Ecology and social system of northern gibbons living in cold seasonal forests

2018·1.2 MB·

by  Guan, Zhen-Hua

ZOOLOGICAL RESEARCH
Ecology and social system of northern gibbons living in
cold seasonal forests
Zhen-HuaGuan1,Chang-YongMa2,Han-LanFei2,BeiHuang3,Wen-HeNing3,Qing-YongNi4,Xue-LongJiang3,Peng-Fei
Fan2,*
1YunnanAcademyofBiodiversity,ForestDisasterWarningandControlKeyLaboratory,SouthwestForestryUniversity,KunmingYunnan
650224,China
2SchoolofLifeSciences,SunYat-SenUniversity,GuangzhouGuangdong510275,China
3StateKeyLaboratoryofGeneticResourcesandEvolution,KunmingInstituteofZoology,ChineseAcademyofSciences,KunmingYunnan
650223,China
4CollegeofAnimalSciencesandTechnology,SichuanAgriculturalUniversity,ChengduSichuan611130,China
ABSTRACT China.
GibbonsinChinarepresentthenorthernmostmargin Keywords: Northerngibbon;Ecology;Socialsystem;
Adaptation;Groupsize
of present day gibbon species distribution (around
N25◦). Comparedtotropicalhabitats,northerngibbon INTRODUCTION
habitats are characterized by low temperatures and
Gibbons (Hylobatidae) are small apes that live in tropical
remarkable seasonal variation in fruit abundance.
and subtropical forests in southeastern Asia (Bartlett, 2011).
How gibbons adapt to their cold and seasonal Theseapesarecharacterizedbyseveralinterrelatedfeatures,
habitats and what ecological factors affect their including long arms for brachiation, terminal branch feeding,
sociality are key questions for understanding their frugivory, pair-living, and territoriality (Brockelman, 2009). In
tropicalforests,gibbonsrelyheavilyonripefruitpulp(Chivers,
ecologyandsocialsystemevolution, theelucidation
1984),withfruitsincludingfigscomprising>60%oftheirannual
of which will contribute to the conservation of these
diet, though siamang (Symphalangus syndactylus) is more
specialpopulations/species. Accordingtopreliminary
folivorous(reviewedinBartlett,2011). Fruitisoftendistributed
short-termstudies,northerngibbonsconsumemore in small and defensible patches, resulting in food competition
leaves and use larger home ranges than tropical among females. Female gibbons are considered intolerant to
gibbons. Interestingly, some Nomascus groups each other and live solitarily (Bartlett, 2011; Kappeler et al.,
2013; Leighton, 1987; Wrangham, 1987), with males unable
consist of more than one adult female. However,
tosuccessfullydefendrangesoccupiedbytwoormorefemales
these preliminary results are not well understood or
(Bartlett,2009).Malesmaythusbenefitfrompair-livingthrough
incorporated into current socio-ecological theories
regarding gibbon species. To better understand
northerngibbons,ourteamhassystematicallystudied
Received: 23October2017;Accepted: 02January2018;Online: 12
threehabituatedgroupsofNomascusconcolor,three
March2018
groups of N. nasutus, and two habituated groups Foundation items: This research was supported by the National
of Hoolock tianxing since 2002. In this paper, NaturalScienceFoundationofChina(31770421,31570386,31160424,
we stress the challenges facing gibbons living in 30900169), the National Young Top-notch Talent Program of China,
northern habitats and summarize their behavioral and Sun Yat-Sen University, and Collaborative Innovation Center for
adaptations to their harsh environments. We also Biodiversity and Conservation in the Three Parallel Rivers Region of
describe the northern gibbon social system and China,StartupFoundationforScientificResearch,SouthwestForestry
discuss the potential relationships between their University(111408)
ecology and sociality. Finally, we highlight future *Correspondingauthor,E-mail:[email protected]
research questions related to northern gibbons in DOI:10.24272/j.issn.2095-8137.2018.045
SciencePress ZoologicalResearch39(4):255–265,2017 255
1) infanticide defense against non-resident, unmated males obvious differences, detailed observations on these gibbons
(Borriesetal.,2011;Opieetal.,2013;vanSchaik&Kappeler, werehamperedinChinabyalackofhabituatedwildgibbons
2003); 2) increased paternal certainty by mate guarding due to intense human hunting pressure and difficult terrain
(Palombit,1996, 1999); 3)limitedopportunitiesforthefemale (Yin et al., 2016). Systematic, longitudinal research became
to evaluate potential sexual partners (Palombit, 1996, 1999); possibleonlyrecentlyafterseveralN.concolor andH.tianxing
and4)enhancedforagingefficiencybysharingknowledgewith groups became habituated to observers in Mt. Wuliang and
females(Brockelman,2009)orbyensuringthatresourcesare Mt. Gaoligong (Fan & Jiang, 2008; Fan et al., 2008, 2009a,
not unknowingly depleted by foraging apart (Terborgh, 1983). 2013;Yinetal.,2016). In2006,N.nasutuswasrediscovered
Females benefit from pair-living through food and territory in a small karst forest patch in Bangliang, Jingxi County,
defense, direct infant care provided by males (reported in Guangxi(Chanetal.,2008).Researcherscouldobservethese
siamangs, Lappan, 2008), and enhanced foraging efficiency gibbons from fixed observation posts located on hill tops or
(Brockelman, 2009). The mated pair use a small home forest gaps due to the steep karst terrain and low canopy
range of on average 42 hm2, and actively defend 82% of height (Fan et al., 2011a, 2012). With accumulating data
the area (Bartlett, 2011) through direct intergroup conflicts fromdifferentspecieslivingindifferenthabitats,thepictureof
(Bartlett, 2003) and regularly occurring loud morning songs northerngibbonecologyandsociality,althoughstillincomplete,
(Geissmann, 2002; Mitani, 1985). Both sexes benefit from isbecomingclearer.
knowledge of this intensively-used territory and goal-directed
CHALLENGESFACINGNORTHERNGIBBONSINCHINA
foragingstrategies(Brockelman,2009).This,inturn,reinforces
territory defense and small home range, and consequently
The human population in China has increased rapidly and
oftenlimitsgibbongroupsize(Brockelman,2009;Brockelman
currently stands at over 1.3 billion (National Bureau of
et al., 2014). Bartlett (2009) first integrated seasonality into
Statistics of China, http://www.stats.gov.cn/english/). The
territory defense. He argued that stable food abundance is a
resulting increase in demand for cropland, together with the
prerequisite for territory defense. However, most information
steel-making campaign of 1958, has led to the clearance
on gibbons comes from only a few studied species (mainly
of vast tracts of forest (Jiang et al., 2006; Zhang, 2000).
Hylobates lar and S. syndactylus) living in lowland tropical
Deforestationandhabitatfragmentationcausedbyexpansion
forests(Bartlett,2009,2011;Brockelmanetal.,1998;Chivers,
of crop cultivation and plantations are the main causes of
1974;Lappan,2008;Palombit,1996,1999).
gibbon decline and extinction in China (Fan et al., 2011a,
Historically, gibbons were distributed widely in China. As
2011b, 2013, 2014; Fan, 2017; Jiang et al., 2006; Zhang et
recentlyas500yearsago,theirmelodicsongscouldbeheard
al., 2010; Zhou et al., 2005), with large-scale hunting in the
alongTheThreeGorgesincentralChinaandevenfurthernorth
1970s and 1980s also having a considerable impact. A total
(close to N35◦) (Turvey et al., 2015; Zhou & Zhang, 2013).
of81365primateskinswerecollectedbyChinesegovernment
Although the known gibbon range has shrunk considerably
officials between 1974 and 1980 (Quan et al., 1981). While
fromnorthtosouth,andisnowrestrictedtoYunnan,Guangxi,
manyskinswerefrommacaquespecies(Macacamulattaand
and Hainan in southern China (Fan, 2017; Turvey et al.,
M. arctoides), gibbons were also hunted during this period
2015; Zhou & Zhang, 2013), these sites still represent the
(Fan, 2017; Quan et al., 1981). In the late 1980s and early
northernmostmarginofpresentdaygibbondistribution(around
1990s,manyChinesegibbonpopulationshaddeclinedtosuch
N25◦,e.g.,N.concolorinWuliangMountain:Jiangetal.,2006;
low levels that recovery was considered unlikely. By the
H.tianxinginGaoligongshan:Fanetal.,2011b,2017),second
late 1980s, the remaining populations of three species had
only to the Hoolock gibbons in India and Myanmar (Groves,
decreased to less than 40 individuals (N. hainanus: Liu et
1967). In this paper, we arbitrarily refer to the populations of
al., 1989; H. lar: Yang et al., 1987; N. leucogenys: Hu et al.,
N. concolor, N. leucogenys, N. hainanus, N. nasutus, and H.
1990), and until recently N. nasutus was considered extinct
tianxing inChinaas“northern”gibbons(Figure1). Itdoesnot
in China (Tan, 1985). To date, the numbers of H. lar and
meanthatthesegibbonsaredistributedinnorthernareasbut
N. leucogenys have not recovered and both species are now
isusedforcomparisonbetweenthesegibbonpopulationsand
assumed to be ecologically extinct in China (Fan et al., 2014;
gibbonslivingin“southern”tropicalforests.
Grueter et al., 2009). After more than 20 years of intensive
Based on short-term studies of unhabituated northern
conservation efforts, N. hainanus remains highly threatened
gibbonsinChina,earlyresearchersreportedonthedifferences
withextinction(Fellowesetal.,2008;Zhouetal.,2005)andis
in ecology and behavior compared to tropical gibbons.
themostendangeredprimatespeciesintheworld(Fan,2017),
For example, northern gibbons were less frugivorous (N.
with only one population of less than 30 individuals surviving
leucogenys: Hu et al., 1990; N. concolor: Chen, 1995; Lan,
in Bawangling. Fortunately, a small population of about 20
1993), occupied larger home ranges (N. hainanus: Liu et al.,
individualsofN.nasutuswasrediscoveredinBangliang,Jingxi
1989; N. leucogenys: Hu et al., 1990; N. concolor: Jiang et
County, Guangxi in 2006 (Chan et al., 2008). The remaining
al., 1994a; Jiang & Wang, 1999), and some groups included
gibbonpopulationsinChinasurviveinmontaneorkarstforests
morethanoneadultfemale(N.concolor: Haimoffetal.,1986,
in several isolated mountain regions that are unsuitable for
1987; N. hainanus: Liu et al., 1989; Jiang et al., 1994a,
cultivation.
1994b;Jiang&Wang,1999). Althoughearlystudiesreported
Gibbonhabitatsinthesenorthernmountainareasaremuch
256 www.zoores.ac.cn
colderthantropicalforests(Table1). Forexample,theannual zeroandforestsaresometimescoveredinsnow(Fan&Jiang,
mean temperature in Dazhaizi, Mt. Wuliang is 16.6 ◦C (at 2008;Fanetal.,2013). Thus,theresidentgibbonslikelyface
2 000 m a.s.l.: Fan & Jiang, 2008) and is even colder at increasedthermoregulatorycostscomparedtotropicalgibbon
Nankang (13.3 ◦C, at 2 200 m a.s.l.: Fan et al., 2013) and populations. Nakayamaetal. (1971)reportedthattheenergy
Banchang,Mt.Gaoligong(13.0◦C,at2300ma.s.l.:Fanetal., expenditure of outdoor-living captive Japanese macaques (M.
unpublisheddata).Atthesesites,temperaturescandropbelow fuscata)at5.2◦Cwas2.5timesgreaterthanthatat29.5◦C.

Figure1Distributionofthegibbonspecies:Nomascus(7species);Hoolock (3species);Hylobates(9species);Symphalangus(1
Figure 1 Distribution of the gibbon species: Nomascus (7 species); Hoolock (3
species)(AccordingtoThinhetal.,2010a,2010b;Fanetal.,2017;IUCN,2017)
Ourgibbonsrpeseecaricehss)it;e sHaryelaolsobmaatrekesd (o9n thsepmeacpi.es); Symphalangus (1 species) (According to Thinh et al.
2010a,b; Fan et al. 2017; IUCN 2017)
Table1Behavioralecologyinformationofnortherngibbons
Annual Annualmean Group Dailypath Home
Our gibbon research sites are also maArltkituedde on the map. Frugivory Mating
Species Locationa rainfall temperature size(n length rangesize Reference
(m) (%) systemb
(mm) (◦C) groups) (m) (hm2)

Yinetal.,2016;
1.Banchang 4.0
Hoolock 1462 13.0 1900–2500 NA >93 NA M Fanetal.,
Mt.Gaoligong (n=4)
tianxing underreview
2.Nankang 3.0 Fanetal.,2013;
1801 13.3 1900–2300 1162±506 88 49 M
Mt.Gaoligong (n=1) Zhangetal.,2014
Jiang&Wang,1999;
Nomascus 3.Dazhaizi 6.6 Fanetal.,2006;
1607 16.6 1900–2700 1391±703 >100 44 P
concolor Mt.Wuliang (n=5) Fan&Jiang,2008;
Fanetal.,2009a
4.Bangliang 6.6 Fanetal.,2010,2011a,
N.nasutus 1565 19.6 1804–1363 1268±512 130 50 P
Guangxi (n=5) 2012,2015
a:LocationsaremarkedonFigure1.b:“P”representspolygynousand“M”representsmonogamous.NA:Notavailable.
ZoologicalResearch39(4):255–265,2017 257
Fruit productivity decreases with increasing latitude and and less fruit than tropical gibbons (Chen, 1995; Hu et al.,
altitude(Hanya&Aiba,2010),andnortherngibbonsareknown 1990; Lan, 1993). This hypothesis was supported by several
toconsumelessfruitthantropicalgibbons(reviewedinFanet later studies with at least one-year duration. For example,
al.,2013).Fruitingseasonalityalsoincreaseswithlatitude,and the overall diet of N. concolor at Dazhaizi, Mt. Wuliang, was
fruitingseasonsarelongerinthetropicsandshortertowardthe comprisedof46.5%leavesand44.1%fruit(Fanetal.,2009a),
poles(Tingetal.,2008). AtMt. Ailao,asitesupportingoneof with similar results reported for H. tianxing in Nankang, Mt.
the two largest populations of N. concolor in China (Li et al., Gaoligong (49.1% fruit and 43.3% leaves, Fan et al., 2013)
2011), figsareabsentandotherfruitisonlyavailableforfour and N. nasutus in Bangliang (50% fruit and 35% leaves, Fan
months of the year (Chen, 1995; Sun et al., 2007). Haimoff et al., 2012). Comparatively, the diets of tropical gibbons are
et al. (1987) argued that Mt. Wuliang represents an extreme typicallycomprisedof64%fruitand25%leaves,exceptforthe
environment for gibbons due to the unavailability of fruit for morefolivoroussiamangs(49%fruitand38%leaves)(Bartlett,
much of the year, during which time gibbons must subsist on 2011). Although northern gibbons consume less fruit than
leaves(alsoseeFanetal.,2009a).InMt.Gaoligong,Nankang, tropicalgibbons,theypreferfruitwhenitisavailable(Fanetal.,
fruit availability drops close to zero between December and 2012). When non-fig fruit is more abundant, H. tianxing feed
February(Fanetal.,2013). Thesefindingsraisethequestion onfewerleaves(Fanetal.,2013). AlthoughFanetal. (2009a)
of how northern gibbons adapt to their cold and seasonal did not monitor fruit availability at Dazhaizi, Mt. Wuliang, the
habitats. N.concolor groupstudiedspentmoretimefeedingonfruitin
Marchofthesecondyearwhenfruitwasmoreavailable(Fan
ECOLOGYOFNORTHERNGIBBONS
etal.,2009a).Whenfruitislessaccessibleorabsent,northern
gibbonsswitchtheirdiettoleavesandbuds(Fanetal.,2009a,
Northern gibbons live in sizable home ranges (N. concolor:
2012, 2013), accounting for 83% of the N. concolor diet in
>100 hm2, N. nasutus: 130 hm2, H. tianxing: >93 hm2 in
March(Fanetal.,2009a),andincreasetheirfeedingtime(Fan
Table1;N.leucogenys:540hm2,Huetal.,1990;N.hainanus:
etal.,2008).
200–500 hm2, Liu et al., 1989, yearly 149 hm2 in Bryant et
When leaves dominant their diets, gibbons decrease their
al.,2016),whichareconsiderablylargerthanthoseoftropical
traveltimeandshortentheirdailypathlengthasleavescontain
gibbons (reviewed in Bartlett, 2011). In mountainous areas,
feweravailablecaloriespergramthanfruit(Raemaekers,1978)
trees are patchily distributed in different microhabitats due
andaremoreabundantandevenlydistributedintheforest(Fan
to variables such as soil, altitude, sunlight, water flow, and
et al., 2008). This travel strategy has also been adopted by
topography (Fan et al., 2011a; Sun et al., 2007; Tian et al.,
tropical gibbons (Chivers, 1974; Bartlett, 2009; Raemaekers,
2006). TreespeciessuchasSaurauianapaulensis andFicus
1978), with two groups of H. lar found to travel on average 1
neriifoliaoccuralongstreamsondampshadyslopes,whereas
330m(rangefrom620mto1930m,n=12months)and1160
Tetrastigma delavagi occurs on the sunny slopes at Dazhaizi,
m(rangefrom720mto1660m,n=12months),theytraveled
Mt. Wuliang(Tianetal.,2006). Ficusglaberrimaisdistributed
short distance when dominantly feeding on leaves (Bartlett,
onslopesandvalleys,whereasPlatycaryalongipesoccurson
2009).However,variationinbothtimespenttravelinganddaily
hilltops. ThekarsthabitatusedbyN.nasutus wasclassified
path lengths are more dramatic in northern gibbons (Fan &
intofourdifferenttypes(Fanetal.,2011a).
Jiang,2008; Zhangetal.,2014). Forexample, thedailypath
Patchilydistributedplantspeciescreatevariablefoodmaps
lengthofN.concolor inMt. Wuliangvariesmonthlyfrom629
for northern gibbons. To obtain sufficient sustenance, the
mto2356m(n=14months)anddailyfrom300mto3144m
group of N. concolor in Mt. Wuliang (Fan & Jiang, 2008)
(n=66 days, Fan & Jiang, 2008). The mean daily path length
and H. tianxing in Mt. Gaoligong (Zhang et al., 2014)
ofH.tianxinginMt. Gaoligongvariesmonthlyfrom508mto1
shift their monthly home range according to the seasonal
926m(n=14months)anddailyfrom345mto2606m(n=63
availability of food species. Although their monthly home
days)(Zhangetal.,2014). Furthermore,traveltimecanshow
ranges(N.concolor:37±12hm2;H.tianxing:28±15hm2)are
seasonaldifferences.Forexample,theH.tianxinggroupinMt.
comparabletothehomerangesoftropicalgibbons(avg.34±9
Gaoligonghasbeenobservedtotravel(onaverage)3.40hin
hm2, calculated from Table 17.3 in Bartlett, 2011, excluding
Junebut1.27hinFebruary(Fanetal.,2013).Seasonalimpact
Nomascus), they occupy a larger total home range to satisfy
ontraveltimehasalsobeenreportedforthetwogroupsofN.
their annual food requirements (Fan & Jiang, 2008; Zhang et
nasutusinBangliang(groupG1: from3.92hinJuneto0.52h
al., 2014). Furthermore, they do not use their large home
inMarch;groupG4: 4.92hinJuneto1.37hinMarch;Fanet
range evenly, but instead heavily utilize smaller areas with
al.,2012).
greater food resources (Fan & Jiang, 2008). They also do
Both sleeping and resting behaviors in northern gibbons
not significantly increase their daily path length compared
are strongly influenced by cold temperatures, with more
with tropical gibbons (northern gibbons in Table 1; tropical
time spent inactive (sleeping and resting) during the 24 h
Hylobates gibbons: avg. 1300m), exceptforsomesiamang
cycle in winter (Fan et al., 2012, 2013). In Nankang, Mt.
species (e.g., S. syndactylus: 0.8 km, reviewed in Bartlett,
Gaoligong, the H. tianxing group spent 20.12 h inactive in
2011).
February,whereasthetwogroupsofN.nasutus inBangliang
In response to the overall low availability of fruit, early
spent 20.23 h (December) and 19.69 h (January) inactive.
researcherssuggestedthatnortherngibbonsatemoreleaves
258 www.zoores.ac.cn
Gibbonsmaintainanenergy-conservingposturewhilesleeping behaviorbetweentwofemaleslivinginthesamegroup. They
orresting(sittingwithhandsclaspingtheirlegs:Bicca-Marques reported that the two females fed in the same tree, sang
& Calegaro-Marques, 1998). Northern gibbons usually sit synchronously, groomed each other, and groomed and were
huddledtogetherontreetopsinthesunshineduringcoldwinter groomedbytheadultmale,butneversleptinthesameplace
days,andevenhuddleandsharesleepingsitesoncoldnights (Fan et al., 2006). They even shared meat when one female
(Fanetal.,unpublisheddata). killed a flying squirrel (Fan & Jiang, 2009) and cooperated
in evicting a “floating” (unmated) female from their territory
SOCIALSYSTEMOFNORTHERNGIBBONS
(Fan et al., 2006). Further longitudinal observations showed
that the two females repeatedly bred with the resident group
Gibbonsusuallyliveinsmallsocialgroupswithoneadultpair
male (Huang et al., 2013) and maintained similar spatial
and 2–3 offspring (Leighton, 1987). However, some northern
relationshipstohim(Fan&Jiang,2010a).Morerecently,Guan
gibbons live in stable polygynous groups with two breeding
etal. (2013)demonstratedthatthesegroupsconsistedoftwo
females (N. hainanus: Zhou et al., 2008; N. concolor: Fan &
breeding females even after replacement of breeding males
Jiang,2010a;Guanetal.,2013;Huangetal.,2013;N.nasutus:
and females, and females actively cooperated in maintaining
Fan et al., 2010, 2015). Gibbon groups with more than one
theirsocialrelationship,ratherthanco-existingmerelythrough
breedingfemalehavealsobeenreportedinotherspecies(H.
toleranceoravoidance.
pileatus:Srikosamatara&Brockelman,1987;Hoolockhoolock:
The rediscovery of a N. nasutus population has provided
Ahsan, 1995; H. lar: Sommer & Reichard, 2000), however,
furtheropportunitytostudytheevolutionofpolygynyingibbons.
noneofthesegroupshaveremainedstableformorethantwo
This population lives in a degraded karst forest patch (Fan
years.
et al., 2011a), which is distinct from the habitat of any other
Gibbon groups with more than one adult female were first
gibbonpopulation. Mostgroupsinthispopulationincludetwo
reportedinN.hainanusinDelacour’sbookOntheIndochinese
adultfemales. Fanetal. (2015)documentedthatN.nasutus
gibbon (Xu et al., 1983), and later in N. concolor from Mt.
benefitsfromlivinginlargergroupsbecausethesegroupscan
Wuliang by Haimoff et al. (1986, 1987). Sheeran (1993) did
invade the home range of smaller gibbon groups and access
not observe any multi-adult female groups in Mt. Wuliang or
morenon-figfruit,thoughlargergroupsalsospendmoretime
Mt. Ailao; based on brief observations in the same areas,
traveling. Female cooperation to evict unmated females has
Bleisch&Chen(1991)reportedthatsomeN.concolor groups
also been observed in this population but no group consisted
includedtwofemaleswhoduettedwiththeadultmale,though
ofmorethantwobreedingfemales,suggestingthatterritories
they argued that this could be a sub-adult daughter singing
defendedbyamalecouldnotsupportathirdfemale(Fanetal.,
with her mother. For a clear demonstration of polygyny,
2015).
close observation of groups with two or more females (with
Long-term population monitoring can provide insight to
young sired by the same male) is required (Bleisch & Chen,
better understand the sociality of northern gibbons. Although
1991). Jiang et al. (1994a, 1999) suggested that the groups
floatingmalesinN.concolor populationshavebeenobserved
they observed were polygynous because the two females
regularly at Dazhaizi (Fan et al., unpublished data), females
presented with offspring of the same body size. They thus
in the polygynous groups do not disperse and form new
proposed several models to explain the evolution of polygyny
groups with these floating males. Two newly formed N.
in N. concolor. First, the large home range occupied by N.
nasutus groups at Bangliang consisted of two adult females
concolor and N. hainanus might provide sufficient space for
(Wei et al., 2017; Shao-Gan Wei, personal communication),
more individuals in one group. Second, mutual tolerance
though solitary males were observed frequently (Fan et al.,
of females or “weak territoriality in females” might facilitate
2010, 2015). Similar results have been reported from a
polygyny. Third, phylogeny might play a role in the evolution
smallpopulationofN.hainanus;althoughsolitarymaleswere
of polygyny in Nomascus gibbons. They also argued that
observedlivinginthesite,oneofthetwonewlyformedgroups
N. concolor has a relatively large semi-pendulous scrotum
consistedoftwofemales(Bryantetal.,2016;Dengetal.,2017).
(Groves,1972),whichshouldpromotehigherspermproduction
Theseresultsrejectthehypothesesthatfemalesareforcedto
and, consequently, support a higher level of sexual activity.
liveintheirnatalgroupsbydelayeddispersalorareforcedto
However, the above findings raise questions of why and how
immigrate into monogamous groups because suitable habitat
thesegibbonsoccupyalargehomerangeandfemalestolerate
andmatesarenotavailable(Bleisch&Chen,1991; Liuetal.,
each other. These questions remained unanswered at the
1989).Consequently,Fanetal.(2015)proposedthatpolygyny
time as no gibbon groups had been habituated for detailed
isanevolutionarilystablematingsystemincertainhabitatsand
behavioralobservation.
forsomespecies.
In2006, Fanetal. (2006)reportedthatallfivegroupsina
To secure their resource requirements, northern gibbons
small subpopulation of N. concolor at Dazhaizi, Mt. Wuliang,
need to maintain a large territory in their heterogeneous
included two adult females who gave birth or carried infants
habitats (Liu et al., 1989; Fan & Jiang, 2008, 2010b; Zhang
during the two-year research period. However, females in
et al., 2014). Within each territory, important food species
the same group bred at different times, perhaps to reduce
occurinlargepatches,whichcanprovideadequatefoodfortwo
reproductive competition. During the study, the researchers
breedingfemalesandtheiroffspring, butperhapsnotenough
habituatedonegroupandwerethefirsttodocumentthesocial
ZoologicalResearch39(4):255–265,2017 259
for three females (Fan & Jiang, 2008; Fan et al., 2015). The Figure2).Southerngibbonsliveinmorehomogenoushabitats

ability to digest substantial amounts of leaves in response to (e.g., S. syndactylus: Chivers, 1974; H. lar: Bartlett, 2009;
fruit scarcity (Fan et al., 2009a, 2012) enables these gibbons Brockelman et al., 2014), with smaller home ranges (Bartlett,
to minimize feeding competition within groups when fruit is 2011). Although they utilize large fruit trees (Bartlett, 2009),
not available and forage in large polygynous groups. Adult intensive interspecific competition depletes food resources,
Nomascus males have a large scrotum and females in the which may promote within-group competition (Marshall et al.,
samegroupbreedatdifferenttimes(N.hainanus: Zhouetal., 2009)(PathIIinFigure2).Thatdoesnotmeanfoodpatchsize
2008; N. concolor: Huang et al., 2013), which both reduce inthetropicalgibbonhabitatisphysicallysmallerthanthatfor
reproductive competition and enables polygyny (Path I in northerngibbons,butthatonaverage,foodavailabilityisless.

Figure2Arevisedmodelfortheevolutionofgibbonsocialandmatingsystems,integratingfooddistribution,patchsize,gibbon
Figure 2 A revised model for the evolution of gibbon social and mating systems,
digestibilityanddiet,inter-speciesfoodcompetitionandreproductivebehaviorinthemodel
integrating food distribution, patch size, gibbon digestibility and diet, inter-
Males benefit from forming polygynous groups through Nomascus species (reviewed above), but no stable group of
increasedmatingopportunities(N.hainanus:Zhouetal.,2008; more than one adult breeding female has been reported. A
sNp.ceonccioelosr: fHouoandg ectoalm.,2p01e3t;iNt.inoansu tausn: dFa nreetpalr.,o20d1u5)c. tivepo bsseibhlearevaisoonr iisnth taht feoo md poatdchesli z e in the habitat of H.
The cooperative female relationships documented above (N. tianxing is smaller than that of Nomascus species (Path III in
concolor: Fan et al., 2006; Fan & Jiang, 2010a; Guan et al., Figure2).Giventhatstablepolygynousgroupshaveonlybeen
2013; N. nasutus: Fan et al., 2015) suggest that females in reported from Nomascus species living in different habitats,
polygynous groups also benefit from larger group sizes. The phylogeny may also play an important role in the evolution of
potential benefits to females include resource access from polygyny in gibbons (Bryant et al., 2015; Di Fiore & Rendall,
successful intergroup encounters (Fan & Jiang, 2010a; Fan 1994;Jiangetal.,1999).
et al., 2015). Resident females in the same group appear to
FUTURERESEARCHDIRECTIONS
producesimilar-agedoffspring. Aftermaturing,theseoffspring
candispersetogether,whichmightincreasetheirsurvivalrate
Standardizedmethods
andprobabilityofestablishingtheirownterritory(Fan&Jiang,
Comparative research using the same or similar methods will
2010a; Fan et al., 2015). In addition, females might benefit
be extremely useful for understanding gibbon ecology and
fromimprovedinclusivefitnessiffemalesbornwithinthesame
social system evolution. First, the same methods should
group disperse together (Fan et al., 2015). Even if females
be applied to quantify forest structure, plant abundance and
do not obtain any direct or indirect benefits from polygyny,
distribution, and food availability (Vogel & Janson, 2011).
bi-femalegroups could formif thecost ofevicting thesecond
Second, the same or similar behavioral definitions and
femaleexceedsthecostoftolerance(Fan&Jiang,2010a;Fan
methodologies should be used to record behavior. For
etal.,2015).
example, several researchers distinguished foraging as “the
WeneedtonotethatH.tianxing livinginnorthernmontane
group moved slowly, spread out over a broad front, feeding
forest shares many similarities in ecology with the three
briefly from many of the trees as they passed through them”
260 www.zoores.ac.cn
fromafeedingboutwhenallgroupmembersfedinthesame Arenortherngibbonsadaptedtodigestingleaves?
tree at the same time. Kappeler (1981) and Ahsan (2001) Northerngibbonseatmoreleavesthandotropicalgibbons(but
recorded foraging, but other researchers did not separate see S. syndactylus in Bartlett, 2011, Table 17.2). However,
foraging from feeding (Bartlett, 2009; Fan et al., 2008, 2012, how they resolve the chemical and mechanical challenges
2013;McConkey&Brockelman,2011). Palombit(1997)used associatedwithleafeating(Lambert,1998),especiallyduring
focal animal observations to record behavior, whereas other cold winters with reduced or no fruit, remains unclear. Thus,
researchershaveusedscansampling(Ahsan,2001; Chivers, comparativeresearchontheirdigestionsystem,includingtheir
1974; Fan et al., 2008, 2012, 2013; Gittins, 1982; Lappan, microbiome,willhelpclarifytheirecologyandsocialsystems.
2007a). Even for researchers using scan sampling, scan
Kinshipamongfemales
intervals often differ (e.g., 5 min: Bartlett, 2009; Fan et al.,
Female kinship may be a factor affecting social relationships
2008,2012,2013;10min: Ahsan,2001;Gittins,1982;30min:
(Clutton-Brock & Lukas, 2012). Females living in polygynous
McConkey & Brockelman, 2011). Furthermore, comparisons
groups may benefit through inclusive fitness if they are kin,
would be strengthened if researchers used the same method
and is highly possible due to the previous observation of two
to analyze data. Although most researchers present diet and
N. nasutus females dispersing together (Fan et al., 2010).
time budget results as percentages (Ahsan, 2001; Bartlett,
However,asitisdifficulttoobservegroupformationorfemale
2009; Fan et al., 2008, 2009a; Gittins, 1982; McConkey &
displacement in the wild (Brockelman et al., 1998), the use
Brockelman,2011),Fanetal. (2012,2013)usedtimedevoted
of non-invasive genetic methods may help determine kin
to different activities and food categories because active time
relationshipsamongfemales(Lappan,2007b).
showedconsiderabledisparityasaconsequenceofvariations
in day length at high latitude areas. It would strengthen Howdonortherngibbonsfindfoodwithintheirlargehome
the ability to compare results if all authors published their ranges?
data as both percentages and actual times for both diet and Donortherngibbonsusespatialmemorytofindfoodresources
time budgets. Finally, altitudinal range must be considered in the same manner as tropical gibbons (Brockelman et al.,
when calculating home range size and daily travel length 2014)? In northern habitats, gibbons appear to prefer ripe
because both variables can be impacted at steep study sites fruit pulp (Fan et al., 2009a, 2013). Scarce but predictable
(Monterrosoetal.,2013). food resources led to the development of the “ecological
intelligence hypothesis” (Milton etal., 1981), that is, primates,
Howdonortherngibbonsdefendtheirlargehomerange?
such as great apes, which rely on ephemeral and scattered
Gibbons are territorial and regularly and aggressively defend
fruitsneedlargerrangesandhaveevolvedadvancedcognitive
theirhomerange,whichisthoughttoenableexclusiveaccess
capacities that facilitate optimal food finding strategies. Does
to a feeding territory (Bartlett, 2009; Brockelman, 2009).
the “ecological intelligence hypothesis” explain the foraging
Northern gibbons occupy home ranges several times larger
behaviorofgibbons? Long-termcomparativeresearchacross
than those of tropical gibbons (N. concolor: Fan & Jiang,
gibbon species and between gibbons and large-bodied apes
2008; N. nasutus: Fei et al., 2012). However, they do
will help elucidate northern gibbon foraging behavior in their
not travel any longer than gibbons that occupy smaller home
largerhomeranges.
ranges.Gibbonsusetheirloudmorningsingingtodefendtheir
territories. However,northerngibbonsdonotincreasesinging Comparisonbetweenforagingbehavior
to defend their larger home ranges (Fan et al., 2009b; Yin et Given the different interspecies food competition at different
al.,2016). Infact,hoolockgibbongroupsappeartodecrease sites, tree diameter at breast height (DBH) or crown size
theirsinginginareaswithlowgroupdensity(Yinetal.,2016). may not be accurate indicators of food availability. We highly
Therefore,thewayinwhichnortherngibbonsdefendtheirlarge recommendusingfeedingpartysize,feedingboutlength,and
territoriesstillrequiresfurtherinvestigation. number of feeding patches visited as indices to represent
foodavailability,especiallyasgibbonsoftendepletetheirfood
Socialrelationshipingroupswithdifferentsocialsystems
patches.However,thisprerequisiteneedscarefulinvestigation.
Intragroup social behavior in gibbons has received little
Iftheseindicesarevalidated,thendetailedcomparisonamong
attention (Bartlett, 2011). From the limited information
the foraging behaviors of gibbons living in different social
available, maleshavebeenobservedgroomingfemalesmore
systemscanbemade.
often than the reverse in the monogamous groups of S.
syndactylus (Chivers,1974; Palombit,1996),H.lar (Palombit, Lifehistoryandculturalbehavior
1996), and H. hoolock (Ahsan, 2001). Guan et al. (2013) Gibbonsborninpolygynousgroupsmaydevelopbettersocial
studied the grooming patterns of two polygynous groups of skills for maintaining relationships due to their interactions
N. concolor and found that females groomed males more with more social partners while growing up. Therefore,
often than the reverse, a pattern also observed in other ontogenymayalsoplayaroleinthemaintenanceofpolygyny.
polygynousprimates(Ahsan,2001).Studyingintragroupsocial Femalegorillasfamiliarfromimmaturityusuallyexhibitfriendly
relationships in populations with different social systems will relationships in adulthood (Harcourt, 1979). Studying the
help to better understand the evolution and maintenance of development of social relationships in gibbons is difficult
socialsystemsingibbons. because of their long lifespans, and thus longitudinal data is
ZoologicalResearch39(4):255–265,2017 261
required to answer the above question. Only with long-term pair formation and social structure in gibbons (Hylobates lar). Behavioral
study and the accumulation of data can we reveal unusual EcologyandSociobiology,42(5):329–339.
observations,suchas“dance”(Fanetal.,2016)and“juggling”
BrockelmanWY.2009.Ecologyandthesocialsystemofgibbons.In:Lappan
behaviors(Deng&Zhou,2016). Currentevidenceimpliesthat
S,WhittakerDJ.TheGibbons:NewPerspectivesonSmallApeSocioecology
thereisagreatdealmoretolearnaboutgibbonspecies,and
andPopulationBiology.NewYork:Springer,211–239.
a wide variety of behavior remains to be explored in future
Brockelman WY, Nathalang A, Greenberg DB, Suwanvecho U. 2014.
studies.
Evolutionofsmall-groupterritorialityingibbons.In:YamagiwaJ,Karczmarski
COMPETINGINTERESTS L.PrimatesandCetaceans: FieldResearchandConservationofComplex
MammalianSocieties.Tokyo:Springer,335–344.
Theauthorsdeclarethattheyhavenocompetinginterests. Bryant JV, Olson VA, Chatterjee HJ, Turvey ST. 2015. Identifying
environmental versus phylogenetic correlates of behavioural ecology in
AUTHORS’CONTRIBUTIONS
gibbons:implicationsforconservationmanagementoftheworld’srarestape.
F.P.F.designedthestudy. F.P.F., C.Y.M., andH.L.F.conductedfieldstudy BMCEvolutionaryBiology,15:171.
onNomascusnasutus andHoolocktianxing, F.P.F., Z.H.G., B.H., W.H.N., BryantJV,BruléA,WongMHG,HongXJ,ZhouZL,HanWT,JeffreeTE,
andQ.Y.N.conductedfieldstudyonN.concolor. F.P.F.andZ.H.G.wrote TurveyST.2016.DetectionofanewHainangibbon(Nomascushainanus)
themanuscriptandmadethefiguresandtableswithotherauthors’input. group using acoustic call playback. International Journal of Primatology,
X.L.J.helprevisedthemanuscript. Allauthorsreadandapprovedthefinal 37(4–5):534–547.
manuscript.
ChanBPL,TanXF,TanWJ.2008.Rediscoveryofthecriticallyendangered
easternblackcrestedgibbonNomascusnasutus(Hylobatidae)inChina,with
ACKNOWLEDGEMENTS
preliminarynotesonpopulationsize,ecologyandconservationstatus.Asian
We gratefully acknowledge all nature reserves and forestry bureaus for PrimatesJournal,1:17–25.
allowing our long-term gibbon research. We are also thankful to our ChenN.1995.EcologyoftheBlackCrestedGibbon(Hylobatesconcolor)
colleagues, nature reserve staff, and rangers who joined our research or intheAilaoMt.Reserve,Yunnan,China.MasterThesis.MahidolUniversity,
surveyteams.WethankMs.Xiao-NaLiforherhelpinconstructingthemap.
Bangkok,Thailand.
Chivers DJ. 1974. The Siamang in Malaya: a field study of a primate in
REFERENCES
tropicalrainforest.ContributionstoPrimatology,4:1–335.
Ahsan F. 1995. Fighting between two females for a male in the hoolock Chivers DJ. 1984. Feeding and ranging in gibbons: a summary. In:
gibbon.InternationalJournalofPrimatology,16(5):731–737. Preuschoft H, Chivers DJ, Brockelman WY, Creel N. The Lesser Apes:
AhsanMF.2001.Socio-ecologyofthehoolockgibbon(Hylobateshoolock) Evolutionary and Behavioural Biology. Edinburgh: Edinburgh University
in two forests of Bangladesh. In: Chicago Zoological Society. The Apes: Press,267–281.
Challenges for the 21st Century. Brookfield, Illinois: Chicago Zoological Clutton-Brock TH, Lukas D. 2012. The evolution of social philopatry and
Society,286–299. dispersalinfemalemammals.MolecularEcology,21(3):472–492.
Bartlett TQ. 2003. Intragroup and intergroup social interactions in DengHQ,ZhouJ.2016.“Juggling”BehaviorinwildHainangibbons,anew
white-handedgibbons.InternationalJournalofPrimatology,24(2):239–259. findinginnonhumanprimates.ScientificReports,6:23566.
Bartlett TQ. 2009. Seasonal home range use and defendability in DengHQ,ZhangMX,ZhouJ.2017.Recoveryofthecriticallyendangered
white-handedgibbons(Hylobateslar)inKhaoYaiNationalPark,Thailand. hainangibbonNomascushainanus.Oryx,51(1):161–165.
In:LappanS,WhittakerDJ.TheGibbons:NewPerspectivesonSmallApe DiFioreA,RendallD.1994.Evolutionofsocialorganization: areappraisal
SocioecologyandPopulationBiology.NewYork:Springer,265–275. for primates by using phylogenetic methods. Proceedings of the National
BartlettTQ.2011.TheHylobatidae: smallapesofAsia.In: CampbellCJ, AcademyofSciencesoftheUnitedStatesofAmerica,91(21):9941–9945.
FuentesA,MacKinnonKC,BearderSK,StumpfRM.PrimatesinPerspective. Fan PF, Jiang XL, Liu CM, Luo WS. 2006. Polygynous mating system
2nded.NewYork:OxfordUniversityPress,300–312. and behavioural reason of black crested gibbon (Nomascus concolor
Bicca-MarquesJC,Calegaro-MarquesC.1998.Behavioralthermoregulation jingdongensis) at Dazhaizi, Mt. Wuliang, Yunnan, China. Zoological
in a sexually and developmentally dichromatic neotropical primate, the Research,27(2):216–220.
black-and-gold howling monkey (Alouatta caraya). American Journal of FanPF,JiangXL.2008.Effectsoffoodandtopographyonrangingbehavior
PhysicalAnthropology,106(4):533–546. of black crested gibbon (Nomascus concolor jingdongensis) in Wuliang
Bleisch WV, Chen N. 1991. Ecology and behavior of wild black-crested Mountain,Yunnan,China.AmericanJournalofPrimatology,70(9):871–878.
gibbons(Hylobatesconcolor)inChinawithareconsiderationofevidence FanPF,NiQY,SunGZ,HuangB,JiangXL.2008.SeasonalVariationsinthe
forpolygyny.Primates,32(4):539–548. ActivityBudgetofNomascusconcolorjingdongensisatMt.Wuliang,Central
Borries C, Savini T, Koenig A. 2011. Social monogamy and the threat of Yunnan, China: Effects of Diet and Temperature. International Journal of
infanticideinlargermammals.BehavioralEcologyandSociobiology,65(4): Primatology,29:1047–1057.
685–693. Fan PF, Jiang XL. 2009. Predation on giant flying squirrels (Petaurista
BrockelmanWY,ReichardU,TreesuconU,RaemaekersJJ.1998.Dispersal, philippensis)byblackcrestedgibbons(Nomascusconcolorjingdongensis)
262 www.zoores.ac.cn
atMt.Wuliang,Yunnan,China.Primates,50(1):45–49. statusoftheHainangibbon(Nomascushainanus): progressofpopulation
FanPF,NiQY,SunGZ,HuangB,JiangXL.2009a.Gibbonsunderseasonal monitoringandotherpriorityactions.AsianPrimatesJournal,1(1):2–9.
stress: the diet of the black crested gibbon (Nomascus concolor) on Mt. Geissmann T. 2002. Duet-splitting and the evolution of gibbon songs.
Wuliang,CentralYunnan,China.Primates,50(1):37–44. BiologicalReviews,77(1):57–76.
Fan PF, Xiao W, Huo S, Jiang XL. 2009b. Singing behavior and singing Gittins SP. 1982. Feeding and ranging in the agile gibbon. Folia
functions of black-crested gibbons (Nomascus concolor jingdongensis) at Primatologica,38(1–2):39–71.
Mt.Wuliang,CentralYunnan,China.AmericanJournalofPrimatology,71(7): Groves CP. 1967. Geographic variation in the hoolock or white-browed
539–547. gibbon (Hylobates hoolock Harlan 1834). Folia Primatologica, 7(3–4):
FanPF,JiangXL.2010a.Maintenanceofmultifemalesocialorganization 276–283.
in a group of Nomascus concolor at Wuliang Mountain, Yunnan, China. Groves CP. 1972. Systematics and phylogeny of gibbons. In: Rumbaugh
InternationalJournalofPrimatology,31(1):1–13. DM. Gibbon and Siamang: Evolution, Ecology, Behavior, and Captive
Fan PF, Jiang XL. 2010b. Altitudinal ranging of black-crested gibbons at Maintenance.Basel:Karger,1–89.
Mt.Wuliang,Yunnan: effectsoffooddistribution,temperatureandhuman GrueterCC,JiangXL,KonradR,FanPF,GuanZH,GeissmannT.2009.Are
disturbance.FoliaPrimatologica,81(1):1–9. Hylobateslar ExtirpatedfromChina? InternationalJournalofPrimatology,
FanPF,FeiHL,XiangZF,ZhangW,MaCY,HuangT.2010.Socialstructure 30(4):553–567.
andgroupdynamicsoftheCaoVitgibbon(Nomascusnasutus)inBangliang, Guan ZH, Huang B, Ning WH, Ni QY, Sun GZ, Jiang XL. 2013.
Jingxi,China.FoliaPrimatologica,81(5):245–253. Significanceofgroomingbehaviorintwopolygynousgroupsofwesternblack
FanPF,FeiHL,ScottMB,ZhangW,MaCY.2011a.Habitatandfoodchoice crestedgibbons: implicationsforunderstandingsocialrelationshipsamong
ofthecriticallyendangeredCaoVitgibbon(Nomascusnasutus)inChina: immigrantandresidentgroupmembers.AmericanJournalofPrimatology,
implicationsforconservation.BiologicalConservation,144(9):2247–2254. 75(12):1165–1173.
Fan PF, Xiao W, Huo S, Ai HS, Wang TC, Lin RT. 2011b. Distribution Haimoff EH, Yang XJ, He SJ, Chen N. 1986. Census and survey of wild
andconservationstatusoftheVulnerableeasternhoolockgibbonHoolock black-crested gibbons (Hylobates concolor concolor) in Yunnan Province,
leuconedysinChina.Oryx,45(1):129–134. People’sRepublicofChina.FoliaPrimatologica,46(4):205–214.
FanPF.2012.TaxonomyandconservationstatusofgibbonsinChina.Acta Haimoff EH, Yang XJ, He SJ, Chen N. 1987. Conservation of gibbons in
TheriologicaSinica,32(3):248–258.(inChinese) YunnanProvince,China.Oryx,21(3):168–173.
Fan PF, Fei HL, Ma CY. 2012. Behavioral responses of Cao Vit gibbon Hanya G, Aiba SI. 2010. Fruit fall in tropical and temperate forests:
(Nomascus nasutus) to variations in food abundance and temperature in implicationsforfrugivorediversity.EcologicalResearch,25(6):1081–1090.
Bangliang,Jingxi,China.AmericanJournalofPrimatology,74(7):632–641. Harcourt AH. 1979. Social relationships between adult male and female
FanPF,AiHS,FeiHL,ZhangD,YuanSD.2013.Seasonalvariationofdiet mountaingorillasinthewild.AnimalBehaviour,27:325–342.
andtimebudgetofEasternhoolockgibbons(Hoolockleuconedys)livingin HuY,XuHW,YangDH.1990.Feedingecologyofthewhite-cheekgibbon
anorthernmontaneforest.Primates,54(2):137–146. (Hylobatesconcolorleucogenys).ActaEcologicaSinica,10(2):155–159.(in
Fan PF, Fei HL, Luo AD. 2014. Ecological extinction of the Critically Chinese)
Endangerednorthernwhite-cheekedgibbonNomascusleucogenysinChina. HuangB,GuanZH,NiQY,OrkinJD,FanPF,JiangXL.2013.Observation
Oryx,48(1):52–55. of intra-group and extra-group copulation and reproductive characters in
FanPF,BartlettTQ,FeiHL,MaCY,ZhangW.2015.Understandingstable freeranginggroupsofwesternblackcrestedgibbon(Nomascusconcolor
bi-femalegroupingingibbons:feedingcompetitionandreproductivesuccess. jingdongensis).IntegrativeZoology,8(4):427–440.
FrontiersinZoology,12:5. IUCN.2017.TheIUCNRedListofThreatenedSpecies.Version2017-2.Red
Fan PF, Ma CY, Garber PA, Zhang W, Fei HL, Xiao W. 2016. Rhythmic List,<http://www.iucnredlist.org>.Downloadedon05December2018.
displaysoffemalegibbonsofferinsightintotheoriginofdance.Scientific Jiang XL, Ma SL, Wang YX, Shreeran LK, Poirier FE, Wang Q. 1994a.
Reports,6:34606. The mating system of black-crested gibbon (Hylobates concolor) and its
FanPF.2017.Thepast,present,andfutureofgibbonsinChina.Biological relationships with ecology, behavior and phylogeny. Acta Anthropologica
Conservation,210:29–39. Sinica,13(4):344–352.(inChinese)
FanPF,HeK,ChenX,OrtizA,ZhangB,ZhaoC,LiYQ,ZhangHB,Kimock Jiang XL, Ma SL, Wang YX, Shreeran LK, Poirier FE, Wang Q. 1994b.
C,WangWZ,GrovesC,TurveyST,RoosC,HelgenKM,JiangXL.2017. Groupsizeandcompositionofblack-crestedgibbons(Hylobatesconcolor).
Description of a new species of Hoolock gibbon (Primates: Hylobatidae) ZoologicalResearch,15(2):15–22.(inChinese)
based on integrative taxonomy. American Journal of Primatology, 79(5): Jiang XL, Wang YX. 1999. Population and conservation of black crested
e22631. gibbons (Hylobates concolor jingdongensis) in Wuliang Nature Reserve,
FeiHL,ScottMB,ZhangW,MaCY,XiangZF,FanPF.2012.Sleepingtree Jingdong,Yunnan.ZoologicalResearch,20(6):421–425.
selection of Cao Vit gibbon (Nomascus nasutus) living in degraded karst JiangXL,WangYX,WangQ.1999.Coexistenceofmonogamyandpolygyny
forestinBangliang,Jingxi,China.AmericanJournalofPrimatology,74(11): inblack-crestedgibbon(Hylobatesconcolor).Primates,40(4):607–611.
998–1005. JiangXL,LuoZH,ZhaoSY,LiRZ,LiuCM.2006.Statusanddistribution
FellowesJR,LokCBP,ZhouJ,ChenSH,YangSB,ChitNS.2008.Current pattern of black crested gibbon (Nomascus concolor jingdongensis) in
ZoologicalResearch39(4):255–265,2017 263
WuliangMountains,Yunnan,China: implicationforconservation.Primates, PalombitRA.1996.Pairbondsinmonogamousapes: acomparisonofthe
47(3):264–271. siamangHylobatessyndactylusandthewhite-handedgibbonHylobateslar.
KappelerM.1981.TheJavanSilveryGibbon(Hylobateslar moloch).Ph.D. Behaviour,133(5):321–356.
dissertation,UniversitätBasel,Basel,Switzerland. PalombitRA.1997.Inter-andintraspecificvariationinthedietsofsympatric
KappelerPM,BarrettL,BlumsteinDT,Clutton-BrockTH.2013.Constraints siamang (Hylobates syndactylus) and lar gibbons (Hylobates lar). Folia
and flexibility in mammalian social behaviour: introduction and synthesis. Primatologica,68(6):321–337.
Philosophical Transactions of the Royal Society B: Biological Sciences, PalombitRA.1999.InfanticideandtheEvolutionofPairBondsinNonhuman
368(1618):20120337. Primates.EvolutionaryAnthropology,7(4):117–129.
Lambert JE. 1998. Primate digestion: interactions among anatomy, QuanGQ,WangS,ZhangRZ.1981.Ontherecentstatusandconservation
physiology,andfeedingecology.EvolutionaryAnthropology,7(1):8–20. ofprimatesinChina.ActaTheriologicaSinica,1(1):99–104.(inChinese)
LanDY.1993.Feedingandvocalbehavioursofblackgibbons(Hylobates Raemaekers JJ. 1978. Competition for food between lesser apes. In:
concolor) in Yunnan: a preliminary study. Folia Primatologica, 60(1–2): ChiversDJ,HerbertJ.Recentadvancesinprimatology:Behaviour.London:
94–105. AcademicPress,327–330.
LappanS.2007a.Socialrelationshipsamongmalesinmultimalesiamang SheeranLK.1993.Apreliminarystudyofthebehaviorandsocio-ecologyof
groups.InternationalJournalofPrimatology,28(2):369–387. blackgibbons(Hylobatesconcolor)inYunnanProvince,People’sRepublic
Lappan S. 2007b. Patterns of dispersal in Sumatran siamangs ofChina.Ph.D.thesis,TheOhioStateUniversity,AnnArbor,Mich,USA.
(Symphalangus syndactylus): preliminary mtDNA evidence suggests SommerV,ReichardU.2000.Rethinkingmonogamy: thegibboncase.In:
more frequent male than female dispersal to adjacent groups. American KappelerPM.PrimateMales: CausesandConsequencesofVariationin
JournalofPrimatology,69(6):692–698. GroupComposition.Cambridge:CambridgeUniversityPress,159–168.
Lappan S. 2008. Male care of infants in a siamang (Symphalangus Srikosamatara S, Brockelman WY. 1987. Polygyny in a group of pileated
syndactylus) population including socially monogamous and polyandrous gibbons via a familial route. International Journal of Primatology, 8(4):
groups.BehavioralEcologyandSociobiology,62(8):1307–1317. 389–393.
Leighton DR. 1987. Gibbons: territoriality and monogamy. In: Smuts B, SunGZ,FanPF,NiQY,FangJL,JiangXL.2007.Habitatstructureofblack
Cheney D, Seyfarth R, Wrangham R, Struhsaker T. Primate Societies. crestedgibbons(Nomascusconcolor)inPinghe,AilaoMountains,Yunnan.
Chicago:ChicagoUniversityPress,135–145. ZoologicalResearch,28(4):374–382.(inChinese)
Li GS, Yang XM, Zhang HY, Li W. 2011. Population and distribution of Tan B. 1985. The status of primates in China. Primate Conservation, 5:
western black crested gibbon (Nomascus concolor) at Ailao mountain, 63–81.
Xinping,yunnan.ZoologicalResearch,32(6):675–683.(inChinese) TerborghJ.1983.FiveNewWorldPrimates:AStudyinComparativeEcology.
LiuZH,ZhangYZ,JiangHS,SouthwickC.1989.Populationstructureof Princeton:PrincetonUniversityPress.
HylobatesconcolorinBawanglinNatureReserve,Hainan,China.American Thinh VN, Mootnick AR, Geissmann T, Li M, Ziegler T, Agil M, Moisson
JournalofPrimatology,19(4):247–254. P,NadlerT,WalterL,RoosC.2010a.Mitochondrialevidenceformultiple
MarshallAJ,CannonCH,LeightonM.2009.Competitionandnicheoverlap radiations in the evolutionary history of small apes. BMC Evolutionary
betweengibbons(Hylobatesalbibarbis)andotherfrugivorousvertebratesin Biology,10:74.
GunungPalungNationalPark,WestKalimantan,Indonesia.In: LappanS, ThinhVN,MootnickAR,ThanhVN,NadlerT,RoosC.2010b.Anewspecies
WhittakerDJ.TheGibbons: NewPerspectivesonSmallApeSocioecology ofcrestedgibbon,fromthecentralAnnamitemountainrange.Vietnamese
andPopulationBiology.NewYork:Springer,161–188. JournalofPrimatology,1(4):1–12.
McConkey KR, Brockelman WY. 2011. Nonredundancy in the dispersal Tian CC, Zhou SB, Jiang XL. 2006. Distribution pattern and dynamics of
networkofageneralisttropicalforesttree.Ecology,92(7):1492–1502. Alnus nepalensis and Litsea glutinosa populations in Nomascus concolor
MiltonK.1981.Distributionpatternsoftropicalplantfoodsasanevolutionary habitat.ChineseJournalofAppliedEcology,17(2):167–170.(inChinese)
stimulus to primate mental development. American Anthropologist, 83(3): TingS,HartleyS,BurnsKC.2008.Globalpatternsinfruitingseasons.Global
534–548. EcologyandBiogeography,17(5):648–657.
Mitani JC. 1985. Gibbon song duets and intergroup spacing. Behaviour, Turvey ST, Crees JJ, Di Fonzo MMI. 2015. Historical data as a baseline
92(1):59–96. for conservation: reconstructing long-term faunal extinction dynamics in
MonterrosoP,SilleroN,RosalinoLM,LoureiroF,AlvesPC.2013.Estimating LateImperial-modernChina.ProceedingsoftheRoyalSocietyB:Biological
home-rangesize:whentoincludeathirddimension?EcologyandEvolution, Sciences,282(1813):20151299.
3(7):2285–2295. vanSchaikCP,KappelerPM.2003.Theevolutionofsocialmonogamyin
NakayamaT,HoriT,NagasakaT,TokuraH,TadakiE.1971.Thermaland primates.In:ReichardUH,ChristopheB.Monogamy:MatingStrategiesand
metabolicresponsesintheJapanesemonkeyattemperaturesof5-38◦C. PartnershipsinBirds,HumansandotherMammals.Cambridge:Cambridge
JournalofAppliedPhysiology,31(3):332–337. UniversityPress,59–80.
OpieC,AtkinsonQD,DunbarRIM,ShultzS.2013.Maleinfanticideleads Vogel E, Janson CH. 2011. Quantifying primate food distribution and
tosocialmonogamyinprimates.ProceedingsoftheNationalAcademyof abundance for socioecological studies: an objective consumer-centered
SciencesoftheUnitedStatesofAmerica,110(33):13328–13332. method.InternationalJournalofPrimatology,32(3):737–754.
264 www.zoores.ac.cn