ORIGINAL ARTICLE

Ami Nakajima • Shinsuke Koike • Takashi Masaki

Takuya Shimada • Chinatsu Kozakai

Yui Nemoto • Koji Yamazaki • Koichi Kaji

Spatial and elevational variation in fruiting phenology of a deciduousoak (Quercus crispula) and its effect on foraging behaviorof the Asiatic black bear (Ursus thibetanus)

Received: 26 March 2011 / Accepted: 27 December 2011 / Published online: 1 February 2012� The Ecological Society of Japan 2012

Abstract In habitats with elevational gradients, differ-ences in the fruiting phenology of a single key foodresource may affect the feeding behavior of an animal.The objectives of the present study were to assess (1)whether or not fruiting phenology and characteristics ofQuercus crispula acorns differed with changes in altitude(900–1,400 m asl) and area; (2) when bears foragedacorns in relation to their phenological development;and (3) where bears engaged in acorn foraging behaviorwith respect to acorn phenology. No difference in thefruiting phenology of acorns at various altitudes andlocations was found, with the exception of changes incolor and abscission period. Acorn abscission periodoccurred later at a site with an elevation of 1,200 m inTochigi and at another with an elevation of 1,400 m inGunma, making the available energy of acorns in thetree canopy (AET) greater and available for a longertime period at those two sites. Foraging of acorns bybears was observed at sites of moderate to high altitudebetween late September and mid-October. A thresholddate when acorns became suitable for foraging by bearscould not be identified, as the size and nutritional valueof acorns increased continuously. Foraging activity of

bears observed at moderate and high altitude sites cor-responded with locations where AET was available ingreater amounts and for a longer period of time forsome sites; however, the small sample size precludedaccurate assessment.

Keywords Feeding habit Æ Acorn Æ Quercus crispula ÆElevational gradient Æ Japan

Introduction

Spatial and temporal variations in food environmentsaffect habitat use by animals (e.g., Morrison et al. 1998).Due to the variations in fruit production among yearsthat are observed in many tree species (Shibata et al.2002), frugivores are known to change their habitat use(Schooley 1994). In addition to inter-annual variation,intra-annual variations (i.e., seasonal variations) inhabitat use can also be observed. In temperate zones,plant phenology changes markedly with the seasons,limiting the flowering, leafing and fruiting periods,which impacts the feeding behaviors of both frugivoresand herbivores (Hejl and Verner 1990; Costello and Sage1994; Keane and Morrison 1999; Kuo and Lee 2003;Vernes et al. 2004; Naves et al. 2006). Furthermore, inhabitats with elevational gradients, seasonal changes inthe availability of food resources are often influenced byaltitude, resulting in seasonal changes in the use of suchenvironments by animals. For example, differences invegetation based on altitude result in temporal changesin habitat use by birds (Loiselle and Blake 1991). Dif-ferences in the fruiting phenology of a single key speciesdistributed over a broad elevational gradient may alsohave an effect on habitat use of specialist birds (Bankoet al. 2002).

Most of the Ursidae are omnivorous and have dietsthat depend largely on fruits. Like other frugivores, theychange their home range as well as their habitat use

A. Nakajima (&) Æ S. Koike Æ C. Kozakai Æ Y. Nemoto Æ K. KajiTokyo University of Agriculture and Technology,3-5-8 Saiwai, Fuchu, Tokyo 183-8509, JapanE-mail: nimh42@hotmail.comTel.: +81-423-675738Fax: +81-423-675738

T. MasakiForestry and Forest Products Research Institute,1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan

T. ShimadaTohoku Center, Forestry and Forest Products ResearchInstitute, 92-25 Nabeyashiki, Shimo-Kuriyagawa,Morioka, Iwate 020-0123, Japan

K. YamazakiZoological Laboratory, Ibaraki Nature Museum,700 Osaki, Bando, Ibaraki 306-0622, Japan

Ecol Res (2012) 27: 529–538DOI 10.1007/s11284-011-0919-z

according to fruit abundance [American black bears(Ursus americanus); Rogers 1987]. Differences in vege-tation distribution at different elevations and theresulting fluctuations in food resource availability alsoimpact habitat use in the Ursidae (Izumiyama and Shi-raishi 2004; Waller and Mace 1997; Servheen 1983).Although bears are generalists, they may temporally beinfluenced strongly by the abundance of a particularkind of food resource, resulting in temporal shifts intheir habitat use with respect to elevation (Koike et al.2008).

The habitat of the Asiatic black bear (Ursus thibet-anus, hereafter referred to as ‘bear’) in Japan encom-passes a wide elevational gradient and overlaps withareas used by humans at lower altitudes. Sometimes,bears move to lower altitudes during autumn, resultingin an increase in the frequency of human–bear conflicts(Yamazaki 2009). The number of human–bear conflictsincreases during years of mast failure (Taniguchi andOsaki 2003; Oka et al. 2004); however, the causalrelationship between these variables remains unex-plored. The timing of intrusion and maturation of hardmasts do not coincide with one another (Oka et al.2004), and because of this discrepancy, it is necessaryto clarify the temporal processes involved in the mat-uration of hard masts in detail, to identify the timing offoraging by bears, and to relate them to each other.The relationship between spatiotemporal patterns ofhard mast availability and bear movement is also un-known.

In the area examined in the present study[900–1,600 m above sea level (asl)], there were five majorvarieties of hard mast: Fagus crenata, F. japonica,Quercus crispula, Q. serrata and Castanea crenata. Ofthose five species, we expected that Q. crispula wouldsignificantly influence bears’ movement within the studyarea. Q. crispula acorns are the dominant variety acrossa broad elevational range within the study area (T.M.,unpublished data); furthermore, Q. crispula producesacorns frequently (once in 2–3 years: Taniguchi andOsaki 2003), has patches of good producers even in afailure year (Mizoguchi et al. 1996; Taniguchi and Osaki2003), and is foraged heavily by bears during autumn incentral and western Japan (Hashimoto and Takatsuki1997). Previously published research has also shown thatbears foraged Q. crispula at the study site heavily duringthe time of the present study (Koike et al. 2011).

The goal of the present study was to examine thefruiting phenology of Q. crispula acorns at differentaltitudes, and to determine the foraging strategies ofbears with respect to the fruiting conditions present. Noreliable data are available on fruiting phenology of thisspecies with respect to altitude, and it was hypothesizedthat the maturation of acorns occurs earlier at higheraltitudes in a manner similar to the coloring of autumnfoliage and, because of this, bears will change theirforaging behaviors accordingly, coming down to loweraltitudes in search of usable food resources. If acornmaturation does not occur earlier at higher altitudes,

bears will forage at sites with the greatest availability offorage irrespective of altitude. We examined seasonalchanges in acorn characteristics that were expected toattract bears (mass, shape, color, nutritional value andremaining numbers on trees) as well as acorn use bybears at various altitudes ranging from 900 to 1,400 masl. Shape and color were included as a characteristic ofinterest to bears as a previous study suggested the pos-sibility of bears searching for food using visual cues(Bacon and Burghardt 1976; Paisley and Garshelis2006), and also because these characteristics may begood indicators of change in the nutritional value ofacorns. In addition, the phenology of Q. crispula acornsin two different areas, the east and west sides of themountain, was examined, as masting of this species hasbeen known to synchronize over small areas (Mizoguchiet al. 1996), and phenological differences might existover areas. The questions addressed by the present studywere (1) whether or not the fruiting phenology andcharacteristics of acorns differed among altitudes andareas; (2) when bears foraged acorns in relation to theirphenological development; and (3) where bears engagedin acorn foraging behavior with respect to acorn phe-nology.

Materials and methods

Study area

The present study was conducted in the Ashio Moun-tains, which span across Tochigi and Gunma Prefecturesin central Japan. Annual precipitation in the study areais 1,254 and 2,236 mm, while annual mean temperatureis 12.1 and 7.2�C as recorded west of Ashio area inNumata City, 439 m asl and north-east of the Ashioarea in Okunikko, 1,292 m asl, respectively. Vegetationin the study area consisted of deciduous broad-leavedforests composed of Q. crispula, Acer spp. and F. crenatain areas of altitudes up to 1,600 m asl. Above that alti-tude, vegetation consisted of mixed forests composed ofTsuga sp. and Betula sp. Below 1,000 m asl there wereplantations of Cryptomeria japonica and Chamaecyparisobtusa, while plantations of Larix kaempferi occurredfrequently between 1,000 and 1,600 m asl. The bio-masses of each of the five major kinds of hard mast inthe study area (F. crenata, F. japonica, Q. crispula, Q.serrata and Castanea crenata) as measured as the totalbasal area of each species, were 217.4, 534.8, 7826.5,3000.2 and 48.7 cm2/400 m2, respectively (A.N.,unpublished data). Biomasses of hard mast species weresurveyed in 28 quadrats (400 m2 each), covering alti-tudes ranging from 900 to 1,600 m asl in an area withinthe six sites used in this study. Bears inhabited the entirestudy area (Ministry of Environment 2004) and, whilethe population density of bears in the area was un-known, a previous study in the same area captured 17individual bears over the course of 3 years (Kozakaiet al. 2011).

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A single study site was established at elevations of900, 1200 and 1400 m asl in both Gunma and TochigiPrefectures (six sites in total, Fig. 1). Sites in Gunmawere located on the west face of the north to southrunning Ashio Mountains, while sites in Tochigi werelocated on the east face. Hereafter study sites located inGunma and those located in Tochigi are denoted asG900, G1200 and G1400, and T900, T1200 and T1400,respectively. At each site, fruiting phenology and acornforaging activity of bears was surveyed as follows.

Fruiting phenology of Q. crispula

Five aspects of fruiting phenology were measured: mass,color, shape, nutritional value and number of acornsremaining on trees. In addition, temporal change in theavailable energy of acorns in the tree canopies (AET)was estimated. In keeping with the methodology of mostprevious studies, measurement intervals of 2 weeks wereused (Bonner 1974, 1976; Hashizume 1979; Masaki et al.1994; Iwabuchi 2006).

Mass

Ten acorns were sampled from the canopy of three treesat each site, with the exception of one (T900, in whichonly 2 trees were sampled), giving a total of 17 treessampled every 2 weeks in the period from 23 May to 24October 2007. Acorns sampled before August were toosmall to mass and were excluded from the analysis. Onlyone tree in G1400 and two in T1200 were sampled onOct 24 as no other trees retained acorns. Sampled acornswere freeze-dried and massed. Mean mass was calcu-lated for each tree giving an index of acorn mass.

Bears do not consume the cupule and pericarp ofacorns (S.K., personal observation) and so acorns withneither cupule nor pericarp were used for measurementsof mass and nutritional value; however, on 13 August,acorns with both a cupule and a pericarp were used insample analysis and, on 30August, acorns with a pericarpwere used, as samples taken on these 2 days were toosmall to separate the acorn from the cupule and pericarp.

Color and shape

The color and shape of all collected acorns were recordedprior to drying. Acorn color was also recorded from di-rect observations made when estimating the number ofacorns on trees at the study sites. For each acorn, colorwas recorded as green, yellow or brown based on thecolor covering more than half of the specimen. Shape wasdefined as the ratio of acorn specimen length and widthshowing above the cupule (Fig. 4).

Nutritional value

From 13 August to 24 October 2007, additional samplesof acorns weighing approximately 3–10 g total dry masswere sampled at 2-week intervals from the same treessampled during mass measurement.

The samples were freeze-dried and milled, and thecrude protein, crude fat, total sugar and tannin contentswere measured. Crude protein was measured as 6.25·nitrogen with a NC-analyzer (Series2 CHNS/O Analyzer2400; Perkin Elmer, Boston, MA) using acetanilide as thecalibration standard. Crude fat was measured byextraction in diethyl ether for 8 h in a Soxhlet apparatus.Total sugar was measured as the sum of water-solublesugar content and starch. Water-soluble sugar and starchwere extracted using hot water extraction and perchloricacid extraction, respectively, and determined using thephenol–sulfuric acid method (Dubois et al. 1956).Absorbance was measured at 485 nm in a microplatereader (Sunrise Rainbow RC; Tecan Trading, Manne-dorf, Switzerland) using D-glucose as the calibrationstandard. Starch was calculated as glucose equiva-lent · 0.9. Tannin content was measured as the index oftannin astringency (i.e., the ability of precipitating pro-teins) using the radial diffusion method (Hagerman 1987)with tannic acid used as the calibration standard.

All measurements were expressed as a percentage ofthe dry mass (g) of the acorn. Nutritional value wasevaluated using available energy (AE) and tannin con-tent, each representing a characteristic that was attrac-tive or unattractive to foraging bears, respectively. AEwas estimated from the following equation:

Fig. 1 Map of the study area,located in the Ashio Mountainrange in Tochigi and GunmaPrefectures, Japan. Locationsof the trees surveyed areindicated by black dots

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AE kJ/gð Þ ¼ 23:7 kJ� protein%ð Þ þ 39:5 kJ � fat%ð Þþ 15:6 kJ � total sugar%ð Þ ð1Þ

Number of acorns on trees

Acorns of Q. crispula are known to experience pre-mature abscission (Kasahara and Sasaki 1991; Kuram-oto 1993). In the present study, observation of acorns ontrees began after premature abscission ceased, and wascarried out every 2 weeks during a period that spanned30 July–24 November 2007, after which time no acornscould be observed on trees within the study sites.Observations were made in the branches of the sunnycrown of sample trees as accessed by climbing the treesor reaching from a car roof. One or two trees wereobserved at each site until over 100 acorns were marked.Between 57 and 165 current-year branches bearingacorns were marked on each individual tree, and boththe number and color of acorns present were recordedduring each observation.

Seed traps were used to estimate the number ofacorns on additional trees (one tree in G900, and fourtrees each in T900, T1200 and T1400). Three such trapswere set each with an opening of 0.5 m2 under the crownof each tree. In order to compare the two methods, seedtraps were also set under the trees examined using directobservation.

Available energy of acorns in the tree canopy

AET was estimated from the following equation:

AET tð Þ ¼ ADTT tð Þ �DWA tð Þ �AEDW tð Þ ð2Þ

where t, ADTT, DWA and AEDW denote the date ofobservation, acorn density at the tree top (acorns perm2), dry mass per acorn and AE per dry mass, respec-tively. ADTT was estimated for each observation dateby summation of fallen seed density recorded in thetraps after each respective date.

After 10 September, it was possible for acorns to beseparated from their cupule and pericarp and a rapidincrease in dry mass and decrease in tannin content wasobserved. Therefore, the number of acorns was esti-mated assuming 10 September as the beginning ofabscission period.

Use of acorns by bears

Acorn foraging activity of bears was estimated by walk-ing a route about 1 km in length at each site and lookingfor feeding signs within 20 m of the path. More than 50trees of Q. crispula were checked for signs of forageduring each search, with searches occurring each weekfrom 13 August to 24 October 2007. Three kinds of signswere observed: branches broken by bears when eatingacorns (i.e., bear shelves), claw marks on tree trunks and

broken pericarps left by bears. To avoid counting thesame tree in subsequent searches, trees identified as usedby bears were marked with tape and photographs of theclaw marks were taken. Any trees with evidence of for-aging that could have been overlooked were identifiedduring searches on 10 December, after the leaves hadfallen and the bear shelves were easy to find.

Statistical analyses

To assess whether the maximum values of dry mass aswell as the width and length ratios taken on 26 Sep-tember differed by altitude and area, a generalized linearmixed model (GLMM) with a Gaussian distribution wasused, with altitude and prefecture (both categoricalvariables) serving as explanatory variables, and eachindividual tree serving as a random factor. The maxi-mum value of AE and minimum value of tannin wereregressed using a generalized linear model (GLM)assuming a Gaussian distribution, with altitude andprefecture serving as explanatory variables. Individualtree data were not included as a random factor becauseonly one data point per date and individual was re-corded. Color change and number of acorns at the treetop were regressed by altitude, prefecture and date (anumeric variable) using a GLMM with binomial distri-bution including individual trees as a random factor.The two estimates for number of acorns at the tree top,taken using direct observation and a seed trap, werecompared by including method as an explanatory vari-able in the GLMM model. To assess whether temporalchanges in foraging signs differed by altitude and area, aGLMM with a binomial distribution was employed,using the cumulative number of feeding signs versus thetotal number of feeding signs at each site at each date asa dependent variable, altitude, prefecture and date asexplanatory variables and individual tree data as arandom factor. For each of the models the ‘‘best’’ modelwas selected using Akaike’s information criterion (AIC).All models were ranked by DAIC ( DAICi = AICi �AICmin), so that the model with the least AIC had avalue of 0. Models for which DAIC £ 2 were consid-ered to have substantial support, while models withDAIC values of 4–7 or 10 had considerably less and noempirical support, respectively (Burnham and Anderson2002). GLM and GLMM were run using R 2.8.0 (RDevelopment Core Team).

Results

Fruiting phenology

Mass

Acorn mass increased slowly until early September at allstudy sites, after which time it increased rapidly (Fig. 2).Of the 17 trees investigated, the dry mass of acorns from

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14 continued to increase before reaching maximum sizeat the time the acorns fell. The most appropriate modelfor determining the maximum mass of acorns as iden-tified using DAIC included altitude as the explanatoryvariable, suggesting that acorns present at 1,200 m werelarger than acorns at other elevations (Tables 1, 2). Thenull model had statistical support similar to that of themodel used above (i.e., DAIC £ 2).

Color and shape

The most appropriate model for acorn color includedaltitude, prefecture, date and the interaction of altitudeand prefecture as explanatory variables (Table 1). InGunma Prefecture, color changed from green to yellowand then to brown earlier at lower altitudes than it did athigher altitudes; however, the same pattern was notobserved in Tochigi Prefecture (Table 2; Fig. 3).

The mean width of acorns increased until 13 August,after which time the ratio of both length and width in-creased. Changes in length and width ratio were almostnegligible after 10 September, with acorn shaperemaining stable after that point (Fig. 4). The null modelfor length and width ratio was selected for use for 26September, when the shape of acorns became stable(Table 1).

Nutritional value

AE increased throughout the study period, while tannincontent of acorns increased until early September, afterwhich point it decreased at all sites until abscission(Fig. 5). The null model was selected for the maximumvalue of AE and the minimum value of tannin (Table 1).Models including prefecture as an explanatory variablealso had substantial support for use in determining AE,while models including altitude and prefecture had

Fig. 2 Temporal change in the dry mass of Quercus crispula acorns(mean ± SD) in the Ashio Mountains, Japan. Mean mass wascalculated using ten acorns from each of three trees at each site(except for T900, where only two trees were examined). The arrowindicates 27 September, the date foraging of acorns by bears wasfirst observed

Table

1AIC

and

DAIC

(inparentheses)values

ofgeneralizedlinearmodel

(GLM)andgeneralizedlinearmixed

model

(GLMM)modelsusingmaxim

um

dry

mass,maxim

um

AE,

minim

um

tannin,colorandnumber

ofacornsontree

topsasresponse

variables,forQuercuscrispula

acornsin

theAshio

Mountains,Japan

Variables

Models

Maxim

um

dry

mass

Maxim

um

AE

Minim

um

tannin

Color

Length

ratio

Width

ratio

Number

of

acornsontree

top

Feedingsigns

alt

(+date)a

139.02(0.00)

68.44(3.26)

72.42(0.41)

135.05(3.56)

�367.59(11.58)

�495.62(13.40)

212.55(6.34)

27.47(3.41)

pref

(+date)

142.31(3.29)

66.83(1.65)

73.77(1.76)

138.33(6.84)

�373.55(5.62)

�503.64(5.38)

212.28(6.07)

24.06(0.00)

alt+

pref

(+date)

141.10(2.08)

70.10(4.92)

74.05(2.04)

137.04(5.55)

�361.97(17.20)

�490.03(19.00)

214.48(8.27)

26.00(1.94)

alt+

pref+

alt

·pref

(+date)

143.20(4.18)

71.84(6.66)

76.99(4.98)

131.50(0.00)

�355.18(23.99)

�481.50(27.53)

206.21(0.00)

26.00(1.94)

Null

(+date)

140.33(1.31)

65.18(0.00)

72.01(0.00)

136.51(5.02)

�379.17(0.00)

�509.02(0.00)

210.29(4.08)

26.95(2.89)

altAltitude,

prefprefecture,AE

available

energy

aExplanatory

variablesusedonly

forthemodel

analyzingcolorandnumber

ofacornsontree

top

533

substantial support for use in determining tannin levels(i.e., DAIC £ 2).

Number of acorns on trees

The proportions of the remaining number of acorns onseven trees estimated both by direct observation andseed traps were compared. For less than half of them(three trees), the two estimates differed significantly.Therefore, seed trap data was used to estimate thenumber of acorns on the trees.

The proportion of the remaining number of acornson trees is shown in Fig. 6. Acorns fell off all examined

trees between 24 October and 14 November 2007, withthe exception of one tree. The most appropriate modelfor the number of acorns on trees included altitude,prefecture, date, and the interaction of altitude andprefecture as explanatory variables (Table 1). Acornswere present on tree tops at G1400 for the longest period(Table 2; Fig. 6). From comparison of the line (theestimated value) and points (the actual data), it wasobserved that a large variation among individual treesexisted.

Available energy of acorns in the tree canopy

AET peaked in late September at G900 and G1200,between late September and early October at T900 and

Table 2 Results of GLMM for the maximum dry mass, color,number of acorns on tree tops and signs of feeding by Asiatic blackbears for Q. crispula acorns in the Ashio Mountains, Japan

Model Coefficient SE

Maximum dry massIntercept 1.852 0.207Altitude (900 m) �0.298 0.308Altitude (1,400 m) �0.794 0.293ColorIntercept 107.444 8.584Date �0.385 0.031Altitude (900 m) �2.337 1.132Altitude (1,400 m) 3.211 1.299Prefecture (Tochigi) 0.464 1.121Altitude (900 m): prefecture (Tochigi) 2.352 1.664Altitude (1,400 m): prefecture (Tochigi) �3.581 1.640Number of acorn on tree topIntercept 5.353 1.062Date �0.211 0.006Altitude (900 m) 0.092 1.295Altitude (1400 m) 4.148 1.432Prefecture (Tochigi) 2.028 1.137Altitude (900 m): prefecture (Tochigi) �1.113 1.453Altitude (1,400 m): prefecture (Tochigi) �5.996 1.574Feeding signsIntercept �20.420 4.619Date 0.365 0.082Prefecture (Tochigi) 2.346 1.15

Fig. 3 Temporal changes in the color of Q. crispula acorns in theAshio Mountains, Japan. Points Actual data, lines values estimatedfrom models. Various symbols and colors are used to representdifferent sites as in Fig. 2. The arrow indicates 27 September, thedate foraging of acorns by bears was first observed

Fig. 4 Temporal change in the width ratio and length ratio of Q.crispula acorns in the Ashio Mountains. a, b, c, d were measured foreach acorn and length and width ratio was calculated using thefollowing equations: length ratio = a�b

a

� �, width ratio = d

c

� �.

Acorns from the same trees as in Fig. 3 were measured. Varioussymbols and colors are used to represent different sites as in Fig. 2.The arrow indicates 27 September, the date foraging of acorns bybears was first observed

Fig. 5 Temporal changes in available energy (AE) and tannincontent per unit dry mass of Q. crispula acorns (mean ± SD) in theAshio Mountains, Japan. Acorn specimens were the same onesused in the determination of temporal changes in color. Varioussymbols and colors are used to represent different sites as in Fig. 2.The arrow indicates 27 September, the date foraging of acorns bybears was first observed

534

T1400, and in early October at T1200 and G1400.Acorns were available in greater amounts and for alonger period at T1200 and G1400 (Fig. 7).

Foraging by bears

Signs of foraging by bears

A claw mark left by a bear was observed on a tree trunkat G1400 on 18 September; however, acorns were leftintact. The first observation of acorn foraging was madeat T1200 on 27 September, followed by observations atG1400 on Oct 2 (Fig. 8). No traces of foraging activitywere observed at G900, T900 and T1400 throughout theentire study period. The most appropriate model forfeeding signs included prefecture as the explanatoryvariable, with sites in Gunma Prefecture showing

signs of feeding later than sites in Tochigi Prefecture(Tables 1, 2). No previously unrecorded feeding siteswere located during searches on 10 December.

Discussion

In the present study, it was hypothesized that the fruit-ing of Q. crispula would occur earlier at higher altitudesthan at lower altitudes, and that, if this was the case,bears would change foraging sites according to differ-ences in available forage, coming down to lower alti-tudes. If fruiting did not occur earlier at higher altitudes,bears would forage at sites with the greatest availabilityof food resources irrespective of altitude. Contrary tothis hypothesis, characteristics of acorn fruiting did notchange from higher to lower altitudes; however, two ofthe three identified foraging sites of bears were found inareas with greater amounts of forage available for longerperiods of time.

Fruiting phenology and characteristicsof Q. crispula acorns

The fruiting phenology and characteristics of acorns didnot differ across altitudes or sites except in the timing ofacorn color change and abscission period. Floweringwas observed earlier at lower altitudes (A.N., personalobservation); however, the phenology of acorn devel-opment appeared to even out across all study sites by thetime growth became significant after early September.Results obtained in the present study were consistentwith those obtained by Iwabuchi (2006), who demon-strated that the development pattern of size in Q. serratadid not differ among areas.

Acorn abscission periods differed by altitude and area(Fig. 6). G1400 had a later abscission period than othersites; however, only one tree specimen was observedthere, so whether this delay was the result of an indi-vidual characteristics could not be determined. InTochigi, where more individuals were observed, thelatest abscission period was recorded at an elevationof 1,200 m and large characteristic variations were

Fig. 6 Temporal changes in the proportion of Q. crispula acorns(mean ± SD) remaining in the tree canopy at study sites in theAshio Mountains. This graph illustrates relative changes in theproportion of acorns, with values taken on 10 Septemberrepresenting a 100% maximum. Points Actual data, lines valuesestimated from models. Various symbols and colors are used torepresent different sites as in Fig. 2. The arrow indicates 27September, the date foraging of acorns by bears was first observed

Fig. 7 Temporal changes in available energy of Q. crispula acornson trees in the Ashio Mountains. Various symbols and colors areused to represent different sites as in Fig. 2. The arrow indicates 27September, the date foraging of acorns by bears was first observed

Fig. 8 Number of foraging signs on Q. crispula left by Ursusthibetanus at study sites in the Ashio Mountains, Japan

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observed between individuals. Previous studies haveshown that variation exists in the abscission period ofindividual Q. crispula specimens; Tanaka and Matsuura(1988) reported that abscission period varied by up toseveral weeks and Kanazawa et al. (1988) reportedvariations of at least 1 week in the abscission period ofQ. crispula individuals. Abscission period may also beinfluenced by the characteristics of individual trees.

Color change did not differ between sites located inTochigi Prefecture (color change at T900 occurred later,while change at T1400 occurred earlier relative tochanges observed in Gunma) and changes in shape werealmost negligible after 10 September, while values ofmass and nutritional value increased linearly after 10September. Bonner (1974, 1976) reported that colorchange was a good indicator of acorn maturation (i.e.,when acorns are able to germinate) for cherrybark oak(Q. falcata var. pagodaefolia Ell.), water oak (Q. nigraL.), willow oak (Q. phellos L.) and shumard oak (Q.shumardii Buckl.). Color change was also observed inwhite oaks (Q. alba L.) when the acorn reached maxi-mum dry weight. In the present study, however, changesin color and shape of Q. crispula acorns did not indicatechanges in acorn mass or nutritional value.

Maximum value of acorn mass and AE and minimumvalue of tannin displayed a weak relationship with bothaltitude and area (the null model was selected as themodel with DAIC £ 2). Large variations in acorn massand chemical content between and within individualtrees have been observed in other acorn-producing spe-cies (Takahashi and Shimada 2008; Gomez 2004; Sorket al. 1983). Variation within and between individualtrees may have had a greater influence on mass, AE andtannin content than altitude and area for Q. crispulaacorns. Since mean acorn mass and AE reached amaximum and tannin content reached a minimum justbefore abscission, the timing of maximization and min-imization was influenced by the falling period, not byaltitude or area. This suggests that the abscission periodmight have influenced the mass, AE and tannin contentof acorns as well. Previous research has demonstratedthat the weight of Q. crispula has a significant positiverelationship to the warmth index at sites in Japan (Hiuraet al. 1997) and that Q. serrata has smaller acorns athigher altitudes (Iwabuchi et al. 2006). These studiessuggested that the difference in the length of the growingseason among sites or elevations does matter. Results ofthe present study suggest that various other factors notconsidered here, such as production level (Q. crispula:Kanazawa 1982; Tanaka et al. 1989) and tree size (Q.serrata: Iwabuchi 2006) could affect acorn size.

The increase in tannin content observed prior to thestart of September may have been caused by the inclu-sion of cupule and pericarp tissue in samples analyzedbefore 10 September. While exceptions do exist, mostacorns have higher tannin content in the cotyledon thanin the pericarp (Fleck and Layne 1990). The proportionof pericarp compared to cotyledon decreases as acornsgrow, which will increase the overall proportions of

tannin. Mature acorn cotyledons tend to have lowertannin content than immature cotyledons (Fleck andLayne 1990). In the present study, the tannin contentwas higher in early September than it was in late Octo-ber.

AET is influenced by acorn size, energy content perdry mass and the number of acorns on trees. Values ofAET differed among various elevations even thoughdifferences in individual characteristics were slight, al-though interpretations of AET values must be madewith caution, as some sites had only one tree with seedtraps in order to estimate the density of acorns on treetops. Since the mass and nutritional value (higher en-ergy, lower tannin levels) of acorns increased when theabscission periods was pushed back, an area in whichindividual trees have late abscission periods will producemore AET. T1200 and G1400 had a later falling periodthan the other study sites, which resulted in their havinga greater, delayed AET peak.

Bear foraging in relation to acorn characteristicsand phenology

During the year in which the present study was under-taken (2007) Q. crispula yielded a good crop of acorns,with production per unit of crown area for the speciesreaching 304.8 kcal/m2, while the same production in Q.serrata, F. crenata, F. japonica and C. crenata was only154.0, 0.0, 0.0 and 34.0 kcal/m2 on average, respectively(T.M., unpublished data. Sampling area and methodshown in Kozakai et al. 2011). Therefore, it was con-cluded that the hard mast of species other than Q.crispula exerted less influence over bears’ foragingbehavior.

In the present study, the timing of bear foragingactivity in terms of acorn phenology could not bedetermined, and the factor that triggered commence-ment of foraging behavior was not elucidated. No dif-ferences in acorn characteristics were observed whensamples collected prior to the commencement of forag-ing activity were compared to those collected after for-aging activity, or when samples collected at bothforaging and non-foraging locations were compared.During previous examination of the species Prunus ja-masakura, the time at which fruit became available asforage was clear, as the sugar content rose significantlyat maturation (Koike et al. 2008). In the present study,energy per acorn increased continuously with growth(i.e., a threshold date at which acorns become maturewas not apparent) and the amount of energy per acornvaried among individual fruits. These factors made itdifficult to identify a precise time when acorns becomeavailable as forage for bears. At G900, bear feedingsigns, such as feces and the presence of bear shelves onindividuals of the species Cornus controversa, were foundin August within the same sample site used in the presentstudy (A.N., personal observation). This indicated that afood resource existing prior to the availability of Q.

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crispula hard mast might have influenced the timing offoraging of Q. crispula hard mast by bears. If so, thetiming to start foraging on hard masts may vary amongyears with different availability of summer food. Okaet al. (2004) discussed the discrepancy between the tim-ing of intrusion of bears into human areas and matu-ration of hard masts based on the general period whenbears forage on hard masts, but there may have beenyears when bears foraged on hard masts earlier thangeneral years, causing the discrepancy. From late sum-mer to autumn, bears feed on various kinds of fruitspecies and changes in feeding behaviors can be ob-served between seasons and years (Koike 2010). Fur-thermore, fruit production varies annually within andamong forage species other than Q. crispula (Shibataet al. 2002). In order to understand how fruit producingspecies affect one another with respect to the timing ofbear acorn foraging activity, it is necessary to conductfurther studies observing their fruiting phenology.

Bears foraged in locations where AET was availablein greater amounts and for a longer period at T1200 andG1400, except for G1200 which did not have greateramount of AET. At G1200 and G1400 only one tree wasused in order to observe abscission period and ADTT,making it impossible to assess whether the period ofacorn availability at those sites influenced the bears’selection of foraging location. Previous research has notadequately examined the temporal effect of plant phe-nology on site selection of bears (Davis et al. 2006),making further research into site selection with respectto phenology necessary. Signs of bears foraging onacorns were observed only at T1200, G1200 and G1400,while the other sites were not utilized. As acorn pro-duction during the year of the study was good, bearsmay have had access to ample food resources at thesame site, making travel between sites unnecessary. Inyears of poor mast production, however, bears’ move-ment patterns are altered, with changes such as increasesin the distance between intensively used areas havingbeen noted in the same area used in the present study(Kozakai et al. 2011) as well as in other parts of Japan(Arimoto et al. 2012). Furthermore, American blackbears, which have a physiology similar to that of theAsiatic black bear, have exhibited an increase in thehorizontal span of their home range (Pelchat and Robert1986; Powell et al. 1997; Kasbohm et al. 1998) as well asa tendency to travel farther in search of food resources(Reynolds and Beecham 1980; Garshelis and Pelton1981; Noyce and Garshelis 1997), sometimes even up to200 km, during years when food production is low(Rogers 1987).

In conclusion, no observable difference in acornphenology among altitudes and no significant relation-ship between acorn phenology and foraging by bearscould be elucidated. These results may indicate thatacorns of Q. crispula are a flexible resource for bears. AsQ. crispula is the dominant hard mast-producing speciesover a wide elevational range and has variation in thecharacteristics of its acorns, fruit of this species may be

available for forage by bears in at least one location for alarge period of time, suggesting that Q. crispula acornsact as a stable food resource for bears.

Acknowledgments The authors would like to thank Dr. NobuoKanzaki for his encouragement; Dr. Mitsue Shibata for teaching usto climb trees; Dr. Akiko Takahashi for helping with chemicalanalysis; Mr. Yui Nemoto and Mr. Shinichi Haneo for providinginformation on the study area; Mr. Ikeda Takashi for helping withfield work; Mr. Yukio Goto for advice on tree climbing; Dr.Masashi Kiyota for helping with statistical analysis; and colleaguesin the laboratory for supporting our work. This study was partlyfunded by the Ministry of Environment, Japan (‘‘The study projecton the Japanese black bears’ mass intrusion into human settle-ments’’) and the Grant-in Aid for Japan Society of the Promotionof Science Fellows (No. 197287).

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