hout 1995). and Bunnell 1995). Most reports describe adult and sub Systems in which meat resources are spatially aggre- adult males killing young-of-the-year or yearling cubs gated in late summer and fall, such as salmon streams (Craighead et al. 1995a; Dean et al. 1986; Derocher and (Onchorhynchus spp.) in the Pacific Northwest (Heard Wiig 1999; Olson 1993; Taylor et al. 1985). Several of the 1991; Salo 1991; Sandercock 1991), create conditions reports indicate the killing of the sow in defense of her where an individual female may face a trade-off situation. cubs, while others document the killing of young by The need of reproductive female brown bears to nonsire females (Dean et al. 1986; Hessing and Aumiller accumulate adequate fat stores in late summer and early 1998). Although the victim was consumed in most fall would likely result in a decision to frequent salmon instances, cannibalism could not be invoked as the cause streams and consume the protein- and lipid-rich spawning of aggression in all cases (Dean et al. 1986; Hessing and salmon. This would be especially true for mated and Aumiller 1998). Thus, similar to other species such as lactating females (i.e., females accompanied by young-of- African lions (Panthera leo; Packer and Pusey 1984) and the-year and yearlings) that would face high energetic red deer (Cervus elaphus; Bartos and Madlafousek 1994), demands in the following winter. In contrast, aggregations infanticide in bears is more likely related to male of bears along salmon streams would create conditions of reproductive success (Swenson et al. 1997). high risk of infanticide from both males and nonsire Weilgus and Bunnell (1995) reported that in areas with females. Thus, females accompanied by young-of-the-year high mortality of older males, where influx of immigrant, and yearlings would likely avoid aggregations of other nonsire males was high and social hierarchywas unstable, bears along salmon streams, a decision that will result in female brown bears avoided preferred habitats to reduce low consumption of salmon. risk of infanticide. In areas with low male mortality, In this study, we investigated consumption of salmon by females did not demonstrate such spatial segregation brown bears on Admiralty and Chichagof Islands in (Wielgus and Bunnell 1995), suggesting that risk of Southeast Alaska from 1982 to 2000. In these areas, infanticide may play an important role in determining studies on resource selection found different selection for availability of high-quality resources for reproductive some habitat types by males and females (Titus et al. females. Similar observations of spatial segregation due to 1999), although both genders made high use of riparian predation on cubs by nonsire bears were made for areas in association with spawning salmon during late Yellowstone grizzly bears (Mattson and Reinhart 1995). summer (Titus and Beier 1999). We hypothesized that Swenson et al. (1997) described lower cub survival in a females with young offspring will consume less salmon hunted population of brown bears in Sweden compared and will be found furtheraway from salmon streams than with a non-hunted population. These authors attributedthe adult males and mated or non-breeding females because lower survivorship and resulting reduction in population females with young offspring will be more at risk from growth to killing of cubs by immigrating nonsire males infanticidal nonsire males and females. In addition, we (Swenson et al. 1997). Similarly, Weilgus and Bunnel predicted that the same individuals would use different (2000) determined that reproduction rates in three foraging patternswhen accompanied with young offspring populations of bears were consistent with expectations compared with periods when cubs are absent. We also based on infanticide by nonsire immigrant males. In explored the effect of female size, as a surrogate for contrast,other studies indicated that dominant females had dominance, on levels of salmon consumption in an attempt higher reproductive success (Craighead et al. 1995a), to evaluate the potential effect of dominance on decision suggesting that female rather than male dominance could making in reproductive brown bears. influence risk of infanticide and thus foraging decisions made by reproductive females. In brown bears, the combined costs of hibernation, Materials and methods gestation, and lactation place large energetic demands on reproductive females (Barboza et al. 1997; Farley and Study areas Robbins 1995; Hilderbrand et al. 1999a, 1999b, 2000; Watts and Jonkel Because and lactation in Admiraltyand Chichagof Islands (57°52TSf135°18'W; Fig. 1), two 1988). gestation of the three large northernislands of the AlexanderArchipelago, are bears occur while the female is sequestered in a den, partof the TongassNational Forest. The archipelagohas a maritime energy requirements for supporting a female and her 467 climate;summers are cool and wet and winters are characterizedby Brown bears in the AlexanderArchipelago deep snow (2,360 mm annualprecipitation). The snow-free period extends from to November at lower early May early elevations. Brown bears on Admiralty,Baranof, and Chichagof islands (ABC at elevations is in Vegetation higher typically alpine tundra, and islands) of the Alexander Archipelago occur in high densities forest lower elevations coastal, old-growth of Sitka spruce (Picea (AdmiraltyIsland: 400-450 bears/1,000km2; Chichagof Island: 320 and western hemlock with a well- sitchensis) (Tsuga heterophylla) bears/1,000km2; Miller et al. 1997). Brown bears in our study areas Vaccinium developedunderstory (mainly Oplopanaxhorridus, spp., usually den at high elevations with females entering their dens Menziesia and Rubus New ferruginea , spp.). growth of grasses earlier (late October) and emerging later (mid-May) than males (Poaceae), sedges (Cyperaceae),beach peas (Lathyrusjaponicus), (Schoen et al. 1987). After emergence from dens bears travel to and skunk shoots occurs in cabbage (Lysichitumamericanum) May lower elevations in late April and May and begin feeding on new and June and lasts throughOctober. Berries (blueberries,Vaccinium growth vegetation, often in estuaries,grass flats and Rubus muskegs. By spp.; salmonberries, spectabilis; cloudberries,R. chamae- mid-June many bears are found in subalpineand alpinehabitats until stink current Ribes Pacific crab morus; fruits, bracteosum; apple, mid- following vegetationgreen-up. Mating often occurs during Malus devil's club and mush- July fusca\ fruits, Oplopanax horridus), this period. From late-July throughearly Septembera high portion rooms (Bolitus sp., Hygrophorusspp., Mycena spp., Omphalinea of the bear populationis associatedwith salmon-spawningstreams; and Russula become available from late to late spp., spp.) July some individual bears, however, do not visit salmon-spawning Our area numerousstreams that October. study encompasses support streams and remain at higher elevations throughoutthe year. Pacific By an annual run of spawning salmon (Onchorhynchus early September bears begin leaving the riparian areas, while O. keta and O. from the end of gorbuscha, , kisutch) July to the spawning salmon remain abundantand easily accessible. Through end of November. Potential mammalianprey species for bears on the early fall, many of the bears are associated with avalanche the islands include long-tailed voles (Microtus longicaudas) and chutes, a habitattype with abundantberry crops (Schoen and Beier Sitka black-tailed deer (Odocoileus hemionus sitkensis). The 1990; Titus et al. 1999). intertidalzone has a rich fauna including crabs (such as Telmessus cheiragonous, Hemigrapsus oregonensis, H. nudus, Pugettia gra- cilis), blue mussels (Mytilus trossulus), clams, and fishes (such as of bears and Oligocattusmaculosus, Icelinus borealis , Leptocottusarmatus). Capture collection of samples We captured,immobilized with Telazol (7-10 mg/kg of estimated body weight; Fort Dodge Animal Health, Fort Dodge, Iowa, USA), and radio collared (Telonics, Mesa, Ariz., USA) more than 200 brown bears from 1982 through 2000. Subadult bears received

Fig. 1 Location of study areas (shaded) on Admiraltyand ChichagofIslands, southeast Alaska. USA 468 surgical-tubingbreak-away radio collars. We capturedmost of the querying the GIS for the minimum distance to the nearest salmon bears by dartingfrom helicoptersin rugged alpine habitats,mostly streamfor 38 males and 79 females (n =117) duringthe spawning in June and early July. About 20% of the bears were capturedwith season in 1990 to 1995. For each bear,the averagedistance in each foot snaresnear a local landfill or on well-used trails along salmon- year was calculated to account for multiple locations and unequal spawning streams. Capture and handling methods followed the sample sizes among bears. This resulted in a value of average Alaska Departmentof Fish and Game's animal welfare policy to distance per year. Several bears had multiple years of data (total of assurethat bears received humanecare and treatment.Over the 19- 181 datapoints), resultingin pseudo-replication.This was addressed year study we believe we capturedbears in representativehabitats in following analyses by blocking the analysis by bear (i.e., bear acrossthe study areasand thatthere was no bias regardingcapturing numberwas enteredas a randomfactor). most bears in alpine habitats and subsequently assessing their riparianhabitat use patterns.Cub survival was determinedvisually duringre-sighting of females in years following the fitting of radio food collars. Sampling types Measurementsof and neck circumferencewere body length, girth for each season were collected for stable obtainedto the nearest 1 cm. Skull length and width were measured Samples isotope analysis to the nearest 1 mm. measurementswere obtainedfor based on description of diets for brown bear in the Alexander Weight many derived fecal and of the capturedbears using hanging scales to the nearest 5 kg. For Archipelago through analysis (McCarthy 1989) bears that were not estimates were determinedbased on included: grasses; sedges; beach peas; skunk cabbage shoots and weighed, berries stink current the morphometricmeasurements of the bear in comparisonto other roots; (blueberries,salmonberries, cloudberries, bears for which both and were obtainedand fruits, Pacific crab apple, devil's club fruits); mushrooms;pink, weight morphometrics Sitka black-tailed based on the of the crew Beier, J. Schoen, chum, and coho salmon; long-tailed voles; deer; experience tagging (L.R. crabs and blue mussels. Tissue of salmon and deer were K. Titus).Blood and hair sampleswere collected from 56 individual samples female and 23 male bears. obtained from encounteredcarcasses or obtained from fishermen values of blood collected in June- and hunters (Ben-David et al. 1997a, 1997b). Vegetation and Isotopic samples July likely were collected at 100 m intervals 11 and diets, because occurred mushroom samples along representspring early-summer sampling transects m from to habitats 60-70 days afterden emergence,a time which would allow for diet vegetation (1,000 long) riparian upland to be into blood cells et al. (Ben-David et al. 1998). Additional samples of vegetation were signatures incorporated (Hilderbrand collected at elevations and at beach habitats.Muscle 1996). Hair samples collected duringthe same period representlate higher fringe summerand fall diets of the because hair in samples from long-tailedvoles were collected from two companion previous year growth studies et al. and Barnard Each bears occurs in late summer and fall (a period that lasts about (Ben-David 1997a; Hanley 1999). 90 and hair is terminatedwhen the animals enter carcasswas also preparedas a museum specimen (includingfrozen days) growth and archivedat the of Alaska Museum. hibernationin late October (C.T. Robbins, personal communica- tissues) University tions). Otherstudies of large mammalssuggest that dietaryisotopic values are fully expressedin hair after 10-12 weeks (Sponheimeret al. 2003). Analysis of stable isotope ratios For 22 of the females, multiple samples were obtained. These hair from the same included both blood and samples trapping Tissues blood cells, hair, muscle samples, and vegetation occasion as well as from several different in (clotted samples captures were frozen until preparationfor determinationof different These allowed us to in samples) kept years. investigatechanges foraging stable isotope ratios. Although lipid contentsmay deplete values of patternsfor the same individualsunder different reproductive states. 613C of tissues (DeNiro and Epstein 1978; Kelly 2000), samples Females observed with young-of-the-year during the sampling were not defattedbecause clotted blood cells, hair, and vegetation session in spring/early-summerwere defined as mated for the contain low amounts of and no difference was detected in the lipids analysis of hair samples, because the hairs were replacedduring 613C in salmon fat and defattedmuscle tissues (Ben-David 1996). fall It that these females had older previous to capture. is possible were dried at 60° to 70°C for 48 h and then groundto fine in it is that these did not den with Samples offspring toe but likely offspring a - L (Crescent Dental, Chicago, the female thatwinter. we treatedthese females as if were powder using Wig Bug grinder Thus, they 111.).Samples of intertidal crabs were then dissolved in 95% not accompanied by young offspring in our analysis. Females acid solution to remove calcium carbonatesand re- with and cubs in the hydrochloric captured yearlings 2-year-old spring/early dried. a (1-1.5 mg for animaltissues and summersession were defined as females with for Subsequently, sub-sample young offspring 8-10 for was weighed into a miniaturetin cup the which was in their hair mg plant tissues) previous fall, represented samples. (4x6 mm) for combustion.We used a Europa20/20 continuousflow isotope ratio mass spectrometerto obtain the stable isotope ratios. Each sample was analyzed in duplicate and results were accepted Accessibility and distance to salmon streams only if the variancebetween the duplicatesdid not exceed thatof the peptone standard(613Cstd=- 15.8, 615Nstd=7.0,CV=0.1) We located radio collared bears from a small aircraft (Kenward 1987) duringdaylight hours once or twice every 2 weeks throughout the year from 1990 to 2000. The location of each bear was Data analysis determinedwith a global positioning system (GPS) unit and plotted on 1: while high-resolution,orthophoto maps (scale 31,680) circling To determinewhether male and female diets significantly differed in the aircraft above the location. Error was determined during between seasons we used MANOVAwith 613Cand 615N as of marked individuals and was estimated at 50-110 m. 2-way recaptures the dependentvariables, and season and sex as the factorsas well as Aerial locations were digitized and transferred to geographic a sex season interaction and Wichern 1988). Because information GIS of the areas by (Johnson system (GIS). Digital maps study several samples were collected from the same individuals in were obtained from the USDA Forest Service, Tongass National different seasons and we added individual ID as a random Forest. These demarcatedstream used anadro- years maps segments by factor to control for pseudo-replication.Because values of 613Cin mous fish. hair are enriched l-2%o to muscle and blood of streamsto each individualbear samples by compared Accessibility salmon-spawning in the same individual et al. 1996; Nakagawa et al. was assessed based on home location Convex (Hilderbrand range (Minimum 1985; Tieszen and Fagre 1993), we correctedhair values relativeto Polygon, Kenward 1987) on the landscape. A home range that red blood cells l%o et al includeda fish streamwas consideredto by (Hilderbrand 1996). segment of an anadromous the IsoSource and Gregg 2003) we have salmon available.Distance to salmon streamwas obtained Using program (Phillips by determined the cutoff point, which represented less than 10% 469 relative contributionof salmon to the diet of bears. Although linear mixing models may be inadequateto determinerelative contribution of food items to the diet of consumers(Ben-David and Schell 2001; Phillips 2001; Phillips and Koch 2002; Robbins et al. 2002), the cutoff point we derived is similar to that (6.1%o)obtained from a differentmodel describedby Hilderbrandet al. (1996; Robbins et al. 2002). To derive the cutoff point, we used diet-tissueenrichment of 2%ofor carbonwhen mammalianprey, avian prey, and berrieswere consumed, and l%owhen salmon or invertebrateswere consumed, based on results from feeding experiments in captivity on mink (Mustela vison) and black bears (Ben-David 1996; Ben-David and Schell 2001; Hilderbrandet al. 1996). Also, based on the captive experimentswe used fractionationvalues of 3%ofor nitrogen (Ben- David 1996; Hilderbrandet al. 1996). Before conducting the analysis, we verified that potentialfoods significantlydiffered from each otherusing a K nearest-neighborrandomization test (Rosing et al. 1998). We furtherexplored differences in diet between mated females and those accompaniedby young-of-the-yearand yearlingsbased on this cutoff point. This analysis was conductedwhile accountingfor the availabilityof salmon streamsbased on the location of the home range on the landscape. We tested whether the isotopic values of females that adopted differentforaging strategiesdiffered between when they were mated and when accompaniedby young using a Wilcoxon test of 2 related samples (Zar 1984). We investigated the effects of sex and reproductive state on average distance to salmon streamswith a one-way ANOVA with category (males, females with no cubs, females with cubs of the year, and females with yearlingsand 2-year-olds)as the independent variableand distanceas the dependentone with bear ID as a random factorto account for pseudo-replication.This analysis was followed by Scheffe multiple comparisonsto identify the sex and reproduc- tive states that significantlydiffered from each other. We then explored whether the dominance of the female influencedher foragingpatterns. Because we had no data on social interactionsamong our study animals we used age and size as surrogatesto dominance and comparedsize of those females with young that consumed >10% salmon with females with young that consumed <10% using a Mann-Whitney test (Zar 1984). All analyses were conductedusing SPSS for Windows and significance level was set at exlevel of 0.05.

Results

Stable isotope ratios of blood and hair samples collected from individual bears exhibited high variability (Fig. 2; n =56 females, 23 males, and overall 129 data points Fig. 2 Values of 613C and 615N for male (triangles) and female because of repeated sampling of several individuals). A (circles) brownbears on Admiraltyand ChichagofIslands, southeast in values occurred between the Alaska, between 1982 and 2000. Blood samples (n =64 from 43 significant change isotope the season and hair two seasons and individuals)represent spring early-summer (A) genders (Fig. 2; 2-way MANOVA, samples (n =65 from 37 individuals) represent late-summerfall overall model P <0.01, 613C corrected, P O.001, and season (B). Mean values ± SE are given for possible food items in 615N, P =0.002). While no significant difference in each season with sample sizes denotedin parentheses.Stable isotope ratios was detected between males and females ratios of grasses, sedges, beach pea, and roots of skunk cabbagedid isotopic not differ from each in summer P significantly other (K nearest-neighbor early (Fig. 2; 2-way MANOVA, gender randomization test, P >0.3) and were pooled as one group- =0.08), such difference became significant in the fall grasses/sedges. Similarly, voles and deer (P =0.8), resulted in a (Fig. 2; 2-way MANOVA, gender P =0.01). This change single group, as did all species of berries(P =0.2). Following these was most evident from the increase in values of 615N in grouping stable isotope values of food items significantly differed from each other 613C values of hair were corrected collected from males, the (P <0.05). by samples represented by signif- l%ofor tissue fractionationin all statisticalanalyses icant interactionbetween season and gender (Fig. 2; 2-way MANOVA, interaction 613C corrected, P =0.2; and 615N, P =0.05). data, occupied home ranges that had no access to salmon Comparison of isotope values for mated females with and thus did not consume salmon when they were mated those of females with young-offspring revealed that or accompanied by young (Fig. 3). Two of these females, females in our study adopted three foraging strategies. sampled when they were neither mated nor accompanied Five of the 26 females for which we also had reproductive by young, had depleted isotopic values indicative of lack 470 of salmon in the diet regardless of reproductive state (no. =16) had 615N values >6.2%o(Fig. 3). In contrast,4 out of 43, 615N=1.82%0;no. 60, 615N=2.38%o). 16 females with cubs avoided consuming salmon Of females that had access to salmon streams and altogether, and of the other 12, 3 consumed less salmon reproductiveinformation (n =21), all mated individuals (n than they did when they were mated (Fig. 3). For 11 of those 21 females with access to salmon streams we had data encompassing both reproductive states. Five of those altered foraging strategies and exhibited significantly lower values of 615N when accompanied by young then when mated (Wilcoxon, P =0.043), while 6 did not (Wilcoxon, P =0.249). One individual (no. 141) had lower values of 615N when accompanied by young than when mated in one reproductive event (1994), but no difference in another (2000; Fig. 3). Radiotelemetry data indicated that females with spring cubs were found, on average, further away from streams during the spawning season compared with females with no young, but both did not differ from males and females with yearlings and 2-year-olds (Fig. 4; ANOVA, P =0.011). In addition, only 33% of females with young cubs were found within 1,000 m of salmon streams

Fig. 3A-C Values of 613C and 615N for female brown bears representingthree foraging strategieson Admiraltyand Chichagof Islands, southeastAlaska, between 1982 and 2000. Toppanel (A) representsfemales that consumed salmon when mated and when accompanied by young; middle panel (B) females that changed foragingstrategies; and (C) females inhabitinghome rangeswithout Fig. 4 Average distance to salmon stream in meters (± SE) {Top access to salmon streams. Open symbols representdata for mated panel), and the proportionof animalsfound less than 1,000m from a females, whereasfilled symbols representfemales with young cubs. stream{Bottom panel) for differentsex and reproductiveclasses of Circles represent individuals for which data is available in both brown bears on Chichagof Island, southeastAlaska, between 1990 reproductivestates. Squares represent females with no repeated and 1995. Different letters representsignificant differences at the samples. A cutoff point for consumption of >10% of salmon cx=0.05 level among groups as determined by Scheffe multiple correspondswith a 615N value of 6.2%o comparisons.Sample sizes are reportedabove bars 471 Table 1 Size measurementsfor Measurement High salmon (n =12) Low salmon (n =6) P value females accompaniedby young that consumed large amountsof Mean SE Mean SE salmon and those that consumed - - low amountsof salmon (i. e., Age (years) 13.3 1.4 14.3 1.9 0 55 less Ihan 10% of on diet) BodyJ length& v(cm) J 169.8 5.2 164.2 6.0 0.41 Admiraltyand Chichagof Is- lands, southeastAlaska, USA. Girth (cm) 119.5 4.1 110.8 4.7 0.41 Differencesbetween female Neck (cm) 64.6 1.9 58.5 2.2 0.03 were evaluatedwith a groups skull length (cm) 34.1 0.8 33.3 1.0 0.52 Mann-Whitney test Skull width (cm) 20.1 0.4 19.8 0.5 0.28 Weight (kg) 175.8 9.6 132.2 13.6 0.007

compared with 59% of females with no cubs (Fig. 4). Of salmon streams is a learned behavior acquired from their the 79 females for which we had telemetry data, 7 were mothers or a result of their social status is unclear, and sampled both when they were mated and when they had merits further investigation. young cubs. Six of those 7 females were found further The observation that all mated females with access to away from salmon streams when accompanied by young- salmon streams consumed salmon was expected. Although of-the-year. milk consumption of captive bear cubs in the den Cub survival to the following year was reliably constituted only 9% of the estimated annual milk intake, established for only 6 of 21 females with access to salmon lactating female black and grizzly bears lost body mass streams and foraging data. Of those 6, five consumed throughout hibernation, but maintained body weight after salmon when the cubs were young and one significantly they had resumed feeding (Farley and Robbins 1995). The reduced salmon consumption. rate of weight loss by denning, lactating females relative to Analysis of effects of size on consumption of salmon non-lactating bears was 45% higher for black bears and for those females accompanied by young revealed that 95% higher for grizzly bears (Farley and Robbins 1995). age, body length, girth, skull length, and skull width were These data emphasize the high costs of gestation and not different between females with differing foraging lactation during hibernationfor mated females and support patterns (Table 1). Circumference of neck, however, was our conclusion that mated lone females, in particular, significantly smaller in the females that consumed little would benefit from a diet including spawning salmon salmon when accompanied by young (Table 1). Similarly when this resource becomes available. body mass, measured in the following spring, was Of females with access to salmon streams, stable isotope significantly lower in females that consumed little salmon values indicated that only half of those with young when accompanied by young (Table 1). offspring consumed salmon, while the others significantly reduced the amounts they consumed. In addition, telem- etry data indicated that females with young cubs were Discussion found significantly furtheraway from salmon streams than females with no young. This observation is striking given The upstreammigration of spawning salmon was followed that the former group likely included females with both by a significant change in diet for brown bears in our study foraging strategies. It is possible, however, that females areas (Fig. 2). Several other studies using direct observa- with young offspring will have lower energetic require- tions, fecal analysis, and stable isotope analysis docu- ments than mated females in fall. The high costs of mented similar patterns in coastal British Columbia and hibernation without lactation (Barboza et al. 1997; Farley Alaska (Hilderbrandet al. 1999a, 1999b, 2000; Jacoby et and Robbins 1995; Hilderbrandet al. 2000) preclude the al. 1999; McCarthy 1989; P. Hessing, Alaska Dept of Fish possibility of nursing active, non-hibernating yearlings and Game, personal communication). That bears will and 2-year-olds (C.T. Robbins, personal communications). consume large amounts of salmon when this nutrient-rich Although no data on milk production during hibernationin resource becomes available is not surprisingin view of the those succeeding years is available, no occurrences of high reliance of bears on stored lipids and protein during active mammary glands in adult hibernating bears with hibernation (Barboza et al. 1997; Farley and Robbins yearlings or 2-year-old cubs were reported (C.T. Robbins, 1995). Farley and Robbins (1995) demonstrated that personal communication), and lactating females stopped weight loss of adult non-breeding bears during hibernation milk production when young-of-the-year reached 300 days was proportional to their metabolic body weight and of age prior to hibernation (Farley and Robbins 1995). ranged from less than 70 g/day to over 500 g/day. Such Nonetheless, our observation that females with young that mass loss illustrates the importance of accumulation of fat consumed small amounts of salmon had significantly stores prior to denning for all sex and reproductive lower body mass the following spring than those females categories of bears (Hilderbrand et al. 2000). Thus, it is with young that consumed large quantities of salmon unclear why several females in our study consistently suggests that reduction in consumption of salmon carries avoided consumption of salmon. Whether the tendency of high energetic costs for females with young. Also, the these females to select home ranges that do not encompass observation that several females with young offspring 472 made use of the available salmon and that the majority of represent lower quality habitats despite the high avail- males include large amounts of salmon in their diets, ability of salmon, because alternative meat resources are suggests the decision of females with young offspring to scarce (only deer carcasses and voles). Thus, reproductive avoid salmon streams may be in response to factors other output for these females will likely be lower than that of than nutritionalrequirements. females that consume salmon (Bunnell and Tait 1981; Can the risk of infanticide be implicated in the decision Hilderbrandet al. 1999a, 1999b; Rogers 1987; Stringham of female brown bears in our study to alter foraging 1990a, 1990b). Alternatively, such low reproductive rates strategies when accompanied by young? It is hard to may be related to high densities of bears in our study areas imagine another scenario that will result in consumption of and represent density-dependent effects. These density salmon by all mated females with access to salmon effects, however, are likely to result in high incidents of streams and reduction in use of this resource in half of infanticide as encounters between females with young and those females when they had young. On the Kenai nonsiring individuals will be high. In addition, our Peninsula, Alaska, where salmon runs are longer in population is hunted and likely experiences lower stability duration than in our system, all females with young of the male hierarchy and higher risk of infanticide offspring consume large amounts of salmon (S.D. Farley (Weilgus and Bunnell 1995, 2000) because mostly large and G.V. Hilderbrand, Alaska Dept of Fish and Game, males are targeted. In comparison, the population in personal communication). In that system, both spatial and Yellowstone National Park that has a lower habitat quality temporal segregation appears to be the mechanism for but higher reproductiverates is protected. Whether the low reducing the risk of infanticide (S.D. Farley and G.V. reproductive rates in our populations are related to body Hilderbrand, Alaska Dept of Fish and Game, personal condition of females as a result of avoidance of salmon communication). The degree of the risk of infanticide may streams, or a result of density effects on infanticide, or an also differ between these two areas because the density of interaction of the two merits further investigation. brown bears is higher on the ABC islands than on the Determining survival of offspring of females that avoid Kenai Peninsula. The high density on the ABC islands salmon streams compared with offspring of females that combined with the fact that >60% of all brown bear frequent these habitats should be the first step in such radiotelemetry locations during August were < 1,000 m studies. Unfortunately, our data on survivorship of cubs from a salmon stream (Titus and Beier 1999) indicates that are meager, as most bears were not visually observed for bears are highly concentrated along specific portions of several years after they were fitted with radio transmitters. streams and that the probability of encountering other The factors influencing the decision of a female with bears on a regular basis is high. Finally, although we have young offspring to frequent or avoid salmon streams are never observed an event of infanticide in our population, still unclear. Weilgus and Bunnell (1995, 2000) suggested on several occasions we encountered bear feces that that the stability of the dominance hierarchy among males contained hairs of brown bear cubs. determined the spatial segregation of females with young Moreover, recent studies demonstrated that in popula- offspring. That at least one individual in our sample tions of bears inhabiting locations with abundant food adopted different foraging strategies in two separate resources, age at first reproduction and interval between breeding events may provide support for this hypothesis. litters are lower, and litter size is higher compared with Nonetheless, whether siring males will be less likely to kill those inhabiting low quality areas (Bunnell and Tait 1981; young is unknown and merits further investigation. Hilderbrandet al. 1999a, 1999b; Rogers 1987; Stringham Analysis of paternity using DNA microsatellite analysis 1990a, 1990b). The high availability of salmon for brown (Craighead et al. 1995b) concurrent with isotope analysis bears on Admiralty and Chichagof Islands suggests that on consumption of salmon by the female will provide brown bears in our study areas should have relatively low strong indirect evidence for the male dominance hypoth- age at first reproduction, low interval between successful esis. litters, and high litter sizes compared with bears inhabiting Alternatively, it is possible that the dominance of the low quality areas. For brown bears on the ABC islands, female determines whether she will frequent salmon however, mean age at first reproduction was estimated at streams. Our analysis of female size and age as surrogate 8.1 years and mean litter size ranged from 1.8 to 1.9 to dominance was inconclusive potentially because of depending on years and study area. Interval between small sample sizes. Although neck circumference was successful litters (from weaning to weaning) was 3.9 years significantly smaller in the females avoiding salmon with a range from 3 to 6 years (Schoen and Beier 1990). In streams, a parameter that may influence the females comparison, mean age at first reproduction for grizzly fighting ability, all other variables were not (Table 1). bears in the Yellowstone ecosystem was estimated at 6.3 Smaller neck circumference and lower mass of the females years and mean litter size at 2.1 cubs per litter. Interval avoiding salmon streams could have been a result of this between successful litters was 2.9 years (Craighead et al. decision rather than its cause. These measurements were 1995a). obtained in the spring following hibernation, while the The lower than expected reproductiverates we observed decision to avoid salmon streams was made prior to in our populations may be related to lower body condition denning. Whether these females experienced smaller neck as a result of avoidance of salmon streams by some of the circumference and lower body mass at the time they reproductive females. For those females, our study areas decided to avoid salmon streams is unknown. Also, it is 473 unclear whether size alone would accurately represent Bartos L, MadlafousekJ (1994) Infanticidein a seasonal breeder: and thus dominance in female bears. the case of red deer. Anim Behav 47:217-220 aggressiveness Ben-David M Seasonal diets of mink and martens: Our demonstrates that the decision to consume (1996) effects of study spatial and temporal changes in resource abundance. PhD salmon made by females foraging under the risk of Thesis, University of Alaska Fairbanks.Fairbanks, Alaska infanticide may be complicated and relate not only to Ben-David M, Schell DM (2001) Mixing models in analyses of diet nutritional and and of using multiple stable isotopes: a response. Oecologia 127:180- requirements, quality availability 184 resources, but also to interactions. Our data intraspecific Ben-David M, Hanley TA, Klein DR, Schell DM (1997a) Seasonal suggest that females make different foraging decisions changes in diets of coastal and riverine mink: the role of based on their reproductive state (mated or accompanied spawning Pacific salmon. Can J Zool 75:803-811 by young), as well as social conditions during specific Ben-David M, Flynn RW, Schell DM (1997b) Annual and seasonal In such decisions be changes in diets of martens: evidence from stable isotope reproductive attempts. bears, might 111:280-291 made based on the of the male analysis. Oecologia stability hierarchy, the Ben-David M, Hanley TA, Schell DM (1998) Fertilization of female mating history, or her own social status. Alter- terrestrialvegetation by spawning Pacific salmon: the role of natively, making a foraging decision could result in flooding and predatoractivity. Oikos 83:47-55 detrimental to that effort. The Bowyer RT, Kie JG, Van BallenbergheV (1998) Habitatselection consequences reproductive neonatal black-tailed deer: role of the social of males and by climate, forage or risk of hierarchy females, mating predation?J Mammal 79:415^125 history, and paternity in affecting the risk of infanticide Bunnell FL, Tait DEN (1981) Population dynamics of bears- and foraging decisions of female brown bears merit further implications. In: Fowler CW, Smith TD (eds) Dynamics of investigation. large mammalpopulations. Wiley, New York, pp 75-98 CowlishawG (1997) Trade-offsbetween foragingand predationrisk determine habitat use in a desert baboon population. Anim AcknowledgementsThis paper is dedicatedto thememory of Dr. Behav 53:667-686 MalcolmRamsay. Malcolm Ramsay (Professor at the Universityof CraigheadJJ, SumnerJS, Mitchell JA (1995a) The grizzly bears of Saskatchewan,Saskatoon) spent decades studying the ecology and Yellowstone: their ecology in the Yellowstone ecosystem, behavior of polar bears in the Canadianhigh Arctic. We had the 1959-1992. Island, Washington,D.C. pleasureof discussing our ideas on trade-offsencountered by bears Craighead L, Paetkau D, Reynolds HV, Vyse ER, Strobeck C on numerousoccasions. Malcolmprovided insightful comments and (1995b) Microsatelliteanalysis of paternityand reproductionin constructive criticism to our work. On 20 May 2000, Malcolm Arctic grizzly bears. J Hered 86:255-261 Ramsay died in a helicopter crash during researchout of Resolute Dean FC, Darling LM, Lierhaus AG (1986) Observations of Bay, Nunavut. The SoutheastAlaska brown bear researchprogram intraspecifickilling by brown bears, Ursus arctos. Can Field- was initiatedby J. Schoen. His foresightin collecting and archiving Nat 100:208-211 samples during the early years of the project made it possible to DeNiro MJ, Epstein S (1978) Influenceof diet on the distributionof follow females throughdifferent reproductive phases and deserves carbonisotopes in animals.Geochim CosmochimActa 42:495- our highest appreciationand gratitude.We appreciatethe assistance 506 of numerousADF&G staff with field-work. L. Bennett and other DerocherAE, Wiig O (1999) Infanticideand cannibalismof juvenile fixed-wing pilots provided safe flying, and the long-term skilled polar bears in Svalbard{Ursus maritimus).Arctic 52:307-310 assistance of helicopter pilot B. Englebrechtwas instrumentalin Diehl S, Cooper SD, KratzKW, Nisbet RM, Roll SK, WisemanSW, obtainingmany of the samplesused in this paper.G. V. Hilderbrand, Jenkins TM Jr. (2000) Effects of multiple, predator-induced S.D. Farley,C.T Robbins,G.M. Blundell, and R.W. Flynn provided behaviors on short-term producer-grazerdynamics in open insightful discussions on bear ecology and stable isotope analysis. systems. Am Nat 156:293-314 R.W.Flynn and TV. Schumacherassisted in GIS analyses.We thank Farley SD, Robbins CT (1995) Lactation,hibernation and weight C. Restrepofor assistancein samplepreparation in the laboratory.N. dynamics of American black and grizzly bears. Can J Zool Haubenstock,P. Rivera, and T Howe performedthe stable isotope 73:2216-2222 analysis. G.V. Hilderbrandand D. Esler, M. Festa-Bianchetand 3 Grand TC (2002) Alternative forms of competition and predation anonymous reviewer provided insightful comments on earlier dramaticallyaffect habitatselection underforaging-predation - versions of the manuscript.This study was funded primarily by risk trade-offs.Behav Ecol 13:280-290 the Alaska Departmentof Fish and Game (ADF&G) and the Federal Hanley TA, BarnardJC (1999) Food resourcesand diet composition Aid in Wildlife RestorationProgram (Studies 4.17 and 4.26). The in riparian and upland habitats for Sitka mice, Peromyscus Alaska Region of the U.S. Forest Service provided financial sitkensis. Can Field-Nat 113:401^07 assistancefrom 1989 to 93 for the Chichagof Island portion of the Heard WR (1991) Life history of pink salmon {Oncorhynchus study and we appreciate the support from the Hoonah Ranger gorbuscha). In: Groot C, Margolis L (eds) Pacific salmon life District. histories. 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