Large males fight and court more across a range of social environments: an experiment on the two...

Journal of Fish Biology (2012)

doi:10.1111/j.1095-8649.2012.03296.x, available online at wileyonlinelibrary.com

Large males fight and court more across a range of socialenvironments: an experiment on the two spotted goby

Gobiusculus flavescens

S. Wacker*†‡, K. de Jong*§, E. Forsgren*‖ and T. Amundsen*

*Department of Biology, Norwegian University of Science and Technology, NO-7491Trondheim, Norway, †Department of Behavioural Biology, WWU Munster, D-48149 Munster,Germany and ‖Norwegian Institute for Nature Research, P. O. Box 5685 Sluppen, NO-7485

Trondheim, Norway

(Received 9 September 2011, Accepted 28 February 2012)

The present study explored how male size relates to mating competition across a natural range ofmale and female densities in the two-spotted goby Gobiusculus flavescens. Across this range ofsocial environments, large males were more than twice as likely as small ones to chase other males,to become nest-holders, and to court females, but large males were not significantly more likely toengage in agonistic fin displays. Overall, the study showed that large males court and fight morethan small ones across a wide, yet natural, span of social environments. Having a large body sizeappears to confer competitive advantage for males in any social environment of the study species.Further studies are needed to disentangle whether the benefit of large size is mainly in competitionover resources, over matings as such, or both. © 2012 The Authors

Journal of Fish Biology © 2012 The Fisheries Society of the British Isles

Key words: aggression; body size; courtship; mating competition; resource holding potential; sexualselection.

INTRODUCTION

Mating success in animals is influenced by intrasexual competition for access tomatings and resources needed to mate, and by male and female mate choice (Ander-sson, 1994; Espmark et al., 2000). Competition over matings is usually strongestin males (Andersson, 1994) and is mainly manifested in efforts to attract females(courtship) and in intrasexual agonistic acts aimed to deter competitors. One trait ofmajor importance for male competitive ability, and hence mating success, is bodysize. A positive relationship between body size and mating success in males has beenfound in a wide variety of taxa, including arthropods, fishes, amphibians, reptiles,birds and mammals (Andersson, 1994; Blanckenhorn, 2005).

Large males are often found to engage more in courtship and agonistic behaviourthan small males, which may partly explain why they typically secure more matings

‡Author to whom correspondence should be addressed. Tel.: +47 73596257; email: [email protected]§Present address: Museum of Natural History and Archaeology, Norwegian University of Science and

Technology, NO-7491, Trondheim, Norway

1© 2012 The AuthorsJournal of Fish Biology © 2012 The Fisheries Society of the British Isles

2 S . WAC K E R E T A L .

(Archer, 1988; Reynolds, 1993). In agonistic encounters between differently sizedmales, small males are expected to withdraw due to their lower resource holdingpotential (RHP; Parker, 1974; Enquist & Leimar, 1983). Nonetheless, small malescan sometimes engage in escalated contests as much as, or more than, large males(Morris et al., 1995; Moretz, 2003; Just et al., 2007). This could happen becausesmall males may, under certain circumstances, be able to compensate for their lowerRHP with increased aggressiveness, and because large males do not need to behaveequally aggressively to obtain a resource, due to their higher RHP (Just & Morris,2003; Morrell et al., 2005; Logue et al., 2011). In terms of efforts to attract mates,large males are expected to court more because of their greater ability to pay therelated costs (e.g. predation risk and energy expenditure; Zahavi, 1977; Andersson,1982; Reynolds, 1993). On the other hand, small males may aim to compensate fortheir lower attractiveness to females with higher levels of courtship displays, whereaslarge, attractive males may not need to display as much to secure mating (Parker,1983; Jennions & Backwell, 1998; Colleter & Brown, 2011).

The relative costs and benefits for small and large individuals in mating competi-tion may be affected both by mate availability and density of same-sex competitors(Morrell et al., 2005; Silva et al., 2010). For instance, when mate availability ishigh and mating competition relaxed, large males may benefit from avoiding costlycompetition [Reynolds, 1993; although Silva et al. (2010) found the opposite effect],relying on mating opportunities resulting from their greater attractiveness to females.Small males, by contrast, may under the same conditions benefit from aggression andcourtship to compensate for their lower attractiveness, because their expected bene-fits are relatively high when females are in excess (Morrell et al., 2005). When mateavailability is low, on the other hand, large males would have to compete for the fewfemales available and small males might refrain from competition because of smallexpected benefits (Morrell et al., 2005). As a consequence, the relationship betweenmale body size and mating competition need not be fixed but may vary with thesocial environment (abundance of same and opposite sex individuals). While thereis growing evidence for social environment effects on mating success of differentlysized males (Grant et al., 1995; Lindstrom & Seppa, 1996; Jones et al., 2004), sur-prisingly few studies have addressed such effects on the relationship between sizeand mating competition behaviour (Kodric-Brown, 1988; Otronen, 1996; Mills &Reynolds, 2003).

The present study explored size-related differences in male mating competitionin the two-spotted goby Gobiusculus flavescens (Fabricius 1779). Gobiusculusflavescens is a small (total length, LT, 35–55 mm) marine fish, which is very com-mon in shallow waters along rocky shores of Western Europe. Males defend nests inmacroalgae (Saccharina latissima and Laminaria digitata) or empty mussel shells(mostly Mytilus edulis) in shallow waters (typically <5 m depth) to which theyattract females for spawning (Gordon, 1983; Mobley et al., 2009). Several femalescan spawn in a single nest (Gordon, 1983; Mobley et al., 2009). Males providepaternal care until hatching (including defence, cleaning and fanning) (Skolbekken &Utne-Palm, 2001). Both males and females can reproduce several times during a sin-gle breeding season (May to July) and normally live for only 1 year (Johnsen, 1945).Successful sneaking appears to be rare in the studied population (0·1% of the off-spring; Mobley et al., 2009), even under strong competition (K. Mobley, S. Wacker,E. Forsgren, S. Shuster & T. Amundsen, unpubl. data).

© 2012 The AuthorsJournal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2012.03296.x

M A L E S I Z E A N D M AT I N G C O M P E T I T I O N 3

Gobiusculus flavescens experience an exceptionally flexible social environment,with densities of same-sex competitors and potential partners varying temporally(Forsgren et al., 2004) and spatially (T. Amundsen, E. Forsgren, K. Lindstrom, A. C.Utne-Palm, unpubl. data). Wild populations may experience a 10-fold decrease inmale density over the course of a breeding season. By contrast, female densityis much more stable, resulting in an increasingly female-biased sex ratio over thebreeding season (Forsgren et al., 2004). Experimental treatments reflecting naturalvariability in social environments were established to test effects on mating compe-tition for small and large males.

MATERIALS AND METHODS

The study was carried out at Sven Loven Centre for Marine Sciences, Kristineberg (58◦15′ N; 11◦ 27′ E), at the mouth of the Gullmarsfjord on the Swedish west coast from 26May to 2 July 2006. Data generated by this experiment have been analysed and published inrespect to overall levels of mating competition in males and females (de Jong et al., 2009).Here, previously unpublished data on the relationship between social environment, male bodysize and mating competition are analysed and presented.

G E N E R A L M E T H O D S

Gobiusculus flavescens were caught by hand netting in shallow waters (0·5–2 m depth) at12 islands near (0·1–3 km) the research station. The fish (stored in buckets) were transportedby boat to the research station (transport time <30 min). In the laboratory, they were imme-diately sorted by sex and initially kept in single-sex aquaria (10–50 fish per aquarium; size85 × 25 × 30 cm). The males were soon (usually the same day) transferred to individualstorage aquaria of 25 × 30 × 30 cm. The LT was measured to the nearest 0·5 mm usinga grid, and wet body mass was determined to an accuracy of 0·01 g using a Mettler bal-ance, after carefully blotting the fish to remove excess water. In order to individually identifyeach fish during observations, subcutaneous coloured VIE tags were injected (Visible ImplantElastomer, Northwest Marine Technology Inc.; www.nmt.us). Previous work indicates thatVIE tags do not affect behaviour (Whiteman & Cote, 2002) or mortality (Griffiths, 2002)in comparably sized gobies. Colour coding was randomized with respect to size-class andtreatment. Before marking, fish were anaesthetized in a 2-phenoxyethanol/saltwater solution(120 μl l−1) for c. 60 s. A strip of 3–4 mm VIE was injected subcutaneously close to thedorsal fin, and the fish was placed in oxygenated sea water to recover. There were no indica-tions of negative effects of the marking procedure on behaviour or mortality. Males were keptfor 62 ± 14 h (mean ± s.d., n = 126) and females for 40 ± 30 h (n = 127) before beingintroduced into experimental treatment aquaria. All fish used in this study were released intoa suitable habitat near the research station after the experiment.

E X P E R I M E N TA L D E S I G N

In order to study the relationship between body size and male competition, various com-petitive situations were created, while standardizing LT differences between males. Eachtreatment contained males of different sizes. To manipulate the social environment, treat-ments included the following numbers of males and females (M:F): 2:4, 4:8, 8:4 and 4:2.Thus, treatments varied the density both of same-sex competitors and of potential mates.In doing so, the treatments produced three different male (and female) densities and twomarkedly different sex ratios (0·33 and 0·66; [M (M + F)−1]; Kvarnemo & Ahnesjo, 1996)within the range of sex ratios occurring naturally in the population studied (Forsgren et al.,2004). Trials of the four treatments were conducted simultaneously to standardize potentialtemporal effects.



Table I. Size (total length, LT, and body mass, M) of Gobiusculus flavescens males (foursize-classes) used in an experiment to test body size effects on competition in various

social environments

Size-class

Very small Small Large Very large

n 28 35 35 28LT range (cm) 3·5–4·0 4·0–4·3 4·2–4·6 4·5–5·2Mean ± s.d. (cm) 3·87 ± 0·12 4·10 ± 0·07 4·34 ± 0·11 4·76 ± 0·20M range (mg) 333–585 437–665 527–769 648–1144Mean ± s.d. (mg) 461 ± 56 552 ± 48 648 ± 59 823 ± 148

Eight sets of replicates (32 trials) were carried out during the study. In the last set of repli-cates, a non-identified skin disease affected several fish, which showed aberrant behaviour.The last set of replicates was therefore excluded from the analyses. A single male from thepenultimate set of replicates (but not the entire set of replicates) was excluded for the samereason (4:8 treatment, very small male). Thus, the number of valid (analysed) sets of replicateswas seven (28 trials, 97 focal male observations). One female died (for unknown reasons)during the experiment and was replaced by a similarly sized fish.

In order for treatments to solely involve potential competitors and mates, only males andfemales judged to be ready to mate were used. Hence, round, mature females (Svensson et al.,2006) and males that had proven to be in mating mode were selected. The latter was achievedby screening males for interest in females, before the experiment (de Jong et al., 2009).

Males and females of four size-classes were used to standardize the size contrasts withintreatments and to simulate a near-natural size range (Table I). When a treatment includedfour fish of the same sex, one fish from each size-class was used. Similarly, two fish fromeach size-class were used if a treatment included eight fish of one sex, and only fish fromeach of the two central size-classes in treatments with two fish of the same sex. The size-classes reflected the approximate normal distribution for LT in the population in both sexes(T. Amundsen & E. Forsgren, unpubl. data). Within each trial there was a minimum differenceof ≥0·5 mm between individuals of adjacent size-classes, and a mean ± s.d. difference of2·9 ± 1·5 mm (n = 91). Because of a limited availability of individuals of certain LT at somesampling occasions, however, the size-classes overlapped slightly across replicates (Table I).

All aquaria used in this study were provided with a constant water supply from an intake at7 m depth. Gravel and artificial algae were provided as shelter (Amundsen & Forsgren, 2001;Pelabon et al., 2003; Borg et al., 2006; Fig. 1). Experimental aquaria were 60 × 38 × 35 cmand were exposed to natural light through windows, supplemented with artificial light thatfollowed the natural light regime (58◦ 15′ N). Mating and physical contact between the twosexes was prevented, whereas individuals within each sex were allowed to interact freely.Matings were prevented in order to keep densities of mating-ready males and females con-stant throughout each trial. A transparent and perforated Plexiglas divider allowed visual andolfactory but not physical contact between males and females (compartment lengths 40 and20 cm, respectively, for males and females; Fig. 1). There was one water supply and one wateroutlet in each compartment and the water flow was balanced. Each aquarium was suppliedwith a number of artificial nests (PVC tubes of 14 mm inner diameter and 80 mm length)identical to the number of males in the actual treatment (Fig. 1). These nest tubes are suitablefor both small and large males (pers. obs.). The locations of aquaria in the experimental roomwere randomized for the four treatments and visual contact between aquaria was blocked.Fish were fed twice a day ad libitum with Artemia sp. nauplii.

The established treatments involved male and female densities within the natural range forthe species. Females commonly occur in shoals that are as dense or denser than in the presentstudy (pers. obs.). The male densities established were higher than average densities in thenatural breeding habitat (Forsgren et al., 2004), but suitable nest substrata in the wild can



7 3

5 1

8 4

6 2

Fig. 1. Top view of aquaria used to test how male size affects competition in Gobiusculus flavescens invarious social environments mimicking natural variation in the species. Male (M) compartment (left),female (F) compartment (right), transparent divider ( ), algae ( ) and stones ( ) (numbered 1–8);nest tubes were provided as follows: 8M:4F treatments: structures 1–8 (as shown); 4M:2F and 4M:8Ftreatments: structures 3–6; 2M:4F treatments: structures 4 and 6.

result in inter-nest distances smaller than those in the high male density treatments (c. 15 cm)of the present study (pers. obs.).

O B S E RVAT I O N S

In order to allow fish to habituate to experimental conditions without visual access to theother sex, a non-transparent divider was placed alongside the transparent divider overnight[17 ± 4 h (mean ± s.d., n = 28)] before the start of the experiment. In the morning of thefirst observation day, this divider was carefully lifted. A first observation (day 1) was carriedout 8 ± 4 h (n = 28) afterwards. A second observation took place 3 days later (day 4).

Courtship and agonistic behaviours for each focal male were recorded by continuous obser-vation during 10 min. For each treatment and observation session, two or four focal maleswere observed successively. Accordingly, in treatments with eight individuals of one sex,one of the two fish of each size-class was randomly selected for observation by tossing acoin. The order of observation was determined at random within a treatment. Treatments wereobserved consecutively, in a randomized order.

The following male courtship behaviours were recorded: fin displays (male erects dorsalfin), quivers (male quivers his whole body) and leads (male swims to his nest with undu-lating body movements; Amundsen & Forsgren, 2001; Pelabon et al., 2003). Male agonisticbehaviours recorded included fin displays (similar to courtship but directed to a male), chases(male darts towards another male) and attacks (chases resulting in physical contact; Forsgrenet al., 2004; de Jong et al., 2009). Also the number of nest entries by the focal male wasrecorded, and the male’s position scan sampled every 20 s. Positions were noted as: within theassociation area (≤5 cm from the female compartment), within the nest area (≤1 fish lengthfrom a nest) and elsewhere (every other position). The head of the focal fish determined itsrecorded position. A male was treated as a nest-holder in the analyses if he had either entereda nest or stayed at least 20% of the time in a nest area. The definition of nest-ownership isconservative as it is based on only 10 min of observation per individual.



DATA A NA LY S E S

Analyses are based on observations made on day 4 of the experiment because, on day 4,the fish would probably be more consistently acclimated to experimental conditions, andalso more likely to show consistent responses to the experimental social environment (dueto longer exposure). At the time of the first observation (day 1), fish had only been in theexperimental tanks for 1 day. It is known from previous work on the species that, for manyfish, it takes more than a day to become sufficiently acclimatized to display natural breedingbehaviours. In the wild, breeding males are relatively stationary and apparently territorial,staying much of the time quite close to their nests, or inside them (Forsgren et al., 2004; deJong, 2011). Neighbouring territorial males are, therefore, likely to repeatedly encounter eachother over periods of up to several weeks (I. Muck, S. Wacker & T. Amundsen, unpubl. data).

Data of individuals within each trial were not independent and residuals of all responsevariables deviated from a normal distribution. Generalized linear mixed models (GLMM) inR version 2.8.1 (R Foundation for Statistical Computing; www.r-project.org) were thereforeused to test for effects of male LT on mating competition behaviours. The LT was entered asa continuous explanatory variable and the observed behaviours as response variables. To testfor differences in the strength of the relationship between LT and mating competition (i.e. theslope fitted by the model) among treatments, sex ratio (two-level categorical variable: 0·33and 0·66) and male density (three-level categorical variable: two, four and eight males) andtheir interaction with LT were included in the model. To account for the lack of independenceof data, aquarium was included as a random factor, allowing both slopes and intercepts tovary on aquarium level. First, the full model was fitted and then low effect, non-significantinteractions and explanatory variables removed stepwise, based on mean ± s.e. and P -values.This procedure was unambiguous for all models. After each step of simplification, whetherthe fit of the model decreased significantly (α = 0·1) was tested, using χ2 tests. Finally,the fit of the reduced model was inspected by plotting the predicted relationship against theobserved data.

Agonistic chases and attacks are similar apart from the physical contact with the opponent(in the case of ‘attacks’), and were pooled in the analyses (chases). Only 32% of the malesperformed agonistic chases and this count variable was therefore transformed into a binomialvariable. Most males (77%) performed agonistic fin displays and the variable was treated asa count variable, including non-behaving males. The three recorded courtship behaviours (findisplays, quivers and leads) were pooled into one variable (sum per individual) to avoid multi-ple testing. As only 59% of the males courted during the observations, courtship behaviour wasfirst analysed as a binomial variable. Similar analyses were thereafter performed with the fre-quency of courtship behaviour as response variable, including only males that courted. Thesecourtship behaviours usually occurred in a defined sequence: fin display, quiver, lead swim(pers. obs.). Most sequences were terminated after fin displays or quivers. Nest-ownershipwas recorded and analysed as a binomial variable. Time spent in the association area (nearthe females) was analysed as proportion data. When frequencies of behaviour were analysed,the observed overdispersion was accounted for by adopting a quasi-poisson error structure.Linear predictors are reported in logits for binomial response variables and in ln for countresponse variables. All tests were two-tailed.

RESULTS

N E S T OW N E R S H I P

The likelihood of a male to take up a nest increased significantly and gradually withmale body size [Table II and Fig. 2(a)]. Males of the largest size-class were morethan twice as likely to hold a nest than males of the smallest size-class (Table II).Neither sex ratio nor male density interacted significantly with the effect of bodysize on the likelihood of nest-ownership. Interaction effects, male density and sexratio were therefore removed from the model. Nest-holders spent a mean of 45%



Table II. Relationship between body size, social environment and male mating behaviour inGobiusculus flavescens. Estimates from GLMM on the effect of totallength (LT) on the occur-rence of mating competition behaviours and predicted likelihoods to perform these behavioursfor average sized males of the smallest and largest size-classes across treatments, in an exper-iment to test body size effects on competition. For courtship, estimates are also reported formale-biased and female-biased treatments separately (P -value for sex ratio × LT interaction).

All linear predictors are in logits

Predicted likelihood

n Slope ± s.e. P

Smallestsize-class

Largestsize-class

Nest ownership 97 2·45 ± 0·81 <0·01 0·35 0·83Agonistic chases 97 2·24 ± 0·85 <0·01 0·12 0·50Agonistic fin displays 97 2·02 ± 1·43 >0·05 0·70 0·93Recipient of agonistic chases 97 −1·20 ± 0·68 >0·05 0·58 0·32CourtshipAcross treatments 97 3·25 ± 1·10 <0·01 0·36 0·91Female biased sex ratio 41 5·24 ± 1·96 0·31 0·98

>0·05Male biased sex ratio 56 1·25 ± 0·99 0·41 0·68

(upper and lower quartiles: 18 and 66%) of the observation time in the nest area andentered the nest a median of 12 times during 10 min of observation (upper and lowerquartiles: 5·5 and 20·0). The mean proportion of males holding a nest was 0·71, 0·52and 0·57 in treatments with two, four and eight males, respectively, and did not differsignificantly among treatments (GLM, d.f. = 1, 26, Z = −0·5, P > 0·05).

AG O N I S T I C B E H AV I O U R

The likelihood for a male to chase another male increased significantly with malebody size [Table II and Fig. 2(b)]. The male size effect on chases seemed to be mainlycaused by the low likelihood of chases by males of the smallest size-class [Fig. 2(b)].Males of the largest size-class were four times as likely to perform chases as malesof the smallest size-class (Table II). By contrast, there was no significant effect ofmale body size on the frequency of agonistic fin displays (GLMM, n = 97, t = 0·79;slope ± s.e. = 0·61 ± 0·77) or the proportion of males that performed agonistic findisplays [Table II and Fig. 2(c)]. Notably, the majority of males of all size-classesperformed agonistic fin displays [Fig. 2(c)]. Body size did not significantly affectthe number of agonistic fin displays a male received (GLMM, n = 97, t = −0·83;slope ± s.e. = −0·33 ± 0·40) or the likelihood for a male to receive agonistic chases(Table II). Male density or sex ratio did not significantly interact with the effect ofbody size on any of the tested agonistic behaviours. Interaction effects, male densityand sex ratio were therefore removed from all four models on agonistic behaviour.

Among nest-holders, 45% (25 of 55) of the males performed agonistic chases,whereas among non-nest-holding males only 8% (six of 42) made chases (GLMM,n = 97, P < 0·001). The proportion of nest-holding males that performed agonis-tic chases was 0·14 (one of 7), 0·57 (eight of 14), 0·47 (eight of 17) and 0·47(eight of 17) for males of the very small, small, large and very large size-class,



Per

cent

occ

uren

ce

Size class

100 (a) (b)

(c) (d)

80

60

40

20

0Very small Small Large Very large Very small Small Large Very large

100

80

60

40

20

0Very small Small Large Very large Very small Small Large Very large

Fig. 2. Proportion of Gobiusculus flavescens males of four size-classes that (a) held a nest, (b) aggressivelychased other males, (c) performed agonistic fin displays to other males, and (d) courted females, in anexperiment on body size effects on competition (n = 28 for small and large, n = 20 for very small andn = 21 for very large males).

respectively. Across treatments, LT had no significant effect on the likelihood ofagonistic chases among nest-holders (GLMM, n = 55, Z = 0·9, P > 0·05; slope ±s.e. = 0·89 ± 1·04). Agonistic behaviours occurred in all 28 trials and agonistic findisplays were much more frequent than chases (327 fin displays and 101 chasesduring 97 observations; binomial test, P < 0·001).

C O U RT S H I P B E H AV I O U R

Across treatments, large males were more likely to court females than were smallones [Table II and Fig. 2(d)]. The likelihood to court appeared to increase graduallywith male size [Fig. 2(d)], and was more than twice as high among males of thelargest size-class as among males of the smallest size-class (Table II). The interactioneffect of sex ratio and body size on the occurrence of courtship behaviour wasnot significant (Table II), but removing it from the model would have significantlyreduced the fit of the model. The non-significant interaction suggested a strongereffect of body size on courtship in the female biased sex ratio treatments (Table II).Male density did not affect the relationship between male body size and the likelihood



to court. The interaction between male density and body size and the factor maledensity per se were thus removed from the model.

Among nest-holders, 80% (44 of 55) showed courtship behaviour whereas only31% (13 of 42) of non-nest-holding males courted (GLMM, P < 0·001). Acrosstreatments, LT had no significant effect on the proportion of nest-holders that courted(GLMM, n = 55, Z = 1·3, P > 0·05; slope ± s.e. = 1·67 ± 1·30). The proportionof nest-holders of each size-class that courted was 0·86 (six of 7), 0·57 (eight of 14),0·88 (15 of 17) and 0·88 (15 of 17), for very small, small, large and very large sizemales.

A separate model was fitted to test whether the frequency of courtship was relatedto LT, including only males that courted. Male density could not be included in thismodel, due to small sample size in some categories. The interaction term and sex ratiowere excluded from the model, as they were not significant. In the reduced model,there was no significant effect of LT on the frequency of courtship behaviour amongcourting males (GLMM, n = 57, t = 0·10; slope ± s.e. = 0·67 ± 0·60). When onlycourting males were included, the median (n) frequencies of courtship behaviours(pers. obs.) for the four size-classes were: very small: 3·0 (9), small: 7·0 (14), large:17·5 (18) and very large: 8·5 (16).

Courtship occurred in 26 of 28 trials, with a total of 655 fin displays, 415 quiversand 297 lead swims during 97 focal male observations. There was no significanteffect of body size on the proportion of time males spent in the association area nearthe females (GLMM, n = 97, t = 1·07; slope ± s.e. = 0·07 ± 0·07; observed meanproportions of time per size-class: very small: 0·09, small: 0·16, large: 0·23 and verylarge: 0·11). There were no significant effects of sex ratio or male density on therelationship between LT and time spent in the association area; these were thereforeremoved from the model.

DISCUSSION

Across the range of social environments, large males were much more active incourtship of females and in chasing male competitors, than were small males. Largemales were also more likely to hold a nest. They were, however, no more likely thansmall ones to visually display to competitors, as such behaviour occurred frequentlyamong males of all size-classes. The analyses revealed no significant effects ofsex ratio or density on the behavioural engagement of differently sized males inmale–male competition.

S I Z E E F F E C T S O N M A L E – M A L E C O M P E T I T I O N

There was no indication for small males compensating for their lower RHP andlower attractiveness to females with increased aggressiveness and courtship. Neitherwas a curvilinear relationship between body size and agonistic behaviour observed(Emlen & Oring, 1977; Logue et al., 2011). Instead, the results suggest that thevery smallest males almost completely refrained from escalated agonistic behaviours,whereas the occurrence of such aggressive acts was rather similar among medium-sized and large males [Fig. 2(b)]. The likelihood of courtship, in contrast, increasedgradually with male size [Fig. 2(d)].



That small G. flavescens males engage little in costly mating competition whenfaced with larger competitors is especially plausible because of the species’ flexiblesocial environment. Reproductive success of small males is likely to be low whenmating competition is intense, but should increase over the course of the breedingseason, when mating competition relaxes (Forsgren et al., 2004). Small G. flavescensmales may thus benefit from staying out of costly mating competition when com-petition is strong, in contrast to species where small males have no alternative thanto compete, even when competition is high (‘desperado effect’; Grafen, 1987). Thepresent results suggest that female choice and male competition act in concert inpromoting a higher mating success among large than small males, at least whenfemales are in short supply, as female G. flavescens prefer large and courting males(Borg et al., 2006).

That large males more often performed chases than small males, while malesof all sizes performed agonistic fin displays, is in line with classical theory whichpredicts small males to enter low-intensity competition (displays) but to withdrawbefore escalation (chases) due to their lower RHP (Maynard Smith, 1982; Enquist &Leimar, 1983). Both the energetic costs and the risk of physical injury increase withincreasing escalation (Parker, 1974; Maynard Smith, 1982; Ros et al., 2006), andexpected benefits for small males are low when contests are mainly decided by bodysize per se rather than aggressiveness (Morrell et al., 2005). Notably, the smallestmales rarely performed chases even when holding a nest.

T H E RO L E O F R E S O U R C E C O M P E T I T I O N

Small and large male G. flavescens have been found to court to a similar degree ina non-competitive situation (Amundsen & Forsgren, 2003). Moreover, all males inthe experiment courted in a single-male screening set-up before the treatments. Therelationship between body size and courtship in the present study was thus probably aresult of male–male competition. Large males, however, may have suppressed smallmale courtship in two different ways: directly or via competition for resources neededto mate (Ahnesjo et al., 2001; Klug et al., 2010). Direct courtship interference (i.e. amale agonistically interrupting another male’s courtship) by larger males has beenreported in other goby species (Bisazza et al., 1989; Kangas & Lindstrom, 2001).Such interference was anecdotally observed but not systematically recorded in thepresent experiment (S. Wacker & K. de Jong, pers. obs.), and has also been observedin the wild in G. flavescens (pers. obs.).

Even though the breeding substratum was not limited (there were as many nesttubes as males in each treatment), a higher RHP and more escalated aggressivebehaviours on the part of larger males may have prevented nearby nest establishmentby smaller males and led to larger males more often holding a nest. That is, males mayhave competed for space (breeding territories) rather than breeding substratum per se.Limiting the number of neighbouring males would result in fewer competitors inmating competition and may thereby lead to greater expected mating success. Intensecompetition for breeding resources is common among substratum-breeding fisheswith paternal care and animals with resourced-based breeding systems in general(fishes: Magnhagen, 1994, 2006; Borg et al., 2002; Lindstrom & Pampoulie, 2005;general: Emlen & Oring, 1977; Andersson, 1994). Most of the nest-owner males inthis study performed courtship, with no difference between size classes. An advantage



of large males in resource competition may thus have caused the observed body sizeeffect on courtship.

The above scenario assumes that resource competition and mating competition areseparate processes that take place in succession, so that a male first needs to competesuccessfully for a resource to become ‘qualified to mate’ (Ahnesjo et al., 2001;Klug et al., 2010). The relationship between these two processes, however, may notalways be straightforward. Here, two alternative scenarios are outlined: (1) a reversedtemporal order, with mating competition preceding resource competition. That is,males compete for females before they have secured a nest site or territory. Only thosemales that are successful in mating competition then enter a potential competition forresources required to breed. While this scenario is unlikely for the majority of males,based on natural history knowledge for the species, it is possible that less competitive,small males may adopt such a strategy and (2) resource and mating competition occursimultaneously, implying that competitive behaviours cannot be conclusively relatedto one or the other type of competition, practically or theoretically. This may be thetypical case for species where males defend a territory rather than a specific nest site,and where the main function of the territory is to increase success in mate acquisition,by reducing the likelihood that other males interfere. In this scenario, competition forthe resource becomes at the same time competition for matings. If such a scenarioapplies, all male–male competition in the experimental tanks of the present studymay have been territorial conflicts, with large, dominant males aggressively limitingsmaller males’ access both to nests and to females at the same time.

While the present study conclusively shows that male size matters in competition,including effects on nest ownership, courtship and aggressive behaviours, it doesnot show conclusively whether the competition is mainly over resources requiredto breed, over females or over both at the same time. Further studies are neededto disentangle mating and resource competition and to investigate their interplay inG. flavescens. Competition for territories and for mates may be functionally relatedin many territorial animals, including many substratum breeding fishes.

S O C I A L E N V I RO N M E N T A N D S I Z E - R E L AT E D M A L E – M A L EC O M P E T I T I O N

The social environment (densities of competitors and sex ratio) had no statisticallysignificant effect on the relationship between body size and male–male competition,suggesting the absence of any strong interaction effect between male size and socialenvironment on male–male competition. In particular, there was no sign of smallmales competing more actively than large males in any of the established treatments.Even though only a little more than half of the males of the present study took upa nest, the proportion of nest owners did not differ among treatments. The treat-ments thus produced both variation in overall numbers of competing males and acorresponding variation in numbers of nest holders. The study, however, may nothave had sufficient power to detect subtle effects of sex ratio and male density onsize-related male–male competition. Hence, more studies are needed to conclusivelyanswer whether the social environment can affect the relative engagement of largeand small males in mating competition.

In conclusion, this study reveals a clear positive relationship between male bodysize and male–male competition across the natural range of social environments in



a species experiencing extensive natural variation in densities of competitors andpotential mates. In contrast to suggestions that small or intermediate males maysometimes engage more in mating competition than large males, the results suggestthat large males consistently behave more competitively than small ones. This patternsupports classical theory based on the higher RHP of larger males. Further studiesare required to answer whether the benefit of large male body size mainly affectedcompetition for resources, or for mates, and how these two processes of competitioninteract.

We thank L. Ottosson, M. Meland, J. Eriksen and C. Brevik for help with collection andhusbandry of fish. G. Hysing Bolstad, A. Svensson and H. Parn kindly helped with statisticalanalyses. L. Cats Myhre and K. Mobley provided helpful comments on the manuscript. Wealso thank the managers and staff of the Sven Loven Centre for Marine Sciences for hospitalityand generous assistance. The study was financially supported by the Research Council ofNorway (MARE programme; grant to E.F.), the Royal Swedish Academy of Science andthe German Academic Exchange Service (DAAD; grant to S.W.). The study was carried outunder licence from the Swedish Ethical Committee on Animal Research (Goteborg).

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