Being on time: size-dependent attendance patterns affect male reproductive success

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Animal Behaviour 93 (2014) 77e86

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Animal Behaviour

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Being on time: size-dependent attendance patterns affect malereproductive success

Kristine Meise*, Paolo Piedrahita, Oliver Krüger, Fritz TrillmichDepartment of Animal Behaviour, University of Bielefeld, Bielefeld, Germany

a r t i c l e i n f o

Article history:Received 9 January 2014Initial acceptance 12 March 2014Final acceptance 3 April 2014Published onlineMS. number: 14-00022R

Keywords:asynchronous female oestrusGalapagos sea lionmale reproductive strategypolygynous mating systemsize-dependent attendance patterns

* Correspondence: K. Meise, Department of AnimBielefeld, Morgenbreede 45, 33615 Bielefeld, German

E-mail address: [email protected] (K

http://dx.doi.org/10.1016/j.anbehav.2014.04.0190003-3472/� 2014 The Association for the Study of A

When reproduction occurs seasonally, males are expected to concentrate their reproductive effort whenthe abundance of females in oestrus is highest. In colonial species, large body size and prior residencycorrelate with the ability to establish dominance and ultimately to achieve matings. However, in additionto dominance, attendance in proximity to females may also enhance male mating success. If femalescome into oestrus highly asynchronously, males are unable to attend females for the entire breedingseason. We expect the attendance of the most competitive males to increase with the availability ofreceptive females while less competitive males may primarily attend colonies when more competitivemales are rare. In Galapagos sea lions, Zalophus wollebaeki, large males defend semiaquatic territories,but are unable to hold these over the entire reproductive season. They are sighted most often during thepeak reproductive season. In this study, we found that nonterritorial males frequented the colony lessduring this time. However, the percentage of days intermediate-sized and resident males were sightedincreased towards the peak of the reproductive season. Reproductive success was positively correlatedwith male attendance and therefore highest among territorial males. However, the correlation betweenattendance and reproductive success also existed for nonterritorial males. This suggests that male Gal-apagos sea lions adjust their attendance to the competitive situation in the colony. By increasingattendance during the peak of female oestrus, territorial males increase their chance of reproducingsuccessfully. By adopting size-dependent strategies, nonterritorial males are able to achieve fitness whilestill growing.� 2014 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Timing is an essential element of a successful life history strat-egy as most habitats are subject to seasonal fluctuations in foodabundance and climate. These factors influence the chance ofraising offspring successfully. As a consequence, a species’ repro-ductive season usually covers only part of the year (e.g. Boyd &Duck, 1991; Bunnell, 1980; Rubenstein & Wikelski, 2003). Femalesare expected to reproduce when food availability is high, thuseasing parental care and enhancing offspring survival. This leads tosynchrony in female reproductive activity and, in turn, forces malesto synchronize their mating effort.

In polygynous mating systems in which males increase theirreproductive success by monopolizing access to females (resource-defence polygyny, Emlen & Oring, 1977; female-defence polygyny,Davies, 1991), there is intense maleemale competition. Manyempirical studiesprovide evidence thatmale attendanceat breedingsites varies considerably. In Antarctic fur seals, Arctocephalus gazella,the largest bulls establish territories early in the breeding season

al Behaviour, University ofy.. Meise).

nimal Behaviour. Published by Els

(Arnould & Duck, 1997; Hoffman, Boyd, & Amos, 2003). Early arrivalis correlated with long territory tenure and high reproductive suc-cess (Arnould & Duck, 1997; Hoffman et al., 2003). The oppositepattern was found for three-spined sticklebacks, Gasterosteus acu-leatus: small males, unable to establish territories in the presence oflarger rivals, benefit from arriving early at the breeding ground;however, early arrival is selected against as predation pressure ishigh at the beginning of the season (Candolin & Voigt, 2003;Rowland, 1983). Large males arrive later when females are presentand the larger number of individuals provides some protectionagainst predators. They have no disadvantage from arriving late asthey can take over territories from smaller males (Candolin & Voigt,2003). These examples indicate that males adjust their attendancepatterns not only to seasonal differences in the abundance ofreceptive females, but also with regard to individual attributes thatinfluence resource-holding potential (e.g. Forstmeier, 2002; Kokko,1999; Parker, 1974).

Although size is a key predictor of male competitiveness(Anderson, 1994), large body size is not the only factor accountingfor male dominance. Prior residency can modify size-relateddominance effects (Haley, 1994). If animals have gathered reliable

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K. Meise et al. / Animal Behaviour 93 (2014) 77e8678

information about the quality of the habitat, they may be willing toinvest more in fights (Davies, 1978; Maynard Smith & Parker, 1976).Accordingly, prior residents might dominate in aggressive en-counters. In addition, repeated encounters with conspecifics duringprevious seasons can lead to the development of social relation-ships among neighbouring individuals. These may help to avoidserious fights (Fisher, 1954; Getty, 1987). Prior residency may thuslead to high dominance status or to long-term social relationshipsand may enable males to attend the breeding site for longer andsuccessfully defend a section of the breeding ground, thusincreasing their reproductive success.

Understanding interindividual differences in attendance andhow males may adjust attendance with regard to the competitivesituation in the colony is vital for insights into the evolution ofalternative male mating strategies in polygynous mammals like theGalapagos sea lion, Zalophus wollebaeki. They are nonmigratory andmaintain colonies year-round (Trillmich, 1986). During the coolerpart of the year, characterized by lowwater temperature and higherfood abundance (Feldman, 1986), females give birth to a single pup(approximately between September and January). They come intooestrus 3e4 weeks later (Heath, 1989). The largest and mostcompetitive males establish territories along the water’s edgewhere females haul out to rest and suckle their young (Wolf &Trillmich, 2007). As space is limited, only 5e8% of males manageto establish a territory within a given season (Meise, Krüger,Piedrahita, & Trillmich, 2013). Nonterritorial males are regularlyobserved in the breeding colony, but gather in less suitable inlandhabitats largely avoided by females (Wolf, Kauermann, & Trillmich,2005). As female oestrus occurs highly asynchronously, territorialmales are unable to monopolize access to females (Trillmich &Trillmich, 1984). Nonterritorial males were shown to sire a sub-stantial proportion of the annual pup production (Meise et al.,2013; Pörschmann, Trillmich, Mueller, & Wolf, 2010). Importantly,attendance in the colony, more than fighting ability, seems to in-crease an individual’s chance of reproducing.

In many pinniped species, males fast during the reproductiveseason and, as a consequence, lose a large percentage of initial bodymass (Boyd & Duck,1991; Coltman, Bowen, Boness, & Iverson,1997;Lidgard, Boness, Bowen, & McMillan, 2005; Trillmich & Trillmich,1984). Thus, attendance on the breeding ground is costly not onlyin terms of potential injuries, but also in terms of lost foragingopportunities (Deutsch, Haley, & Le Boeuf, 1990). Small malescannot afford to stay for the entire breeding season, as in additionto risking serious injuries, their fat reserves would not last(Coltman, Bowen, Iverson, & Boness, 1998). They face a trade-offbetween attendance at the breeding ground to get access to fe-males and the need to forage to maintain or increase body size tobecome more competitive for future reproduction.

If males vary in attendance at the colony, we predict that insituations in which female oestrus occurs highly asynchronously,the largest, most competitive males will increase attendance to-wards the peak of female oestrus. In contrast, smaller, lesscompetitive males might benefit from the absence or low numberof rivals during the early or late part of the reproductive season. Weinvestigated how attendance patterns differ with regard to time ofyear and individual male body size and prior residency. We putparticular emphasis on the documentation of the attendancepattern of nonterritorial males. Assuming that warmer watertemperatures lead to a reduction in prey abundance, which is ex-pected to induce increased foraging effort (Jeglinski, Werner,Robinson, Costa, & Trillmich, 2012; Trillmich & Dellinger, 1991),we predicted that males will be least in attendance during thewarm, nonreproductive season (February to May). During thereproductive season attendance should be longer the larger a maleis. Accordingly, we predict that territorial males will spend by far

most time in the colony, especially during the peak of the repro-ductive season, but that attendance will also increase with bodysize and prior residency in nonterritorial males. By being presentduring the peak of female oestrus, the more competitive territorialas well as large, resident nonterritorial males are expected to in-crease their reproductive success. Smaller, less competitive malesor males without prior knowledge about the (social) environmentare expected to be present when rivals are few, such as at thebeginning of the reproductive season.

METHODS

The present study was conducted on Caamaño, a small isletlocated in the central Galapagos Archipelago (0�450S, 90�160W). Itharbours one of the largest breeding colonies of Galapagos sea lionswith approximately 1200 individuals, including about 300 adultmales (�5 years old). Since 2003, many animals have been indi-vidually marked. To apply the markings animals were capturedwith hoop nets providing a small opening, which allowed the an-imals to breathe normally. They weremanually restrained with oneperson holding the head, a second person holding the front flippersand a third person to perform the tagging and measuring. Werefrained from using anaesthetics for several reasons. Anaesthe-tizing wild otariids is often risky: heart and respiratory failures mayoccur, long recovery times increase risks of overheating in a tropicalenvironment such as the Galapagos Islands, and drugged animalsescaping into the water before complete immobilization maydrown (e.g. Melin et al., 2013; Trillmich & Wiesner, 1979).Furthermore, our capture process took only about 6e8 min. This isabout the same time it takes to observe the first effects of anaes-thetics (Trillmich & Wiesner, 1979). Thus, by manually restrainingthe animals we reduced the handling time for the animals to aminimum. Passive transponders (ID-100B, Trovan, Euro ID Identi-fication Systems GmbH, Germany, diameter: 2.12 mm, length:11.5 mm, weight: 0.1 g which corresponds to 0.002% of average pupbody mass) were inserted subcutaneously above the shoulderblades using an IM 200 Syringe implanter (Trovan, Euro ID Identi-fication Systems GmbH, Germany). For many years, passive tran-sponders have been used to identify individuals in our study colonyand have never shown any short-term or long-term adverse effects.Numbered flipper tags (Allflex ear tags, size 0, U.K.) were applied byfirst punching a small hole with a sterile leather punch into theleathery part of both front flippers’ trailing edge. The resultingtissue sample of about 1.5 mm in diameter was collected for geneticanalysis. Thereafter, the flexible plastic tags were applied. Animalsshowed a brief startle reaction to the punching, but were neverobserved to pay attention to the tags. No bleeding or inflammationoccurred (Wolf, Mawdsley, Trillmich, & James, 2007). Oncereleased, most animals stayed close to the place where captureshad taken place and even explored the measuring tools beforeslowly moving away (also see Jeglinski, Mueller, Pörschmann, &Trillmich, 2010).

Nontagged males too large to be captured could be identified bynatural marks or nonpermanent bleaching of their fur (WellaBlondor 12%, lasting for at least 3 months). Males were bleached byapplying the bleaching substance to neoprene patches representingdifferent letter combinations which were then gently pressedagainst the males’ fur. This worked best on resting animals whichrarely showed a reaction to the bleaching process. To determine theindividuals’ genetic profile and allow identification over years(Meise et al., 2013), we took biopsy samples using a longbow and anarrow equipped with a biopsy needle. Skin samples were takenfrom the chest where males have a thick leathery skin and ablubber layer of more than 4 cm which cannot be penetrated bythe short biopsy needles we used (tip length of 1 cm; see also

1

2

3

4

5

6

0

Nu

mbe

r of

pu

ps

born

eac

h d

ay

September October November December January

Prereproductive

season

Peakreproductive

season

End ofreproductive

season

Figure 1. Daily number of pups observed during the reproductive season. Data are shown for the reproductive season 2007 (empty circles) and 2008 (filled circles) as these fieldseasons were slightly longer than in 2009e2012 and data were available until the end of January. Lines represent nonparametric fits using the LOWESS smoother in R. They wereshifted by 21 days, thus providing an estimate of the number of oestrous females that can be expected per day in each of the three parts of the reproductive season (lightgrey ¼ 2007, dark grey ¼ 2008). We only considered pups whose exact birth date was known. A small number of pups born in late August or early February were not included in thisgraph. Lines should be interpreted as a rough representation of how the number of oestrous females changes over time.

Resident Visitor

Small

Intermediate

Large

Territorial Largest males

Figure 2. Classification of males according to their predicted competitive potential.Resident males are predicted to be more successful in competing than visitors. For bothresident and visiting males the competitive potential is assumed to increase with bodysize. Territorial males were the largest in the colony and are therefore considered themost competitive ones.

K. Meise et al. / Animal Behaviour 93 (2014) 77e86 79

Pörschmann et al., 2010). Biopsies caused males to get up and scantheir environment, but they quickly settled down again (generallywithin a few minutes). No animal was observed to run away fromthe researcher into the sea.

Data were collected between September and December 2009 to2012 (in the following referred to as the reproductive season) andbetween March and April 2010e2012 (2e3 weeks, with theexception of 7 weeks in 2012; in the following referred to as thenonreproductive season). Censuseswere conducted every 3e6 daysat different times of the day. We noted the total number of adultindividuals on the islet, counting sexes separately. During thereproductive seasons 2009e2012, and the nonreproductive season2012 we further conducted two to four resight rounds per dayduring which we recorded the presence of all individually markedmales. In addition to the differentiation between reproductive andnonreproductive season, we distinguished between the beginningand the peak of the reproductive season. The preseason endedwhen 25% of the pups were born. It differed slightly between years,but the transition between pre- and peak season always fell be-tween the middle and end of October. The peak season lasted untilthe end of the field seasons in mid-December. Unfortunately, nodata were available for the end of the reproductive seasons whichcorresponds to the end of December and January (Fig. 1). Accord-ingly, for the analysis each year was split into three parts: the pre-and peak season (both reproductive season) and the nonrepro-ductive season.

Individual Parameters

Over all years of the study, 259 adult males were identified. Wecollected data on individual attributes such as body size, territori-ality and prior residency status as well as male reproductive suc-cess. Depending on these individual attributes males were definedas more or less competitive (Fig. 2).

For the first time, sample sizes allowed us to investigate therelationship between age and body length in this species. Exactbirth dates were known for adult males born between 2003 and

2007. Accurate age estimates existed for males tagged within thefirst 2 years of life when age estimates, based on body measure-ments, are reliable (total N ¼ 107; Jeglinski et al., 2010). For othermales, no accurate age estimates were available, but we consideredmales observed as adults during the first years of this project(2003e2005) to be older than 10 years during the study period(2009e2012).

Between 2009 and 2012, 122 males were captured and standardbody length measurements taken. Accurate estimates of bodylength were also derived from photogrammetric analyses (corre-lation between measured (captures) and estimated (photogram-metry) body length: rS ¼ 0.921, Nmales ¼ 16, P < 0.001; meandifference between measured and estimated body length: 2%; co-efficient of variation of estimated body length calculated for malesthat have been repeatedly photographed within less than 3months ¼ 2.9%; Meise, Mueller, Zein, & Trillmich, 2014). More than100 males were photographed in at least one field season. Maleswere assigned to three size categories: small (<160 cm bodylength), intermediate (160e180 cm) and large (>180 cm). As adultmales grow approximately 4.5 cm per year, individuals found in thecentre of one category will be found in the same category in the

K. Meise et al. / Animal Behaviour 93 (2014) 77e8680

following year (Meise et al., 2013). Assigning these males to thesame category in 2 consecutive years increased sample sizewithouttaking new measurements each season. On the other hand, thesame individual can be found in different size categories indifferent years as continuous growth also led to individuals beingassigned to different size categories over the years.

Each season, 5e10% of the observed males established terri-tories. Males were defined to be territorial when they showedspecific behaviours for more than 3 days (e.g. patrolling in front ofdefined subsections, herding females, border displays; Meise et al.,2013). Males do not hold territories during the nonreproductiveseason. To assess how previous territoriality affects attendancepatterns during the nonreproductive season, we categorized malesaccording to their territorial status in the previous reproductiveseason.

We further classified males as residents or visitors. Prior resi-dence is here defined as sightings in a previous year and residentswere defined as adult males that have been observed in the colonyin at least 4 of the last 6 years. Furthermore, we categorized 5- and6-year-old males as residents if they were born on the islet andregularly observed as subadults (<5 years of age). Males seen lesswere classified as visitors. Sampling effort to identify permanentlyand nonpermanently marked individuals was comparable amongthe last 6 years (2007e2012). Thus, we were able to expand ourdata set to cover the seasons 2007 and 2008 and to get more reli-able estimates about residency status. We only classified malesidentifiable by tags or natural marks or males with known geno-type which allowed the identification of individuals over years.Skin samples for genetic analysis were available for all permanentlyand the majority of nonpermanently marked males (in total 93.5%of all males). Genotyping was conducted on an Applied Biosystems3130x1 Genetic Analyser using 22 microsatellites which have beenshown to be in HardyeWeinberg equilibrium (Hoffman, Steinfartz,&Wolf, 2007; Wolf, Tautz, Caccone, & Steinfartz, 2006). The geneticidentification of nonpermanently marked males over years wasdone in Cervus 3.0 (Kalinowski, Taper, & Marshall, 2007; Marshall,Slate, Kruuk, & Pemberton, 1998). Male individuals were assumedto be identical if at least 20 loci matched leading to an overallprobability of identity of 0.995.

Each season, we took skin samples of all pups born on the island(Table 1). Pups were captured by hand and briefly restrained whilesmall tissue samples (1.5 mm) were taken with a sterile leatherpunch from the interdigital membrane of the hind flippers. Pupsshowed a brief startle reaction to the punching, but no negativelong-term effects were observed. Wounds were examined duringrecaptures about 1 week up to 3 months later and no inflammationhas ever been observed. For paternity analysis, we constructedyearly lists of possible fathers. All males of known genotype thatwere 5 years or more old were considered as potential fathers in-dependent of whether or not they were observed in the colony inthe year of conception (Table 1; Pörschmann et al., 2010). Maleswere assumed to be capable of fathering offspring until found dead.

Table 1Numbers of individuals included in paternity analysis

Season Pups bornper season

Mothers withknown genotype

Number ofpossible fathers

Assignedpaternities

2010 112 59 518 792011 231 124 601 1912012 139 82 667 112

The table shows the numbers used to determine paternities: the total numbers ofpups born (and sampled) per season, the number of mothers whose genotype wasknown and included in the paternity analysis to improve accuracy of assignments aswell as the number of males considered as possible fathers (>5 years). Paternitiescould be assigned to nearly 80% of the newborns.

Paternities were assessed using the maximum likelihood approachimplemented in Cervus. The analysis is based on pairwise com-parisons and locus-by-locus likelihood scores. It takes the knownmaternal genotypes (Table 1) and the allele frequency distributionin the population into account. Paternity assignment was based onsimulations of 100 000 offspring considering a genotyping error of0.003 and under the assumption that the proportion of malessampled is 0.85 (Pörschmann et al., 2010). Each offspring assignedby Cervus with 95% confidence level was used for subsequentanalysis. Males were defined to be reproductively successful if theysired at least one pup in the season.

We also investigated whether males from Caamaño sired pupsin sea lion breeding colonies on Santa Fé (Bahia Paraiso, distance:30 km, 0�480S, 90�020W) and Floreana (Post Office Bay, distance: 65km, 01�130S, 90�260W). Data on Santa Fé were collected between2008 and 2010 and kindly provided by Paddy Brock (N ¼ 103;Brock, Hall, Goodman, Cruz, & Acevedo-Whitehouse, 2012). Thedata on Floreana were collected during the same time period byJana Jeglinski (N ¼ 67; Jeglinski et al., 2012). For paternity analysis,we reduced the proportion of males assumed to have been sampledto 0.5 asmales from Caamañowere rarely seen in the other colonies(P. Brock & J. Jeglinski, personal communication). Although thisprobability seems relatively high, we think it is conservative to usea high value because matings occur aquatically and individuals areknown to haul out in other colonies while foraging (Villegas-Amtmann, Simmons, Kuhn, Huckstadt, & Costa, 2011). Otherwisewe followed the protocol described above.

Statistical Analysis

All statistical analyses were carried out using R 2.15.3 (The RFoundation for Statistical Computing, Vienna, Austria, http://www.r-project.org, R Development Core Team, 2010). We applied ageneral linear model (GLM) to assess whether the number of males(log-transformed) varied with regard to the time of the season. Forthe analyses on individual patterns in male attendance, weconcentrated on males that were identifiable throughout the sea-son. This included permanently marked individuals and malesbleached at the beginning of the season. Furthermore, we onlyconsidered males seen at least three times per season to avoidincluding males that lost their bleach marks immediately. Atten-dance was defined by the number of days males were observed inthe colony within a given season. No additional temporal param-eters such as visit duration or interbout intervals were examined asmales rarely stayed longer than a day in the colony (median ¼ 1day) and interbout intervals and number of days sighted weretherefore negatively correlated. As each part of the season differedslightly in length, we determined the percentage of days each malewas observed. General linear mixed models (GLMM) were used todetermine which factors influenced male attendance patterns. Thepercentage of days a male was observedwas regressed against timeof season as categorized above, territoriality, body size and resi-dency status following a square-root transformation of theresponse variable. Information about body size was only availablefor a subset of individuals (N ¼ 162). We repeated our analysesusing a data set in which we included individuals with knownterritorial status, irrespective of the availability of size estimates(N ¼ 259). Furthermore, we conducted a separate analysis fornonterritorial males only (N ¼ 155) to assess the impact of bodysize and residency status.

In a second step, we tested whether the probability of repro-ducing was influenced by differences in attendance pattern duringthe reproductive season (pre- and peak season). We appliedgeneralized linear mixed models with Poisson distribution to testwhether the number of paternities was influenced by attendance

K. Meise et al. / Animal Behaviour 93 (2014) 77e86 81

pattern, taking differences in individual attributes into account. Thefirst model was based on the complete data set (N ¼ 207) and weused territoriality and the interaction between territoriality and thepercentage of days sighted as fixed factors. For the second model,we restricted the data set to nonterritorial males only (N ¼ 137) andtested the effect of body size, residency status and the interactionsbetween each factor and the percentage of days observed for malereproductive success. Subsequently, we repeated the modellingusing the percentage of days sighted per time of the season as afixed factor.

Animal ID was included as a random factor in each model asmost individuals have been observed in more than one season.Models were compared using the maximum likelihood approachand the best-fitting models were selected based on Akaike’sinformation criterion corrected for small sample sizes (AICc,Anderson, Burnham, & White, 1998). If more than one model had adelta AICc smaller than two, we calculated average model param-eters. Differences were considered significant at the P < 0.05 level.We present means � SE unless stated otherwise.

Ethical Note

The study presented here complies with the laws of Ecuador andwas performed under permission of the Galapagos National ParkService (PC-001-03 Ext. 5, PC-043-09, PC-007-11, PC-026-12). Thegenetic data from Santa Fé and Floreana were collected under thepermits PC-18-09, PC-046-09, PC-101-10, PC-032-10 and PC-11-08,PC-043-09.

RESULTS

No significant differences were found in the number of maleGalapagos sea lions identified per year (KruskaleWallis test:c23 ¼ 1:667, P ¼ 0.644). In total, 190 � 16 different males

(mean � SD) visited the colony each reproductive season. Malesrarely stayed longer than a day in the colony (median visitduration ¼ 1 day), but the total number of days they were sightedwithin a given season differed substantially. While some maleswere only observed 3 days within a reproductive season, others

Prereproductive

Time of the

Peakreproductive

Nonreproductive

FemalesMales

100

80

60

40

20

120 (a)

Tota

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um

ber

of i

nd

ivid

ual

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un

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Figure 3. (a) The total number of adults found hauling out and (b) the percentage of timinterquartile range (IQR; boxes), 1.5 � IQR (whiskers) and outliers (circles).

hauled out more regularly, up to 62 days (80% of the season). Suchdifferences were predicted to reflect the individual’s competitiveability in the colony and thus to depend on season and individualtraits.

Seasonal Differences

The total number of adult males counted within a given censuschanged with time of season (ANOVA: F2,85 ¼ 50.947, P < 0.001;Fig. 3a). Numbers increased during the reproductive season, but thehighest numbers of males were counted in the nonreproductiveseason. During the reproductive season, the increasewas correlatedwith the number of females hauling out (rS ¼ 0.604, N ¼ 71,P < 0.001). However, in contrast to males, no difference in thenumbers of females was found between the peak season and thenonreproductive season (GLM: t ¼ 0.996,N ¼ 85, P ¼ 0.322; Fig. 3a).

The increase inmale abundance from the pre- to the peak seasonwas partly explained by the influx of a larger number of differentindividuals (t test: t5.85 ¼ 2.799, P ¼ 0.032). As nonpermanentmarkings did not necessarily last until the nonreproductive season,fewer individuals with marks were observed in the nonreproduc-tive season. Thus, it was not possible to test whether the largernumber of males counted in the nonreproductive seasonwas due toa larger number of different individuals. However, daily resightrounds of tagged individuals revealed that the mean sightingprobability of individuallymarkedmales increased from14% duringthe prereproductive season to 23% during the peak reproductiveseason and was highest at 30% in the nonreproductive season(ANOVA: F2,972 ¼ 137.527, P < 0.001; Fig. 3b). Thus, the largernumber of males counted per census in the nonreproductive seasonis at least partly explained by increased individual attendance.

Individual Attendance Patterns

The percentage of days males attended the colony in each partof the season was influenced by three different individual param-eters: territoriality, body size and prior residence (full model,Table 2). During the reproductive season, territorial males weregenerally sighted more often than nonterritorial males (24 � 2.1%

N=231N=22 N=231 N=22 N=130 N=5

Peakreproductive

season

100

80

60

40

20

0

Nonreproductive

Prereproductive

TerritorialNonterritorial

(b)

Perc

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e spent ashore at different times of the year. Box plots show medians (black bar),

Table 2The effect of territoriality, body size and residency on male attendance patterns (general linear mixed model)

Variables K AICc D AICc AICc weights

Dependent Independent Random

Attendance: full model (N¼162)Days Time*(territorialityþresidencyþsize) ID 17 2648.6 0 0.689Days Time*(territorialityþresidency)þsize ID 13 2650.5 1.86 0.272Days Time*(territorialityþresidency) ID 13 2654.7 6.02 0.034Attendance: time, territoriality (N¼259)Days Time*territoriality ID 8 4359.9 0 1Days Timeþterritoriality ID 6 4419.8 59.95 0Attendance: time, size, residency (nonterritorial males, N¼155)Days Time*(residencyþsize) ID 14 2498.1 0 0.671Days Time*(residencyþsize)þresidency*size ID 16 2501.0 2.90 0.157

Interaction terms were calculated between time of the season and each individual attribute. Additive variables are indicated by þ, interactions by *. Number of estimatedparameters (K), Akaike’s information criterion for small sample sizes (AICc), deviation from the AICc of the best model (D AICc) and AICc weights are shown. Onlymodels with adelta AICc not bigger than two and the next best model are listed.

K. Meise et al. / Animal Behaviour 93 (2014) 77e8682

of the days; t ¼ 8.920, P < 0.001), and their attendance increasedtowards the peak of the reproductive season (29.4 � 2.7%;t ¼ 7.312, P < 0.001). Territorial and nonterritorial males did notdiffer in attendance during the nonreproductive season (Fig. 3b).However, we resighted only 50% of the marked territorial males inthe nonreproductive season compared with 86% of the markednonterritorial individuals.

Attendance of Nonterritorial Males

To avoid bias caused by territorial males being the largest andalso being most in attendance (see above), we restricted thefollowing analysis to nonterritorial males (Table 2). Male Galapagossea lions grow continuously during adulthood as shown by signif-icant differences in body length found between age classes(ANOVA: F4,107 ¼ 27.519, P < 0.001; Fig. 4). They reach a maximumbody length of about 210 cm. As age and size are highly collinear,we only considered body size in our analyses regarding maleattendance. We predicted differences in attendance patterns withregard to body length as adult males were expected to adjust theirattendance patterns to the competitive situation in the colony.Nonterritorial males of all size classes spent approximately 15% ofthe days in the colony at the beginning of the reproductive season.Generally, attendance increased towards the peak of the repro-ductive season, but it was highest for intermediate-sized males(25.9 � 1.2% of the days; t ¼ 3.768, P < 0.001). During the nonre-productive season there was a tendency for the largest males to besighted least often (9.5 � 3.2% less; t ¼ �1.758, P ¼ 0.079).

5–6 7–8 9–10 10–11

Age (years)

> 12

N=27N=52 N=48 N=35 N=8100

120

140

160

180

200

Bod

ymle

ngt

hm

(cm

)

Figure 4. Growth rates of adult male Galapagos sea lions. Accurate age estimates wereavailable for males between 5 and 11 years of age. Males were categorized to be olderthan 12 years when they were observed as adults during the first years of this projectand therefore known to be older than the known-aged males at the time body lengthwas measured. Box plots show medians, interquartile ranges (IQR), 1.5 � IQR andoutliers (circles).

Prior residence in the colony also influenced sighting probabil-ity. Independent of body size, visitors were less likely to be sightedduring the reproductive season. At the peak of the reproductiveseason, resident males were observed on 23.7 � 2.1% of the days inthe colony while visitors were only sighted 14 � 2.0% of the days(t ¼ �4.879, P < 0.001). No differences in attendance were foundduring the nonreproductive seasonwhen both groups attended thecolony about 32% of the days (t ¼ �0.149, P ¼ 0.882).

Male Attendance Patterns and Reproductive Success

We were able to assign fathers to nearly 80% of the pups borneach year. The GLMM confirmed the previous finding (Pörschmannet al., 2010) that the probability of siring a pup increased withprolonged attendance in the colony during the reproductive season(z ¼ 5.140, P < 0.001; Table 3). The slope of this increase did notdiffer between territorial and nonterritorial males (z ¼ 1.017,P ¼ 0.309; Fig. 5). However, while 74% of the territorial malesobserved per season gained reproductive success (2.5 pups/male,N ¼ 13), only 31% of the nonterritorial males sired a pup (1.4 pups/male, N ¼ 108; z ¼ 2.476, P ¼ 0.013; Table 3). This is probablybecause of the more continuous attendance of territorial males. Asonly 10% of the males were able to establish a territory, most maleswere nonterritorial. Thus, 80.5% of the pups (range 79e83%) wereactually sired by nonterritorial males.

In a second GLMM, we attempted to explain variation inreproductive success of nonterritorial males, residents as well asvisitors (range 0e6 pups/year). Body size explained most of thevariance. Intermediate-sized males had higher reproductive suc-cess than small and large nonterritorial males (z ¼ 2.240, P ¼ 0.025;Table 3). This pattern can be explained by the lengthy attendance ofintermediate-sized males during the peak season. Within sizeclasses, there was no further effect of increasing attendance onreproductive success. However, for resident males tested sepa-rately, the probability of siring a pup tended to increase withattendance (z ¼ 1.948, P ¼ 0.051; Table 3).

As we found that the time of the season had a significant effecton attendance patterns of nonterritorial males, we included thisfactor in further analyses regarding reproductive success. Thepositive correlation between reproductive success and maleattendance was independent of the time of the season (z ¼ 0.537,P ¼ 0.591; Table 4). Males that successfully sired a pup spent moretime in the colony during pre- and peak season. This finding is notsurprising as the percentage of time nonterritorial males were seenin the preseason is correlated with the percentage of time theywere seen in the peak season (rS ¼ 0.430, N ¼ 22 P < 0.001;although not for territorial males: rS ¼ 0.123, N ¼ 231, P ¼ 0.472).

Table 3The effect of attendance patterns on male reproductive success using the percentage of days sighted during the reproductive season as a fixed factor (generalized linear mixedmodels)

Variables K AICc D AICc AICc weights

Dependent Independent Random

Reproductive success: attendance, territoriality (N¼207)Paternities Territorialityþdays ID 4 448.1 0 0.607Paternities Territoriality*days ID 5 450.1 2.04 0.220Reproductive success: attendance, size, residency (nonterritorial males only, N¼137)Paternities Sizeþdaysþresidency ID 6 268.6 0 0.239Paternities Sizeþdays ID 5 268.8 0.20 0.217Paternities Size ID 4 270.0 1.42 0.118Paternities Sizeþdays*residency ID 7 270.2 1.58 0.109Paternities Sizeþresidency ID 5 271.0 2.41 0.072

Additive variables are indicated by þ, interactions by *. Number of estimated parameters (K), Akaike’s information criterion for small sample sizes (AICc), deviation from theAICc of the best model (D AICc) and AICc weights are shown. Only models with a delta AICc not bigger than two and the next best model are listed.

K. Meise et al. / Animal Behaviour 93 (2014) 77e86 83

Accordingly, we found the same effect of territoriality and seasonalattendance patterns on male reproductive success as we found forthe overall attendance patterns: male reproductive success washigher among territorial males (z ¼ 4.808, P < 0.001). No additionaleffect of the timing of attendancewas found in nonterritorial males.

Not all fathers were observed in the colony during the year theysired a pup; about 17.5% were not sighted in the year of conception.Given that many breeding colonies are within swimming distance(Villegas-Amtmann, Costa, Tremblay, Salazar, & Aurioles-Gamboa,2008), it seems possible that males from other colonies matewith females giving birth on Caamaño. As we have genetic dataonly from Caamaño males, we tested in reverse whether pups bornin neighbouring colonies could have been sired by males fromCaamaño. Of 103 pups sampled on Santa Fé (over 3 years) and 63pups sampled on Floreana (over 3 years), only two and one,respectively, were sired bymales from Caamaño. These results haveto be interpreted with care. On the one hand we sampled only asmall proportion of each pup cohort (16% of the pups born on SantaFé and 14% of the pups born on Floreana) and the number of pa-ternities might be slightly higher. On the other hand the assump-tion that we sampled 50% of the possible fathers is likely to beexaggerated and the number of paternities might be lower. Still, theresults show that males rarely sire pups in colonies other than thehabitually visited one.

0 321 4

0

10

20

30

40

50

60

70

Number of pups sired

Territorial

Nonterritorial

Perc

enta

ge o

f d

ays

sigh

ted

Figure 5. Male reproductive success in relation to their attendance in the colony. Boxplots show medians, interquartile ranges (IQR), 1.5 � IQR and outliers (circles).

DISCUSSION

Fluctuations in food abundance lead to seasonal reproduction inthe nonmigratory Galapagos sea lion. Nonterritorial males adjustedtheir attendance patterns to the availability of receptive femalesduring the reproductive season, but were most often observedduring the nonreproductive season. The percentage of days malesspent in the colony differed in accordance with individual attri-butes which may influence intrasexual encounters. During thereproductive season, territorial males were seen more often thannonterritorial males and residents more than visitors. For body size,our observations suggest that the competitive situation in thecolony has an important effect on male attendance. By prolongingattendance in the colony, especially during the peak of femaleoestrus, nonterritorial as well as territorial males were found toincrease their chance of reproducing successfully.

Seasonal Attendance Patterns

Seasonal differences in male attendance patterns seem bestexplained by annual fluctuations in sea surface temperatures whichare negatively related to food abundance, thus leading to seasonalbreeding in Galapagos sea lions, and thereby to seasonal malereproductive activities. Alternative explanations such as moultingor predator avoidance can be ruled out as Galapagos sea lionsmoultthroughout the year and sharks, their main marine predator, arepresent year-round.

Females give birth during the cold part of the year characterizedby high productivity of the marine habitat (Feldman, 1986). Duringthe warm, nonreproductive season, they spend less time ashore asthey have to forage more in order to sustain themselves and theirdependent offspring (Trillmich, 1990). Similarly, males were ex-pected to extend their foraging trips in order to regain or increasebody fat reserves for future reproduction. However, in contrast toour expectations, nonterritorial males were most frequentlyobserved ashore during the nonreproductive season. Two factorsseem to be responsible. First, in contrast to other species, in whichmales fast during the entire breeding season (e.g. Antarctic fur seal,Arnould & Duck, 1997), male Galapagos sea lions alternate betweenforaging at sea and attendance in the colony as foraging areas areclose to the breeding colony (Villegas-Amtmann et al., 2008).Nonterritorial males seem to maintain body condition throughoutthe reproductive period, making prolonged foraging trips duringthe nonreproductive season unnecessary. Only territorial males,which spend most time ashore, need to regain body condition(Trillmich & Dellinger, 1991) and were therefore not or rarelysighted in the subsequent nonreproductive season. Second, wesuggest that the contrasting patterns found for males and females

Table 4The effect of attendance patterns on male reproductive success using the percentage of days sighted within the pre- and the peak season as a fixed factor (generalized linearmixed models)

Variables K AICc D AICc AICc weights

Dependent Independent Random

Reproductive success: time, attendance, territoriality (N¼207)Paternities Territoriality ID 3 761.8 0 0.583Paternities Territorialityþtime*days ID 5 763.6 1.82 0.234Paternities Territorialityþtime*daysþterritoriality*time*days ID 7 764.1 2.32 0.183Reproductive success: time, attendance, size, residency (nonterritorial males, N¼137)Paternities Size ID 4 455.5 0 0.399Paternities Sizeþtime*days ID 6 456.7 1.15 0.225Paternities Sizeþresidency ID 5 457.1 1.55 0.183Paternities Sizeþtime*daysþresidency ID 7 457.9 2.34 0.124

Additive variables are indicated by þ, interactions by *. Number of estimated parameters (K), Akaike’s information criterion for small sample sizes (AICc), deviation from theAICc of the best model (D AICc) and AICc weights are shown. Only models with a delta AICc not bigger than two and the next best model are listed.

K. Meise et al. / Animal Behaviour 93 (2014) 77e8684

are related to the competitive situation in the colony. During thereproductive season, aggressive interactions amongmales aremorelikely (Pérez-Alvarez, Carrasco, Sepúlveda, & Quiñones, 2013). Asthese are associated with a high risk of injury (or overheating), lesscompetitive males should reduce attendance in the colony duringthe reproductive season.

Size-dependent Attendance Patterns

Individual differences in male attendance patterns support theassumption that seasonal differences are related to competition inthe colony. Territorial males spent up to 80% of the reproductiveseason ashore. They increased their attendance towards the peak offemale oestrus. This contrasts with theoretical predictions (Kokko,1999) that the most competitive males should establish territoriesearly to have access to high-quality territories. However, as terri-torial Galapagos sea lions can easily displace less competitive rivalsfrom territories, they do not losemuch fitness by spending less timein the colony early in the reproductive season (Candolin & Voigt,2003).

Nonterritorial males spent less time in the colony during thereproductive season, but in contrast to our expectations, thenumber of different individuals and the duration of attendanceincreased with the number of receptive females. The variation inindividual attendance patterns was expected to be affected bymalebody size. Large body size implies a lower specific metabolic rate,leading to an increased capacity for prolonged fasting (Heusner,1982). Furthermore, larger males are more competitive and morelikely to be able to compete with territorial males. However, we didnot find a linear relationship between attendance and body size,but an increased sighting frequency of intermediate-sized males.They were more often observed during the peak season than largenonterritorial males. As male body size is correlated with age, theobserved pattern might be related to the larger males’ advancedage and thereby may indicate senescence. Old males of other spe-cies have been found to alter their behaviour, taking less part indominance interactions and attraction of females (e.g. McElligot,Altwegg, & Hayden, 2002; Mysterud, Solberg, & Yoccoz, 2005).The fact that territorial Galapagos sea lions are the largest males inthe colony and spend most time ashore argues against this inter-pretation. However, if the territorial males’ larger size signals asilver-spoon effect, for example being born in a year of high pro-ductivity that permits rapid growth (Mueller, Pörschmann, Wolf, &Trillmich, 2011), then they need not be the oldest males in thecolony.

An alternative explanation is that intermediate-sized males areless conspicuous than large nonterritorial males. They can hideamong females (maximum female body length ¼ 176 cm, Trillmich,

Jeglinski, Meise, & Piedrahita, 2014) when the territorial male isclose by, thus avoiding being spotted and chased away (Le Beouf,1974; Meise, Piedrahita, Krüger, & Trillmich, personal observa-tions). In contrast, large males can easily be identified amongresting females. As fights are more dangerous among similar-sizedopponents (Haley, 1994; Parker, 1974), large males may avoid thecolony during the reproductive season, spending more timeforaging and thereby increasing body mass. The avoidance ofaggressive interactions by not participating in mate competitionmight improve future reproductive success as a higher body massincreases the future chance of taking over a territory. The findingthat large nonterritorial males also spent less time in the colonyduring the nonreproductive season supports the assumption thatthey invest in growth and future reproduction. To assess which ofthese explanations best describes differences in male attendancepatterns, we need a larger sample of known-age large males.

Within the reproductive season, resident males were morefrequently sighted in the colony than visitors, suggesting that priorresidency has an additional effect on attendance. As nonterritorialmales do not defend sites where breeding females gather, wesuggest that this effect is not related to advantages in establishingdominance, but rather to familiarity with competitors (Dittmann,Ezard, & Becker, 2007; Fisher, 1954). Repeated encounters enablemales to accurately assess their contestant’s competitive ability anddevelop long-lasting relationships, thereby reducing aggressiveencounters (e.g. Beletsky & Orians, 1989; Ydenberg, Giraldeau, &Falls, 1988). As resident males show a high degree of spatial pref-erences and site fidelity (Meise et al., 2013), familiarity amongmales using the same resting areas within a colony can be expected.Visiting males lack such long-term relationships. We assume thatthey minimize attendance during the peak season in order to avoidaggressive interactions, but cannot rule out that they have theirbase in a different colony and are therefore seen less often.The finding that visitors and residents are equally likely to beobserved during the nonreproductive season characterized by alow aggressive potential argues against the possibility that visitorswere simply members of different colonies. It rather suggests thatfamiliarity among males develops during the nonreproductiveseason. Our results suggest that intrasexual competition is a keyfactor modulating attendance of male Galapagos sea lions. Malesadopt size-dependent strategies to avoid agonistic interactionswith competitive rivals. A familiar neighbourhood apparently in-creases male attendance in a colony.

Male Reproductive Success in Relation to Differences in Attendance

Males have to be present during the time of female oestrus inorder to reproduce. In accordance with previous findings, male

K. Meise et al. / Animal Behaviour 93 (2014) 77e86 85

reproductive success increased with prolonged attendance in thecolony during the reproductive season (Pörschmann et al., 2010). Asterritorial males were by far most often seen in the colony, they hadmost access to females and gained the highest reproductive successper individual. Becoming territorial is therefore by far the mostsuccessful reproductive strategy. Still, more than 80% of the annualpup cohorts to which we could assign a father were sired by non-territorial males. Compared with other polygynous species, this isan exceptionally high proportion (e.g. Hoffman et al., 2003).

In the Galapagos sea lion, female oestrus occurs highly asyn-chronously. Previous studies predicted that the more asynchro-nous female oestrus is, the higher is the dominant males’reproductive success (Isaac & Johnson, 2003; Ostner, Nunn, &Schülke, 2008; Say, Pontier, & Natoli, 2001). However, the rela-tionship is not as simple in the Galapagos sea lion. The discrepancycan be explained by differences in male behaviour, namely theseasonal separation between foraging and reproduction. Forexample, male primates do not fast during the reproductive seasonas other species, for example ungulates (Miquelle, 1990) and pin-nipeds (Deutsch et al., 1990) do. If female oestrus is highly asyn-chronous, males are unable to fast over the entire season andmonopolize matings (Coltman et al., 1997, 1998). Dominant malesbenefit from timing their reproductive effort to the period when amaximal number of females become receptive (Mysterud et al.,2008; Preston, Stevenson, & Wilson, 2003; Twiss, Poland, Graves,& Pomeroy, 2006). By increasing attendance towards the peak innumber of females in oestrus, territorial Galapagos sea lion malesincrease the chance of reproducing. This situation provides non-territorial males with opportunities to reproduce early or maybealso late in the season, especially as females are free to move be-tween sites and choose among available mates (Pörschmann et al.,2010).

For nonterritorial males, the probability of siring a pup alsoincreased with attendance in the colony. The chance of reproducingdiffered between size classes. Intermediate-sized males, whichwere seen most often during the peak season, gained the highestreproductive success among the nonterritorial males suggestingthat timing of attendance affects the probability of reproducing.However, we did not find a direct link between attendance duringthe peak season and reproductive success. Both successful andunsuccessful males showed increased attendance during the peakseason. Several studies provide evidence that less competitivemales have a higher chance of siring offspring late in the seasonwhen more competitive rivals are exhausted (reviewed inMysterud, Langvatn, & Stenseth, 2004). Unfortunately, we do nothave information about attendance patterns at the end of thereproductive season to test whether the success of intermediate-sized males might be related to a prolonged attendance at theend of the season. Still, it seems surprising that intermediate-sizedmales sired a larger proportion of pups than the large nonterritorialmales.

Lidgard et al. (2005) found a similar relation between body sizeand reproductive success. They argued that the increased repro-ductive success of intermediate-sized males was influenced bygreater agility in agonistic interactions. As, in our study, territorialmales are the largest but also most successful males in the colony,we do not consider agility to be responsible for the size effect. Weassume that in contrast to large males, intermediate males aresmall enough to sneak unobserved into territories to approach andattract females (Fabiani, Galimberti, Sanvito, & Hoelzel, 2004; LeBeouf, 1974). As Galapagos sea lions are living in an environmentcharacterized by drastic changes in the availability of resources dueto El Niño events which affect survival probabilities (Trillmich &Limberger, 1985), using alternative mating tactics seems adaptivein order to secure fitness (Gross, 1996).

Large nonterritorial males seem to face a trade-off betweencurrent reproduction and aggressive interactions with territorialmales. Thus, they might switch to roaming between colonies orextensive foraging to increase body mass. Females move up to80 km during a single foraging trip and regularly haul out inneighbouring colonies (Villegas-Amtmann et al., 2008). As malesprovide no parental care, they do not have to return to theirhabitual colony at regular intervals. They probably swim evenfurther than females and may encounter oestrous females from orin other colonies. However, roaming males sired only a low per-centage (2%) of pups in different colonies. This is consistent withour finding that visitors sire a low number of pups. Therefore, wehypothesize that large nonterritorial males invest primarily in bodygrowth for future reproduction.

Our results suggest that the timing of male reproductive effort inrelation to the distribution of oestrous females over time isimportant to understand the coexistence of different male matingstrategies. For less competitive, nonterritorial males mating effortseems to reflect a compromise between encountering oestrousfemales and avoiding intrasexual competition. By adjusting atten-dance with regard to the presence of male and female conspecifics,Galapagos sea lion males seem able to increase reproductive suc-cess and in particular to gain some fitness while still growing, thatis, before reaching peak competitiveness. This might be the onlyway males growing up under poor conditions can achieve anyfitness at all. Future studies will have to examine how flexible thesestrategies are by following known-age individuals longitudinallythroughout their life history.

Acknowledgments

The study was funded by the German Research Foundation(TR 105/18-2), the German Academic Exchange Service and theEthological Society. The Galapagos National Park Service providedpermission to work on Galapagos. We thank the Charles DarwinStation for cooperation and logistical support. We are grateful toPaddy Brock and Jana Jeglinski for sharing their DNA samples fromSanta Fé and Floreana with us. Elke Hippauf and Prisca Viehöferhelped with genetic analysis. Ulrich Pörschmann gave valuableinput during the initial development of this study. Finally, we thankall field assistants who helped to collect data.

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