Female choice impacts residential male takeover in golden snub-nosed monkeys (Rhinopithecus roxellana)

2018·0.87 MB·

by  Fang, Gu

ZOOLOGICAL RESEARCH
Female choice impacts resident male takeover in golden
snub-nosed monkeys (Rhinopithecus roxellana)
GuFang1,JingChen1,Ru-LiangPan1,2,3,Xiao-GuangQi1,2,*,Bao-GuoLi1,2
1CollegeofLifeSciences,NorthwestUniversity,Xi’anShaanxi710069,China
2ShaanxiKeyLaboratoryforAnimalConservation,NorthwestUniversity,Xi’anShaanxi710069,China
3SchoolofAnatomy,PhysiologyandHumanBiology,UniversityofWesternAustralia,PerthWesternAustralia6009,Australia
ABSTRACT than male conflict, females more often initiated and
affectedtakeoverandoutcome,implyingthatthesocial
In primate species with social systems consisting
status and competitive ability of the males played
of one-male breeding units (OMUs), resident male
lesserrolesduringtakeover.
takeover represents a major challenge to individual
Keywords: Rhinopithecus roxellana; Female mate
reproductive success and mating strategies. The
choice; Takeover; Resident male tenure; Social
goldensnub-nosedmonkey(Rhinopithecusroxellana)
networkanalysis
is characterized by large multilevel societies (MLS)
comprisedofseveralOMUsandall-maleunits(AMUs); INTRODUCTION
however,thefactorsandmechanismsassociatedwith
In mammal species with polygamous breeding groups, a new
residentmaletakeover,whichofferimportantinsight male can enter an established group and forcibly expel the
into primate reproduction and social strategies, are residentadultmale(Pauletal.,2000; vanSchaik,2000). This
still poorly understood. Based on 5-year monitoring processiscalledmalereplacementortakeover(Rudran,1973;
Wheatley,1982). Residentmalesmonopolizethereproductive
data from a free-ranging herd of golden monkeys
behavior of the adult females and maintain their long-term
fromtheQinlingMountainsinChina,wecategorized
position in the group after male takeover (Inoue & Takenaka,
three phases of an OMU, that is, a rising phase,
2008). Correspondingly, females may engage in several
developing phase, and declining phase. The rising alternativebehavioralstrategiesinresponsetochangesinsocial
anddecliningphaseswereunstableperiodsinwhich dynamicsduringmaletakeover.Forexample,femaleemigration
male takeover in an OMU might occur. Factors canoccurimmediatelyafterthecollapseofasocialgroupwhen
the previous male leader is ousted (Pusey & Packer, 1987).
causingtakeover,suchasleadermalerank,fighting
Alternatively, females may also leave their former unit before
ability, reproduction rate, and affiliation (proximity,
conflictortakeover,resultinginpossibleunitcollapse.Therefore,
allogrooming),wereanalyzedformalesandfemales femaletransferandmatingchoicecanplayimportantrolesfor
and for different OMUs. Results indicated that the newmalematingopportunities(Swedell,2000).
new resident male’s fighting ability was lower than
that of the former resident male in 23 cases. After
replacement, the rank order of the new resident Received: 11October2017;Accepted: 02January2018;Online: 12
male significantly declined. Females involved in a March2018
takeover increased their distance from the resident Foundation items: This study was funded by the National Science
maleanddecreasedmatingfrequencyduringthethree FoundationofChina(31470455,31622053,31730104),NationalKey
monthspriortotakeover. Femaleswithinfantsunder Program of Research and Development, Ministry of Science and
one-year-oldhadamarkedeffectonthespecifictime Technology of China (2016YFC0503200), and Northwest University
oftakeoveroccurrence. Theseresultssuggestedthat GraduateInnovationandCreativityFunds(YZZ17156)
femalechoicewasthemainfactordecidingwhethera *Correspondingauthor,E-mail:[email protected]
takeoverattemptwassuccessful. Furthermore,rather DOI:10.24272/j.issn.2095-8137.2018.035
266 SciencePress ZoologicalResearch39(4):266–271,2018
Residentmalemigrationcaninfluencethesocialorganization, N33◦45(cid:48)–33◦50(cid:48), altitude of 1 400–2 890 m a.s.l.), Shaanxi
mating strategies, and genetic structure of a species or Province, China (Qi et al., 2008). Vegetation in the area
population (Kuester & Paul, 1999), especially in polygamous includes deciduous broadleaf forest (1 400–2 200 m a.s.l.),
primates that form multilevel societies (MLS). Only a small mixedconiferousanddeciduousbroadleafforest(2200–2600
number of primate species, including hamadryas baboons ma.s.l.),andconiferousforest(above2600ma.s.l.)(Li&Zhao,
(Papio hamadryas), gelada baboons (Theropithecus gelada), 2007). The region exhibits striking seasonality: the average
and snub-nosed monkeys (Rhinopithecus spp.), are reported annualtemperatureis10.71◦C,withamaximumof31.51◦Cin
toliveinMLS,withinwhichone-maleunits(OMUs)travel,feed, Julyandminimumof−14.31◦CinJanuary,andaverageannual
and rest together to form a cohesive band (Dunbar, 1988; rainfallis894mm(Lietal.,2001).
Grüeteretal.,2017). Inwildhamadryasbaboons,mostfemales
Studytroop
showtheiracceptanceoftheintrudingmalefollowingatakeover
Two troops reside in the study area (i.e., East and West
after a series of behavioral stages (Swedell, 2000). In gelada
Range Troops: ERT and WRT) (Li et al., 2000), separated
baboons, however, females residing in the same OMU are
by the Nancha River. The WRT consists of the GNG-herd
closely related, forming matrilines, so males must aggressively
and DJF-herd. The GNG-herd was the focal study herd and
compete for reproductive opportunities to maintain their tenure
contained a breeding band of 7–13 OMUs and an all-male
asresidentleaders(Dunbar,1988). Inthecaseofsnub-nosed
band. Behavioral observations were made at 0.5 to 50 m,
monkeys,thebandsareusuallyfollowedbyoneormoreall-male
which allowed behavioral patterns as well as individual ages
units(AMUs)comprisedofseveraladult,sub-adult,andjuvenile
and genders to be recorded under proximity with provisioned
males(Grüeter&vanSchaik,2009). IntheYunnansnub-nosed
food. Handfeedingandphysicalcontactbetweenresearchers
monkey (R. bieti), a resident male’s rank is very important in
andanimalswereavoided,soallbehavioralpatternsoccurred
regardtosuccessfultakeover(Zhuetal.,2016).
undernaturalenvironmentsandcircumstances.
Golden snub-nosed monkeys (R. roxellana) are an
Individual identification was made according to body
endangered primate species, as evaluated by the IUCN, and
characteristics, such as pelage coloration, crown hair pattern,
are characterized by a polygamous MLS system (Qi et al.,
scarsorevidenceofpreviousinjury,andshapeofgranulomatous
2014,2017).SeveralOMUsforageandresttogether,forminga
flangesonbothsidesoftheupperlip(Qietal.,2008,2009).
breedingband. Bachelorbandsformedbyoustedmales,both
former resident males and young males who have reached Definitionofbehaviorandtakeover
sexual maturity, are usually found nearby. During the mating We defined resident male replacement as behavior involving
season, the bachelor groups are often observed approaching aggressive action, including contacting, chasing, and
thebreedingbandstoseekreproductiveopportunities(Qietal., threatening an individual, aggression in response to rejection
2014). Asacountermeasure,haremmalescanformalliances of the attacked, or counter-aggression (Grüeter, 2004). If
toevictsolitarymales(Qietal.,2017). Thus,maletakeoverin the interval between conflict events between two OMUs was
R.roxellanaisinfluencedbyadultmalesfrombachelorgroups. longer than 30 s, two conflicts were recorded, otherwise only
It has been reported that conflict occurs during takeover in R. oneconflictwasrecorded.
roxellana (Wang et al., 2004; Zhao et al., 2011). In addition,
Datacollection
haremfemalepreferencecanaffectthetakeoverprocess(Qiet
The size and composition of the OMUs were recorded in
al.,2009). However,thespecificmechanismsoftakeovers,as
March 2008 after all individuals in the herd were identified.
well as the social, reproductive, and demographic factors that
Other data used in this study were collected from March to
influence the timing and success of male takeovers, remain
June, September to the following January, and from August
unclear. Therefore, we carried out a study on the golden
2012 to December 2016. In total, data included 36 OMUs
snub-nosedmonkeysfromtheQinlingMountainstoclarifythe
and 396 monkeys. All individuals in an OMU were scanned
mechanisms of male takeover and hypothesized that male
duringtheobservationperiodtoclarifywhetheratakeoverhad
fightingabilityhadlimitedimpactontakeoverevents.Thisstudy
occurred.AgonisticbehavioramongOMUswasrecordedbyall
wascarriedbycollectingdataonmaletakeoverevents, social
occurrencesampling(Altmann,1974). Allogroomingbetween
ranks,andfactorsthatmayaffectaffiliationbetweenmalesand
males and females was recorded. Copulation, involving
females before and after takeover, including spatial proximity,
mountingandheterosexualgenitalcontactbyintromissionand
grooming, reproductive success, and female birth rate. Our
pelvicthrusts(Li&Zhao,2007),wasrecordedbyalloccurrence
research provides valuable evidence to help understand the
sampling, with the initiator and receiver both identified. We
mechanism(s)involvedinmaletakeoverandreproductiveand
chose one breeding band as the observation target each
matingstrategiesinR.roxellana.
observationday(1000–1400h)andallogroomingwasrecorded
MATERIALSANDMETHODS for259d,totaling906.5h.
Studysite Dataanalysis
This research was conducted in the Yuhuangmiao region of Individual social rank was scored according to previous
the Zhouzhi National Nature Reserve (ZNNR), located on the research(deVries,1998).Thebirthratewascalculatedbased
northernslopesoftheQinlingMountains(E108◦14(cid:48)–108◦180(cid:48), onthefollowingformula:
ZoologicalResearch39(4):266–271,2018 267
total observation duration of one OMU, recorded by the hour;
BR= (cid:80)(cid:0)FIii(cid:1) (1) andnisthenumberofadultfemales.
D We used the independent t test to compare differences in
where I is the number of births observed in the reproductive the reproduction rates of a harem male in different periods of
i
season; F is the number of adult females during the same tenure.
i
period; and D is the duration observed and recorded by year
RESULTS
(Eisenbergetal.,1981).
The reproductive rate in an OMU, as well as male OMUmaletakeoverandmale-maleconflict
reproductivesuccess,wasdeterminedasfollows: From August 2012 to December 2016, we recorded 36
OMUs, of which nine already existed in 2012, 19 underwent
I
R= (2) restructuring during the study period, and eight remained
2F
unchanged. Ofthe36OMUs,12femalestransferredandfour
whereIisthesumofinfantsintheOMUinvolvedinatakeover OMUs disappeared from the study troop. For the 16 male
inthefirstreproductionseason; andF isthenumberofadult takeoverevents,only13werethoroughlyrecordedbeforeand
femaleswithoutaninfantinthereplacedOMU. after, withsocialrank, tenure, andaffiliationbetweenfemales
ThefrequencyofcopulationwasdeterminedbyC/P/T,where and males documented in detail. Thus, male replacement in
C isthetimeobservedduringtheobservationperiod;T isthe theseOMUswasconsideredsuccessful(Table1).
Table1VariationofOMUandtransferofformerharemmalesafterreplacement
Formofreplacement Replacement Date Rankstatus Injury Parturitionornot# Maletransfer+
BZ→TB 2012.8 16→18 No a
FZ→LZ 2013.12 10→15 FZ 2/20/2 b&a
PK→VS 2014.2 2→13 VS 2/20/2 b
BB→HT 2013.3 1→8 No 2/31/3 b&c
Directreplacement
SX→G3 2013.9 12→12 3/41/4 c
HB→BQ 2015.10 a
XJ→LD 2015.11 No b
PK→KO 2016.9 a
ST→SQˆ→HK 2012.12 13→14 ST 1/21/2 b&c,b&c
HK→LZˆ→YH 2013.10 14→15 LZ∗ b,b&c
Sequential/indirectreplacement PKˆ→BG→QS 2016.11
JB→WX→ST 2013.10-2014.4 9→15 WX∗ 1/10/1 b
DXJ→XCˆ→G3 2016.11 DXJ∗ b
CapitallettersintheReplacementcolumnrepresenttheIDofeachindividuals. ∗:Residentmalesgotinjuryduringthefirstreplacement. ˆ:
Residentmalewhosetenurewasshorterthan10days.#:Theleftrowwasthenumberoffemalewhowasinreproductiveseasondelivery;the
rightrowwasthefemalewhowasinreproductionseasondidnotdelivery.+:a,emigratedtoothertroop;b,transferredintoAMU;c,rebuildOMU.
Residentmaletakeoveraccountedfor60%ofOMUchanges the three months prior to takeover than that observed in
inourstudy. RankordersignificantlydeclinedinthenewOMU OMUsassembledfor3–7yearswithouttakeover(independent
compared with the former OMU (independent sample t test: sample t test: allogrooming: t=2.754, df=11, P<0.05;
t=3.073, df=7, P<0.05), and the reproductive rate of females proximity: t=5.149, df=11, P<0.001; copulation: t=8.103,
following takeover was not significantly different than that of df=11, P<0.001). Furthermore, for OMUs that experienced a
femalesnotinvolvedinatakeover(independentsamplet test: takeoverandrebuiltwithinthreemonths,bothallogroomingand
t=0.244,df=6,P>0.05). proximityweresignificantlyweakerthanthatobservedinOMUs
Of the 13 takeovers, only five involved conflict, totaling assembledfor3–7yearswithouttakeover(independentsample
23 conflict events. Furthermore, the rate of a new resident t test: allogrooming: t=3.291, df=11, P<0.001; proximity:
male losing the conflict was significantly higher than of it t=4.052, df=11, P<0.01); however, mating frequency was
winning(independentsamplet test: t=9.349,df=23,P<0.001, significantly higher (independent sample T test: t=−11.056,
Figure1). df=11,P<0.001,Figure2).
Affiliationofmalesandfemalesbeforeandaftertakeover Residentmaletenureaffectstakeover
With regard to the OMUs in which takeovers occurred, According to differences in the number of adult females and
affiliation between males and females became weaker in infants, as well as the reproductive rates, three distinct OMU
268 www.zoores.ac.cn
developmentperiodsweredefined: (1)risingphaseinthefirst Monthsofoccurrence
year;(2)developingphasefromyears1–8,duringwhichadult Therewasasignificantdifferenceintakeovermonthbetween
female numbers were stable; and (3) declining phase after 8 OMUscontainingadultfemaleswithinfantsyoungerthanone
years due to a significant reduction in the number of adult year and females without young infants (Kruskal-Wallis test:
femalesandinfantsaswellasreproductiverates(independent χ2=11.18, df=3, P<0.05). For OMUs containing females
samplet test:t=−3.254,df=38;P<0.01). with infants under one-year-old, male replacements occurred
from December to the following March, whereas for OMUs
comprised of females without young infants, takeovers were
***
randomthroughouttheyear.
DISCUSSION
n) This study attempted to clarify resident male takeover
es ( scenariosingoldensnub-nosedmonkeys.Ourstudyanalyzed
m
Ti factorsinvolvedinresidentmaletakeoverbasedonlong-term
observationandindividualidentification.
Limitedroleofmalesintakeover
Our results showed that the new resident male often lost
the conflict with the former resident male, and social rank
order of the newly formed unit was significantly lower than
that of the former unit, suggesting that weak conflict ability
and lower-ranked males could successfully replace resident
Figure 1 The outcome of replacement fight (five days
males in R. roxellana. This result conformed to our previous
recordingafterreplacement)
hypothesis. Specifically, males played a lesser role in the
ColumnA:Thereplacementfightwasnotobserved;B:thetimeschallenged takeoverprocessasformerresidentmalescouldwinthefight
malewinduringreplacementfight;C:thetimeschallengedmalelostduring butstilllosetheharem.
replacementfight.***:P<0.001. Ingoldensnub-nosedmonkeys,residentmalesinbreeding
bandsalwaysfacethedangeroftakeoverduetotheexistence
of all-male groups. In these groups, males struggle to gain
breeding opportunities, and thus fighting for takeover occurs
* * *
* * * frequently. However, fierce conflict can lead to substantial
injuryregardlessofwinningorlosing.Inthewild,smallinjuries
x canhavesevereconsequences,evenresultingindeath,which
e
nd canbealong-termthreattoanimalpopulations. Therefore, if
on i takeoveroutcomeisdecidedbyfightingabilityalone, itwould
Affiliati bRe. hroaxremllfaunlaformpaolepsuladtoionnodtevdeislopplamyenfietrdcuerincgoneflvioctludtiounri.ngThtuhse,
process of male takeover, as supported by evidence from
captive populations. Renetal.(2007) reported that this not
onlyreducestheprobabilityofinjury, butalsolowersthecost
ofmaletakeover. Thisbehavioralpatternisalsoseeninother
Affiliation type
species, including wild barbary macaques (Macaca sylvanus)
Figure 2 The affiliation between male and female before and
andsomegroup-livingmammals(Johnstone,2000;Nonacs&
afterreplacement
Hager,2011).
Column A: the OMU which undergo the replacement and rebuild within
Femalechoiceintakeoverinitiation
threemonths;B:OMUthatbuild3–7years;C:theOMUwhichbeforethe
Femalesinvolvedinatakeoverincreasedthedistancefromand
replacementwithinthreemonths.*:P<0.05.
showedanalienatedassociationwiththeformerresidentmale
and decreased mating frequency and mating chances in the
From 2001 and 2014, the tenure of four of the resident three months prior to takeover. Thus, our evidence strongly
malesrangedfrom4to9months(average5.6±2.7,mean±SD), indicated that male takeover in R. roxellana was primarily
whereasthetenureoftheotherfivewas10years.SevenOMUs associated with female behavior changes. Females have the
stayedinthestudytroopformorethanoneyear, butlessthan option of direct mate choice by joining or deserting the new
8.5years(average3.50±2.43,mean±SD).Takeoverfrequency male, or by leaving when the resident male is the target of
in the first year (rising phase) and tenth year (declining phase) harassment (Sicotte et al., 2017). Male takeovers are largely
weresignificantlyhigherthanthatintheotheryears(developing determined by female transfer and mate choice, which both
period)(Wilcoxonranksumtest:Z=−2.981,P<0.01). play critical roles in female social and reproductive strategies
ZoologicalResearch39(4):266–271,2018 269
(Sterck et al., 1997; van Schaik, 1989). Rhinopithecus seasons(Cords,2004). However, thetimingofresidentmale
roxellana females expressed their choice by alienating the takeovers in R. roxellana does not support this prediction, as
former resident male and mating less often, thereby directly also reported for R. bieti (Cui et al., 2006; Kirkpatrick et al.,
initiatingandinfluencingthetakeoverprocess. 1998). However, females with an infant less than one year
Wealsofoundthatmatingfrequencywassignificantlyhigher old transferred to new OMUs during the interval between the
after the takeover. It may be that females balance the cost mating and breeding seasons. This may be related to the
of wasting investment in having offspring against the risks of multiple male mating exhibited in this species, which is likely
failingtobondwiththenewmale(Mori&Dunbar,1985). We a tactic used to confuse paternity as sneaky mating between
argue that female mate choice is the primary factor initiating females and non-resident males was observed in the present
male takeover. Given the limited male sexual coercion and study. Thus,itmaybebeneficialforfemaleswhohaveavery
low levels of female aggression, females appeared to select younginfanttoinitiatetakeoverduringthistime.
OMUsbasedonthequalityofadultmales,whichmayreduce Although other factors can influence takeover, our results
the ability of the resident male to monopolize access and indicated that female choice was the main factor triggering
increase the opportunity of females to mate with different takeover and outcome. A male’s social status and his
males; however, this requires further research. In our study, competitive ability played lesser roles. Female mate choice
mating frequency was significantly higher after male takeover wasanotherdriverthatdecidedwhetheramalehadachance
thanthatbefore. Thismaybeawayinwhichfemaleschoose atsuccessfulreproduction.
mates and increase genetic diversity. Furthermore, mating
aftermaletakeoverhelpstoestablishgoodsexualrelationships COMPETINGINTERESTS
and assists unit members to accept each other and quickly
stabilize the OMU. Females likely initiate male takeover to Theauthorsdeclarethattheyhavenocompetinginterests.
reduceinbreedingandensurethattheiroffspringaresiredby
differentmalesovertheirreproductivelifetime. AUTHORS’CONTRIBUTIONS
Residentmaletenureaffectstakeover X.G.Q.andB.G.L.designedthestudy. J.C.performedthefieldwork. F.G.,
Ourresultsdemonstratedthattakeoverfrequenciesinthefirst X.G.Q.,J.C.andR.L.P.wrotethemanuscript.Allauthorsreadandapproved
year (rising phase) and tenth year (declining phase) were thefinalmanuscript.
significantly higher than that in the other years (developing
period). Ithasbeenreportedthatresidentmaletenureisthe ACKNOWLEDGEMENTS
mostimportantfactorthatnegativelyaffectsmalereproductive
We are thankful to the Zhouzhi National Nature Reserve for providing
success(Sommer&Rajpurohit,1989). Femalesarelesslikely
permissiontocarryoutourresearch. WealsothankSu-YunZhang,Kang
tobeinseminatedbymaleswithrelativelyshortorlongtenures,
Huang,andeveryonewhohelpedusduringfieldworkandallmembersofthe
which may lead to potential reproductive competition (Qi et
GoldenSnub-NosedMonkeyResearchTeamintheCollegeofLifeScience,
al., 2009). Thus, a female more often chooses a male with
NorthwestUniversity.
a suitable tenure (Inoue & Takenaka, 2008). In our case, the
reproductive rate after the eighth year was significantly lower
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