Relative costs of courtship behaviours in nest-building sand gobies

Animal Behaviour 77 (2009) 541–546

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Relative costs of courtship behaviours in nest-building sand gobies Karin H. Olsson a, *, Charlotta Kvarnemo a, Ola Svensson a, b,1 a b

¨teborg University Department of Zoology, Go Department of Biological Sciences, University of Hull, U.K.

a r t i c l e i n f o Article history: Received 12 March 2008 Initial acceptance 28 April 2008 Final acceptance 26 October 2008 Published online 27 December 2008 MS. number: 08-00180R Keywords: courtship Gobiidae nest building parental effort paternal care Pomatoschistus minutus sand goby sexual signalling

Courting males often use multiple signals to advertise their quality to females. Assuming that courtship traits are energetically costly, one would expect a limit to the overall courtship effort of an individual and that a high courtship effort takes its toll on individual condition. We tested this experimentally using a small marine fish, the sand goby, Pomatoschistus minutus, whose males attract females through courtship displays and well-built nests (mussel shells covered with sand). At the end of a 5-day period of supplemental food, or repeatedly induced courtship or construction of nests (or none of these, as a control), we tested whether male display intensity, nest quality (nest cover and nest opening size) and body condition were affected. Males provided with food in excess were in significantly better condition and had significantly higher nest quality than control males. Display rate, however, was not significantly affected by feeding regime. Fish that had been manipulated to perform increased courtship or nest building did not suffer in terms of reduced condition, display rate or nest quality. However, individual fish that displayed intensely after treatment also built better-covered nests. Both of these traits are important in female choice. Moreover, fish that displayed intensely before the treatment continued to do so after treatment, a result that is compatible with signalling of genetic or phenotypic quality. Our results suggest that (1) nest cover is an honest signal of male condition, although we found no cost of nest building per se and (2) courtship display does not signal male condition. Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Courtship behaviour is thought to demonstrate an individual’s genetic or parental qualities to its mate when attempting to secure a mating opportunity (Møller & Jennions 2001). Females are thus expected to gain information about their potential mate from such advertisement signals (Andersson 1994). For example, this is true for the desert beetle Parastizopus armaticeps: females choose mates based on body mass, which is related to deeper breeding burrows and thus increased offspring survival (Rasa et al. 1998). Similarly, females of the cricket Teleogryllus oceanicus react quicker to males whose songs correspond to an elevated immune response (Tregenza et al. 2006). In birds, female barn swallows, Hirundo rustica, select partners based on tail length, which is believed to be a signal of good genes (Soler et al. 1998). In teleosts, female common gobies, Pomatoschistus microps, are known to prefer males with well-camouflaged nests (Jones & Reynolds 1999); such males are in better condition and less prone to show filial cannibalism (Kvarnemo et al. 1998). Courtship may include multiple signals to the female, who in turn may use a number of cues in her choice of a mate. Multiple

* Correspondence: K. H. Olsson, Department of Zoology, Go¨teborg University, Box 463, SE-40530 Gothenburg, Sweden. E-mail address: [email protected] (K.H. Olsson). 1 O. Svensson is now at the Department of Zoology, Go¨teborg University.

cues may include a combination of informative viability indicators and uninformative or Fisherian attractiveness cues, but can also be a set of cues that facilitate detection or provide additional information (Candolin 2003). However, while different signals may give information about different mate qualities, a majority of studies have found multiple traits to be uncorrelated (Candolin 2003). Female Trinidadian guppies, Poecilia reticulata, prefer large males, but also intense courtship displays, two traits that are correlated only under low light conditions (Reynolds 1993). Moreover, male behaviour may be guided by the cost/benefit ratio that applies to the particular set of traits and behaviour of that individual. This ratio may be influenced by the condition of the individual (Kotiaho 2001; Svensson et al. 2004), predation risk (Forsgren 1992; Reynolds 1993) and the apparent attractiveness of the male (Forsgren 1997b). In addition, individual males might not necessarily attempt to master all available forms of courtship, but rather focus on a subset of traits. Consistent with this, displacement fanning in male sand gobies, Pomatoschistus minutus, was found to correlate with large nests or intense courtship displays, but not both (Svensson & Kvarnemo 2005). For signals such as courtship to be honest, they need to be costly to perform. Otherwise, any individual could perform them and the importance of the signal would be nullified. That courtship is dependent on energy stores has, for example, been shown in male red-sided garter snakes, Thamnophis sirtalis parietalis (Shine &

0003-3472/$38.00 Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2008.10.021

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Mason 2005). Some studies on teleosts also show that sexual traits increase energy expenditure: in the swordtail Xiphophorus montezumae, experimentally shortened sword length decreased metabolism during both swimming and courtship (Basolo & Alcaraz 2003) and in the cichlid Tilapia zilli, escalated fighting increased energy expenditure (Neat et al. 1998). However, it is not the energy expenditure per se, but a greater negative fitness effect of it for low-quality males than for high-quality males, that ensures the honesty and evolutionary stability of sexual traits (Kotiaho 2001). This has been shown for the drumming wolf spider, Hydrolycosa rubrofasciata (Kotiaho 2000) and is in line with the handicap model (Zahavi 1975, 1977). Consistently, male sand gobies that, in a field experiment, received a food supplement spent more time in the vicinity of their nests, mated sooner, received more eggs and had better fat reserves, than unfed males (Lindstro¨m 1998). Honesty can also be ensured by the social context, such as male– male competition in the case of three-spined sticklebacks, Gasterosteus aculeatus: starved males reduced their signalling under male–male competition (Candolin 1999, 2000). Furthermore, the cost of courtship may be reflected in a reduced parental effort, as shown in egg-tending two-spotted goby, Gobiusculus flavescens males (Bjelvenmark & Forsgren 2003). Our aim in this study was to investigate the relative cost of two aspects of courtship for the sand goby: nest building and courtship display, measured both in terms of a change in behaviour after versus before treatment and by assessing the physical condition of the male. The effect of supplemental feeding was also investigated. The hypothesis was that courtship displays and nest building are energetically expensive. Treatments, in which the males were manipulated to perform these behaviours repeatedly, should worsen their condition, so they should be less likely to perform well at the end of the experiment, compared to a control group. Fish that had been fed ad libitum, on the other hand, were expected to be in better condition and improve their performance, compared to the control fish. METHODS Study Species The sand goby is a small fish found in marine and brackish waters along the coasts of northern Europe, breeding on shallow sandy bottoms (Miller 1986). Typically breeding for one season only, the sand goby is polygamous, with both males and females spawning sequentially with different mates. The male builds a nest by excavating an empty mussel shell and shovelling sand on top of it with his tail. Females are nonterritorial, while males defend the area close to the nest site. Males court females by displays, which include erect fins and short rapid bursts of swimming. The male breeding coloration includes an iridescent blue anal fin, a blackrimmed anal fin and darkened tail, pelvic and dorsal fins, as well as a blue-black and white spot on the dorsal fin (reviewed in Forsgren 1999), but melanization may be weak or even nonexistent (Svensson & Kvarnemo 2007). Large males have an advantage in competition over nest sites (Magnhagen & Kvarnemo 1989) and both sneaky fertilizations and parasitic spawning by other nestholding males take place (Jones et al. 2001; Singer et al. 2006; Svensson & Kvarnemo 2007). Several females may deposit eggs in the nests during a single brood cycle (Jones et al. 2001). The male provides all parental care, including fanning, grooming and defence against predators, until hatching, some 1–3 weeks later, depending on temperature (Forsgren 1999). Female sand gobies base their mate choice on multiple cues, such as courtship displays, displacement fanning, male size, breeding coloration and the sound made by the male during nest inspection by the female (reviewed in Svensson & Kvarnemo 2005).

Females also prefer to spawn with males that already have eggs in their nests (Forsgren et al. 1996). Hatching success may not necessarily be dependent upon male size, but care is subject to considerable variation, and females have been shown to discriminate between good and poor fathers (reviewed in Forsgren 1997a), although it is still unclear which particular male traits signal this ability. Experimental Procedure The experiment was conducted between 10 May and 15 June 2006 at the Sven Love´n Centre for Marine Sciences, Kristineberg (58 150 N, 11280 E) on the Swedish west coast. Sand gobies used in trials were caught in a nearby bay, Bo¨kevik, using a hand trawl. Immediately after capture, the fish were separated by sex and placed in 115-litre storage tanks with a layer of sand approximately 1 cm deep. All tanks were continuously supplied with fresh sea surface water (from 5 m depth, above the halocline and thermocline) of ambient salinity and temperature (7.5–17  C, warming up as the study progressed). However, of 47 males, 13 males experienced a decrease in temperatures and 19 males experienced an increase in temperatures (greater than 0.5  C) after treatment, compared to before. All treatments were run in parallel but owing to tank availability not all replicates ran simultaneously. Light conditions in the laboratory followed natural ones at that time of year with natural light through a window being reinforced with light from fluorescent tubes in the ceiling. Natural conditions imply few hours of night-time darkness with a protracted dusk and dawn. Fish in storage tanks were fed daily on chopped meat from blue mussel, Mytilus edulis. No fish was kept in captivity for more than 3 weeks. We investigated the relative cost of nest building, courtship display and restricted feeding by assessing the nest appearance and courtship display before and after a treatment period of 5 days, during which the males were assigned to one of four treatment groups: (1) daily feeding with excess chopped mussel meat, (2) daily nest destruction to induce repeated nest construction, (3) the presence of females to induce courtship displays, or (4) none of these as a control. Both the presence of females and the destruction of nests are regular occurrences in the wild: specifically, artificial nests covered by sand but untended by a male are destroyed within 24 h (K. H. Olsson, unpublished data). In the second treatment group, the covering of sand on top and in front of the nests was wafted away once a day. We noted the following day whether the nest was rebuilt or not after which the procedure was repeated. In the third treatment group, two females were placed in a perforated plastic container with some gravel in it, clearly visible to the male, and present in his tank for 6 h each day of the experiment. A new pair of females was used each day. The males of the other treatments all had a plastic vial in their tanks for 6 h each day, which contained no fish. The males of treatments 2–4 were not fed during the treatment period. The condition of the males was assessed by lipid extraction, which, being fatal to the fish, could only be performed postexperimentally. After the experiment, all females and any male that failed to build a nest initially were released into the sea where they were caught. Before the experiment, the males were not fed for 3 days. A male was then placed in a 20-litre tank (36  21 cm and 25 cm deep) containing a layer of fine sand, approximately 3 cm deep, and a halved clay flowerpot (diameter 6.5 cm) to serve as a standardized nesting site. At this stage all males were stimulated to build a nest by the visual presence of two ripe females, which were kept in a perforated plastic container, to prevent matings from occurring. A male was given 3 days to build a nest; if by then no nest had been constructed we replaced the male (in total 22 males).

K.H. Olsson et al. / Animal Behaviour 77 (2009) 541–546

The completed nest was photographed, and the volume of the sand covering the nest was estimated by comparing it to a photographic scale prepared by pouring sand onto a flowerpot in steps of 0.5 dl of sand (Svensson & Kvarnemo 2005). We assessed the size of the nest opening from the photo by comparing the visible arc of the flowerpot to a known length. The male was then introduced to two new females, selected for apparent fecundity and roundness, in the plastic container. After an acclimatization period of about 15 min, we recorded 1 h of courtship display using a Sony digital video camera (DCR-TRV30E). Courtship display was counted as the total number of courtship moves (fin displays, shivers and leading manoeuvres towards the nest, each counted as one move) that the male performed during the 5 min following the first such move. Each male was then randomly assigned to one of the treatment groups (feeding, nest destruction, presence of females or control). At the end of the 5-day treatment period, regardless of treatment all nests were destroyed and each male was again presented with the same halved flowerpot and two females in a perforated container. After the nest was rebuilt (the males were again given a maximum of 3 days to complete this), it was graded and display behaviour was recorded in the same manner as before. Four males failed to rebuild their nests, but were included in the analyses as we judged this to be a possible effect of treatment. The total length of the fish was measured (1 mm), before it was killed by placing it in a 2-phenoxy ethanol solution (2 ml/litre) for 10 min, after which it was immediately frozen at 18  C. It was then desiccated at 60  C for at least 24 h. The fish were weighed individually on a Sartorius (LE26P) microbalance (0.001 mg). The lipid content of each fish was extracted during 8 h in 100 ml of petroleum ether. Lipid mass was measured as the difference in mass before and after lipid extraction. Ethical Note The fish were fed at least once before the experiment started and a food deprivation period of 5–8 days has been used in many behavioural studies on sand gobies (e.g. Lissåker et al. 2003; Svensson et al. 2004; Lissåker & Kvarnemo 2006). These studies have shown no apparent adverse effects of food deprivation periods of this length. Because the experiments were conducted early in the breeding season, the sand gobies would be expected to be relatively unaffected by earlier breeding efforts and to be in peak condition. Since the tanks were continuously supplied by natural sea water, minute food particles did reach the males throughout the treatment period. Thus, the limited feeding in treatment groups 2, 3 and 4 was only moderately strict. Moreover, a study on the related common goby found that males eat less than females during the reproductive period while tied to their nests (Magnhagen 1986). This research was done with an ethical permit from the Swedish National Board for Laboratory Animals. Data Analysis In total, 47 males were used (mean length SE ¼ 54  4.3 mm, range 47–65 mm), 11 in the control group and 12 each in the other treatment groups. We judged that this was the minimum sample size required to give the statistical analyses enough power. When necessary, we used the following transformations to gain normality and homoscedasticity, allowing all data to be subjected to parametric tests: arcsine Ox (nest cover), 3Ox (nest opening), Ox (courtship) and log (lipid mass and lean body mass and the temperature difference before and after treatment (þ5)). Excess feeding, nest destruction and presence of females were always compared against the control group. All analyses of variance (ANOVA) or covariance (ANCOVA) were based on general linear models (GLM), and we used a repeated measures design whenever

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the analysis focused on a comparison of male performance before and after treatment. In these analyses treatment effects were measured as the interaction between the repeated measure (preand post-treatment) and the treatment. To account for differences in water temperature between the two times when nest attributes and display were measured, we also included the temperature difference as a covariate in these analyses. Similarly, when analysing body condition we entered lean body mass as a covariate and measured lipid mass. All nonsignificant (P > 0.2) interaction terms were deleted from such ANCOVAs, before we tested for main effects. All data were analysed using SPSS version 15.0 (SPSS Inc., Chicago, IL, U.S.A.), except partial correlations, which were performed using Statview 5.0 (SAS Institute Inc., Cary, NC, U.S.A.). The arc of the nest not covered by sand was measured using ImageTool version 3.00 (C. D. Wilcox, S. B. Dove, W. D. McDavid & D. B. Greer, http://ddsdx.uthscsa.edu/dig/) and converted into nest opening area with the formula area ¼ na  sinðarc length=na Þ, where na ¼ length of the noncovered arc of the artificial nest. RESULTS Treatment In the food excess treatment, the lipid content of the male, nest cover and nest opening differed significantly from the control (Table 1, Fig. 1). However, food in excess had no significant effect on male display (Table 1, Fig. 1). We found no significant effects of increased nest-building or courtship display effort on nest cover, nest opening, display behaviour or lipid content of the male (Table 1, Fig. 1). The repeated measures ANCOVAs showed significant impacts of temperature on both measures of nest building and display in all groups except the display treatment (Table 1), that is, increased temperature led to decreased nest cover, increased nest opening area and decreased display rate in analyses of the food excess treatment Table 1 Treatment effects of the three treatments tested against the control Measured trait

Prepost treatment

F1,20

P

Food excess treatment versus control Nest cover (dl) 5.65 0.028 4.10 0.056 Nest opening (cm2) Display (count) 3.65 0.071 Lipid mass (mg)*

Covariation with temperature or *body mass

Treatment effects

F1,20

F1,20

6.93 4.57 5.21 2.25

P 0.016 0.045 0.034 0.15

6.86 4.41 0.74 8.92

Increased courtship display treatment versus control Nest cover (dl) 0.29 0.87 0.48 0.48 Nest opening (cm2) 0.21 0.65 1.05 0.32 Display (count) 0.57 0.46 1.33 0.26 5.60 0.028 Lipid mass (mg)* Increased nest-building effort treatment versus control Nest cover (dl) 8.64 0.008 13.79 0.001 5.49 0.030 9.06 0.007 Nest opening (cm2) Display (count) 9.79 0.005 5.21 0.002 1.14 0.30 Lipid mass (mg)*

Figure

P 0.016 0.049 0.40 0.007

Fig. 1a Fig. 1b Fig. 1c Fig. 1d

<0.01 0.21 0.02 8.92

0.94 0.65 0.89 0.89

Fig. 1a Fig. 1b Fig. 1c Fig. 1d

0.09 0.07 0.74 1.02

0.33 0.80 0.25 0.32

Fig. 1a Fig. 1b Fig. 1c Fig. 1d

Treatment effects are measured as the interactions between prepost treatment  treatment and tested with repeated measures ANCOVA with temperature difference as covariate, except tests marked * which were tested with ANCOVAs with lean body mass as covariate. The presented covariation is interactions between prepost treatment  temperature, except tests marked * which show the covariation with lean body mass. Nest cover is the volume of sand covering the nest site, nest opening is the area of the nest opening, display is the number of courtship moves during the first 5 min after the first such move, lean body mass is male dry mass without lipids, lipid mass is the mass loss of the male caused by lipid extraction and temperature difference is the difference in water temperature between the preand post-treatment measures of nest attributes and display behaviour. Significant P values are given in bold.

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4

3.5 (a)

(b)

3.5

3 Nest opening (cm2)

Nest cover (dl)

3 2.5 2 1.5 1

2 1.5 1 0.5

0.5 0

2.5

Control

Feeding

Display

0

Nest

60

Control

Feeding

Display

Nest

Feeding

Display

Nest

18 (c)

16

(d)

50 40

Lipid mass (µg)

Display (counts)

14

30 20

12 10 8 6 4

10 2 0

Control

Feeding

Display

Nest

0

Control

Figure 1. Sand goby males were assigned to one of four treatment groups: daily feeding (feeding) with excess chopped mussel meat, females present to induce courtship display (display), daily nest destruction (nest) to induce repeated nest construction, or none of these (control). The figure shows mean þ SE values of (a) sand volume covering the nest, (b) entrance diameter and (c) number of courtship displays, measured before and after the treatment period, and (d) lipid mass, measured afterwards. -: After treatment; ,: before treatment.

versus the control and the increased nest-building effort treatment versus the control. Males were given a maximum of 3 days after the treatment period to rebuild their nests. The time needed to complete nest building after treatment did not differ significantly between any of the treatment and control groups (one-way ANOVA: F3,43 ¼ 0.20, P ¼ 0.90). Of the 12 males included in the nest destruction group, three males failed to rebuild their nests at all and the nine remaining males rebuilt their nests an average of 2.6 times out of 5. However, linear regressions within this treatment group showed no effect of rebuilding effort on the individual males’ change in nest quality, change in courtship display or lipid levels (number of times rebuilt versus change in nest opening area: r ¼ 0.255, F1,10 ¼ 0.696, P ¼ 0.42; number of times rebuilt versus change in courtship display: r ¼ 0.438, F1,10 ¼ 2.38, P ¼ 0.15; number of times rebuilt versus lipid levels: r ¼ 0.089, F1,10 ¼ 0.80, P ¼ 0.78). Nest quality refers to the nest parameters nest cover and nest opening area measured pre- and post-treatment as described in the methods, whereas nest-building effort is the number of times the nest was rebuilt during the treatment.

temperature was performed on all males regardless of treatment, to assess the potential association between different courtship traits. In a partial correlation matrix, each correlation between two variables is carried out while keeping all other variables constant. As expected, nest cover was negatively correlated with nest opening area, and lipid content was positively correlated with lean body mass (Table 2). Furthermore, nest cover was positively correlated with display, and nest opening area tended to be positively, although not significantly, correlated with water temperature (N ¼ 47, Table 2). Possible trends over time in the behaviour of individual fish were assessed using Pearson correlations between pre-treatment and post-treatment nest cover, nest opening and courtship display (N ¼ 47). Pre- and post-treatment nest cover tended, although not significantly, to be correlated (r45 ¼ 0.27, P ¼ 0.064), whereas nest opening was not correlated over time (r45 ¼ 0.13, P ¼ 0.37). Pretreatment courtship display was correlated with post-treatment courtship display (r45 ¼ 0.46, P ¼ 0.001). The behaviour trends of individual fish remained the same when treatment group 1 (food in excess, which had a significant effect on nest cover and nest opening) was excluded.

Behaviour Trends

DISCUSSION

A partial correlation between post-treatment nest cover, posttreatment nest opening, courtship, lipid mass, lean body mass and

In the present study, males provided with food in excess were in significantly better condition (high lipid content) and had

K.H. Olsson et al. / Animal Behaviour 77 (2009) 541–546 Table 2 Partial correlation on male attributes Nest Nest cover opening (dl) (cm2) Nest cover (dl) Nest opening (cm2) Display (count) Lean body mass (mg) Lipid mass (mg) Temperature ( C)

 þ þ þ 

Display Lean (count) body mass (mg)

0.793*** 0.422** 0.159   þ  þ þ 

Lipid mass (mg)

Temperature ( C)

0.012 0.088 0.025 0.107 0.230 0.263y 0.268y 0.018 0.025 0.427** 0.021 þ 0.170 0 0

Upper right: partial correlation on male attributes and temperature after treatment. Nest cover is the volume of sand covering the nest site, nest opening is the area of the nest opening, display is the number of courtship moves during the first 5 min after the first such move, lean body mass is male dry mass without lipids, lipid mass is the mass loss of the male after lipid extraction and temperature is the water temperature at the time when nest attributes and display were measured. Lower left: how male traits are predicted to be correlated if they were all positively correlated based on what we expect females to prefer. N ¼ 47. yP < 0.1; **P < 0.01; ***P < 0.001.

significantly higher nest quality (nest well covered, i.e. large volume of sand as well as small nest opening) after the treatment period, compared to control males. Display rate, however, was not significantly affected by feeding regime. In concert with this result, but in contrast to the positive effect of increased feeding on nest building, male condition was not correlated with post-treatment courtship display or any nest attributes, when analysed in a partial correlation across all treatments. Surprisingly, males manipulated to perform courtship displays and nest building repeatedly did not differ from the control in nest attributes, courtship display or condition. Moreover, our results support a pronounced effect of individuality regarding display intensity, which is consistent over time regardless of treatment. Therefore, repeated measures designs are essential for these types of studies. The link between nest quality and general condition of males has been demonstrated several times previously in Pomatoschistus (Kvarnemo et al. 1998; Lindstro¨m 1998; Jackson et al. 2002), as has the function of nest crypsis as defence (Lindstro¨m & Ranta 1992; Jones & Reynolds 1999). Furthermore, in the common goby, filial cannibalism is associated with poorly covered nests (Kvarnemo et al. 1998) and consistently, in both sand gobies and common gobies, females prefer to spawn in well-covered nests (Jones & Reynolds 1999; Svensson & Kvarnemo 2005). The size of the nest opening, however, is affected by a host of factors, such as water oxygen levels (Jones & Reynolds 1999; Lissåker et al. 2003), presence of egg predators (Lissåker & Kvarnemo 2006) and sneaker males (Svensson & Kvarnemo 2003, 2005). The nest opening area is thus highly variable and nest cover may give a more reliable estimate of both male and nest quality (Svensson & Kvarnemo 2005). Similarly to gobies, the nest size in magpies, Pica pica, is a sexually selected trait signalling parental quality (Soler et al. 2001) and experimentally increased food availability results in increased nest size (De Neve et al. 2004). Furthermore, nest building has the potential to signal immunofunction in both birds (passerines, Soler et al. 2007) and fish (the three-spined stickleback, Barber et al. 2001). In the three-spined stickleback, individual males differ consistently in nest-building abilities over time (Rushbrook et al. 2008). Thus, even though traits associated with ‘good’ genes and those associated with parental care are not necessarily the same (Soler et al. 1998; Møller & Jennions 2001; for example extrapair paternity in birds results in social mates providing direct benefits (care) and fertilizing mates indirect benefits (genes)). However, in the sand goby, direct and indirect benefits are mainly provided by the same individual (Svensson & Kvarnemo 2005).

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In previous studies of gobies, male display has been negatively correlated with nest cover, body length (Svensson & Kvarnemo 2005) and condition measured as lipid mass (Svensson et al. 2004) and it has been suggested that a male, rather than being a jack-ofall-trades, focuses on a subset of traits to attract females. In contrast, in the present study, courtship display was positively correlated with nest cover (strongly so) and body mass (a nonsignificant trend). It is not easy to tell why the different studies differ in their results, as the experimental set-ups differed in many small details (e.g. courtship display was not measured in the same way) and did not contain the same set of variables (which is important given that partial correlations measure the degree of association between two variables, with the effect of a set of other variables removed). In our opinion, however, our current results are more straightforward than the previous results because, based on what we expect the female to prefer, these male traits are positively correlated (Table 2). This means that a male that is attractive in one way is also attractive in another. Lipid mass was not correlated with display, indicating that courtship display was probably not very energetically costly in the environment we provided. Nevertheless, a more exposed environment or complex social setting and a longer treatment period may very well prove courtship display to be costly. There were significant impacts of temperature on nest building and display in the analyses of the feeding and nestbuilding treatment groups (which both include the control). The larger the increase in temperature between the recordings before and after treatments, the larger the increase in the nest opening area and decrease in sand cover and display. This is likely to be explained by the fact that warmer water contains less dissolved oxygen, which may increase the cost of physical activity at higher temperatures, at the same time as the metabolism of exothermic animals increases with higher temperature (Hochachka & Somero 1984; Kramer 1987). However, by including the difference in temperature between pre- and post-treatment measurements as a covariate in our analyses, we have controlled for these effects. Individual males showed a strong correlation between pretreatment and post-treatment courtship display and a nonsignificant tendency to do so regarding nest cover. These correlations, especially for display, suggest a rather powerful individual effect, whether reflecting the genotype of the individuals or phenotypic effects (beyond condition in terms of lipid content) of low flexibility. This is in line with the concept of behavioural trends (Sih et al. 2004), according to which individuals of different behavioural types are expected to behave in a consistent manner regardless of what might be the optimal behaviour in a particular situation. For example, individual great tits, Parus major, with different personalities vary in their antipredator responses, which has implications for nest defence (Hollander et al. 2008). In sand gobies, courtship display may hence indicate an aggressive or bold behavioural type with high levels of nest defence (Svensson et al. 2004). To conclude, experimentally manipulated courtship display and nest-building efforts did not have a negative impact on male condition or later courtship display and nest quality. On the other hand, supplemental feeding resulted in significantly increased nest cover and a smaller nest opening and had a positive impact on male condition. Display rate, however, was not affected. Individual courtship display was a consistent quality over time, but whether or not courtship displays indicate any aspect of genetic quality remains an open question. The partial correlation in the present study was more straightforward compared to previous studies (Svensson et al. 2004; Svensson & Kvarnemo 2005): with regard to what we expect the female to prefer, male traits were positively correlated.

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