Behavioral Responses of Cao vit gibbon

American Journal of Primatology74:632–641(2012)RESEARCH ARTICLEBehavioral Responses of Cao Vit Gibbon(Nomascus Nasutus)to Variations in Food Abundance and T emperature in Bangliang,Jingxi,ChinaPENG-FEI FAN∗,HAN-LAN FEI,AND CHANG-YONG MAInstitute of Eastern-Himalaya Biodiversity Research,Dali University,Yunnan,People’s Republic of ChinaThe Cao Vit gibbon is a critically endangered species with only about110individuals remaining in a degraded karst forest along the China-Vietnam border.Behavioral data from this site are particularly useful in understanding gibbon behavioral adaptations to different sets of ecological conditions and will contribute to the conservation of the species.We studied seasonal variation in the time budget and diet of the Cao Vit gibbon in response to variation in food availability and ambient temperature by observing two groups for1,379hr between January and December2009.We used5-min scan samples to record the activity of gibbons.Both ambient temperature and food availability varied from month to month.Gibbon groups increased resting time and huddled together in sleeping places in cold months.Gibbons spent more time feeding on fruit when fruit was more abundant suggesting that fruit was their preferred food.Alternatively,leaf eating was negatively correlated with leaf availability which suggested that leaves may be used as a fallback food.Gibbons increased their diet diversity when they ate more leaves.This might be a strategy to cope with toxins or digestion inhibitor accumulation associated with feeding from a limited number of leaf species.Individuals consumed more buds when Broussonetia papyrifera produced buds in March and April.During this period,they decreased traveling time and engaged in less frequent social interactions.Gibbons spent more time searching for and feeding on invertebrates during June and October.However,we did not collect data on invertebrate abundance and therefore cannot determine the relationship between invertebrate feeding and availability.We conclude thatflexibility in consuming diverse food types and food species, and in responding to the availability of preferred foods,has enabled the Cao Vit gibbon to survive in a degraded karst forest habitat.Am.J.Primatol.74:632–641,2012.C 2012Wiley Periodicals,Inc.Key words:Cao Vit gibbon;Nomascus nasutus;seasonal variation;diet;time budgetINTRODUCTIONNonhuman primates are found in a wide vari-ety of habitats,from tropical and subtropical forests [e.g.orangutans:Knott&Kahlenberg,2007;gib-bons:Bartlett,2007],mangrove forest[proboscis monkeys:Bismark,2010],to temperate forests[Yun-nan snub-nosed monkeys:Xiao et al.,2003;Japanese macaques:Hanya,2004]and grassland[geladas: Iwamoto&Dunbar,1983].In most of these habi-tats,seasonal influences produce temporal variation in food availability.Even in tropical regions close to the equator,seasonal differences in mean tem-perature are small butfluctuation in rainfall may be marked,which produces seasonal availability of food resources[Matsuda et al.,2009;McConkey et al., 2003;Pavelka&Knopff,2004;Stone,2007].For-aging animals therefore are required to make deci-sions regarding which resources to exploit,in order to ensure that they obtain sufficient nutrition and maintain good health[Bartlett,2009;Fan et al., 2009;McConkey et al.,2003;Pavelka&Knopff, 2004;Stone,2007].Therefore,many primate species are characterized by seasonal changes in feeding be-havior that represents a response to the abundance of food resources[Bartlett,2009;Di Fiore&Rodman, 2001;Hill,1997;Matsuda et al.,2009;McConkey et al.,2003;Pavelka&Knopff,2004;Stone,2007].One model of optimal foraging predicts that primates are expected to expend more time/energy in search of food during a season of high food avail-ability to maximize their net energy gain,while Contract grant sponsor:National Natural Science Foundation of China;Contract grant number:30900169;Contract grant spon-sor:International Foundation for Science(IFS);Contract grant sponsor:Conservation Leadership Programme(CLP);Contract grant sponsor:Fauna and Flora International(FFI).∗Correspondence to:Peng-Fei Fan,Institute of Eastern-Himalaya Biodiversity Research,Dali University,Dali,Yunnan 671003,P.R.China.E-mail:fanpf1981@Received4August2011;revised28December2011;revision accepted17January2012DOI10.1002/ajp.22016Published online in Wiley Online Library(wileyonlinelibrary. com).C2012Wiley Periodicals,Inc.Seasonal Variation of Cao Vit Gibbon’s Behavior/633reducing the energetic costs of foraging when food is scarce[Norberg,1977].Alternatively,temperate primates may switch to poorer quality food sources in the lean season[Fan et al.,2009;Poulsen et al., 2001;Xiang et al.,2007],resulting in more time spent feeding in order to compensate for reduced nutritional value[Bartlett,2009;Fan et al.,2008; Nakagawa,1989].Moreover,animals living at higher latitudes experience seasonal changes not only in food availability but also ambient tem-perature[Bartlett,2009;Fan et al.,2009;Hill, 1997],resulting in energetic challenges associ-ated with thermoregulatory costs[Hanya,2004]. Nakayama et al.[1971]reported that the en-ergy expenditure of outdoor-living captive Japanese macaque(Macaca fuscata)at 5.2◦C is 2.5times greater than that at29.5◦C.To save energy, Japanese macaques decrease traveling and feed-ing when the temperature is low and the ther-moregulatory costs are severe[Hanya,2004].West-ern black-crested gibbons(Nomascus concolor), living in a high-altitude habitat in the Wuliang Mountains,decrease traveling and increase resting in the cold winter months[Fan et al.,2008].Thus, factors associated with seasonal changes in temper-ature and food production have a direct influence on primate diet and activity patterns.The Cao Vit gibbon,also known as the east-ern black-crested gibbon(N.nasutus),was rediscov-ered in Vietnam in2002and in China in2006[Fan et al.,2010].The only remaining population,with around110individuals,lives in a karst forest along the Chinese-Vietnam border[Fan et al.,2010].Their habitat is located further north(N22◦55 ,E106◦29-30 )than most other gibbon populations and experi-ences marked seasonal variation in temperature and rainfall[Fan et al.,2010].Different from many other gibbon populations,most Cao Vit gibbons live in sta-ble bifemale family groups[Fan et al.,2010].In a study by Fan et al.[2011],they were found to con-sume over81plant species,with19species each ac-counting for≥1%of the overall feeding time.These 19species contributed77.8%of the gibbon diet[Fan et al.,2011].The goal of this study was to examine how Cao Vit gibbons respond to seasonal variation in food availability and temperature in the Bangliang Na-ture Reserve,Jingxi,China.Given the extreme cli-matic and environmental conditions present at this site,behavioral data from this gibbon population provide critical insights into the effects of habitat extremes on gibbon behavioral plasticity and social organization.METHODSStudy SiteWe carried out this study in the Bangliang Na-ture Reserve in Jingxi County,Guangxi,China,a region continuous with the Cao Vit gibbon Conser-vation Area in Trung Khanh,Cao Bang,Vietnam. The forest type is a tropical monsoon forest within a karst limestone landscape[Fan et al.,2010,2011]. The gibbon habitat had been degraded by selective logging,wood collection for fuel,charcoal making, and agricultural encroachment prior to the time the species was rediscovered in China[Fan et al.,2011]. This gibbon population is now protected by the Ban-gliang Nature Reserve in China and by the Cao Vit Gibbon Conservation Area in Vietnam.Currently, the height of the forest canopy is approximately 10.5m which is the lowest reported forest inhabited by gibbons.However,the plant diversity remains high.Fan et al.[2011]recorded114tree species and 51species of woody lianas or epiphytes in44, 20×20m plots.Temperature and RainfallWe used a HOBO pro RH/Temperature Data Logger(RG3-M)to record the temperature every half hour and rainfall continuously in the study area from January2008to December2009[Fan et al.,2010]. Annual mean temperatures were19.6◦C in2009and monthly mean temperatures ranged from12.1◦C in January2009to25.2◦C in August2009.The mini-mum temperature(3.4◦C)was recorded in Novem-ber,and maximum temperature(40.8◦C)in April. Annual precipitation was1,363mm in2009.There was a marked rainy season between May and Octo-ber[Fan et al.,2010].Behavioral Data CollectionThree gibbon groups live exclusively(G1)or partly(G2and G4)in Bangliang Nature Reserve, China[Fan et al.,2010].From January2008to December2009(except February2008),we spent 7–27days each month,totalling485days,observ-ing gibbon behavior.Given that traditional or stan-dard primate observational techniques are impossi-ble at this site due to the steepness of the landscape, the gibbons were observed from several established observation posts at distances of between50and 500m(most observations were made at a distance of100–300m),using8×30binoculars(Steiner sa-fari)or a spotting scope(Leica Apo-Televid7720–60) [Fan et al.,2011].A scan sampling method at5-min intervals was used to record the activity of gibbons[Altmann, 1974].For each observation sample,a1-min scan was made recording the behavior of all visible mem-bers.Each individual was observed for5sec and its predominant behavior recorded[Di Fiore&Rod-man,2001].During most1-min scans,the gibbon was engaged in a single behavior.In a small num-ber of cases,the gibbon was engaged in more than one recognized behavior.In these cases,we con-tinued to observe the animal for some additionalAm.J.Primatol.634/Fan et al.TABLE I.Sample Sizes for Data Collected on Two Cao Vit Gibbon Groups in Bangliang Nature Reserve between January and December2009G1G4Month Days Hours Scans Records Days Hours Scans Records 9January9(5)646041,4017(2)453661,107 9February6(4)595961,3169(3)655471,306 9March6(5)576131,7056(4)464541,526 9April9(3)676361,1997(1)373411,077 9May9(2)686321,1084(2)393961,094 9June12(2)816371,2899(2)676231,713 9July10(2)624769599(0)38284726 9August10(1)695039449(1)605341,537 9September7(3)625901,29010(0)503781,010 9October12(1)735681,0248(2)48417989 9November9(2)645351,0026(1)37289672 9December11(3)575191,12710(2)645761,476 Total110(33)7836,90914,36494(20)5965,20514,233 The numbers of full-day-observations are shown in parentheses.seconds until a predominant behavior was identi-fied.We recorded activity as resting,traveling,feed-ing,grooming,calling,playing,and other.Resting included any inactive posture(sitting,lying,and hanging);the category also included instances of auto-grooming,which always occurred during rest. Traveling comprised movement(bipedal walk,sus-pension,leap,bridge,and climb).Feeding comprised picking,chewing,or swallowing food.Grooming re-ferred to manipulating,stroking,or picking through the hair of another individual.Calling comprised only the solo/duet heard at the time of the5-min scan. Playing refers to social play between≥2individu-als.Conflict activity between groups,alarm calling, and unidentified behaviors were scored as“other”. When an individual was feeding,we recorded the food species and specific part eaten(fig,fruit,leaves, buds,flower,invertebrates,and other).MacKinnon &MacKinnon[1980]described gibbons as“fig ex-ploiters”,and on average,figs are reported to make up a quarter of the gibbon diet[Bartlett,2007]. To provide comparative data with other gibbon re-search,we seperatedfigs from other non-fig fruit when recording plant part consumed.Plant species not positively identified in thefield were collected for verification by Xu Weibin,a botanist from Guangxi Institute of Botany,Chinese Academy Sciences.Whenever possible,groups were observed for the full day.Because of fog,rain,and the topography of the landscape,full-day-observations were difficult. Overall,we obtained53full-day observations and 151partial-day observations(Table I).We recorded the time that each individual gibbon entered(N= 108)and left(N=74)its sleeping tree to calculate the total period of activity.Only data collected be-tween January and December2009were used in this study.We observed G1for783hr across110days (14,363activity records)and G4for596hr across 94days(14,233records)(Table I).Group G2was onlyoccasionally observed because most of its home rangewas located inside Vietnam.Therefore,data for G2were excluded from this analysis.During the studyperiod,G1consisted of one adult male,two adultfemales,one juvenile and two infants;G4consistedof one adult male,two adult females,four juveniles,and one to two infants[Fan et al.,2010].Food AvailabilityAs previously described[Fan et al.,2011],we es-tablished44,20×20m botanical plots,accountingfor0.7%of the combined home ranges of G1and G4,across different topographical regions(slope,ridge,valley,and col).For each plot,we recorded the lo-cation and altitutde of the plot and for all trees ≥10cm DBH(N=911),we recorded plant species, tree height,trunk height,DBH,and the crown di-ameter.Eight hundred and thirty eight trees(92%)were identified to species by Xu Weibin.Each of the911tree individuals,as well as lianas and epiphytespresent on these trees were monitored for seasonalavailability of food types(fruit,figs,leaves,buds,andflowers)for3days every month.We estimatedthe abundance value(percent of crown cover)of eachfood type ranging from0–4(0<1%;1=1–25%,2=26–50%,3=51–75%,4=76–100%)for each tree[Poulsen et al.,2001].For fruiting trees,the percent-age of the crop that was ripe was estimated becausegibbons usually do not consume unripe fruit.We as-sume that DBH is a proxy measure of tree crownvolume[Chapman et al.,1992].We multiplied theabundance value with the DBH of each individualplant and then summed all these scores to yield amonthly abundance index for each food type.We es-timated the proportion of lianas and epiphytes cov-ered on the individual tree crown and multiplied thisAm.J.Primatol.Seasonal Variation of Cao Vit Gibbon’s Behavior/635 Fig.1.Food availability for Cao Vit gibbons in Bangliang Nature Reserve from January to December2009.proportion by the tree DBH to get a proportional DBH for lianas and epiphytes.As we were inter-ested only in assessing the relationships between gibbon behavior and the relative abundance of food items,plant species not eaten by gibbons were not in-cluded in calculating food abundance scores.Overall, 452trees,lianas and epiphytes,provided food items for gibbons during the study period.Because the gib-bons spent only3%of their feeding time consuming flowers[Fan et al.,2011],we did not calculate their abundance in our analyses.Data AnalysisWe calculated food diversity in the gibbon’s monthly diet using the Shannon-Wiener Index [McConkey et al.,2003].Only those feeding records in which the food species was identified were used for this analysis.The behavior of dependent and semi-dependent infants was excluded in all analyses.The gibbon diet and time budget is reported to show di-urnal variation[Fan et al.,2008,2009;Raemaekers, 1978].In order to ensure that diet and time budget were not biased by uneven data collection across the day,data were averaged for each hour before mean monthly diet and time budgets were computed[Hill et al.,2003].We combined grooming,playing,and singing as social behavior in all analysis.The time that gibbons entered and left their sleeping trees was used to calculate the average active time for each month.Then,we multiplied the monthly percentage time budget with the average active time to get ac-tual time per day(in hours)spent in feeding,travel-ing,social interactions,and other behaviors[Hanya, 2004;Hill et al.,2003].Variables were not trans-formed because none of the variables were found to differ significantly from a normal distribution (Kolmogorov-Smirnov:P>0.05for all variables). Step-wise regression was used to analyze the effects of temperature and food abundance(independent variables)on the time allocated in different activities (dependent variables).Spearman correlation was used to analyze the relationship between variables.All research reported in this manuscript was per-mitted by the Guangxi Provincial Wildlife Protection Office and the Bangliang Nature Reserve Adminis-tration Bureau,and adhered to the legal require-ments of China and the American Society of Prima-tologists(ASP)Principles for the Ethical Treatment of Non Human Primates.RESULTSFood AvailabilityAs indicated in Figure1,resource abundance varied across the year.Fruit production was rela-tively high from May to September2009,while the relative abundance of buds peaked in April2009. Figs lacked the temporal pattern of seasonal abun-dance observed in fruits and buds,with fewfigs available in March and April2009.Leaves eaten by the gibbons were available throughout the year,al-though their relative abundance was reduced during the dry winter season.Time BudgetFeeding accounted for23.9%of both groups’day-time budget.Traveling accounted for18.8%and 30.0%of the daytime activity budget of groups G1and G4,respectively.Social behavior includ-ing grooming,playing and singing accounted for 11.3%in G1and16.9%in G4.Over the same 12months,G1on average spent2.48hr/day feed-ing,2.00hr/day traveling,and1.22hr/day engaged in social behavior.G4exhibited certain differences from G1(2.48hr in feeding, 3.19hr in travel-ing,and1.83hr in social behavior).Including time in sleeping trees,G1and G4spent18.26hr and 16.45hr inactive(resting and sleeping),respec-tively.Am.J.Primatol.636/Fan etal.Fig.2.Time allocated to different activities across a 24-hr day by two Cao Vit gibbon groups between January and December 2009in Bangliang,China.Both G1and G4showed marked monthly vari-ation in their time budgets (Fig.2).We found some differences between G1and G4,but both groups increased resting when temperature was low and decreased time engaged in social in-teractions when buds were more abundant (Table II).Feeding BehaviorFruit,including figs,accounted for half of the Cao Vit gibbon feeding time.The remainder of the diet was made up of leaves,buds,inverte-brates,flowers,and others (Fig.3).We multi-plied the proportional diet and feeding time to estimate the actual time spent feeding on differ-ent food types.On average,G1spent 0.63hr/day feeding on fruit,0.54hr/day on figs,0.23hr/day on buds,0.70/day on leaves,and 0.29hr/day on inverterbrates.G4spent 0.92hr/day feeding on fruit,0.32hr/day on figs,0.48hr/day on buds,0.49/day on leaves,and 0.09hr/day on inverter-brates.There was marked seasonal variation in the Cao Vit gibbon’s feeding time on different food types over the course of our study for both groups (Fig.4).Food availability has a significant influence on gibbon feeding behavior.Stepwise regression anal-ysis showed both groups spent more time consum-ing fruit when fruit was more abundant (Table III).The productivity of figs did not influence the feed-ing time on figs for either groups.G1ate more buds and leaves when buds were more available.G4ate more buds when figs were not abundant and ateAm.J.Primatol.Seasonal Variation of Cao Vit Gibbon’s Behavior /637TABLE II.Stepwise Regression Analysis Testing the Effects of Monthly Food Abundance and Mean Temperature on Monthly Time BudgetsFood productivityBudFruitFigLeaveMean temperatureFeedingG1r p G4r −0.599p 0.040RestingG1r 0.397−0.611p 0.0400.005G4r −0.970p 0.000TravelingG1r −0.798p 0.002G4r 0.796p 0.002SocialG1r −0.651p 0.022G4r −0.760p0.004Monthly time budget was the dependent variable while monthly food abundance of different food types and mean temperature were selected as independentvariables.Fig.3.Dietary pattern (percent time feeding on different food types)of two Cao Vit gibbon groups between January and Decmeber 2009in Bangliang,China.more leaves when leaves were less abundant dur-ing the winter seasons (Table III).Gibbon groups spent more time searching for and feeding on inver-tebrates during periods when buds were less abun-dant (G1)or when there were more leaves (G4)(Ta-ble III).We found a negative correlation between time spent on feeding leaves and invertebrates in each of our two study groups (Spearman correla-tion:G1:r =−0.755,P =0.005;G4:r =−0.786,P =0.002).The total number of food species used per month ranged from 9to 25in G1,and 5to 21in G4(Table IV).The Shannon-Wiener index also varied from month to month (Table IV).Step-wise regres-sion analysis showed that the Shannon-Wiener index was higher when gibbons consumed more leaves and fewer buds (G1:T buds ,r =−0.548,P =0.012;T leaves ,r =0.614,P =0.002;T figs ,r =0.392,P =0.049;G4:T buds ,r =−0.449,P =0.007;T leaves ,r =0.813,P <0.001).DISCUSSIONThis is the first detailed study of seasonal vari-ation in the activity budget and feeding behavior of Cao Vit gibbons.Fan et al.[2011]reported the proportional diet based on all feeding records col-lected between January 2008and December 2009.Because the data set and methods of analysis used by Fan et al.[2011]are different from those used in the present study,the proportional diet are dif-ferent between the two studies (reported as fruit:36.1%;figs:21.9%;leaves:16.9%;buds:14.3%;in-vertebrates:7.0%;flower:3.0%in Fan et al.,2011).Ambient temperature in Bangliang varied con-siderably from month to month.The mean tempera-ture was <15◦C while the minimum temperature was <4◦C between November and January.Cao Vit gibbons increased time spent resting in the cold months,and a stepwise regression analysis showed that temperature significantly influenced the rest-ing time of both groups.This might be explained asAm.J.Primatol.638/Fan etal.Fig.4.Feeding time allocated to different food types by two Cao Vit gibbon groups between January and December 2009in Bangliang,China.TABLE III.Stepwise Regression Analysis Testing the Effects of Monthly Food Abundance on Time Spent Feeding on Different Food TypesFood productivityBudFruit FigLeaveT fruitG1r 0.854p 0.000G4r 0.786p 0.002T budsG1r 0.599p 0.039G4r −0.614p 0.034T leavesG1r 0.705p 0.010G4r −0.807p 0.002T invertebratesG1r −0.686p 0.014G4r 0.656p0.021Feeding time on food types was considered the dependent variables while food abundance was selected as the independent variable.a strategy to save energy during cold temperatures.In addition to increased resting time,Cao Vit gibbons usually huddled together in their sleeping places in cold months while they sleep separately or apart in warmer months (unpublished data).A similar be-havioral pattern of increased resting and huddling together in sleeping places in cold months was re-ported in another northern gibbon population,west-ern black-crested gibbons in the Wuliang Mountain [Fan &Jiang,2008;Fan et al.,2008].G1and G4were found to spend approximately equal amounts of time feeding,but differed in the way in which they divided their remaining activity time.We speculate that the time required for feed-ing is less flexible than time devoted to other activ-ities.G4spent more time in travelling and in so-cial behavior and less time resting than G1.During the research period,G4contained one adult male,two adult females,four juveniles,and one depen-dent infant and G1contained one adult male,two adult females,one juvenile and two dependent in-fants.Therefore,G4had seven foraging individuals while G1had only four because dependent infants do not forage by themselves.Individuals living in a larger gibbon group may need to travel greaterAm.J.Primatol.Seasonal Variation of Cao Vit Gibbon’s Behavior/639 TABLE IV.Number of Species Consumed and Shannon-Wiener Index for Each Study Month in Two Cao Vit Gibbon Groups between January and December2009in Bangliang,ChinaNumber of food Shannon-Wienerspecies consumed indexG1G4G1G4 9January2114 2.36 2.10 9February2220 2.31 2.23 9March13100.580.88 9April1513 2.03 1.36 9May1913 1.90 1.46 9June1411 1.95 1.44 9July95 1.33 1.12 9August96 1.65 1.25 9September99 1.50 1.49 9October2111 2.35 1.37 9November1714 1.47 2.02 9December2521 2.54 2.26 Mean1612 1.83 1.58distances tofind sufficient food[Chapman&Chap-man,2000].Time engaged in social interactions did differ between groups.G4had four juveniles and they commonly played together when the adults were resting(personal observations),which may have contributed to the differences in time allocated to social behavior in these two groups.Gibbons are described as frugivores,and nearly all gibbon species spend more time feeding on ripe fruit than on leaves[Bartlett,2007].Like other gib-bon species[Bartlett,2009;Chivers,1972],but un-like crested gibbon at Mt.Wuliang[Fan et al.,2009], Cao Vit gibbons spent about50%of their feeding time consuming fruits includingfigs.Both groups spent more time feeding on fruit than leaves between May and September(Fig.4)when fruit was more avail-able(Fig.1).During months of fruit scarcity,Cao Vit gibbons supplemented their diet with leaves,buds, and invertebrates.Although both groups consumed more leaves than other food types between December and Febru-ary,leaves were not a preferred food resource.This is based on our observations that leaf eating was neg-atively correlated with leaf abundance.G4showed a negative correlation between leaf productivity and feeding time on leaves while G1showed a posi-tive correlation between bud productivity and feed-ing time of leaves(Table III).Because bud produc-tivity was significantly negatively correlated with leaf productivity(Spearman correlation:r=−0.733, P=0.007,Fig.1),G1actually ate more leaves when leaves were less available.Cao Vit gibbons increased dietary diversity(Table IV)during periods when they consumed more leaves.A pattern in which di-etary diversity increased when preferred foods were scarce has been reported in several primate species [Japanese macaque:Agetsuma&Noma,1995;hy-brid gibbon:McConkey et al.,2003;proboscis mon-key:Matsuda et al.,2009].Although this may be explained by a strategy designed to cope with tox-ins or the accumulation of digestion inhibitors when exploiting a limited number of leaf species[Matsuda et al.,2009],we do not have data on leaf chemistry to test this argument.Buds were the most important food(based on feeding time)in March for G1,and in March and April for G4(Fig.4),coinciding with months dur-ing which Broussonetia papyrifera produced buds.B.papyrifera was the most commonly consumed food species for Cao Vit gibbons in Bangliang in2008and 2009[Fan et al.,2011].When B.papyrifera produced buds,gibbons concentrated their feeding efforts on this species,which contributed86.7%and77.8%of the monthly feeding records in March for G1and G4, respectively.Therefore,dietary diversity was lowest in March(Table IV).Because B.papyrifera was usu-ally distributed in large patches(personal observa-tion),gibbons did not need to travel long distances to feed on buds,and traveling time was lowest in March(Fig.2).When gibbons consumed more buds, both groups decreased their levels of social activity (Table II).On average,insects account for7%of the gib-bon diet[Bartlett,2007].Annually,G1spent13.5% and G4spent4.8%of their time in searching for and feeding on invertebrates.However,both groups spent more time foraging for invertebrates between June and October than during other months(Fig.4). Noticeably,insectivory accounted for>40%of the G1’s monthly feeding time in June.Because we did not have data on invertebrate abundance,we cannot determine the relationship between invertebrateAm.J.Primatol.。