Estimation of feeding history by measuring carbon and nitrogen stable isotope ratios in hair of Asiatic black bears Rumiko N. Mizukami1'4, Mitsuaki Goto2, Shigeyuki Izumiyama3, Hidetake Hayashi2, and Muneoki Yoh1 UnitedGraduateSchool of Agricultural Science, TokyoUniversityof Agricultureand Technology, 3-5-8 Saiwaicho,Fuchu, Tokyo 183-8509, Japan 2ShinshuBlackBear Research Group,2-9-8 Kaichi,Matsumoto,Nagano 390-0876, Japan 3WildlifeManagementOffice,Inc., 5-8 Fuda-ku,Kawasaki214-0011, Japan Abstract: To investigatefeeding habits,carbonandnitrogenstableisotope ratioswere measuredin hair (Ursus thibetanus)inhabitingan alpine area,includingthe Northern sampledfrom Asiatic black bear(rs JapaneseAlps and the peripheryof villages in Nagano Prefecture,in centralJapan.Asiatic black bears in the NorthernJapaneseAlps are subjectto little humaninfluence,but in ruralareashumanencounters with bears seeking food in cornfieldsand garbagehave become an issue thatneeds to be resolved. We investigatedthe feeding habitsof bearsby analyzingthe isotopic changesalong the entirelengthof hair n nuisance bears, showed slightly higher 615N and 613C values than n e including samples. Rural bears, that rural nuisance bears may have greater access to anthropogenicfood bears, suggesting alpine resourcesthantheiralpinecounterparts.Hairsampleswere furtherexaminedby growthsection analysis (GSA), in which sectioned samples from the root to the tip are used for isotopic analysis, to estimate feeding historyduringhair growth.Hairsof alpinebearsexhibitedlow 615Nand 613Cvalues from the root to the tip, and the deviation was small. In contrast,hairs of ruralbears, particularlyof nuisance bears, showed large deviationsin isotope values. One bear capturedin a cornfieldshowed high 613C values at its hairroot.Anotherbearthatthrivedon garbageshowed high 615Nand 613Cvalues at its hair root, similarto those of Japanesepeople. One capturedbear,assumedto be partof nuisanceactivities, showed low 615Nand 613Cvalues from hairroot to tip, suggesting that capturedbears are not always the ones causing damage. By comparingand classifying GSA fluctuationpatterns,we estimatedthe dependence of nuisance bears on human-relatedfood sources. We expect these methods to provide relevantinformationfor bear conservationand managementprograms. Key words: Asiatic black bear,carbonisotope, feeding history,growthsection analysis,hair,nitrogenisotope, stable isotopes, Ursus thibetanus Ursus16(1):93-101(2005)
An estimated 10,000-15,000 Asiatic black bears (Ursus thibetanus)inhabit Honshu, Japan's largest and most populated island (Hazumi 1994). However, bear habitatis thoughtto be decreasingnationwide;bearsare extinct in Kyushu and endangeredin Shikoku. Further, bear populations in Honshu are becoming isolated, particularlyin the western part of the island, where some populationshave been labeled as threatenedin the JapaneseRed Databook publishedby the Ministryof the Environment(Ministryof the Environment2002).
[email protected] 93
Asiatic black bear depredationlevels remain high in Japan. Over 1,000 Asiatic black bears are killed each year to control nuisance activity, in addition to the roughly 1,000 bears that are killed during the hunting season (Hazumi 1994). Nuisance activity includes stripping tree bark; raiding crops, orchards, apiaries, and fish farms;feeding fromcompostheapsand garbage; and attackinghumans and livestock (Azuma and Torii 1980, Furubayashiet al. 1980, Watanabe1980, Hazumi 1994, HuygensandHayashi 1999, Yoshida2003). When bear depredationis discovered, local hunters set cage traps to capture and kill the bear. However, the systematic killing of nuisance bears has not reduced overall depredationrates (Huygens and Hayashi 1999,
94
FEEDINGHISTORYIN ASIATICBLACK BEAR * Mizukami et al.
consumer tissues can be related to those in consumers'diets (DeNiro and Epstein 1978, 1981; Minagawa and Wada 1984). The turnover of stable isotopes in tissue is related to the metabolic activity of that tissue (Tieszen et al. 1983), so the isotopic signatureof differenttissues from the same consumercan provide short-and long-termdietaryinformation(Hobson 40? and Clark 1992, 1993). Hair is particularly useful in analysis of isotopic signaturesbecause, in comparisonwith tissues such as blood (red blood cells and plasma), bone collagen, skin, 350
muscle, and adipose, it (1) archives
temporal(e.g., seasonal)fluctuationsin diet isotope composition; (2) can be obtainedin a non-invasivemanner;and NorthiPacific Ocean (3) preserves diet information over time excepting quiescent phases (Nakamuraet al. 1982;Michaelet al. 2003, Fig. 1. Study area, Nagano Prefecture, Japan. Shaded area represents Nakashita 2003, Mizukami et al. in distribution of Asiatic black bears in 2000 (Nagano Prefecture, 2002). press).Nakashita(2003) and Mizukami et al. (in press) proposed the growth section analysiss (GSA) methodand showed thatbearhair Huygens et al. 2004), partlybecause the killed bears are not always the ones causing the damage. Although the may reflect fe,eding habits and therefore enable the 1999 Wildlife Protectionand HuntingLaw stipulatesthat reconstructionof feeding history. the conservation and management of bears must be conducted on a scientific basis, nuisance bears are systematicallykilled withoutany scientificassessmentof Study arear and methods the efficacy of this method in reducingdepredation. We conducte ed our study in Nagano Prefecture,which We comparedthe feeding habits of alpine bears and is located in c< entralHonshu, the main island of Japan ruralbearsincludingnuisancebearsanddeterminedtheir (Fig. 1). The prefectureis mountainous, with several peaks above 2,,500 m in elevation and the highest over feeding historiesby means of carbonand nitrogenstable ge tracts of mountainous areas are un3,100 m. Larg isotope analysis. The analysis allowed us to evaluate whether bears that were caught in cage traps were inhabitedby hiumans,and a majorityof the 2.2 million actuallynuisance bears. people are conecentratedon a few plains. Agriculturehas Obtainingdietaryinformationoften dependson direct historically be(en an importantpart of the prefectural feeding observations and scat and stomach content economy, but its importance has been decreasing; it analyses, and may be biased by the limited observation representedonlly 4.7% of the gross prefecturalproductin 1994 (Huygens, andHayashi2001a, Huygenset al. 2001). time, the absence of soft-bodiedprey, or the presenceof bony parts from prey that may or may not have been ely 1,300-2,500 Asiatic black bears are Approximate assimilated by wildlife (Hilderbrand et al. 1996, distributedthro)ughoutthe prefecture(NaganoPrefecture Nakashita2003, Mizukamiet al. in press). The analysis 2002), and theey are not considered endangered (Sato of stable isotopes in animal tissue overcomes some of 2003). Arable land reaching the edge of forested these disadvantages(Robbinset al. 2004). mountains is i:ntensively used for agriculture.Because Carbon (613C) and nitrogen (615N) isotope signatures of this, conflict s betweenhumansandAsiatic blackbears of animal tissue provide information about diet, and are common (Huygens and Hayashi 1999, Nagano hence the environment in which the animal lived, Prefecture2002). Bears debarktrees in plantationsand because carbon and nitrogen stable isotope ratios in raid crops, orc:hards,apiaries, fish farms, and garbage ........
Ursus 16(1):93-101 (2005)
HISTORY FEEDING BLACKBEAR* Mizukami et al. 95 IN ASIATIC
Table 1. Asiatic black bears used in the hair growth section analysis (GSA) for a study in the Nagano Prefecture.
Category Sample
Sampling date
Alpine
bear 1 bear2 bear 3
Rural
bear 4 bear 5
16 Jun 2002 11 Jun 2002 23 Sep 2001 28 Aug 2001 6 Sep 2001
bear 6 bear 7
14 Sep 2001 25 Aug 2003
Valuesof hars wholehairs
Sex
Cutting lnthin Weight lengthin Reasonfor (kg) 613C(%) 615N(%o)sections (mm) Site of capture capture
M M F
102 20 51.5
-23.4 -22.8 -23.9
0.4 2.8 1.9
5 5 3
mountains mountains mountains
for study forstudy forstudy
F F
77.5 -90
-21.4 -22.4
3.2 3
3 3
nuisance nuisance
M F
96.5 60
-20.1 -23.0
5.4 2.8
3 5
in cornfield garbage site at hotel resort woods near cornfield
disposal sites. Raiding cornfields and garbage disposal sites in resort areas is the most serious problem in the studyarea.Bearsliving in deep mountainranges(such as the NorthernJapaneseAlps) are thought to make little use of anthropogenicfood. The diet of non-nuisance bears shifts from oak (Quercus spp.) acors left over from the previous fall and dwarf bamboo (Sasa spp.) leaves and shoots in spring, to succulent forbs and soft mast in summer,to hard mast, including oak acorns, chestnuts (Castanea crenata), walnuts (Juglans mandshurica),and Korean stonepine (Pinus koraiensis)seeds, in autumn.They also consume insects throughoutthe growing season, particularly in summer, and occasionally scavenge serow (Naemorheduscrispus) (Takada 1979, Huygens 2001, Huygens and Hayashi 2001b, Huygens et al. 2003). Sample collection Hairwas sampledfrom 22 alpinebears(those thatlive in the mountains,mainly the NorthernJapanese Alps) and 49 ruralbears in 2001-03. All bears in this group were confirmedby radiotelemetryto have no access to humans (Izumiyamaand Shiraishi 2004). Rural bears lived near humans and included bears that caused nuisance activities. Most of the bears in the present study were capturedusing barreltrapsand anesthetized with a blowgun. The otherbearswere caughtby various means (either capturedin traps set for wild boars [Sus scrofa] or Japanesemacaques [Macacafuscata], killed by huntersdue to nuisanceactivity,or huntedduringthe hunting season, Nagano Prefecture2002). Whole hairs, including hair roots, were plucked from the back and shoulders of captured bears. Hair was stored in plastic bags and transferredto the laboratory without treatment. Permission for capturing Asiatic black bears for academic uses was obtained from Nagano Prefecture. Ursus 16(1):93-101 (2005)
nuisance suspected nuisance
Sample analyses Hair samples were rinsed with 2:1 chloroformmethanol solution to remove lipids, then air-dried. Samples were then analyzed in 2 ways. Whole hairs from all samples were analyzed to generate average values of entirehairs.To estimatediet over time with the GSA method, hair samples were cut from root to tip in sections of 3 or 5 mm. The correspondingsections of hairs were gathered to obtain a sufficient amount for analysis and analyzed separately.We used hair samples from 3 alpine bears (bears 1-3), 3 nuisancebears (bears 4-6), and 1 rural bear (bear 7) suspected of nuisance activity (Table 1). The 3 alpine bears confirmed by radiotelemetryto have no access to areas inhabitedby humans were selected as typical alpine bears. The 3 nuisance bears were selected as typical nuisance bears because they destroyed a cornfield (bear 4), ate hotel garbage(bear5), and lived in a resortarea (bear6). The hair of a ruralbear (bear 7) that lived near a cornfield was tested by GSA to determine if it was actually depredatingcrops. Samples were enclosed in a tin cup and combusted in an elemental analyzer (FlashEA1112;ThermoQuest, Bremen, Germany)interfacedto an isotope ratio mass spectrometer(ThermoQuestDelta Plus, ThermoQuest), in which the carbon and nitrogen isotope ratios were analyzed.The resultsare reportedas partsper thousand
of the isotope (%O)relative to a standard X(RSTANDARD) AS FOLLOWS:
613C or 61N
= [(Rsample/Rstandard) - 1] X 103,
where R is 13C/12C or 15N/14N. Rtandard for 613C or
615N was the Pee Dee Belemnite (PDB) standardor atmospheric nitrogen (AIR), respectively. Standard deviations of the isotope analysis were 0.1%o and 0.2%0 for 613C and 615N, respectively. GSA was
BLACK BEAR * Mizukami et al. FEEDINGHISTORYIN ASIATIC
96
ruralbearswere slightlyhigherthanthose of alpinebears (U = 345.0, P < 0.05). The higher mean 6'5N value of ruralbears may reflect a higher proportionof foods of animal origin in the diet of those bears. Both 613Cand 615Nvalues of ruralbears have largerranges than those of alpine bears, probablydue to the wider diversity of foods of ruralbears. The range tends to expand toward the values for Japanesehair, and this probablyindicates that rural bears take foods of wider diversity. We speculatethat high 613Cand '5N values imply nuisance bears, and that high 613Cvalues show a dependencyon corn, a C4 plant. Plants are classified as C3 or C4 based on metabolic criteria,andthe stableisotope signaturediffersfor C3and C4 plants.Corn is one of the few C4 plantsin the region and the only one that is common enough to be an importantbearfood. Therefore,the stableisotope pattern in hair that matchesthat of a C4 plant strongly suggests that the bear eats corn.
Table 2. 613C and ('5N values of whole hair of alpine and rural Asiatic black bears in Nagano Prefecture, central Japan, 2001-03. s13C(O) n
Mean SD
Alpine bear 22 -23.2 Rural bear 49 -22.6
s'5N(oo) Mean SD Range
Range
1.9 2.5
0.6 -24.0--21.9 1.3 -24.1--16.7
1 0.4-4.1 1.2 0.2-5.4
repeated twice for each hair section. The differences in results between duplicate samples were within analyticalerror.
Results Analysis of whole hair The 613C and 6'5N values of alpine bears were -23.2%0 (SD = 0.6%o) and 1.9%o (SD =
1.0%o),
respectively,whereasthose of ruralbears were -22.6%o (SD = 1.3%0) and 2.5%0 (SD = 1.2%o), respectively
(Table 2 and Fig. 2). Slightly higher 613Cvalues were obtained for rural bears than for alpine bears, but the difference was not statisticallysignificant(Mann-Whitney U-test: U = 387.5, P > 0.05). The 615N values of
Analysis of hair sections In alpinebears,the deviationsof 613Cwere very small and those of 615N were smaller than those of nuisance bears(Fig. 3). The 613Cand 615Nvalues of bear 1 ranged from -24.3--23.1%o
10
0
Japanese hair
5
o
o
herbivores
?
od,
-22.9%o and from -0.5-3.4%.,
z
Z2 IO
o
.f3 3
plants
C4 !:tip
0 C3
-5 -35
and from -0.9-
1.4%o,respectively.The range of 615N of bear 1 was the narrowestamong the 6 bears (Fig. 3), indicatingthat bear 1 ate similar foods throughout hair growth. The 613C and 565N values of bear 2 ranged from -23.5--22.1 %o and from 0.3-4.3%, respectively, and those of bear 3 ranged from -24.1respec-
tively. Alpine bearsshowed a tendency for bl5N values to be higherat the hair thanat the root and for the values to decrease with time. On the other hand, the 613C and
plants
i
I
I
-30
-25
-20
15
-10
13C(%o)
Fig. 2. 613C and (i5N of whole hairs of alpine and riural Asiatic black bears, with literature values of C3 and C4 plants, herbivores, and Japanese hair for alpine (m) and rural (o) bears (in(eluding nuisance bears). Human hair isotope levels are expected to be close to those of bears that eat garbage. Data on plants, herbivore! s, and hair from Minagawa and Akazawa (1988), Minagawa et al. ( 1986), Minagawa (2001) and Nakashita (2003).
615N values of nuisance bears had wide ranges and demonstrateddifferent patterns(Fig. 3b). The 613C and 615N values of bear 4 ranged from -23.2--14.6%o and from 0.3-4.6%o, respectively, and those of bear 5 rangedfrom-23.8--20.2% and from 0.3-7.7%o,respectively.Bears 4 and 5 showed an increase in 6'3C and 615N values with hair growth. Bear 6 also had wide ranges (613C: -22.5-16.4%o, 615N: 3.0-6.8%o), but the
Ursus 16(1):93-101 (2005)
FEEDING HISTORY IN ASIATICBLACK BEAR *
6'5N values were high throughouthair ha -14
the middle.
Presumed
-15 -16 -17
feeding
history
of
bears by GSA
According to Hilderbrandand Robbins (G. Hilderbrand,Alaska Depart-
a
(before hibernation) if the hair was collected before molting season, or the hair had just grown if it was collected
6
z to
-CL a-
r
a
o-.
'
6
~
5
30
40
Len
20
30
10
6
-17 -
5
-18.
4 " -
3
-,..
-21
2 )
e-0
-22
0-0e
".
-' * '-
-'.
1o
1 0
-24
-1
-25
80
70
60
50
40
30
20
10
0 -1
0
8 7
-1
6 5
-18 -
i -19
4
""-
3 a
-22
-23 -24 -25
-
2
?
1 oo0oa
?o4
oo0 40
30
20
0
00 -1
80
70
10
0
8
? -20 o -21 -22 -23 -24 -25
bear 5
-
."
7 6 5 4 3
0
zZ?
0-0 2
?.--0-0 -o-0o0-e-0-
1 0
.1
I
40
30
20
10
0
Length from the root (mm)
-14
-
20
Length from the root (mm)
E 50
-15 -bear3
-2 21
30
40
rom the root (mm) Lengthf
o .20,-
1
-o.-0
-e .
-14 -15 -16 -17 -18 -19
7
io
2
z 8
z
3
_?-) .----
-
50
-14 -15 -bear 2 -16 -
0 -20 --"""-?
-
-25
0
fromthe the root root (mm) (mm)
A -19
-20 ()
'
.' -21 -22 -23 -24
1 1
"
-1
50
afterthe molting season. Althoughhair
grown in the previous year, the hair that was sampled before the molting season
7
4
3
during the molting season consisted of
shorthairgrown thatyear and long hair
8 .
4
-25
'
hair root
me
-14 -15 - bear4 -16 -17 ~-17-~
5
-23 -4
investigations of Asiatic black bears,
grew in spring and the hair root in fall
7
-
-22
winter coat (Jacoby et al. 1999). In our
in the previous year molts mainly in July (Mizukami unpublished data). Therefore, we assume that the hair tip
-bear
-20
molt yearly during summer, and the summercoat is shorterthanthe fall and
before hiberation. The hair that grew
`
8
0o -21
ment of Fish and Game, Anchorage, Alaska, USA, unpublished data), bears
we found that hair starts to grow in May after hibernation and stops growing
hair tip
hair root
time
low at the root and the tip and high in
97
(b) Nuisance bears
(a)Apirie bears
growth, whereas the 613C values were
Mizukami et al.
60 50 40 30 20 10 Lengthfromtheroot(mm)
0
z ,o00
-14 -15 -bear 6 -16 -17 i *3 _ -18 -19 0 -20 0 -21 -22 -23 -24 -25 60
50
I8 7 ?-?..
6
-_
-
5
.
: O
.
4 3
'"'s
o Io
2 1
0 -1 40
30
20
Length from the root (mm)
10
0
in this study was all long hair that was 613 grown in the previous year. (o) and 615N(u) for hair sections from root to tip as In view of the above, we surmised measured eas by. growth section analysis (GSA) for (a) 3 alpine bears and the feeding history of bears (Fig. 4). (b) 3 nuisanc e bears in Nagano Prefecture, central Japan, 2001-03. Hairof alpinebears 1 and 2 collected in Hairsfrom alpine bears show little variation in 613Cand slight variation June2002 (Table 1) shouldhave grown in 615N, where?asthose from nuisance bears show large deviations in the previous year because they were 6 C and 6 Ncollected before the molting season. In contrast,the hairsof bear3 collected in reflect a decrease in the consumptionof food of animal September2002 seemed to have grownthatyearbecause they were collected after the molting season. The 613C origin, given such seasonal feeding variation.Bear 1, in and 615N values of all alpine bears shifted almost particular,seemed to consume mostly C3 plants. 613C and 6'5N values for nuisance bears were vertically(Fig. 4a). The generaltrendof decreasingwith distributedwidely (Fig. 4b). Bear 4 was killed in the hair growth suggested that those bears consumed only end of August 2001 because it destroyed cornfields foods of C3 plant origin throughoutthe season. Alpine bears seemed to have consumed mainly C3 plants; the (Table 1). Considering the sampling time, the hair of bear4 seemed to have grown that year and reflectedthe small amountof animal proteindetected at the hair tip, which correspondedto spring,suggestingthatthe ratioof feeding history from spring until it was captured.The hair tip showed low 613C and 6'5N values that were food of animalorigin decreasedwith hairgrowth.In fall, within the range of C3 plants. However, 615Ngradually bears prepared for hibernationby consuming mostly increasedand 613Cabruptlyincreasedto values similar acors. The patter of 615N decreasing with time may Ursus 16(1):93-101 (2005)
98
FEEDINGHISTORYIN ASIATICBLACK BEAR * Mizukanmi et al.
(a)Alpinebears
(b) Nuisancebears
10
10
Japanese hair
Japanesehair
-5
hair bp
z to
w fc'
'
- -. ........A :-A hairroot
herbivores
herbivores
hair root
C4 plants
hairtiphair tip
0 C3 pwant
.
i
|is
C3 plants
-;
-5
-5
-35
-30
-25
-20
-15
-10
-35
-30
-25
6'3c(%.)
-15
-20
-10
63C (~)
bear4 10
Japanese hair hair root
-5 at
herbivores
z
.
To
CO~4 plants
U?
0
-
35
hairtip
Cp ants
-30
-25
-20
-15
-10
6513C(%.)
bear5 -5 10
Japanese hair
*.
hairti -5
%
. ..
herbivores
z so
hairroot 04 plants
0 C3 plants
I
I
-5 35
-30
-25
-15
-20
-10
613C(%.)
bear6 Fig. 4. 613C and 615N for Asiatic black bears in Nagano Prefecture, central Japan, 2001-03. (a) Hair sections from root to tip as measured by growth section analysis (GSA) for alpine bears (A = bear 1, D = bear 2, and o = bear 3). (b) Hair sections from root to tip as measured by GSA for 3 nuisance bears. Values of alpine bears were close to C3 plants in 613C and 615N from the root to the tip. In contrast, nuisance bears showed large deviation.
Ursus 16(1):93-101 (2005)
FEEDING HISTORY IN ASIATICBLACK BEAR *
to those of C4 plants, suggesting that bear 4 fed on mainly C3 plants (we assume in the mountains in spring) at first, as it has been reported that bears in Japan feed on oak acorns from the previous fall and succulent forbs and grasses in spring (Takada 1979, Huygens 2001). Bear 4 then startedto consume more foods of animalorigin such as ants and bees, and finally shifted its principalfood to corn. Bear 5 was killed on 6 September2001, when it was caught scavenging for hotel garbage.Based on the time of sampling,we assumethe hairof bear5 was grownthat year. The 613Cand 6'5N values were low at the hairtip, but increased simultaneouslywith hair growth to high values at the hair root, approachingthose of Japanese people. This suggests thatbear5 fed on mainly plantsin the mountainsin springand shiftedgarbagebeforeit was killed. Bear 6 was killed on 14 September2001 because it raided a resort area. This bear's hair also seemed to have grown thatyear as it was collected afterthe molting season. The 613Cand 615N values of bear 6 were high fromhairrootto tip, suggestingthatit foragedon humanrelatedfoods throughouthair growth.In particular,613C and 615Nvalues were high in the middle partof the hair (Fig. 3), implying that bear 6 seemed to have eaten corn and garbagein summer.The GSA suggests that bear 6 had access to human activities, consistent with radiotelemetry data from a local hunter (Shinshu black bear research group NPO, Matsumoto, Nagano, Japan, unpublisheddata). Bear 7 was a ruralbear suspectedof nuisanceactivity thatwas capturedin a trapset neara cornfield.Hairswere collected aftermolting, which meantthat they grew that year (Table 1). Its 63C and 615N values, rangingfrom -24.4-21.8%o
and from 0.63.7%,
respectively, fell
within the range of alpine bears. They were low at the hair tip and increasedgraduallytowardthe hair root in a manner similar to alpine bears (Fig. 5). It is highly likely thatbear7 was not dependenton corn. This result implies that a capturedbear may not always be the one causing damage.
Discussion The present analysis of feeding habits by measuring nitrogen and carbon stable isotope ratios is useful for revealing putative access of Asiatic black bears to human activities, because 613C and 615N values differ between native foods in the mountains and anthropogenic foods such as corn (a C4 plant that is one of the most seriouslydamagedby bears),as well as garbagein ruralareas. Ursus 16(1):93-101 (2005)
10
Mizukami et al. 99
Japanese hair
5
.
--herb .iv .o i....:.
.. ...
..
z ,erbivgjj
i*
f r
.
-ts
0 plants hCnebtral zone
-5
-35
-30
-25
-20
-15
-10
613C(%o)
Fig. 5. Stable isotopes for hair from Asiatic black bear 7, Nagano Prefecture, central Japan. This bear was accused of depredating corn, but the growth section analysis indicates that the bear did not consume corn.
Stable isotope studies to determineanimal food habit have generally focused on whole hairs that reflect the average feeding habit during hair growth. From the resultsof whole hair analysis, indicatingthat ruralbears have slightly higher 613C and b'5N values than alpine bears,we presumedthatthe feeding habits were slightly differentbetween the two. However, whole hair analysis cannot detect the shift of diet over time. For example, the bl3C and 615Nvalues of bear 2 were very similarto those of bear 5, but the GSA results showed different patternsbetween alpine and ruralbears (Figs. 4 and 5). The GSA result for bear 5 suggested that the bear ate garbage, whereas the result of whole hair analysis cannot prove that bear 5 depended on garbage. Likewise, the GSA for bear 4 showed that it depended on corn only in summer. The 615Nvalues of alpine bears were generally high at the hair tip and decreasedtoward the hair root (Fig. 3). Conversely, the 615N values of rural bears except bear 6 were low at the hair tip and increasedwith hair growth. The differentpatternsof 615Nobservedfor the alpine bearscan be explainedas follows. In spring,alpinebears often eat carcasses of animals (e.g., sika deer [Cervus nippon]) which died in winter because of severe conditions in mountainareas. Later,alpine bears climb the mountainsin searchof buds afterthawingin summer, while rural bears at low altitude suffer from food shortages. Alpine bears consume little food of animal
100
FEEDING HISTORY IN ASIATICBLACKBEAR * Mizukami et al.
origin in the alpine belt. In fall, alpine bears move to lower altitudes in search of acoms. Decreasing 615N from the hair tip reflects this habit and demonstrates how alpine bears overcome the severe environmentand food shortages during summer (Izumiyama 2001, Izumiyama and Shiraishi 2004). However, from the verticalfluctuations(Fig. 4a) for alpinebears,we surmise that the slightly higher 615Nis caused by the difference in the C3plantsconsumed,dependingon the site of plant growth,habitat,or elevation.We need to conductfurther studies of 613C and 615N levels in plants and animals consumedby bears. Conversely, in spring rural bears consume mainly plants including, buds and acorns from the previous fall, but suffer from food shortage in summer. In summer,the dependenceof bears on insects, including ants and bees, increases (Takada 1979, Ishida 1995, Hashimotoand Takatsuki1997). This may explain why rural bears showed an increase in 615N with hair growth. Bears that raidedcorfields or garbagebecame nuisance bears. Based on the GSA patterns,we classified bearhabitat into natural and anthropogenic zones (Fig. 5). The naturalzone is the isotopic range for bears that have no access to humanactivities.Because the isotopicrangefor bear7 was withinthe naturalzone, we inferthatit did not depend on cor. We could not detect its eating other crops from this analysis, because most crops are C3 plants. However, we can say that bear 7 did not eat anthropogenicfoods, because most crops around the foothills in this districtare corn in summer.Moreover, we have no informationon any othercrop damagein this town from the inhabitants. On the other hand, the anthropogeniczone is the isotopic range for nuisance bears,and isotope values are close to humanhairand C4 plants. We surmise that bears distributed in the anthropogeniczone living in this district depended on humanactivities.
Acknowledgments
We express our sincere thanks to the following people: E. Wada for advice on stable isotope analysis; membersof Shinshublack bear researchgroup for help in sample collection; J. Tanaka, M. Koyama, and R. Kishimoto for providing samples and valuable information; and hunter groups in Shinanomachi town and Kiso for advice and valuable informationon the bears and the forests. We also thankK. Isobe and O.C. Huygens for reading the draft of the manuscriptand giving valuable comments and encouragement.
Literaturecited 1980. Impactof humanactivities on AZUMA,S., AND H. TORII. survival of the Japaneseblack bear. InternationalConfer-
ence on BearResearchandManagement 4:71-79. DENIRO,
M.J., ANDS. EPSTEIN.1978. Influenceof diet on the
distribution of carbonisotopesin animals.Geochimicaet Cosmochimica Acta42:495-506. , AND
.
1981. Influence of diet on the dis-
tribution of nitrogenisotopesinanimals.Geochimica etCosmochimicaActa45:341-351. FURUBAYASHI, K., K. HIRAI, K. IKEDA,AND T. MIZUGUCHI.
betweenoccurrenceof beardamage 1980. Relationships and clearcuttingin centralHonshu,Japan.International on BearResearchandManagement 4:81-84. Conference HASHIMOTO, Y., AND
S.
TAKATSUKI.
1997. Food habits of
Japaneseblack bears: A review. MammalianScience 37(1):1-19.(InJapanesewithEnglishabstract.) T. 1994.Statusof Japaneseblackbear.International HAZUMI, Conferenceon Bear Researchand Management9(1): 145-148. HILDERBRAND,G.V., S.D. FARLEY, C.T. ROBBINS, T.A. HANLEY,
ANDC. SERVHEEN. 1996. Use of stableisotopes to K. TITUS, determine diets of living and extinct bears. Canadian Journalof Zoology 74:2080-2088. 1992. Assessing avian diets HOBSON,K.A., ANDR.G. CLARK. using stable isotopes I: turnover of '3C in tissues. The
Condor94:181-188. . 1993. Turnoverof 13Cin cellular and of blood: Implicationsfor nondestructive fractions plasma in avian dietarystudies. The Auk 110:683-641. sampling HUYGENS,O.C. 2001. Ecological and sociological aspects of
,AND
Conclusions We validatedthe feeding habitsof individualbearsby GSA to a considerableextent. From the GSA patterns and the hair growth cycle, furtherinformationon bear ecology and its environmentwas obtained.Furthermore, GSA allowed us to evaluate whether a suspected nuisance bear was actually related to damage. Many bearsarekilled because of nuisanceactivitywithoutany scientific evidence. This study provides a scientific method that is applicable to bear conservation and managementprograms.
Asiatic black bear conservationin Nagano Prefecture, centralJapan.Dissertation,ShinshuUniversity,Matsumoto,Japan. 1999. Using electricfences to reduce , AND H. HAYASHI.
central in NaganoPrefecture, Asiaticblackbeardepredation Japan.WildlifeSocietyBulletin27:959-964. . 2001a. Asiatic black bear management , AND central Japan:a commentary. in Prefecture, Nagano plan BiosphereConservation3(2):115-129.
Ursus 16(1):93-101 (2005)
FEEDING HISTORY IN ASIATIC BLACKBEAR* Mizukami et al. 101
. 2001b. Use of stone pine seeds and oak , AND acorns by Asiatic black bears in central Japan. Ursus 12: 47-50.
, M. GOTO, S. IZUMIYAMA,H. HAYASHI,AND T. YOSHIDA.2001. Asiatic black bear conservationin Nagano
Prefecture, central Japan: problems and solutions. Biosphere Conservation3(2):97-106. , T. MIYASHITA,B. DAHLE, M. CARR, S. IZUMIYAMA,T. 2003. Diet and feeding habits SUGAWARA,AND H. HAYASHI.
, K. KARASAWA, AND Y. KABAYA.1986. Carbon and
nitrogen isotope abundance in human feeding system. Chikyukagaku20:79-88. (In Japanese.) MINISTRY OFTHEENVIRONMENT. 2002. Threatened Wildlife of
Japan. Red Data Book. Volume 1. Second edition. Mammalia.JapanWildlife ResearchCenter,Tokyo, Japan. M. YOH,N. OGURA, MIZUKAMI, N.R., M. GOTO,S. IZUMIYAMA, AND H. HAYASHI. In press. Temporal diet changes recorded
by stable isotopes in Asiatic black bear (Ursus thibetanus) hair. Isotopes in Environmentaland Health Studies.
of Asiatic black bearsin the NorthernJapaneseAlps. Ursus 14:236-245.
NAGANOPREFECTURE. 2002. Asiatic black bear management
H. HAYASHI, , F.T. VAN MANEN,D.A. MARTORELLO, AND J. ISHIDA. 2004. Relationships between Asiatic black
NAKAMURA, K.,
bear kills and depredation costs in Nagano Prefecture, Japan.Ursus 15:197-202. ISHIDA,K. 1995. The food and life history of Asiatic black bears. MammalianScience 35(1):71-78. S. 2001. The Asiatic black bears in Northern IZUMIYAMA, Japanese Alps. Pages 45-50 in Omachi Alpine Museum, compiler.The naturalhistoryof the NorthernJapaneseAlps. The ShinanoMainichiShimbun,Japan.(In Japanese.) , AND T. SHIRAISHI.2004. Seasonal changes in elevation and habitatuse of the Asiatic black bear (Ursus thibetanus) in the NorthernJapanAlps. MammalStudy 29:1-8. G.V. HILDERBRAND, C. SERVHEEN, C.C. S.M. ARTHUR,T.A. HANLEY,C.T. ROBBINS, SCHWARTZ, AND R. MICHENER. 1999. Trophic relations of brown bear
JACOBY, M.E.,
and black bearsin severalwesternNorthAmericanecosystems. Journalof Wildlife Management63:921-929. MICHAEL,S., K. AUERSWALD,AND H. SCHNYDER.2003.
Reconstructionof the isotopic history of animal diets by hair segmental analysis. Rapid Communicationsin Mass Spectrometry17:1312-1318. M. 2001. Dietary patternof prehistoricJapanese MINAGAWA, population inferred from stable carbon and nitrogen isotopes in born protein.Bulletin of the National Museum of JapaneseHistory 86:333-357. (In Japanese.) , AND E. WADA. 1984. Stepwise enrichment of 15N along food chains: further evidence and the relation between 615N and animal age. Geochimica et Cosmochimica Acta 38:1135-1140. , AND T. AKAZAWA. 1988. Food intake by Jomon
people. Iden 42:15-23. (In Japanese.)
Ursus 16(1):93-101
(2005)
and conservationplan. (In Japanese.) D.A. SCHOELLER,F.J. WINKLER, AND H.L. SCHMIDT. 1982. Geographicalvariationsin the carbonisotope compositionof the diet and hairin contemporaryman. Biomedical Mass Spectrometry9(9):390-394. NAKASHITA,R. 2003. Feeding habits analysis of Asiatic black bear (Ursus thibetanus)using carbon and nitrogen stable isotopes.Thesis, Tokyo Universityof AgricultureandTechnology, Tokyo, Japan.(In Japanese.) ROBBINS, C.T., C.C. SCHWARTZ, AND L.A. FELICETrI. 2004.
Nutritionalecology of ursids: a review of newer methods and managementimplications.Ursus 15:161-171. SATO,S. 2003. The stateof Asiatic blackbearmanagementand conservation plan in Nagano Prefecture. Mammalian Science 3 (Supplement):17-20. TAKADA, Y. 1979. The food habitsof the Japaneseblack bears in the centralmountainarea,Nagano Prefecture.Journalof the MammalogicalSociety of Japan8:40-53. (In Japanese with English abstract.) K.G. TESDAHL,AND N.A. SLADE. TIESZEN, L.L., T.W. BOUTTON,
1983. Fractionationand turnoverof stable carbonisotopes in animal tissues: implications for 613C analysis of diet. Oecologia 57:32-37. WATANABE,H. 1980. Damage to conifers by the Japanese black bear.InternationalConferenceon Bear Researchand Management4:67-70. YOSHIDA, T. 2003. Confrontationof natureand animals-from investigationof Asiatic black bear and the trainmillipede. Journal of the Japanese Agricultural Systems Society 19(1):86-95. (In Japanese.) Received: 25 February 2004 Accepted: 9 July 2004 Associate Editor: G. Hilderbrand
