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Abstract

Social monogamy has evolved multiple times and is particularly common in birds. However, it is not well understood why some species live in long-lasting monogamous partnerships while others change mates between breeding attempts. Here, we investigate mate fidelity in a sequential polygamous shorebird, the snowy plover (Charadrius nivosus), a species in which both males and females may have several breeding attempts within a breeding season with the same or different mates. Using six years of data from a well-monitored population in Bahía de Ceuta, Mexico, we investigated predictors and fitness implications of mate fidelity both within and between years. We show that in order to maximize reproductive success within a season, individuals divorce after successful nesting and re-mate with the same partner after nest failure. Therefore, divorced plovers, counterintuitively, achieve higher reproductive success than individuals that retain their mate. We also show that different mating decisions between sexes predict different breeding dispersal patterns. Taken together, our findings imply that divorce is an adaptive strategy to improve reproductive success in a stochastic environment. Understanding mate fidelity is important for the evolution of monogamy and polygamy, and these mating behaviours have implications for reproductive success and population productivity.
Ecology and Evolution. 2019;00:1–12.    
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 1
www.ecolevol.org
Received:5March2019 
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  Revised:11Ju ne2019 
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  Accepted:17June2019
DOI: 10.1002/ece 3.5591
ORIGINAL RESEARCH
Mate fidelity in a polygamous shorebird, the snowy plover
(Charadrius nivosus)
Naerhulan Halimubieke1| José O. Valdebenito1| Philippa Harding1|
Medardo Cruz‐López2| Martín Alejandro Serrano‐Meneses3| Richard James4|
Krisztina Kupán5| Tamás Székely1,6
1DepartmentofBiologyandBiochemistry,MilnerCentreforEvolution,UniversityofBath,Bath,UK
2PosgradoenCienciasdelMaryLimnología,UniversidadNacionalAutónomadeMéxico,CiudadUniversitaria,Cd.México,Mexico
3DepartamentodeCienciasQuímico‐Biológicas,UniversidaddelasAméricasPuebla,SanAndrésCholula,Puebla,Mexico
4DepartmentofPhysicsandCentreforNet worksandCollectiveBehaviour,UniversityofBath,Bath,UK
5MaxPlanckInstituteforOrnithology,BehaviourGeneticsandEvolutionaryEcologyResearchGroup,Seewiesen,Germany
6DepartmentofEvolutionaryZoologyandHumanBiolog y,UniversityofDebrecen,Debrecen,Hungar y
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninanymedium,
providedtheoriginalworkisproperlycited.
©2019TheAuthors.Ecology an d EvolutionpublishedbyJohnWiley&SonsLtd.
Krisz tinaKup ánandTamásSzékelyareco‐authorssharedsenioraut horsh iptothiswork.
Correspondence
NaerhulanHalimubieke,Depar tmentof
BiologyandBiochemistry,MilnerCentrefor
Evolution,UniversityofBath,Bath,UK.
Email:hn364@bath.ac.uk
KrisztinaKupán,MaxPlanckInstitute
forOrnithology,BehaviourGeneticsand
EvolutionaryEcologyResearchGroup,
Seewiesen,Germany.
Email:kkupan@orn.mpg.de
Funding information
ThisprojectwasfundedbyChina
ScholarshipCouncil,CONICYTBECAS
CHILE72170569,ÉLVONALKKP‐126949
(theNationalResearch,Developmentand
InnovationOfficeofHungary),CONACY T
(Mexico),throughtheConvocatoriade
InvestigaciónCientíficaBásica2010‐01
(projectnumber157570).
Abstract
Social mono gamy has evolved multiple t imes and is parti cularly common in bir ds.
However,itis not wellunderstood whysome species livein long‐lasting monoga‐
mous par tnerships while othe rs change mates betwe en breeding attempt s. Here,
weinvestigatematefidelityinasequentialpolygamousshorebird,thesnowyplover
(Charadrius nivosus),a s pecies in which both male s and females may have several
breedingattemptswithinabreedingseasonwiththesameordifferentmates.Using
6 years of data f rom a well‐monitored popu lation in Bahía de Ceut a, Mexico, we
investigatedpredictorsandfitnessimplicationsofmatefidelitybothwithinandbe‐
tweenyears.Weshowthatinordertomaximizereproductivesuccesswithinasea‐
son,individualsdivorceaftersuccessfulnestingandre‐matewiththesamepartner
afternestfailure.Therefore,divorcedplovers,counterintuitively,achievehigherre‐
productivesuccessthanindividualsthatretaintheirmate.Wealsoshowthatdiffer‐
ent mating decisions between sexes predict different breeding dispersalpatterns.
Takentogether,ourfindings imply thatdivorce isan adaptive strategyto improve
reproductivesuccessinastochasticenvironment.Understandingmatefidelityisim
portantfortheevolutionofmonogamyand polygamy,andthesematingbehaviors
haveimplicationsforreproductivesuccessandpopulationproductivity.
KEYWORDS
breedingdispersal,Charadrius nivosus,divorce,matefidelity,nestingsuccess,polygamous
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   HALIMUBIEKE E t AL.
1 | INTRODUCTION
Thedecisionofretainingamatefor severalbreedingeventsordi‐
vorcingisakeyelementofreproductivedecisionsinseveralspecies,
asitcanaffectreproductivesuccessandsubsequentsurvivalofthe
parents(Culina, Radersma,& Sheldon, 2014;Neff & Pitcher,2005;
Székely, Thomas, & Cuthill, 2006; Székely, Weissing, & Komdeur,
2014).Socialmonogamy,definedasasystemwhereanadulthasonly
onesocialpartneroftheoppositesexatagiventimeorthroughouta
timeperiod,iscommonlyobservedinbirds,butalsooccursininver‐
tebrates,fish,amphibians,reptiles,andmammals(Lukas&Clutton‐
Brock, 2013; Møller, 2003). Social monogamy partnerships are
highly variable interms of duration.Some species showlong‐term
mate fidelity or even life‐time mate fidelity until one partner dies
(Black,20 01;Reichard&Boesch,2003).O therspecies,however,ex
hibitshort‐termmatefidelity,inwhichanindividualterminatesthe
relationshipattheendofonebreedingattemptandinitiateanother
breedingwithanewmatewhiletheoldpartnerisstillalive(termed,
sequentialpolygamy).Why domalesandfemalesadopt short‐term
matefidelity,whileotherspairforlife?
Severalhypotheseshavebeenputforwardemphasizingtheim‐
pact of either breeding time‐constraints (or breeding success) on
mate fidelity or divorce in socially monogamous species. On the
one hand ,r etaining a mate r educes the tim e and energy co sts of
searchingforanewmatethereforefacilitateafastre‐mating(“fast‐
trackhypothesis,”Adkins‐Regan&Tomaszycki,2007;Perfito,Zann,
Bentley,&Hau,2007).Retainingamatealsoenhancebreedingper
formancetherebyimprovingreproductivesuccess(“matefamilarity
hypothesis,”Ens,Choudhury,&Black,1996;Gabriel,Black,&Foster,
2013;Sánchez‐Macouzet,Rodríguez,&Drummond,2014).In addi‐
tion, successfulbreeding may alsofacilitate retaining themate for
future breeding (B lack, 2001; Flodin & Blomqvist, 2012). On the
otherhand,changingamatemaybebeneficialinlong‐livedspecies,
individualsdivorcetheirpartnertomatewithgoodqualitypartners
inorder to improvebreedingsuccess (“incompatibilityhypothesis,”
Coulson,1966;seealsoKempenaers,Adriaensen,&Dhondt,1998).
Inspecies withshort lifespan(orshortbreeding season),individu‐
alsimprovereproductivesuccess bymating withmultiplematesto
makethe most out of limited time(“extra‐pair mating hypothesis,”
Arnqvist&Nilsson,2000;Birkhead&Møller,1992).
Matingdecisionsmayberelated tobreedingdispersal—thelat
ter defined here as the movement of an adult from one breeding
location to another within or between years (Clobert, Danchin,
Dhondt , & Nichols, 2001; Greenwood, 1980). On the one hand,
breedingdispersalmaydifferbetweenthesexesinresponsetosex
differences in mating strategies sincethe morepolygamous sexis
expectedtodispersefarthertofindnewmatingpartners(D'Urban
Jackson etal., 2017;Greenwood,1980; Székely,2019;Trochetet
al.,2016).On theotherhand,matefidelity can be viewedasaby‐
productofsitefidelityinsomespecies(Bried,Pontier,&Jouventin,
2003;Morse&Kress,1984),whereaschangingthenestsitewould
leadtomatechangeinsomeotherspecies(Pietz&Parmelee,1994;
Thibault,1994).
A furt her factor that may infl uence mate fideli ty is re‐mating
opportunity.Inspeciesorpopulationswithabiasedadultsexratio,
divorceiscommonlyinitiatedbytheraresexsincetheraresexhas
higher mateavailability than the common sex (Liker,Freckleton,&
Székely, 2014; Parra, Beltrán, Zefania, Dos Remedios, & Székely,
2014). For example, experimental studies of species with biased
adult sex ratio showed that by experimentally creating unmated
males and females,re‐matingtimes wereshorterforrare sexthan
forcommonsex(Parraetal.,2014;Székely,Cuthill,&Kis,1999).
Neverth ele ss,studi esofmatef idelit ytend edtofoc usonmon og
amousspeciesacrossbreedingyears,yieldingdifferentadaptiveim
plicationsofmatefidelity(Briedetal.,2003;Dubois&Cézilly,2002).
Monogamous systems aregenerally characterized byhigh level of
breedingphilopatry (Moore & Ali,1984; Saalfeld & Lanctot,2015)
and/orbi‐parentalcareoftheyoung(Eberhart‐Phillipsetal.,2018),
feature s that tend to promot e mate fidelit y.Howe ver,th e causes
and fitn ess implica tions of mate fide lity in sequ ential polyg amous
species t hat exhibit var iable duratio n of pair bonds (e.g., w ithin a
breedingyear), different levelsof philopatry,orbreedingdispersal
arestillpoorlyunderstood.
Here,weinvestigatepotentialpredictorsandfitnessimplications
of mate fide lity in a sequen tial polygamo us shorebird, th e snowy
plover(Charadrius nivosus),aground‐nesting,nearthreatenedshore
birddistributedonsparselyvegetatedcoastsandalkalinelakeshores
acrossthetemp erateandtrop ica lr egionsoftheAme ricas.Theytyp
icallylaya3‐eggclutchwithbothparentsprovidingcareduringthe
incubation stage, chicks are precocial and nidifugous, which only
require uniparental care (usually males) during brood rearing (del
Hoyo, Elliott, Sargatal, Christie, & Juana, 2018).This species is an
idealmodelforinvestigatingmatefidelity:theyhaveaflexiblemat‐
ingsystem,andbothmalesandfemalesmayhaveseveralmatesse
quentiallyin asinglebreedingseasonuptofourbreedingattempts
(Page,Stenzel,Warriner,Warriner,&Paton,2009).Itistypicallyfe
males that mate with more partners than males do,since females
tendtodeserttheirbroodssoonafterhatching,andleavethemales
tolookafter theyounguntil independence(Carmona‐Isunzaetal.,
2017;Warriner,Warriner,Page,&Stenzel,1986).Femaledesertion
hasbeen linkedto male‐biasedadultsex ratio(ASR):0.53(propor‐
tionofmalesintheadultpopulation)wasestimatedbyStenzeletal.
(2011)basedonadultsurvival, whereasmore recentestimatethat
tookintoaccount hatchlingsexratios,chicksurvivaland adultsur‐
vivalestimatedastronglymale‐biasedASR(0.638,Eberhart‐Phillips
et al., 2018). Snowy plovers may still retain their mate between
clutches within or between years. Furthermore, a recentpaternity
analysesshowedlowrates(<5%)ofextra‐pairpaternityinthesnowy
ploversothatsocialpairsareagoodproxyforgeneticrelationships
andthusreflectDarwinianfitness(Maheretal.,2017).
Usingsnowyploversasamodelorganism, hereweinvestigate
whethermatefidelity(ordivorce)isanadaptivestrategythatmaxi‐
mizesreproductivesuccessinaspecieswithlimitedbreedingperiod
(Choudhu ry, 1995; Plaschke , Bulla, Cruz‐Lóp ez, Gómez del Á ngel,
& Küpper, 2019). We focus on thre e main aspects o f mate fidel‐
ity. First, weinvestigate patternsof mate fidelity both within and
    
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 3
HALIMU BIEKE Et A L.
betweenyear sinbothmalesandfemales.S econd,weexploreifpre
vious nesting success predict materetention (or divorce)by males
andfemalesbothwithinandbetweenyears.Finally,weinvestigate
matefidelityinrelationtobreedingdispersalandre‐matingtime:(a)
whethe r breeding disp ersal is relat ed to mate fidelit y both within
andbetween years; (b) whether there‐matingtime may differ be‐
tweendivorcedandretainedmateswithinyears.
2 | METHODS
2.1 | Study site and field methods
ThepresentstudywasconductedatBahíadeCeuta,Sinaloa,Mexico
(23°54′N, 106°57′W). In this population, snowy plovers nest on
extensi ve saline ponds a nd saltpans (ap proximately 150 h ectares;
Carmona‐Isunza,Küpper,Serrano‐Meneses,&Székely,2015).The
breeding season generally occurs from mid‐April to mid‐July, with
30–100 breeding pairs ever y year. Breeding data were collected
from2006to 2011(n=625nests).Datacollectioninthefieldfol
lowed the methods of Székely, Kosztolányi, and Küpper (2008).
Briefly,wesearchedfornestsusingamobilehideintensivelywithin
the study site, we recorded the nest location with handheldGPS,
andtheegg‐layingdatewasestimatedbasedonthefloatationstage
ofeachegginatransparentjarwithcleanwater.Breedingpairswere
capturedwithawalk‐infunneltrap placedoverthenest,andthey
werebandedwithauniquecombinationofthreecolorringsandan
alpha‐numeric met al ring. Nests were monitored every 2–5 days
until20 days of incubation andthen were checkedeverydayuntil
hatchingtoobtainnestingsuccessdata.Broodsweresearchedin
tensivelydailytodeterminethedateofbrooddesertion.Re‐sight
ingsofpreviouslycolorbandedploverswerealsorecorded.
2.2 | Data collection
2.2.1| Quantification of mate fidelity
Snowy plovers that were monitored in this study were actively
choosing t o retain or to divorc e their mates. Th e mating decision
ofeachindividualwasrecordedaseithermateretentionordivorce
inregardtotheirpreviousbreedingattempt.Weevaluated mating
decisionsseparately for bandedmales andfemales in thepopula
tion, since the decisions may influence one another and as such
maynotbeindependent.Individualswereincludedintheanalyses
ifthey satisfiedthe following conditions:(a) we knew the identity
of their mate (s), (b) they were obser ved in at leas t two reprodu c‐
tive atte mpts that were e ither withi no r between ye ars, and (c) if
thereisamatechange,onlythosewhochangetheirmateswhilethe
previousmateisknowntobealiveareincluded.Intotal,149breed
ingevents (Table1A, 75 divorcesinfemales,26divorcesinmales,
and24retentionsineachsex)fittedthecriterionforthewithin‐year
matefidelityanalysisfrom2006to2011.Forploverswithmorethan
twonestswithinayear,onlythedatafromthefirsttwonestswere
included in the within‐year mate fidelity analysis due to the small
number of i ndividuals wi th three or mor e nests: dur ing the study
TABLE 1 Matefidelityinsnowyplover.(A)Numberofmalesandfemalesdivorcedorretainedamatewithinyears,n=149breeding
events.(B)Numberofmalesandfemalesdivorcedorretainedamatebetweenbreedingyears(late–earlymatefidelity,n=102breeding
events;early–earlymatefidelity,n=116breedingevents;2006–2011)
(A) Within years
Year 2006 2007 2008 2009 2 010 2011 Tota l
Numberofdivorcesinfemales 11 21 10 14 12 775
Numberofretentionsinfemales 683 2 3 2 24
Numberofdivorcesinmales 583 3 4 3 26
Numberofretentionsinmales 683 2 3 2 24
(B) Between years
Year 2006–2007 2007–2008 2008–2009 2009–2010 2010–2011 Total
late–earlymatefidelity
Numberofdivorcesinfemales 12 6712 542
Numberofretentionsinfemales 4 1 1 3 2 11
Numberofdivorcesinmales 8 8 11 7438
Numberofretentionsinmales 4 1 1 3 2 11
early–earlymatefidelity
Numberofdivorcesinfemales 13 4 4 7 7 35
Numberofretentionsinfemales 1 4 2 6 3 16
Numberofdivorcesinmales 17 7 8 7 10 49
Numberofretentionsinmales 1 4 2 6 3 16
Note: SeeSection2fordetails.
4 
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   HALIMUBIEKE E t AL.
period,there wereonly sevenfemalesand twomales in total that
hadthreebreedingattempts.
Forindividuals withoneormultiple nests in eachofthetwo
consecutive years, we evaluate between‐year mate fidelity in
twodifferentways(seeFigure1).First,whenanindividual'smate
duringlateseason(see“relativeegg‐layingdate”below,latesea
soniswhen the relative egg‐laying date is >0) in year1,hadthe
sa m eas them ate ine a rlys eason(wh enth erel ativ eeggla ying date
is<0)inyear 2, itwasclassified as mate retention,orotherwise
divorce(hereinafter late–earlymatefidelity).Intotal, 102breed
ingevents(Table1B,42divorcesinfemales,38divorcesinmales
and11retentionsineachsex)fittedthecriteriaforthelate–early
matefidelity.Second, if aplover matedto thesameindividualin
the earl y seasons of both y ear 1 and year 2, th is was classifi ed
asretention,ordivorceotherwise(hereinafterearly–earlymate
fidelit y). In total, 116 breed ing events (Table 1B, 35 di vorces in
females,49divorcesinmalesand16retentionsineachsex)fitted
thecriteriafor theearly–earlymate fidelity.Allindividuals were
classifiedinto threegroups asdivorced males, divorced females,
andretainedpairs(seeSandercock,Lank,Lanctot, Kempenaers,
&Cooke,2000).
2.2.2 | Nesting success and reproductive success
Nestingsuccesswasquantifiedbasedonthefateofthefirstnestof
eachindividualthatwereincludedinourstudy.Thefateofnestwas
recordedaseithersuccessful (at leastone chickhatched)or failed
(no chicks hatched due to predation, destruction, abandonment,
eggsdisappeared<15daysafterestimatedlayingdate,eggsdidnot
hatch,orthenestwasflooded).Wequantifiedreproductivesuccess
asthecumulativenumberofhatchlingseachindividualproducedin
allbreedingattemptseitherwithinorbetweenyears.
2.2.3 | Relative egg‐laying date
Theegg‐layingdatewas usedto quantifybreedingphenology.We
controlledforbreedingphenological differencesbetweenyearsby
convertingegg‐layingdatesintoJuliandates(“lubridate”packagein
R, Grolemund & Wickham,2011),andcalculating therelative egg‐
layingdateusingthez‐transformation(mean=0,SD=1).
2.2.4 | Breeding dispersal
Within‐year breeding dispersal was defined as the straight‐line
distance (in meters) between an individual's successive nests
withinayear.Forbetween‐yearbreedingdispersal,wemeasured
thestraight‐line distance between (a) thelast nestinyear 1 and
thefirstnestinyear2,and(b)thefirstnestsoftwoconsecutive
years.
2.2.5 | Re‐mating time
Re‐mating timeisdefined asthe numberofdaysthatanindividual
spentonestablishinganewclutchafterterminatingcareofthepre
vious brood. Broods were searchedinthe breeding areadaily. If a
parentwasmissingduringtwoconsecutivesightingsorseenpaired
toanotherplover,itwasconsideredtohavedesertedthebrood.We
estimatedthedateofbrooddesertionforaparentasthemid‐point
betweenthe time when theindividualwaslast seen withhis/her
broodandfirstseenwithoutthebrood.Weestimated secondnest
FIGURE 1 Schematicillustrationof
twoestimatesofbetween‐yearmate
fidelityinsnowyplovers:Early‐lateand
early–earlymatefidelities
    
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 5
HALIMU BIEKE Et A L.
egg‐layingdatebasedonthefloatingstageoftheeggs(seeabove).
Weonlyestimatedthere‐matingtimeswithinyears.
2.3 | Statistical analyses
2.3.1 | Comparison of male and female mate fidelity
Weanalyzedmatingdecisionaseithermateretentionordivorceof
aploverfromanindividualitspreviousbreedingattempt.Wecalcu
latedthenumberofmateretentionsandnumberofdivorcesinmales
and females within the population for both within and between
years. Weused thetwo‐proportion ztest (Yau, 2013) tocompare
theproportionofdivorcedfemalesrelativetothefemalepopulation
totheproportionofdivorcedmalesrelativetothemalepopulation
bothwithinandbetweenyears.
2.3.2 | The relationship between mate fidelity and
nesting success
Weconstructedseparatemodelsformales andfemalesto investi‐
gatewhethermatefidelityisrelatedto nesting successwithinand
betweenyears.Here, separationofthe sexeswas necessarysince
nesting success is nonindependent variable within a pair; there
fore,individualsofapairprovidethesamedatapoints.Inthelatter
analyses,matefidelityofanindividualwasthedependentvariable,
and nest ing success was us ed as explanato ry variabl e. Toana lyse
thefemales,weusedgeneralizedlinearmixedmodels(GLMM)with
binomialerrorandincludedIndividualIDandYearasrandomeffect
variables to account for the repeated identities offemales among
years. Formales,weused generalizedlinear model (GLM) withbi‐
nomialerror.
2.3.3 | Reproductive success and mate fidelity
Toinvestigatewhethermatefidelity relatestoreproductivesuc
cess (estimated as the total number of hatchlings from both
clutches),wecompareddivorcedmales,divorcedfemales,retained
pairs using Kruskal–Wallis tests followed by post hoc pairwise
comparisons(Dunntest)to testgroupdifferenceswithinandbe
tweenyears.
2.3.4 | Breeding dispersal and mate fidelity
Modelswerebuilttoinvestigatetherelationshipbetweenbreeding
dispersal and matefidelity groups withinand betweenyears. Log‐
transformed(ln)breedingdispersalwasthedependentvariable,and
matefidelitygroups(divorcedmales,divorcedfemales,andretained
pairs) were the explanatory variable. Linear mixed‐effects model
(LMM)via REMLwasfitted and maintainedIndividual ID andYear
as random effect variables. Then, the estimated marginal means
(emmeans frompackage“emmeans” in R)werecalculated for each
group, posthoc pairwisecomparisons adjusted by Tukey were ap‐
pliedtotestgroupdifferences.
2.3.5 | Re‐mating time and mate fidelity
Toinvestigate whether re‐matingtime differsbetweenmatefidel‐
itygroups(divorcedmales,divorcedfemales,andretainedpairs),we
used Kruskal–Wallistests followed by post hoc pairwise compari‐
sons(Dunntest)totestgroupdifferenceswithinandbetweenyears.
AllstatisticalanalyseswereperformedusingRversion3.5.1(RCore
Team,2018).
3 | RESULTS
3.1 | Mate fidelity between sexes
Within breeding years, malesshowed highermate fidelitythan fe‐
malesusing149breedingevents(Table1A, 75divorcesinfemales,
26 divorces in males, and 24 retentions in each sex) from 2006
to2011, two‐proportionz test, p =.002, n=6years).Thediffer
entnumbersoffemale andmalebreedingattempts are duetothe
factthat more femalesthanmaleshadmultiplebreedingattempts.
Betweenbreeding years, however,we did notfind adifference in
mate fidelity of males versus females (Table 1B, two‐proportion z
test;late–earlymatefidelity:p=1.00,n=5years;early–earlymate
fidelity:p=.55,n=5years).
3.2 | Mate fidelity in relation to nesting success and
reproductive success
Withinbreedingyears, matefidelitywasrelated tonestingsuccess
since divorce was more likelywhen thenesthatchedsuccessfully,
whereas materetentionwasmore likelyifthenestfailed (Table2,
females:GLMM,p<.001,male:GLM,p<.001;Figure2).Between
breedin g years, however, mate fi delity was not r elated to nestin g
success. The latter result was consistent between the late–early
matefidelityandearly–earlymatefidelity(Table2).
Divorcedplovers(bothmalesandfemales)producedsignificantly
more hatchlings within breeding years than those retained their
mate. Reproductive success was not different between divorced
malesanddivorcedfemales(Table3,Kruskal–Wallistests,p<.001,
followed by post hoc pairwise Dunn test; divorced females—re‐
tained pairs: p adjusted < .001, divorced males—retained pairs: p
adjusted=.05,divorcedfemales—divorcedmales: padjusted=.07;
Figure 3). Between breeding years, however,reproductive success
wasnotdifferentbetweendivorcedandretainedindividualsneither
inthelate–earlynorintheearly–earlycomparisons(Kruskal–Wallis
tests;late–earlymatefidelity:χ2 =0.20,df=2,p=.90;early–early
matefidelity:χ2=4.21,df=2,p=.12).
3.3 | Mate fidelity in relation to breeding
dispersal and re‐mating time
Divorcedfemalesbredfurtherawaythandivorcedmalesbothwithin
andbetweenyears(Figure4,Table4).Divorcedmales,however,did
notbreedfurtherawaythanretainedpairs(Table4).
6 
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TABLE 2 Matefidelityinrelationtonestingsuccesswithinandbetweenbreedingyearsinsnowyplover
Response variable Model used Explanatory variable Estimate SE z value p value
Withinyears
Female
Matefidelity Binomial(GLMM) Intercept 0.92 0.42 −2.19 .03
Nestingsuccess 4.38 0.83 5.27 <.0 01
Male
Matefidelity Binomial(GLMM) Intercept −1 5.9 2 5.16 −3.09 .002
Nestingsuccess 29.17 7. 5 9 3.84 <.0 01
Betweenyears:late–early
matefidelity
Female
Matefidelity Binomial(GLMM) Intercept 1.39 0.79 1.75 .08
Nestingsuccess −0.06 0.87 0.07 .95
Male
Matefidelity Binomial(GLM) Intercept 1.50 0.78 1 .92 .05
Nestingsuccess −0.33 0.87 −0.38 .70
Betweenyears:early–early
matefidelity
Female
Matefidelity Binomial(GLMM) Intercept 1.47 1.19 1.23 .22
Nestingsuccess −0.75 1.25 −0.60 . 55
Male
Matefidelity Binomial(GLM) Intercept 2.30 1.05 2.20 .03
Nestingsuccess −1.37 1.10 −1.26 .21
Note: Generalizedlinearmixedmodels(GLMM)withbinomialerrorfamilyandincluding“IndividualID”and“Year”asrandomeffectvariablestoac‐
countfortherepeatedidentitiesoffemaleindividualsamongyears.Formales,generalizedlinearmodel(GLM)withbinomialerrorfamilywasused.
Abbreviation:SE,standarderror.
Statisticallysignificantresultsarepresentedinbold.
FIGURE 2 Matefidelityinrelationto
nestingsuccessin(a)femaleand(b)male
snowyploverswithinayear(seeTable2
forstatistics).Logisticlinearregression
lines(blue)withstandarderror(gray)
Retained
Di
vorced
Failed Successful
Nesting success
(a) Females
Faile
dS
uccessful
Nesting success
(b) Males
    
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HALIMU BIEKE Et A L.
Finally, re‐mating times were not different between divorced
males, divorced females and retained pairs (Kruskal–Wallis test,
χ2=2.00,df=2,p=.37).
4 | DISCUSSION
Previous analyses of mate fidelity were typic ally concerned with
either within‐yearor between‐yearmate fidelityand focus largely
onmonogamoussystems(sometimestermedmatedesertion,mate
abandonmentormatechange;Black,2001;Briedetal.,2003;Flodin
&Blomqvist, 2012). Here,wetake an integrative approach andin‐
vestigate mate fidelity both within and between breeding years.
Using a sequential polygamous shorebird, the snowy plover, we
identifiedfactorsthatpredict matefidelityandits spatial‐temporal
manifestationinasystem,inwhichmalesandfemalesdifferintheir
breedingstrategiesandreproductiveefforts.
Our anal yses revealed t hree major res ults. Firs t, males exh ibit
higherwithin‐yearmatefidelitythanfemales.Thisisconsistentwith
thepreviousstudies of snowyplover sincefemalestend to desert
thebroodwhereasmales are usually theones thatrear the young
(Carmona‐Isunzaetal.,2015;Warrineretal.,1986).Wesuggestthat
male‐biasedadult sex ratioenticesfemale parents more thanmale
parentstodeserttheirbroodandbreedagain(Eberhart‐Phillipsetal.,
2017;Stenzeletal.,2011);therebyresultingindifferentre‐mating
opportunitiesand matefidelities betweenmales and females. The
latterresultsareconsistentwithexperimental and empiricalstud
ies that sh ow altered adult se x ratios influen ces mating decis ions
(Karlsson, Eroukhmanoff, & Svensson, 2010; Liker, Freckleton, &
Székely,2013;Likeretal., 2014;Silva, Vieira, Almada, & Monteiro,
2010).
However,between years bothmale andfemalesnowy plovers
demons trated low mate fid elity. We note however that ou rm ate
fidelity(and consequently,ourdivorce decision as well)was based
onlocalreturningrates:ifpairedbirdsmaybreedoutsidethestudy
area and/or som e of the survive d adults may n ot return to bree d
toCeuta,thesesurvivalestimatescanbebiased.Theannualreturn
ratetoCeutaare41.5%formales(n=378individuals)and35.4%for
females(n=339individuals,2006–2011).Therefore,furtherinves
tigationisrequiredtoestimatemorepreciselythereturnratesusing
morecomprehensivespatialcoveragebyvisitingadditionalbreeding
sitesnearCeutaand/orusingGPStagstomonitorthemovementsof
adultswithinandbetweenyears.
Second,divorcewasmorelikelyafteranesthatchedthanafter
itfailedsincefailedbreederstypicallyre‐nestedwiththesamepart
ner. Therefore, divorced plovers, counterintuitively, reared more
offspringthanfaithfulindividuals.Thisfindingisnotconsistentwith
studiesoflong‐lived birdspecieswhere low breedingsuccess may
trigger divorce (“incompatibility hypothesis,”Black, 2001;Coulson,
1966;Jouventin&Bried,2001).Weproposethatbyabandoningthe
Groups Z p unadjusted p adjusted
Withinyears
Divorcedfemales—divorcedmales 1.97 <.001 .07
Divorcedfemales—retainedpairs 4.08 <.001 <.0 01
Divorcedmales—retainedpairs 1.92 <.0 01 .05
Statisticallysignificantresultsarepresentedinbold.
TABLE 3 Comparisonofreproductive
successbetweenmatefidelitygroups
(divorcedmales,divorcedfemales,and
retainedpairs)withinbreedingyears
(Kruskal–Wallistests,p<.001,followed
byposthocpairwiseDunntest)
FIGURE 3 Reproductivesuccessin
relationtodivorceormatefidelityin
snowyplovers(seeTable3forstatistics).
Medians,upper,andlowerquartiles,as
wellasextremevaluesareshown
0
2
4
6
Divorced females Divorced males Retained pairs
Total number of hatchlings
8 
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   HALIMUBIEKE E t AL.
broodanddivorcing,individualstrytomaximizetheirreproductive
successbyproducingasmanyclutchesovertheseasonaspossible.
Divorce may befacilitated by twoaspects of natural history:first,
nestandchickmortality inthispopulationtendtobehighandsto‐
chastic,andthus,parentsmayneedseveraltrialstoproduceatleast
somefledglings(Cruz‐López,Eberhard‐Phillips,etal.,2017).Second,
thechicks are precocial, andthus, they only requiremodest care:
broodingand protection, butnot feeding (Székely & Cuthill & Kis,
1999).Thewell‐developedhatchlingthengivestheopportunityfor
oneparenttoterminatecareandstartbreedingwithanewpartner
(Houston,Székely,&McNamara,2013;McNamara,Forslund,&Lang,
1999;Székely,Webb,Houston,&McNamara,1996).Materetention
was,however,morelikelyafternestfailure,inwhichcasetheparen
tal duties of both parents terminatedat thesame time; therefore,
the fastest wayto breedagainwas to retain the previous partner
(“fast‐trackhypothesis”;Perfito et al., 2007;Zann, 1994; reviewed
byFowler,1995;alsoseeAdkins‐Regan&Tomaszycki,2007).
However, breeding success in previous years may have little
impact o n the re‐mating de cision of snowy plove rs. We presume
that the breeding time constraint facilitates early breeding with
TABLE 4 (A)Breedingdispersalinrelationtomatefidelitygroups(divorcedmales,divorcedfemales,andretainedpairs)withinand
betweenbreedingyears.(B)Comparisonofbreedingdispersalbetweenmatefidelitygroups(divorcedmales,divorcedfemales,andretained
pairs)withinandbetweenbreedingyears
(A)
Response variable Model used Explanatory variable Estimate SE t value
Withinyears
Breedingdispersal LMM Intercept 6.46 0.16 38.85
Divorcedmales 0.95 0. 26 −3.63
Retainedpairs −0.67 0.26 −2. 5 8
Betweenyears:late–early
Breedingdispersal LMM Intercept 6. 41 0.21 30.25
Divorcedmales −1 . 01 0.30 −3.37
Retainedpairs −0.70 0.39 −1. 7 7
Betweenyears:early–early
Breedingdispersal LMM Intercept 5.87 0. 29 20.48
Divorcedmales 0.95 0.38 −2 .53
Retainedpairs −0.73 0.33 −2 . 23
(B)
Groups Estimate SE df t ratio p value
Withinyears
Divorcedfemales—divorced
males
0.95 0.26 111 3.60 .001
Divorcedfemales—retained
pairs
0.67 0.26 112 2.57 .03
Divorcedmales—retainedpairs −0.28 0. 26 68 −1.0 5 . 55
Betweenyears:late–early
Divorcedfemales—divorced
males
1.01 0.31 72 3.28 .005
Divorcedfemales—retained
pairs
0.70 0. 41 72 1.70 .21
Divorcedmales—retainedpairs −0.32 0.44 85 0.71 .76
Betweenyears:early–early
Divorcedfemales—divorced
males
0.95 0.38 70 2 .51 .04
Divorcedfemales—retained
pairs
0.73 0.35 56 2.09 .10
Divorcedmales—retainedpairs −0.22 0.44 88 −0.50 .87
Note: Thelinearmixed‐effectsmodel(LMM)viaREMLwasfittedandmaintained“IndividualID”and“Year”asrandomeffectvariables.
Abbreviation:SE,standarderror.
Statisticallysignificantresultsarepresentedinbold.
    
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 9
HALIMU BIEKE Et A L.
availablematesinsteadofwaitingfortheformerpartner,especially
sinceearlybreedingisassociatedwithhighernestsurvival(Plaschke
etal., 2019; van dePol, Heg,Bruinzeel, Kuijper,&Verhulst,2006;
Székelyetal.,1999).Sincesnowyploversonlyhaveabout2yearsof
breedinglife(averagebreedinglifeofmales:2.3±1.6years;females:
1.9 ± 1.2 years; Colwell, Pearson, Eberhart‐Phillips, & Dinsmore,
2013),theymaynotdiscriminateagainstpreviousmatesevenifthey
werefailedbreedersFurthermore,returningtothebreedingground
may be stoch astic and this c an also produ ce decoupling be tween
nesting success and mate fidelity (Bried, Frédéric, & Jouventin,
1999;Gilsenan,Valcu,&Kempenaers,2017;Handel&Gill,2000).
Third,wefoundthatfemalestendtodispersefartherthanmales
afterdivorcebothwithinandbetweenbreedingyears.Thisfollows
thegeneralpatternoffemale‐biasedbreedingdispersalobservedin
mostbirdspeciesincludingshorebirds(Clarke, Saether,&Roskaft,
1997;Greenwood& Harvey,1982;Liu& Zhang,2008;Sandercock
etal.,2000).However,inpolyandrousbirdslikesnowyploversthere
isanadditionalreason: findingnewmatewhiletheirpreviousmate
istakingcareofthechicks(D'UrbanJacksonetal.,2017).Formales,
returningtopreviousbreedingsite—thatisoftenthoughtasahigh‐
qualitysiteprovidinggoodbrood‐rearingopportunities(Sandercock
etal.,2000)—isafac torthatreducestheiraptitudemovinglargedis
tancebetweennests.Matefidelityisoftenrelatedtothedegreeof
sitefidelity(Cézilly,Dubois,&Pagel,2000;Cézilly&Johnson,1995),
and while it would betempting to argue that higher mate fidelity
leadtohighersitefidelityinmales,orviceversahighdivorcerateby
females leadtomoreextensivebreedingdispersal,toconcludethe
direct ionality of c ausation—and t o separate whe ther the male s or
thefemales drive these relationships—would require experimental
manipulationofmatefidelity,sitefidelity,orboth.
Together,ourresultssupporttheoreticalargumentsthatdivorce
is an adaptive strategy by which individuals improve their repro
ductivesuccess(Black,1996;Dubois& Cézilly,2002;McNamara&
Forslund,1996).Divorcedbirdsreachedhighernumberofbreeding
attemptsandhigherbreedingsuccessthanindividualsthatretained
theirmates,atleastwithinyears.Wesuggestthatinsnowyplovers,
divorce is result from their effort to maximize reproductive out‐
putduring a giventimeperiod.Thebirds' urge to re‐mateasmany
timesaspossiblewithinabreedingseasonandproducethehighest
possiblenumber of chicks couldbe traded offbylowered survival
oftheirabandoned broods although, giventhe precociality ofthe
young, this costmaynotbeprohibitive(Székely &Williams,1995).
Wesuggestthattheurgeforafastreproductioninsnowyploversis
anadaptiveresponsetolifehistories(i.e.,shortlifespan)andbreed
ing para meters (i.e., sho rt breeding p eriod and breed ing success).
Additionally,time constraintinbreeding confounded withthe bias
FIGURE 4 Breedingdispersal(a)withinyear,andbetweenyear(b,late–early)and(c,early–early)insnowyplover(seeSection2for
explanationsandTable4forstatistics).Breedingdispersalwasestimatedinmetersandlog‐transformed(ln).Medians,upper,andlower
quartiles,aswellasextremevaluesareshown
1
2
3
4
5
6
7
8
Breeding dispersal (meters, log−transformed)
(a)
Divorced femalesDivorced malesRetained pairsDivorced females Divorced males Retained pairs
(b)
Divorced femalesDivorced males Retained pairs
(c)
10 
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   HALIMUBIEKE E t AL.
inpopulationdemography(i.e.,male‐biasedadultsexratio)propels
bothsexes adopt differentmating strategies,resultingin different
spatialdispersalpatterns.Therefore,matechoiceandbreedingdis
persalareimportantcomponentsoftheirbreedingstrategy.Ween
courage furtherinvestigations ofbreeding strategyincludingmate
fidelitybetweendifferentpolygamousshorebirdpopulationsandto
understandthegeneralityofourfindingsacrossthevariousnatural
populationswiththeintentionofinformingconservationdecisions.
ACKNOWLEDGMENTS
Wethankallfieldworkvolunteersandpeoplewhohaveworkedand
supported the conservation project ofSnowy plovers at Bahía de
Ceuta,especially to Clemens pper andCristinaCarmona‐Isunza
for data collection. Thanks to JenniferMcDowall, Luke Eberhart‐
Phillips,KathrynMaher,JuditMokos,andBrettSandercockfortheir
adviceonpreviousversionsofthemanuscript.
CONFLICT OF INTEREST
Wehavenoconflictofinteresttodeclare.
AUTHORS' CONTRIBUTIONS
N.H.,P.H.,andT.S.conceivedtheproject;K.K.,M.A. S.‐M.,and
M.C.‐L. providedthedata;N.H.andK.K.carriedoutthe statisti‐
calanalyses.Allauthorscontributedcriticallytothedraftsandgave
finalapprovalforpublication.
DATA AVA ILAB ILITY STATE MEN T
Data are ava ilable from the D ryad Digita l Repository, http s://do i.
org/10.5061/dryad.3185h66
ETHICS STATEMENT
Allaspec tsofthefieldworkwereauthorizedbythenationalauthori
tiesofMexico(SecretaríadeMedioAmbienteyRecursosNaturales,
SEMARNAT; SGPA/DGVS/01717/10, SGPA/DGVS/01367/11).
Birdswereringedandhandledbytrainedpeopleaimingtocauseas
littledisturbancetobirdsaspossible.
ORCID
Naerhulan Halimubieke https://orcid.org/0000‐0002‐6928‐5986
José O. Valdebenito https://orcid.org/0000‐0002‐6709‐6305
Philippa Harding https://orcid.org/0000‐0003‐0763‐3516
Medardo Cruz‐López https://orcid.org/0000‐0003‐1737‐9398
Martín Alejandro Serrano‐Meneses https://orcid.
org/0000‐0002‐0163‐4983
Richard James https://orcid.org/0000‐0002‐8647‐7218
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How to cite this article:HalimubiekeN,ValdebenitoJO,
HardingP,etal.Matefidelityinapolygamousshorebird,the
snowyplover(Charadrius nivosus).Ecol Evol. 2019;00:1–12.
https://doi.org/10.1002/ece3.5591
... For example, arctic bird species have typically short breeding seasons due to the harsh and stochastic environmental conditions, and tend to exhibit high fidelity to a mate, which is likely to improve offspring survival 17,18 . In contrast, mild environments in temperate and tropical regions tend to provide a more prolonged breeding season so that an individual might initiate multiple clutches with the same or different mates 1,19,20 . The influence of environmental conditions on mating decisions has been observed in a variety of taxa including flies, fish, frogs and birds [21][22][23] . ...
... It has also been suggested that divorcing and rapidly changing a mate may be favoured by some species in order to make the most out of a restricted time budget (e.g. short life span or short breeding season) 1,40 . ...
... In a recent study, Halimubieke et al. 1 reported that snowy plovers (Charadrius nivosus), especially females, are more likely to divorce after successful nesting, simultaneously deserting their current brood, and initiate a new breeding attempt with a different mate, whereas, pairs tend to stay together after failed breeding attempts and initiate a second nesting attempt with the same mate. Divorcing individuals reared more offspring than those that retained their mates. ...
Article
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When individuals breed more than once, parents are faced with the choice of whether to re-mate with their old partner or divorce and select a new mate. evolutionary theory predicts that, following successful reproduction with a given partner, that partner should be retained for future reproduction. However, recent work in a polygamous bird, has instead indicated that successful parents divorced more often than failed breeders (Halimubieke et al. in Ecol Evol 9:10734-10745, 2019), because one parent can benefit by mating with a new partner and reproducing shortly after divorce. Here we investigate whether successful breeding predicts divorce using data from 14 well-monitored populations of plovers (Charadrius spp.). We show that successful nesting leads to divorce, whereas nest failure leads to retention of the mate for follow-up breeding. plovers that divorced their partners and simultaneously deserted their broods produced more offspring within a season than parents that retained their mate. our work provides a counterpoint to theoretical expectations that divorce is triggered by low reproductive success, and supports adaptive explanations of divorce as a strategy to improve individual reproductive success. in addition, we show that temperature may modulate these costs and benefits, and contribute to dynamic variation in patterns of divorce across plover breeding systems. open
... The decision to remain paired with the same partner or to change partners can be vital to lifetime reproductive output (Bradley et al. 1990;Black 2001;Sánchez-Macouzet et al. 2014). While mate switching has the advantage of improving life-long reproductive success by increasing offspring genetic diversity, pairing with a mate of higher quality/compatibility than the current partner, or increasing the number of breeding attempts during the current season (Choudhury 1995;Spoon et al. 2007;Culina et al. 2015;Halimubieke et al. 2019), mate retention can enhance breeding success via better coordination of parental effort (Black 2001;Griggio and Hoi 2011;Dreiss and Roulin 2014;Sánchez-Macouzet et al. 2014). Mate retention decisions can be affected by the quality of the territory held by the partners and the success of the pair's previous breeding attempts (Desrochers and Magrath 1993;Dubois and Cézilly 2002; but see Handel and Gill 2000). ...
... Beissinger 1987;Olson et al. 2008;Kupán et al. 2021). Uniparental brood desertion is well known in mating systems, in which it is a fixed element of the breeding strategy due to benefits from allocation of parental effort to multiple broods sired with different partners within the same season; the costs of desertion are relatively low if the young are fully precocial and biparental care has little advantage for the offspring over uniparental care (Székely et al. 2006;Pierce et al. 2010;Halimubieke et al. 2019). However, premature brood abandonment by one parent has also been observed in some socially monogamous species in which both mates provide extended and demanding parental care, and deserters may not have enough time or resources to raise another set of offspring (Kelly and Kennedy 1993;Osorno and Székely 2004;Vlug 2007;Ledwoń and Neubauer 2017). ...
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In monogamous birds, pair bond maintenance is often dependent on previous breeding success and each parent’s effort, because partners gain information about one another’s quality and contribution to brood rearing. The asymmetries between mates in parental investment have been theoretically linked to a sexual conflict of interests. Year-to-year pair fidelity decisions in relation to birds’ previous-year information about their mates, including territory quality and relative length of brood care, were explored in red‐necked grebes (Podiceps grisegena), a long-lived species with parent-fed young. Overall, mate retention was a major strategy (81.5% of pair-years). The probability of breakage/maintenance of a pair bond was not affected by previous-year hatching success, fledgling production, or territory quality in terms of food abundance for chicks. Reunited pairs bred earlier in the season than new pairs. In pairs that maintained bonds into the subsequent season, females typically terminated care 1–4 weeks before males. The male fidelity indicates that earlier brood abandonment by females may confer some fitness benefits to males and reflect coordination of reproductive effort at the behavioural level rather than exploitation of one partner by another. Significance statement Pair-living animals deciding whether to keep their old mate for future breeding usually consider their previous reproductive success and the partner’s effort. In some monogamous birds, often one of the parents leaves the brood before its mate, which is usually explained in terms of conflict between the sexes over parental care costs. I studied links between previous year’s parental effort and mate retention in red‐necked grebes, a long-lived waterbird. Grebes showed high pair fidelity irrespective of recent breeding success. In pairs that stayed together, females typically terminated brood care earlier than their mates. The male fidelity indicates that the unequal duration of brood attendance can be interpreted as cooperation and not conflict, especially as departing females did not attempt a second brood, while male-only care after female departure was sufficient to raise the young.
... Deserting and re-mating Snowy Plovers attempt to Reproductive success (a) and breeding time (b) of deserting and locally re-mating (N = 9) and full-term caring (N = 5) Snowy Plover females at Ceuta. maximize their reproductive success by rapid divorce after hatching as divorced females produce a higher number of hatchlings than females that retain their mates (Halimubieke et al. 2019). Yet, we confirmed that desertion does not necessarily translate into producing more fledglings . ...
... However, it also shows that chick survival is generally low. Some of the dispersing females may reach higher reproductive success than locally re-mating females (Halimubieke et al. 2019). However, the breeding time of dispersers must be even higher than that of caring or locally re-mating females as some females disperse to great distances, therefore, breeding dispersal must take up further time (Stenzel et al. 1994). ...
Article
Offspring desertion is often a plastic behavioral strategy that requires precise timing as the termination of parental care may have profound consequences for the fitness of parents and offspring. However, the decision process involved with termination of care is still poorly understood. Snowy Plovers Charadrius nivosus show highly flexible brood care with some females deserting the brood early and re-mate, whereas others provide extended care until the young are independent. Using a dynamic modeling framework, we investigated the effect of multiple factors on the decision-making process of female brood care in Ceuta, Mexico over a 7-year period. Females were more likely to stay with larger broods, while their probability of care was lower at the beginning of the season, when re-mating opportunities are higher than later in the season. Offspring condition at hatching did not influence the length of female care. Chick death and offspring desertion frequently coincided, suggesting that deteriorating offspring condition may trigger female desertion. Females deserted broods with high survival prospects when their absence did not impact negatively chick survival. Conversely, females deserted broods with low survival prospects when chick mortality despite female care reduced the value of the brood and re-mating was still possible. This suggests that female Snowy Plovers are sensitive to the needs and the value of their broods and adjust their parental care strategy accordingly. Taken together, we conclude that offspring desertion is a highly plastic behavior that allows females to maximize their reproductive success in a stochastic environment.
... El chorlo nevado tiende a tener un cuidado biparental, aunque sesgado hacia los machos y las poblaciones reproductivas están compuestas en su minoría por hembras , Stenzel et al. 2011, Halimubieke et al. 2019, condición que también se presenta en la colonia reproductiva de la laguna de Atotonilco, donde la población registrada tanto para toda la temporada como en los conteos mensuales, los machos conformaron la mayor parte de la población. Se estima que las poblaciones de chorlo nevado en todos sus linajes han estado sufriendo un "cuello de botella", por lo que las poblaciones efectivas de la especie son bajas y la especie es vulnerable (Jackson et al. 2020). ...
Article
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The snowy plover (Charadrius nivosus) is one of the least abundant shorebirds. It is an endangered species whose populations are in steady decline. Mexico is important for the populations of this species, but there is little information on its reproduction and threats. To obtain data on nesting and potential threats, we monitored the snowy plover population at Atotonilco Lagoon during the breeding season (March-July) in 2020. We conducted counts of individuals and nests, clutch size, approximate egg-laying date, and observations on threats present during this period. Males represented 85% (n = 140) of the total population and the month with the highest number of nests was May (n = 15). The average nest size was 2.5 eggs. Water surface area was variable during the sampling months, but it was not statistically proven that the greater the desiccation, the smaller the nest size (p = 0.09). The main threats identified were motorized vehicles and livestock. The Atotonilco Lagoon is a key site for snowy plover reproduction and management actions should be implemented to increase the presence of water and regulate human activities.
... However, an increased divorce rate after a successful breeding attempt does not necessarily demonstrate that divorce is nonadaptive. Divorce after a successful reproduction has been shown to be an adaptive strategy to maximize LRS in multiple plover species (Halimubieke et al., 2019(Halimubieke et al., , 2020 or inbreeding avoidance in long-tailed tits (Aegithalos caudatus) (Hatchwell et al., 2000). We also found that the divorce probability increases when females have a higher breeding success with their previous partner (Appendix S1: Figure S11). ...
Article
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Many animals form long‐term monogamous pair‐bonds, and the disruption of a pair‐bond (through either divorce or widowhood) can have significant consequences for individual vital rates (survival, breeding, and breeding success probabilities) and life‐history outcomes (lifetime reproductive success, life expectancy). Here, we investigated the causes and consequences of pair‐bond disruption in wandering albatross (Diomedea exulans). State‐of‐the‐art statistical and mathematical approaches were developed to estimate divorce and widowhood rates and their impacts on vital rates and life‐history outcomes. In this population, females incur a higher mortality rate due to incidental fishery bycatch, hence the population is male‐skewed. Therefore, we first posited that males show higher widowhood rates negatively correlated with fishing effort, and females have higher divorce rates because they have more mating opportunities. Furthermore, we expected that divorce can be an adaptive strategy, whereby individuals improve breeding success by breeding with a new partner of better quality. Finally, we posited that pair‐bond disruptions can reduce survival and breeding probabilities due to the cost of remating processes, with important consequences for life‐history outcomes. As expected, we show that males have higher widowhood rates than females and females have higher divorce rates in this male‐skewed population. However, no correlation was found between fishing effort and male widowhood. Secondly, contrary to our expectation, we found that divorce is likely non‐adaptive in this population. We propose that divorce in this population is caused by an intruder who outcompetes the original partner in line with the “forced divorce” hypothesis. Furthermore, we found a 16.7% and 18.0% reduction in lifetime reproductive success (LRS) only for divorced and widowed males, respectively, due to missing breeding seasons after a pair‐bond disruption. Finally, we found that divorced individuals are more likely to divorce again, but whether this is related to specific individual characteristics remains an important area of investigation.
Article
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Parents are expected to make fine-tuned decisions by weighing the benefits of providing care to increase offspring survival against that of deserting to pursue future mating opportunities. A higher incentive for the rarer sex in the population indicates an impact of mating opportunities on parental care decisions. However, in a dynamic breeding system, deserting the offspring and searching for a new mate would influence mating opportunities for both sexes. Sex-specific costs and benefits are expected to influence males’ and females’ parenting strategies in different ways. Here, we investigated Chinese penduline tits, Remiz consobrinus, which exhibit flexible parental care strategies: uniparental care by the male or female, biparental care, and biparental desertion occur in the same population. We show that male penduline tits change their parental behavior over the breeding season; they desert clutches produced early in the season but care for the late season clutches. The change in male parenting behavior is consistent with the seasonal decline in mating opportunities. In contrast, parenting by females did not change over the breeding season, nor was it associated with seasonal variation in mate availability. Taken together, mating opportunities have different associations with parental behavior of male and female Chinese penduline tits. We recommend an inclusion of mating opportunities for both sexes simultaneously in order to understand one of the fundamental decisions in parental care evolution—care or desert. Significance statement Divorce is a common feature of both human and nonhuman animal societies. Theoretical studies suggest that one of the drivers of divorce is enhanced mating opportunity, i.e., parents with higher mating opportunities are more likely to abandon their family than those with low mating opportunities. Here, we investigate the dynamics of parental behavior and mating opportunities in a wild population of a small songbird, the Chinese penduline tit Remiz consobrinus. This species exhibits one of the most diverse avian breeding systems wherein both uniparental (male or female) and biparental rearing can be seen in a single population. We show that male penduline tits abandon their offspring in response to enhanced mating opportunities while the female parental behavior remains unaffected. This implies the relationship between mating opportunities and parental care is more complex than currently acknowledged and requires further investigation.
Article
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Shorebirds (part of the order Charadriiformes) have a global distribution and exhibit remarkable variation in ecological and behavioural traits that are pertinent to many core questions in the fields of evolutionary ecology and conservation biology. Shorebirds are also relatively convenient to study in the wild as they are ground nesting and often occupy open habitats that are tractable to monitor. Here we present a database documenting the reproductive ecology of 1,647 individually marked snowy plovers (Charadrius nivosus) monitored between 2006 and 2016 at Bahía de Ceuta (23°54N, 106°57W) – an important breeding site in north-western Mexico. The database encompasses various morphological, behavioural, and fitness-related traits of males and females along with spatial and temporal population dynamics. This open resource will serve as an important data repository for addressing overarching questions in avian ecology and wetland conservation during an era of big data and global collaborative science.
Preprint
Full-text available
Shorebirds ( partim members of order Charadriiformes) have a global distribution and exhibit remarkable variation in ecological and behavioural traits that are pertinent to many core questions in the fields of evolutionary ecology and conservation biology. Shorebirds are also relatively convenient to study in the wild as they are ground nesting and often occupy open habitats that are tractable to monitor. Here we present a database documenting the reproductive ecology of 1,600 individually marked snowy plovers ( Charadrius nivosus ) monitored between 2006 and 2016 at Bahía de Ceuta (23°54 N, 106°57 W) − an important breeding site in north-western Mexico. The database encompasses various morphological, behavioural, and fitness-related traits of males and females along with spatial and temporal population dynamics. This open resource will serve as an important data repository for addressing overarching questions in avian ecology and wetland conservation during an era of big data and global collaborative science.
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Offspring desertion represents a trade-off between current and future reproductive success. Its timing is crucial as the termination of parental care has profound consequences for the fitness of the parents and their offspring. However, the decision process involved with termination of care is still poorly understood. Snowy Plovers Charadrius nivosus show highly flexible brood care with females either deserting the brood early or providing care for an extended period. Deserting females often quickly re-mate and start a new breeding attempt. Using a dynamic modelling framework, we investigated the decision-making process for continuation or termination of care by females over a seven-year period. The length of female care increased over the season likely reflecting lower re-mating opportunities for deserting females late in the season. Present brood size, assessed daily during the brood care period, was strongly related to the length of female care: females were more likely to stay and care for larger than for smaller broods. Chick death and desertion frequently coincided, suggesting that poor offspring condition served as a trigger for female desertion. Overall, deserting females had a similar number of fledglings to caring females. This suggests that for many females, desertion was not a strategy to escape the shackles of monogamy and secure higher reproductive success through sequential polygamy. Rather, most deserting females made the best of a bad job when conditions were poor and their continued presence did not make a difference for the survival of their young. We conclude that when making the decision to continue or terminate care, Snowy Plover females monitor the condition of their offspring closely and adjust their care flexibly to the value and needs of their young.
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Divorce occurs when both members of a breeding pair survive to the following year but then pair with other individuals instead of reuniting. Divorce is common in birds, but its frequency can vary widely both between and within species, or even between populations across years. Several explanations for divorce have been described, both adaptive and nonadaptive. Many studies have compared the breeding success of faithful and divorced individuals, but fewer have considered the process of divorce, i.e. the events that lead up to divorce. In this study, we used data from eight breeding seasons to investigate divorce in a population of blue tits, Cyanistes caeruleus, in southern Germany. To compare our results to previous work, we first describe the frequency of divorce and compare the breeding success of divorced and faithful pairs. We then use data from an RFID transponder-based system, where all visits of individuals to any nestbox in the study site are automatically recorded throughout the year, to compare the behaviour of pairs in the interbreeding period. We found that the probability of divorce was not affected by breeding success in Year X. However, divorce was predicted by the difference in arrival time to the study site between the members of Year X pairs. Furthermore, during the interbreeding period, compared to their divorced counterparts, members of faithful pairs had more interactions with one another than with other individuals of the opposite sex. In Year X + 1, faithful females started egg laying earlier, had somewhat larger clutches and produced slightly more fledglings, than females that had divorced. We propose that divorce in blue tits is a by-product of separation of the two pair members after the Year X breeding season, leading to asynchrony in the timing of settlement and pair formation in Year X + 1.
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Shorebirds (sandpipers, plovers and allies) are some of the most charismatic animals that breed on all continents and inhabit diverse habitats, and their ecology, behaviour and evolution have attracted much attention ever since the work of Charles Darwin. Here I summarise the insights from 30 years of research on shorebird biology to illustrate the contributions of these to four research fields: breeding system evolution, sex ratio research, speciation and biodiversity conservation. Two major conclusions can be drawn from these insights. First, as shorebirds live in a variety of habitats and exhibit puzzling adaptations to their environments, studying their ecology, behaviour and life histories provides novel insights into the emergence and maintenance of organismal diversity. Second, to uncover patterns and processes in evolution, it is both important and stimulating to combine different research methods, and detailed single-species studies with multi-species comparative approach. My main thesis is that curiosity-driven research into the natural history of non-conventional model organisms provides novel insights into fundamental processes in ecology, behaviour and evolution. I also argue that scientific funding should follow the Goldilocks principle: not too little, not too much, just the right amount.
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Background Marine and intertidal organisms face the rhythmic environmental changes induced by tides. The large amplitude of spring tides that occur around full and new moon may threaten nests of ground-nesting birds. These birds face a trade-off between ensuring nest safety from tidal flooding and nesting near the waterline to provide their newly hatched offspring with suitable foraging opportunities. The semi-lunar periodicity of spring tides may enable birds to schedule nest initiation adaptively, for example, by initiating nests around tidal peaks when the water line reaches the farthest into the intertidal habitat. We examined the impact of semi-lunar tidal changes on the phenology of nest flooding and nest initiation in Snowy Plovers (Charadrius nivosus) breeding at Bahía de Ceuta, a coastal wetland in Northwest Mexico. Results Using nest initiations and fates of 752 nests monitored over ten years we found that the laying season coincides with the lowest spring tides of the year and only 6% of all nests were flooded by tides. Tidal nest flooding varied substantially over time. First, flooding was the primary cause of nest failures in two of the ten seasons indicating high between-season stochasticity. Second, nests were flooded almost exclusively during the second half of the laying season. Third, nest flooding was associated with the semi-lunar spring tide cycle as nests initiated around spring tide had a lower risk of being flooded than nests initiated at other times. Following the spring tide rhythm, plovers appeared to adapt to this risk of flooding with nest initiation rates highest around spring tides and lowest around neap tides. Conclusions Snowy Plovers appear generally well adapted to the risk of nest flooding by spring tides. Our results are in line with other studies showing that intertidal organisms have evolved adaptive responses to predictable rhythmic tidal changes but these adaptations do not prevent occasional catastrophic losses caused by stochastic events.
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Monogamous birds exhibit considerable interspecific variation in rates of mate fidelity between years, but the reasons for this variation are still poorly understood. In a 4-year study carried out in western Alaska, mate-fidelity rates in Semipalmated Sandpipers (Calidris pusilla; mate fidelity was 47% among pairs where at least one mate returned and 94% among pairs where both mates returned) were substantially higher than in Western Sandpipers (Calidris mauri; 25 and 67%, respectively), despite the similar breeding biology of these sibling species. Divorce was not a response to nesting failure in Western Sandpipers, and mate change had no effect on the reproductive performance of either species. Nor were mate-fidelity rates related to differential rates of breeding dispersal, because the species did not differ in site fidelity. Reunited pairs and males that changed mates showed strong site tenacity, while females that changed mates moved farther. Differences in local survival rates or habitat are also unlikely to explain mate fidelity, since the two species did not differ in local survival rates, φ (Western Sandpipers: $ φ = 0.57 ± 0.05 (mean ± SE), Semipalmated Sandpipers: $ φ = 0.66 ± 0.06), and they bred in the same area, sometimes using the same nest cups. Although we were able to reject the above explanations, it was not possible to determine whether mate retention was lower in Western Sandpipers than in Semipalmated Sandpipers because of interspecific differences in mating tactics, time constraints imposed by migration distance, or a combination of these factors. Western Sandpipers exhibited greater sexual size dimor-phism, but also migrated for shorter distances and tended to nest earlier and more asynchronously than Semipalmated Sandpipers. Finally, we show that conventional methods underestimate divorce rates, and interspecific comparisons may be biased if breeding-dispersal and recapture rates are not considered. 1958 Resumé : Le oiseaux monogames font preuve d'une variation interspécifique considérable de leur fidélité à un parte-naire d'une année à l'autre et les causes de cette variation sont toujours mal comprises. Au cours d'une étude de 4 ans dans l'ouest de l'Alaska, les taux de fidélité au partenaire mesurés chez des Bécasseaux semipalmés (Calidris pusilla; 47 % des couples dont au moins l'un des partenaires est revenu et 94 % dont les deux partenaires sont revenus) se sont avérés plus élevés que ceux mesurés chez l'espèce-soeur, le Bécasseau d'Alaska (Calidris mauri; 25 et 67 %, respectivement), en dépit de la similitude de la biologie de leur reproduction. Le divorce n'est pas une réaction à l'insuccès de la nidification chez le Bécasseau d'Alaska et le changement de partenaire n'a pas d'effets sur la performance de reproduction, ni chez l'une, ni chez l'autre des deux espèces. La fidélité n'est pas non plus reliée à des taux différentiels de dispersion pour la reproduction, puisque les deux espèces manifestent la même fidélité à un site. Les couples reformés et les mâles qui changent de partenaire ont une fidélité tenace au site alors que les femelles qui chan-gent de partenaire s'en éloignent. Des différences dans le taux de survie enregistré localement et l'habitat sont égale-ment des facteurs peu probables de fidélité au partenaire puisque les taux de survie enregistrés localement ne diffèrent pas chez les deux espèces (Bécasseau d'Alaska: $ φ = 0,57 ± 0,05 (moyenne ± erreur type), Bécasseau semipalmé: $ φ = 0,66 ± 0,06) et que celles-ci se reproduisent dans la même région, utilisant parfois des nids posés sur le même support. Nous avons pu réfuter toutes ces explications, mais il n'pas été possible de déterminer si la fidélité au partenaire est plus faible chez le Bécasseau d'Alaska à cause de différences interspécifiques dans les stratégies d'accouplement, à cause de contraintes temporelles imposées par la distance de migration ou à cause de ces facteurs combinés. Le dimor-phisme sexuel est plus important chez le Bécasseau d'Alaska, mais cet oiseau migre aussi sur de plus courtes distances et sa période de nidification est plus hâtive et moins synchronisée que celle du Bécasseau semipalmé. Enfin, nous Can. démontrons que les méthodes classiques sous-estiment la fréquence des divorces et que les comparaisons interspécifi-ques peuvent n'être pas valides si la dispersion de reproduction et les taux de recapture ne sont pas pris en compte. [Traduit par la Rédaction] Sandercock et al.
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The adult sex ratio (ASR) is a fundamental concept in population biology, sexual selection, and social evolution. However, it remains unclear which demographic processes generate ASR variation and how biases in ASR in turn affect social behaviour. Here, we evaluate the demographic mechanisms shaping ASR and their potential consequences for parental cooperation using detailed survival, fecundity, and behavioural data on 6119 individuals from six wild shorebird populations exhibiting flexible parental strategies. We show that these closely related populations express strikingly different ASRs, despite having similar ecologies and life histories, and that ASR variation is largely driven by sex differences in the apparent survival of juveniles. Furthermore, families in populations with biased ASRs were predominantly tended by a single parent, suggesting that parental cooperation breaks down with unbalanced sex ratios. Taken together, our results indicate that sex biases emerging during early life have profound consequences for social behaviour.
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Significance Sex biases are widespread in nature and represent a fundamental component of sexual selection and population biology—but at which point in life history do these biases emerge? We report a detailed individual-based demographic analysis of an intensively studied wild bird population to evaluate origins of sex biases and their consequences on mating strategies and population dynamics. We document a strongly male-biased adult sex ratio, which is consistent with behavioral observations of female-biased polygamy. Notably, sex-biased juvenile rather than adult survival contributed most to the adult sex ratio. Sex biases also strongly influenced population viability, which was significantly overestimated when sex ratio and mating system were ignored. Our study, therefore, has implications for both sexual selection theory and biodiversity conservation.
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Extra-pair paternity is a common reproductive strategy in many bird species. However, it remains unclear why extra-pair paternity occurs and why it varies among species and populations. Plovers (Charadrius spp.) exhibit considerable variation in reproductive behaviour and ecology, making them excellent models to investigate the evolution of social and genetic mating systems. We investigated inter- and intra-specific patterns of extra-pair parentage and evaluated three major hypotheses explaining extra-pair paternity using a comparative approach based on the microsatellite genotypes of 2,049 individuals from 510 plover families sampled from twelve populations that constituted eight species. Extra-pair paternity rates were very low (0 to 4.1% of chicks per population). No evidence was found in support of the sexual conflict or genetic compatibility hypotheses, and there was no seasonal pattern of extra-pair paternity (EPP). The low prevalence of EPP is consistent with a number of alternative hypotheses, including the parental investment hypothesis, which suggests that high contribution to care by males restricts female plovers from engaging in extra-pair copulations. Further studies are needed to critically test the importance of this hypothesis to plover mate choice. This article is protected by copyright. All rights reserved.
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Sexual selection may act as a promotor of speciation since divergent mate choice and competition for mates can rapidly lead to reproductive isolation. Alternatively, sexual selection may also retard speciation since polygamous individuals can access additional mates by increased breeding dispersal. High breeding dispersal should hence increase gene flow and reduce diversification in polygamous species. Here we test how polygamy predicts diversification in shorebirds using genetic differentiation and subspecies richness as proxies for population divergence. Examining microsatellite data from 79 populations in ten plover species (Genus: Charadrius) we found that polygamous species display significantly less genetic structure and weaker isolation-by-distance effects than monogamous species. Consistent with this result, a comparative analysis including 136 shorebird species showed significantly fewer subspecies for polygamous than for monogamous species. By contrast, migratory behaviour neither predicted genetic differentiation nor subspecies richness. Taken together, our results suggest that dispersal associated with polygamy may facilitate gene flow and limit population divergence. Therefore, intense sexual selection, as occurs in polygamous species, may act as a brake rather than an engine of speciation in shorebirds. We discuss alternative explanations for these results and call for further studies to understand the relationships between sexual selection, dispersal and diversification. This article is protected by copyright. All rights reserved.