Variations in diet composition of sympatric Trachypithecus francoisi and Macaca assamensis in the limestone habitats of Nonggang, China

2018·3.5 MB·

by  Zhou, Qi-Hai

ZOOLOGICAL RESEARCH
Variations in diet composition of sympatric
Trachypithecus francoisi and Macaca assamensis in
the limestone habitats of Nonggang, China
Qi-HaiZhou1,*,Zhong-HaoHuang1,HuaWei1,Cheng-MingHuang1,2,*
1KeyLaboratoryofEcologyofRareandEndangeredSpeciesandEnvironmentalProtection,MinistryofEducation;GuangxiKeyLaboratory
ofRareandEndangeredAnimalEcology,GuangxiNormalUniversity,GuilinGuangxi541004,China
2KeyLaboratoryofAnimalEcologyandConservationBiology,InstituteofZoology,ChineseAcademyofSciences,Beijing100101,China
ABSTRACT principal determining factors (Hadi et al., 2012; Nadjafzadeh
Comparative studies of sympatric species are & Heymann, 2008; Porter, 2001; Powzyk & Mowry, 2003;
Singh et al., 2011; Tomblin & Cradford, 1994). For example,
essentialforunderstandingbehavioralandecological
inthePeleonanforestofSumatra, Presbytispotenziani feeds
adaptation as well as the mechanisms that can
moreselectivelyonfruits,whereassympatricSimiasconcolor
reduce resource competition to allow coexistence. feedspredominantlyonleaves(Hadietal.,2012). Inaddition,
François’ langurs (Trachypithecus francoisi) and sympatric primates can adopt different foraging strategies in
Assamese macaques (Macaca assamensis) are responsetotemporalchangesinfoodresources(Dammhahn
& Kappeler, 2008; Porter, 2001; Standford, 2006; Thorén et
sympatric primate species found in the limestone
al., 2011; Tutin & Fernandez, 1993). For example, gorillas
seasonal rainforests of Nonggang Nature Reserve,
(Gorilla gorilla) in Lopé Reserve, Gabon, rely on non-fruit
southwestern Guangxi, China. To explore their
foods when succulent fruits are scarce in the dry season,
different adaptation strategies, we collected data on whereas sympatric chimpanzees (Pan troglodytes) continue
diet using scan sampling at 15-min intervals. Our to find and consume considerable quantities of fruit (Tutin &
resultsrevealedthatFrançois’langursshowedamore Fernandez,1993). Manyofthesevariationsreflectdifferences
in morphology, digestive physiology, and the temporal and
flexible diet composition than Assamese macaques.
spatial distribution of food resources (Hadi et al., 2012;
François’ langurs increased dietary diversity and
Nadjafzadeh&Heymann,2008;Powzyk&Mowry,2003),and
mature leaf consumption in response to seasonal
representecologicalnicheseparation,allowingthecoexistence
scarcityofpreferredyoungleavesandfruits,whereas ofsympatricprimates.
Assamesemacaquesreliedheavilyonyoungbamboo TheFrançois’langur(Trachypithecusfrancoisi)andAssamese
leaves (Indocalamus calcicolus) in most months.
These variations reflect the differences in digestive
Received: 24November2017;Accepted: 28March2018;Online: 03
physiology,morphology,andthetemporalandspatial
April2018
distributionoffoodresources.
Foundation items: This study was supported by the National Nature
Keywords: François’langurs;Assamesemacaques; Science Foundation of China (31670400, 31672285, 31660616),
Dietcomposition;Limestonehabitat
Guangxi Natural Science Foundation (2015GXNSFDA139013),
INTRODUCTION Key Laboratory of Ecology of Rare and Endangered Species and
EnvironmentalProtection, MinistryofEducation, China, andGuangxi
Comparative studies of sympatric species are essential for
Key Laboratory of Rare and Endangered Animal Ecology, Guangxi
understanding behavioral and ecological adaptations, as
NormalUniversity
well as the structure of animal communities (Fleagle et
al., 1999; Fleagle, 2013). Many studies have revealed *Corresponding authors, E-mail: [email protected];
considerable variation in foraging strategies among sympatric [email protected]
primate species, with food type documented as one of the DOI:10.24272/j.issn.2095-8137.2018.046
284 SciencePress ZoologicalResearch39(4):284–290,2018
macaque (Macaca assamensis) are sympatric species that inforagingstrategiescanexplaintheircoexistence.
reside on the limestone hills of southwestern Guangxi, China
(Zhang et al., 2002). Despite differences in morphology MATERIALSANDMETHODS
and digestive system (Chivers, 1994), previous studies have
Studysitesandsubjects
documented similar food habits between the two species,
with both found to be predominantly folivorous but with fruit This study was conducted from October 2005 to September
consumed when available (Ahsan, 1994; Chalise, 2003; Hu, 2006 in Nonggang Nature Reserve (E106◦42(cid:48)–E107◦4(cid:48),
2011; Zhou et al., 2006). Thus, these similarities imply N22◦13(cid:48)–N22◦33(cid:48), Figure 1), Guangxi Province, China. The
the possibility of food competition between the two species. reserve comprises three areas, Nonggang (5 426 hm2),
To date, however, no comparative studies have reported on Longhu (1 034 hm2), and Longshan (3 949 hm2), which are
the foraging strategies of sympatric François’ langurs and separated by farmland and villages. The reserve consists of
Assamese macaques, which is important for understanding limestone hills ranging from 400 m to 600 m a.s.l. (Guangxi
theircoexistencemechanisms. ForestDepartment,1993). Thevegetationischaracterizedby
In this paper, we compared the diet of François’ langurs limestoneseasonalrainforest. Annualprecipitationwas1373
andAssamesemacaqueslivingsympatricallyinthelimestone mm (October 2005–September 2006) and 952 mm (October
habitats of southwestern Guangxi, China. We aimed to: 2006–September 2007). There are two distinct seasons: a
(1) determine how food resources differ between them; (2) rainy season from April to September with >80 mm monthly
investigate how they adjust behavior in response to seasonal rainfallandadryseasonintheremainderoftheyearwith<80
changesinfoodresources;and(3)explorewhetherdifferences mmmonthlyrainfall(Zhouetal.,2007).
Daxin
N
County
Longhu
Wude
Longgang
Camp
Lenglei
Xiangshui
Nonggang
Longzhou
Shangjin
Xiaxiu
Guizhou Hunan
Longshan
Guangxi
Province
Yun
Guang
nan Longzhou dong Ningming County
County
Vietnam
Figure1MapofNonggangNatureReserveshowingthestudysiteandsurroundingarea
Our study site is found within the northwestern portion of females, two adult individuals of unidentified sex, and four
Nonggang (Figure 1). We selected one group of François’ juveniles.
langurs(n=9)andtwogroupsofAssamesemacaques(Group
1,n=15;Group2,n=12)whorangednearesttoourtemporary Ecologicalsampling
camp. Thehomerangesofthethreestudygroupsoverlapped We conducted vegetation surveys in the main study area at
witheachother. TheFrançois’langurgroupconsistedofone the onset of behavioral data collection. We used a stratified
adult male, five adult females, and three infants. Assamese randomsamplingmethodfortheplacementofvegetationplots.
macaque Group 1 consisted of two adult males, four adult We placed 13 plots (50 m×10 m) in the main study area,
females, four adult individuals of unidentified sex, and five including four in valley basins and nine on hillsides. The
juveniles,andGroup2consistedoftwoadultmales,fouradult plots covered most vegetation types described by Shu et al.
ZoologicalResearch39(4):284–290,2018 285
(1988).Withintheplots,alltreeswith≥5cmdiameteratbreast examine seasonal variations in the use of different food
height were tagged. In total, we monitored 312 trees from categories. We used Spearman rank correlations to test
30familiesatmonthlyintervals,andrecordedthepresenceof the relationship between the abundance and consumption
young leaves, fruits, and flowers. The relative abundance of of different plant parts. All tests were two-tailed, with a
different plant parts was expressed as a percentage of trees significancelevelof0.05.
bearing the plant parts of interest each month, regardless of
RESULTS
thesizeofthecanopy. Huangetal. (2010)describedmonthly
phenologychanges.
During the study period, we identified 92 plant species
Datacollection consumedbyFrançois’langursand69plantspeciesconsumed
by Assamese macaques. Major foods (accounting for >1%
WeconductedbehavioralobservationsoftheFrançois’langur
of total feeding records) contributed to a large proportion of
group for 126 d (7–22 d each month) and of the Assamese
the total diet (François’ langur: 80.6%; Assamese macaque:
macaquegroupsfor58d(3–9deachmonth). Eachday,data
85.2%, Table 1). However, the François’ langurs used more
collection began when the monkeys were first encountered,
plantspeciesasmajorfoodsthandidtheAssamesemacaques.
and ended when they disappeared or entered their sleeping
Annual diversity and evenness of use of major food plants
sites. We used scan sampling with 15-min intervals. Each
werehigherforFrançois’langurs(H=2.563,J=0.817)thanfor
scan lasted 5 min, followed by 10 min of inactivity until the
Assamesemacaques(H=1.164,J=0.468). Thisindicatedthat
next scan began. We recorded the activity of each individual
Assamesemacaquesconcentratedonfewerfoodspeciesthan
seen during each scan. We watched each individual for 5 s
François’langurs:thetop10foodspeciesaccountedfor82.8%
afterdetection.Thebehaviorsincludedfouractivitycategories:
of the Assamese macaque diet, but only for 54.3% of the
resting, moving, feeding, and social behavior (e.g., grooming
François’ langur diet. In particular, Indocalamus calcicolus, a
andplaying).Toavoidsamplingbiastowardcertainindividuals
smallbamboospecies,contributedto62%oftheannualdietof
oraparticularage-sexclass, wecollectedbehavioralrecords
Assamesemacaques.
onasmanydifferentindividualsaspossibleduringascanso
There was no significant difference in monthly number
that all individuals in the focal group were included, but we
of plant species eaten by François’ langurs and Assamese
sampled no individual more than once. When the individual
wasfeeding,werecordedplantspeciesandpartseaten,e.g., macaques (Z=−0.356, n=10, P=0.722, Figure 2). However,
inter-specific differences in seasonal dietary diversity in
youngleaf,matureleaf,fruit,flower,seed,orother(e.g.,petiole
responsetofoodavailabilitywereobserved. François’langurs
andstem). Duringthestudyperiod, atotalof8168behavior
consumed more plant species in the dry season than in
recordswereobtainedfrom3052scansamplesforFrançois’
the rainy season (U=4.000, n =6, n =6, P=0.025). Monthly
langurs,whichincluded1599feedingrecords. Wecollected6 1 2
numberofplantspecieseatenbylangurscorrelatednegatively
525behaviorrecordsfrom1666scansamplesforAssamese
macaques,whichincluded1259feedingrecords. with monthly fruit availability (rs=−0.840, n=12, P=0.001).
For Assamese macaques, there was no significant seasonal
Dataanalysis differenceinmonthlynumberoffoodspecies(U=9.000,n =5,
1
BecausefewrecordswerecollectedinSeptemberorOctober n =5,P=0.548).
2
2005fortheAssamesemacaquegroups,weexcludeddatain Ingeneral, bothspecieswerehighlyfolivorous, withleaves
these months from later analyses. We also excluded records accountingfor71%and77.4%oftheoveralldietforFrançois’
for dependent infants and juveniles because these animals langurs and Assamese macaques, respectively (Figure 3).
werenotactingindependently. Wedeterminedthepercentage Fruits contributed to only a small proportion of the overall
of different plant species in the diet of each study group diet (17.4% for François’ langurs and 13.4% for Assamese
by calculating the percentage of feeding records devoted to macaques).However,therewasmarkedinter-specificvariation
them among annual total feeding records. We calculated in annual food category composition (Figure 3). Assamese
theShannon-Weaverdiversityandevennessindicesbasedon macaquesatemoreyoungleaves(Z=−2.701,n=10,P=0.007),
consumptionofplantspecies. TheShannon-Weaverdiversity whereas François’ langurs consumed more mature leaves
(cid:80)
index was calculated using the equation: H’=− P×lnP (Z=−2.666,P=0.008)andotheritems(e.g.,seedsandpetioles,
i i
(where P is the proportion of feeding records of the ith plant Z=−2.521, P=0.012). Moreover, inter-specific variation in
i
species) and the evenness index was calculated using the seasonal dietary shift in response to food availability was
equation:J=H’/Hmax=H’/lnn(wherenisthenumberofspecies detected. François’ langurs consumed more young leaves
eaten). Food category composition was expressed as the in the rainy season than in the dry season (U=4.000, n =6,
1
percentage of different plant parts in the monthly diet of the n =6, P=0.025, Figure 4). The consumption of young leaves
2
studygroupusingmonthlytotalfeedingrecords. Annualfood correlated positively with their abundance (rs=0.865, n=12,
category composition was obtained by averaging the monthly P<0.001). Conversely, the consumption of mature leaves
percentages. (U=0.000, P=0.004)washigherinthedryseasonthaninthe
We used the Wilcoxon signed-rank test to examine rainyseason. Asignificantandnegativecorrelationwasfound
inter-specificvariationsintheoverallpatternofuseofdifferent betweentheconsumptionofyoungleavesandmatureleaves
food categories. The Mann-Whitney U test was used to (rs=−0.685, n=12, P=0.014). In addition, langurs consumed
286 www.zoores.ac.cn
seeds only in the dry season (U=6.000, P=0.022), and the statistically significant (U=11.000, n =5, n =5, P=0.754). It
1 2
proportion to monthly diet varied from 6% (March) to 22% is worth noting that young leaves of Indocalamus calcicolus
(January).ForAssamesemacaques,youngleavescontributed contributedtothebulkofthemacaques’totaldiet(Table1)and
tothehighestproportionofthemonthlydietalmostyear-round youngleafconsumptioninmostmonths(Figure5). Macaques
(Figure 4). In contrast to François’ langurs, Assamese increased the consumption of this item in the dry season
macaques consumed more young leaves in the dry season compared with the rainy season, but the difference was not
than in the rainy season, even though the difference was not statisticallysignificant(U=8.000,P=0.421).
40
François langur
35
Assamese macaque
n) 30
n (
e
at 25
e
s
e
ci 20
e
p
s
nt 15
a
pl
er of 10
b
m
u 5
N
0
Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug
Month
Figure2MonthlynumberofplantspecieseatenbysympatricFrançois’langursandAssamesemacaquesatNonggang
100
Other
90 Flower
%) 80 Fruit
s ( 70 Mature leaf
ord 60 Young leaf
ec 50
g r 40
n
edi 30
e
F 20
10
0
François langur Assamese macaque
Species
Figure3AnnualdietcompositionofsympatricFrançois’langursandAssamesemacaquesatNonggang
DISCUSSION as a food source may be an effective strategy for Assamese
macaquestosurviveinlimestonehabitats. Incontrast,François’
In this study, both primates exhibited marked differences langurs showed more flexibility in food choice, as reflected in
in their choice of food species. Compared to François’ their higher dietary diversity and evenness indices. Moreover,
langurs, Assamese macaques concentrated more foraging François’ langurs tended to select less common plant species
effortonafewfoodspecies,especiallyIndocalamuscalcicolus, as favored foods. Of the top 10 food species, only two
which accounted for 62% of their diet. This small bamboo (Pithecellobium clypearia, Clausena anisum) belonged to the
is superabundant and endemic to limestone hills (Liang et al., dominanttreespeciesinthehabitat(Zhouetal.,2006).
1988).Thus,usingmorereadilyavailablecommonplantspecies
ZoologicalResearch39(4):284–290,2018 287
Althoughbothprimateswerehighlyfolivorous,theyexhibited Assamesemacaquesmaintainedahighlevelofyoungleaves
dietarydifferences: François’langursconsumedmoremature in the diet almost year-round, even an increase in young leaf
leaves and less young leaves than Assamese macaques. consumption in the dry season. This could be related to the
These variations may reflect differences in feeding strategies fact that Assamese macaques relied heavily on young leaves
in response to changing food availability. In typical colobine ofIndocalamuscalcicolus,whichcontributedtothebulkoftheir
species diets, young leaves and fruits are often preferred dietinmostmonthsandexhibitedasimilartendencytoyoung
foods (Oates, 1994; Yeager & Kool, 2000). When young leaf consumption. Young leaves of this bamboo species are
leavesandfruitsbecamescarcerinthedryseason,François’ plentiful throughout the year, and their availability is invariant
langurs significantly increased their consumption of mature betweenseasons(personalobservation),whichmayprovidea
leaves. Matureleavesareabundantandavailable, butrichin long-termstaplefoodresourceforthemacaquesinlimestone
cellulose and poor in nutrition (Richard, 1985). They usually habitats. Thus, the bamboo-dominated diet could be a key
serveasfallbackfoodsforprimatesduringperiodsofpreferred factor in the differences in fallback foods between Assamese
food scarcity (Marshall & Wrangham, 2007). In contrast, macaquesandFrançois’langurs.
100
FArsasnaçmoeiss lea nmgaucraque Young leaf
80
60
40
20
0
Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug
100
Mature leaf
80
60
40
20
0
Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug
100
%) 80 Fruit
s (
ord 60
c
e
g r 40
n
edi 20
e
F
0
Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug
100
Flower
80
60
40
20
0
Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug
100
80 Other
60
40
20
0
Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug
Month
Figure 4 Monthly percentage of feeding records devoted to different food items in the diet of sympatric François’ langurs and
AssamesemacaquesatNonggang
288 www.zoores.ac.cn
Table1PlantspeciesusedasmajorfoodsbysympatricFrançois’langursandAssamesemacaquesatNonggang
François’langur Assamesemacaque
Species Family Parta F%b Species Family Parta F%b
Ficusnervosa Moraceae YL,ML,F,FR 9.39 Indocalamuscalcicolus Bambusoideae YL 62.02
Pithecellobiumclypearia Mimosaceae YL,ML,S 7.82 Ficusnervosa Moraceae YL,ML,F,FR 4.01
Aristolochialonggangensis Aristolochiaceae YL,ML,ST 5.94 Guihaiaargyrata Palmae F,P 3.64
Canthiumdicoccum Rubiaceae YL,ML,F,FR 5.76 Sinosideroxylonpedunculatum Sapotaceae YL,FR 3.55
Embeliascandens Myrsinaceae YL,ML 5.57 Canthiumdicoccum Rubiaceae YL,ML,F,FR 2.28
Ventilagocalyculata Rhamnaceae YL,ML,F,FR 4.57 Burretiodendronhsienmu Tiliaceae YL 1.55
Ficusglaberrima Moraceae YL,ML,FR 4.26 Crotoneuryphyllus Euphorbiaceae YL 1.55
Puerariathunbergiana Papilionaceae YL,ML 4.13 Ficusmicrocarpa Moraceae YL,FR 1.46
Wrightiapubescens Apocynaceae YL,ML,F,S 3.50 Ventilagocalyculata Rhamnaceae YL 1.37
Clausenaanisum Rutaceae FR 3.32 Berchemiafloribunda Rhamnaceae YL,F,P 1.37
Zeniainsignis Caesalpiniaceae YL 3.19 Lepionurussylvestris Sapotaceae YL,ML 1.18
Pseudostreslusindica Moraceae YL,ML 2.88 Sapiumrotundifolium Euphorbiaceae FR 1.18
Sabiaswinhoei Sabiaceae YL,ML 2.57
Randiaspinosa Rubiaceae YL,ML 2.50
Sinosideroxylonpedunculatum Sapotaceae YL,FR 2.32
Urobotryalatisquama Opiliaceae YL,ML,F 2.07
Cuscutachinensis Convolvulaceae YL,ML 2.00
Tirpitziaovoidea Linaceae YL,ML,F 1.75
Burretiodendronhsienmu Tiliaceae YL 1.69
Ficusgibbosa Moraceae YL,ML,FR 1.63
Boniodendronminor Sapindaceae YL,ML 1.50
Teonongiatonkinensis Moraceae YL,ML 1.25
Cudraniacochinchinensis Moraceae YL,ML 1.01
aPartseaten:YL,youngleaf;ML,matureleaf;FR,fruit;S,seed;F,flower;P,petiole;ST,stem.bF%:Percentageoftotalfeedingrecords.
As colobines, langurs possess digestive systems distinct the ground and grasp the stem with one forelimb while they
fromthecercopithecinemacaques. Langurshaveanenlarged pluckyoungleaveswiththeother.
and sacculated forestomach, which serves as the primary
fermentation chamber (forestomach fermentation) (Chivers, 80
1994). In contrast, macaques have an enlarged caecum 70
or colon as the primary fermentation chamber (caecocolic %) 60
fermentation) (Chivers, 1994; Hladik, 1978). The former is s ( 50
mostefficientformammalsthatrelyonfoodshighinstructural ord 40
ctLhaaarmbtpborheiymrtd,ar1ari9tlye9s8fe,)ew.dhTehorunesra,esFatrdhaielnyçladotiitgsee’rslaistinbmgleuorfssotocedaffisnc(icAeonlentxsfaounrmdmeearm,m1am9tu9ar3les; eding rec 3200
leaves in large quantities as fallback foods in response to Fe 10
0
preferredfoodscarcity,whereasAssamesemacaquesdepend Nov Dec Jan Feb Mar Apr May Jun Jul Aug
moreonyoungleaves. Month
In addition to digestive physiology, dietary variation may Figure 5 Monthly percentage of feeding records devoted
be related to differences in positional behavior reflected in to young leaves of Indocalamus calcicolus by Assamese
anatomy (Chalise, 2003; Fleagle, 2013; McGraw, 1998). It
macaquesatNonggang
is likely that different postural abilities enable species to
exploit different food resources. Although sitting is the
In summary, sympatric François’ langurs and Assamese
most common feeding posture for both primate species,
macaquesatNonggangadopteddifferentforagingstrategiesin
Assamese macaques adopted the stank/forelimb-suspended
responsetochangesinthetemporalandspatialdistributionof
posturemorefrequentlythanFrançois’langursduringfeeding
preferredfoods,whichappearstoreducecompetitionforfood
(unpublished data for François’ langurs, Huang et al.,
resourcesandallowsforsympatry.
2015). Thestank/forelimb-suspendedposturewasusedmost
frequentlywhenAssamesemacaquesfedonyoungleavesof
COMPETINGINTERESTS
Indocalamuscalcicolus. Macaquesalwaysstandbipedallyon
Theauthorsdeclarethattheyhavenocompetinginterests.
ZoologicalResearch39(4):284–290,2018 289
AUTHORS’CONTRIBUTIONS McGraw WC. 1998. Posture and support use of old world monkeys
(Cercopithecidae): the influence of foraging strategies, activity patterns,
Q.H.Z.andC.M.H.designedthestudy. Q.H.Z.andH.W.conducteddata
and the spatial distribution of preferred food items. American Journal of
collection.Q.H.Z.wrotethemanuscript,andC.M.H.revisedthemanuscript.
Primatology,46(3):229–250.
Allauthorsreadandapprovedthefinalmanuscript.
Nadjafzadeh MN, Heymann EW. 2008. Prey foraging of red titi monkeys,
ACKNOWLEDGEMENTS
Callicebuscupreus,incomparisontosympatrictamarins,Saguinusmystax
WeareverygratefultoGuangxiForestryBureauandNonggangNational andSaguinusfuscicollis.AmericanJournalofPhysicalAnthropology,135(1):
NatureReserveforpermittingustoconductourresearchatthestudysite. 56–63.
Oates JF. 1994. The nature history of African colobines. In: Davies AG,
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