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Mar 25, 2010 - Abstract When parental care is costly, parents should avoid caring for unrelated young. Therefore, it is an advantage to discriminate between ...
Behav Ecol Sociobiol (2010) 64:1325–1331 DOI 10.1007/s00265-010-0947-7

ORIGINAL PAPER

Offspring recognition and the influence of clutch size on nest fostering among male sand gobies, Pomatoschistus minutus Ola Svensson & Maria Lissåker & Kenyon B. Mobley

Received: 4 November 2009 / Revised: 24 February 2010 / Accepted: 27 February 2010 / Published online: 25 March 2010 # Springer-Verlag 2010

Abstract When parental care is costly, parents should avoid caring for unrelated young. Therefore, it is an advantage to discriminate between related and unrelated offspring so that parents can make informed decisions about parental care. In the present study, we test the hypothesis that male sand gobies (Pomatoschistus minutus) recognize and differentially care for their own offspring when given a choice between a nest with sired eggs and a second nest with eggs sired by an unrelated male. The sand goby is a species with exclusive and costly paternal care. Male parasitic spawnings (e.g., sneaking) as well as nest takeovers by other males are common. Our results show that nests containing sired eggs were preferred and received significantly more care, as measured by nest building and nest occupancy, than nests with foreign eggs even when males cared for both nests. These findings suggest that males respond to paternity cues and recognize their own clutches. Relative clutch size also had a significant effect on male parental care. When sired clutches were larger than foreign clutches, males preferred to care for their own nest. In the few cases where males chose to take care of foreign Communicated by M. Hauber O. Svensson (*) Department of Zoology, University of Gothenburg, Box 463, SE-405 30 Gothenburg, Sweden e-mail: [email protected] M. Lissåker Department of Zoology, Stockholm University, SE-106 91 Stockholm, Sweden K. B. Mobley Department of Ecology and Environmental Science, Umeå University, Linnaeus Väg 6, SE-901 87 Umeå, Sweden

nests, the foreign clutch was larger than their own clutch. Taken together, our results provide evidence that both paternity cues and clutch size influence parenting decisions among male sand gobies. Keywords Certainty of paternity . Filial cannibalism . Nest choice . Parental care . Paternity assurance . Sperm competition

Introduction In a wide range of taxa, egg dumping, brood mixing, cuckoldry, and parasitic fertilizations lead to parental investment in unrelated young (Wisenden 1999; Hauber and Sherman 2001; Arnold and Owens 2002; Tallamy 2005). Parents are predicted to reduce care toward current investments if unrelated offspring are present. However, for parents to apportion care preferentially to their own offspring, they must have reliable information about kinship (Neff and Sherman 2002). If they are unable to identify their own offspring and thus reduce care of the entire brood as a result of low parental assurance, not only the unrelated young but also their own offspring will suffer from reduced care. Offspring recognition and parental care have been thoroughly investigated in birds and mammals (CluttonBrock 1991; Sheldon 2002; Widdig 2007). Today, examples of offspring recognition abound in other taxa such as spiders (Evans 1998; Japyassu et al. 2003), copepods (Lazzaretto and Salvato 1992), and lizards (Main and Bull 1996). In these species, parents are clearly able to recognize their own offspring, and olfactory cues often seem to facilitate identification. A wide variety of teleosts have also been shown to recognize kin or offspring, including

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salmonids (Brown and Brown 1996), cyprinids (Loiselle 1983), centrarchids (Neff 2003b), and cichlids (McKaye and Barlow 1976). Even if individuals had available cues to parentage, they might not adjust their care accordingly. Using theoretical modeling supported by empirical examples, Neff and Sherman (2002) argued that a cue which can be immediately evaluated by the individual should only influence an individual’s decision if it predicts the reproductive value more reliably than a “predisposition”. The predisposition includes information gained during the individual’s lifetime but is shaped over evolutionary time. For example, if cuckoldry is virtually absent early in the breeding season but is variable later in the season, males can be certain of high paternity early in the season and safely ignore any cue to the contrary during this period. However, late in the season when this predisposition is not reliable, the male must rely on available paternity cues (Neff and Sherman 2002). In fishes with male parental care, only a handful of studies have investigated a link between offspring recognition and the degree of parental care given to offspring. Some studies demonstrate that males may terminate care if paternity is low or uncertain. For example, male threespined sticklebacks (Gasterosteus aculeatus) terminated care by completely cannibalizing clutches containing both sired and foreign eggs compared to a sham-manipulated clutch containing only their own eggs (Frommen et al. 2007). Several studies provide evidence for a relationship between perceived paternity and nest defense and/or filial cannibalism, e.g., bluegill sunfish (Lepomis macrochirus; Neff and Gross 2001; Neff 2003b), pumpkinseed sunfish (Lepomis gibbosus; Rios-Cardenas and Webster 2005), and the scissortail sergeant (Abudefduf saxatilis) (Manica 2004). Other studies have found no relationship between sneaking or perceived paternity on either filial cannibalism or paternal care such as in the common goby (Pomatoschistus microps; Svensson et al. 1998), the sand goby (Pomatoschistus minutus; Svensson and Kvarnemo 2007; Lissåker and Svensson 2008), and the fifteen-spined stickleback (Spinachia spinachia; Östlund-Nilsson 2002). The present study investigates the potential for offspring recognition in male sand gobies. There are several reasons why we would expect selection on male sand gobies to directly recognize their own nest and for males to adjust their care in relation to male or offspring-generated cues of paternity. First, nest site and egg defense are costly in sand gobies, and males are known to abandon their nests if the costs of continued parental care outweigh the immediate benefit to the male’s reproductive success (Kvarnemo 1995; Lindström 1998; Lissåker et al. 2003). Additionally, there is great variation in cuckoldry (male parasitic spawning) in natural populations of sand gobies (Jones et al. 2001) and

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males react strongly to sneaker males (Svensson and Kvarnemo 2005; Svensson and Kvarnemo 2007). Therefore, the essential requirements for an effect of certainty of paternity on care are fulfilled (Sheldon 2002). Other factors such as ecological conditions may select male sand gobies to recognize their nests. Males leave the nest to search for mates or to chase away intruding males (Lindström and Hellström 1993; Forsgren 1997) and therefore must be able to find their own nest again. Nests are also found close together in the wild (0.1 were removed from the models. Relative clutch size was calculated as initial sired clutch area divided by the sum of the initial areas of the two clutches (sired+ foreign) and was therefore larger than 0.5 if the sired clutch was larger than foreign clutch and below 0.5 if the sired clutch was smaller than the foreign clutch. Males were ranked as follows: (1) foreign eggs dead or foreign nest not rebuilt, (2) eggs survived in both nests and both nests were rebuilt and occupied for at least 1 day, and (3) sired eggs dead or sired nest not rebuilt. If a male could more accurately discriminate his own sired clutch from a

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foreign clutch if it differs in size (regardless if it is smaller or larger), we predicted the absolute value of the clutch size difference to be correlated with the ranking above (always positive and calculated as the absolute value of sired clutch area minus the foreign clutch area divided by the sum of the two areas). On the other hand, if males increase care to large clutches, we predicted the relative clutch size (calculated the same way as in the ANCOVAs) to be correlated with male care decisions. We used Spearman Rank correlations to test these predictions. To fulfill the assumptions of parametric tests, nest cover, nest occupancy, and egg mortality were arcsine square root transformed, nest opening width, and proportional egg mortality were square root transformed, and relative clutch size was log transformed. All statistical tests were performed in SPSS 15.0 (SPSS Inc., Chicago).

Results Sired nests received significantly more paternal care than foreign nests. Sired nests had significantly more nest cover, significantly smaller nest opening width, and were occupied more frequently than foreign nests (Table 1). However, egg mortality was not significantly higher in foreign nests compared to sired nests (Table 1). Initial clutch size did not differ between those sired by the focal male and those sired by the foreign male (mean ± SD, sired 11.8±3.0 cm2, foreign 11.6±4.0 cm2, paired t test: t14 =0.202, p=0.84). No brood which contained living eggs at the end of the experiment suffered from more than 50% partial clutch cannibalism. We accounted for clutch size statistically, and relative clutch size (covariate) had significant effects on nest cover and nest occupancy but had no significant effect on nest opening width (Table 1). There was no effect of

relative clutch size on either the area or proportion of egg mortality, so it was removed from both models. If the males made their discrimination decision early and did not change nest preference, the measurements from day 1 should predict the measurements on day 6. As predicted, the nest cover and nest opening width on day 1 significantly predicted nest cover and nest opening width on day 6 (linear regressions on the difference between the sired and foreign nests on day 1 and 6, nest cover (R2 = 0.71, F1,14 =31.18, p0.1 were removed from the model. Data were transformed before analyses. Untransformed mean ± SD values are given

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0.8 0.75

Relative clutch size

0.7 0.65 0.6 0.55 0.5 0.45 0.4 0.35 0.3

Sired clutch

Both clutches

Foreign clutch

Fig. 1 The relationship of relative clutch size (sired clutch area divided by summed clutch areas) and whether males predominantly cared for sired nests (sired; n=8), both nests (both; n=4), or foreign nests (foreign; n=3). Males preferentially cared for their own nests in the sired and both categories. Relative clutch size was higher than 0.5 if the sired clutch was larger than foreign clutch and below 0.5 if the sired clutch was smaller than the foreign clutch

male, can distinguish and preferentially care for the nest with their own sired clutch. On average, all three measures of paternal care (nest cover, nest opening width, and nest attendance) were significantly directed toward their own sired clutch. However, egg mortality was higher in the foreign nests compared to the own sired nests, although this difference was not significant. A likely explanation for the lack of an effect on egg mortality is that instead of consuming all eggs in one nest or leaving them to die, males sometimes tended both nests. Still, the observed reduction of nest building and attendance toward foreign nests would likely be fatal for the eggs in the natural environment. Additionally, clutch size had a significant effect on nest choice, and in a few cases, males preferred foreign nests with a larger clutch to their own. Presenting individuals with a simultaneous choice as in the present study has theoretically and empirically been argued to be a sensitive test of offspring recognition (Beecher 1991; Wagner 1998). In Lissåker and Svensson (2008), males were left to care for a nest with their own sired clutch or a nest with a foreign clutch. Males did not discriminate against foreign clutches suggesting that males could not reliably discriminate against a foreign clutch under no-choice conditions. In natural populations of sand gobies, male parasitic spawnings are common but rarely affect the entire clutch (Jones et al. 2001). The paternity of reproductively parasitized males also remains high in experimental studies (78– 100% of the total clutch, Malavasi et al. 2001; Svensson and

Kvarnemo 2007). Assuming that it is beneficial for a male to continue to care for a clutch as long as it contains a high enough number of eggs that he has sired to cover the costs of caring for it (in terms of, e.g., energy expenditure and time), it should not matter if some of the eggs are fathered by other males. Accordingly, no relationship between male parasitic spawning and parental care has been detected in sand gobies (Svensson and Kvarnemo 2007) or common gobies, P. microps (Svensson et al. 1998). When testing if nonparental sand gobies take care of foreign eggs, both laboratory and field studies have shown that males immediately consume all eggs after a nest takeover (Lindström and Hellström 1993; Lissåker and Svensson 2008). Hence, the only contexts where sand gobies significantly discriminated against foreign young were when they had not taken part in a spawning event (Lindström and Hellström 1993; Lissåker and Svensson 2008), or when they simultaneously compare two nests (present study). However, the males in Lissåker and Svensson (2008) may not have been certain enough that the eggs were not theirs. Thus, the failure to discriminate may have been a consequence of conservative decision making rather than a perceptual inability to discriminate. If we use the terminology of Neff and Sherman (2002), the cues that were available in Lissåker and Svensson (2008) are less reliable than the evolved predisposition, i.e., paternity is high if the male participated in a spawning event in his own nest. When males are comparing nests, as in the present study, there should be no evolved predisposition guiding the males, and they have to rely on the available cues. Such context-dependent offspring discrimination, and more general (non-offspring) kin recognition, has repeatedly been documented in a wide range of animals such as amphibians (Pfennig 1997; Gibbons et al. 2003), birds (Beecher 1991; Hauber et al. 2006), fishes (Bandoli 2002; Neff 2003a; Bandoli 2006), and insects (Starks et al. 1998; Buczkowski and Silverman 2005). Therefore, our result conforms to a well-developed field of behavior ecology. In the present study, parental care decisions were not only influenced by certainty of paternity but also by clutch size. Thus, as judged from their parental behavior, the males’ perceived certainty of paternity is higher in the sired clutch compared to the foreign clutch, but importantly, it is not zero in the latter. To us, this means that the clutch/nest recognition in sand gobies is uncertain; otherwise, males should never care for a foreign clutch. Furthermore, in Pomatoschistus, parental investment increases with the reproductive value of the clutch, and the reproductive value of the clutch increases with clutch size (Magnhagen and Vestergaard 1993; Kvarnemo et al. 1998; Lissåker et al. 2003; Lissåker and Svensson 2008). Sand gobies can thus be expected to acertain certainty of paternity and the perceived reproductive value through clutch size and make

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a parental care decision based on the highest potential payoff. If the potential pay-off is smaller in the sired clutch with high certainty of paternity due to a smaller clutch size compared to the foreign clutch with low certainty of paternity, the male is expected to care for the foreign clutch. In addition, female sand gobies prefer to mate with males that have already mated and have eggs present in their nests (Forsgren et al. 1996). However, the hypothesis that males take care of foreign eggs in order to attract females appears unlikely because males that have not recently spawned immediately consume all eggs after taking over a nest (Lindström and Hellström 1993; Lissåker and Svensson 2008). We can also reject the hypothesis that sand goby males prefer to take care of large clutches to better attract females; when females are given a choice between males with large or small clutches, they prefer to spawn with the males with small clutches (M. Lissåker and C. Kvarnemo, unpublished). The same preference is found in the fifteen-spined stickleback, Spinachia spinachia; females prefer males with experimentally reduced clutches over males with larger clutches (Östlund-Nilsson 2002). Indeed, if the relationship between clutch size and male nest preference in the present study was caused by female preference for eggs in the nest, we would expect males to preferentially care for smaller clutches. Offspring recognition can be accomplished through visual, tactile, acoustic, olfactory, or gustatory signaling systems or a combination thereof (Sherman et al. 1997). Currently, it is unclear what signaling mechanisms may allow offspring and/ or nest recognition in sand gobies. The hypothesis that they use differences in size between the two clutches to successfully discriminate against foreign clutches appears unlikely. If this was true, males would have taken care of their own sired clutches when they were smaller than the foreign clutches but would fail to discriminate between the two clutches when they were of similar in size. Furthermore, the nest substrates (ceramic flower pots) were identical in both nests, and the clutches were of similar shape. Hence, chemical cues, e.g., from the mucus sand gobies prepare the nest with (Svensson and Kvarnemo 2005), are more likely candidates than visual or tactile discrimination. To conclude, although the mechanisms for offspring (or nest) recognition are not well understood, we provide evidence that parents can recognize and care for their own clutch even if parentage is obscured through nest rearrangement. This study also contributes to the understanding of parental care by demonstrating a trade-off between a preference to care for offspring with high certainty of paternity and a preference to care for large clutches. The latter likely stems from selection to provide high quality care to broods with high reproductive value. Future investigations in offspring recognition and parental care decision making in gobies should include manipulation of

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clutch size and potential chemical cues that may influence offspring recognition in this species. Acknowledgments We thank Kristina Axelson, and Laila Fröberg with field and husbandry aspects of this project, Malte Andersson, Adam Jones, and Charlotta Kvarnemo for useful discussions and guidance and Mark Hauber, Kai Lindström, Cock van Oosterhout, and three anonymous referees for valuable comments on the manuscript. We would also like to thank the staff at Klubban Biological Station for use of their facilities.

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