Behavioral Ecology Vol. 15 No. 2: 199-204
Behavioral Ecology vol. 15 no. 2 © International Society for Behavioral Ecology 2004; all rights reserved
Have your cake and eat it too: male sand gobies show more parental care in the presence of female partners
a Department of Ecology and Systematics, Zoological Laboratory, P.O. Box 65, 00014 University of Helsinki, Finland b Marine Research Institute, Division of Population Genetics, c/o Biotechnology House, Keldnaholt, IS-112 Reykjavík, Iceland c Department of Zoology, P.O. Box 118525, University of Florida, Gainesville, FL 32611-8525, USA
Address correspondence to K. Lindström. E-mail: kai.lindstrom{at}helsinki.fi.
Received 12 September 2002; revised 15 February 2003; accepted 25 March 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Traditionally, male parental effort and mate attraction effort are expected to be in conflict as they compete for the same resource budget. However, the quality of care provided by the male may be of a direct benefit to females and may provide an important mate choice cue. In a laboratory experiment, we examined how males modified their parental behavior with respect to mating opportunity by allowing male sand gobies to mate with a single female either in a big or small nest (a constraint on future mating potential). We then exposed half of these males to the visual stimulus from additional females and recorded male egg fanning and nest building (two components of care), courtship behavior, and reproductive success through out the brood cycle. We found that males fanned longer and more frequently and did more nest construction in the presence of females and in big nests. Males guarding large nests courted females more than did males guarding small nests. All males consumed eggs during the brood cycle, but complete clutch cannibalism was most frequent when males were guarding small nests in the absence of females. The pattern of filial cannibalism that we observed suggests that males prematurely terminated care when their reproductive potential was low, that is, when there was little nest space for additional mating and no mates present. We found no support for a trade-off between mate attraction and parental care. Indeed, taken together our results suggest that males may use parental care as a courtship strategy and that males who invest in mate attraction also have higher parental effort.
Key words: courtship, filial cannibalism, males, mate attraction, parental behavior, sand gobies.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Parental care is usually viewed as a means to increase the survival and quality of offspring at the expense of future mating success (Clutton-Brock, 1991
). On the other hand, it has been suggested that the quality of care provided could function as a cue in mate choice for the opposite sex and therefore would be under sexual selection (Hoelzer, 1989; Iwasa and Pomiankowski, 1999; Møller and Thornhill, 1998; Tallamy, 2000). Historically, the primary link between parental care theory and sexual selection has been through mating system theory (Emlen and Oring, 1977; Reynolds, 1996). Mating system theory proposes that parental care will limit the opportunity for sexual selection. For example, species without care or with uniparental care are expected to show higher levels of polygamy than do species with biparental care. When males provide parental care, we expect care to constrain mating success and thus limit the opportunity for sexual selection (Trivers, 1972). In more general terms, investment in care and mate attraction may be seen as investment in current versus future reproductive success. Typically, there is a trade-off between these, and usually, it is assumed that natural selection optimizes the solution to this trade-off (Williams, 1966). However, if care entails an element of mate attraction, then investment in current reproduction will simultaneously function as an investment in the future, and the situation changes.
Females are expected, and in some species have been shown, to base their mating decisions on male quality and male parental quality (Andersson, 1994; Östlund and Ahnesjö, 1998; Petersen, 1995; Wiegmann and Baylis, 1995). In the latter case, there is sexual selection acting on care and therefore we expect the following: (1) that males will provide more care than is optimal under natural selection alone, and (2) signals of care quality will evolve (Iwasa and Pomiankowski, 1999; Kirkpatrick, 1985; Wolf et al., 1999). Furthermore, it has been argued that the most cost-effective signal of care quality may be care itself (Tallamy, 2000). If care is under sexual selection, we might expect males to "signal" parental quality or, in other words, to use care as courtship. The hypothesis that care is under sexual selection is not new; it has long been suggested that sexual selection has played a major role in the evolution of male parental care (Baylis, 1981; Gross and Sargent, 1985; Hoelzer, 1989; Tallamy, 2000). So far, however, there are few empirical studies that evaluate this contention.
In fishes, males often are the sole care providers and may simultaneously be exposed to intense sexual selection. One reason for this is that in fishes, care rarely limits a male's mating potential (Gross and Sargent, 1985). Hence, there may be an exceptionally strong coincidence of sexual selection and paternal care among fishes. Care provided exclusively by the male occurs in more than 60% of fish families with parental care (Gross and Sargent, 1985). Typically, males guard the eggs against egg predators and fan them, thus providing the developing embryos with oxygenated water (Breder and Rosen, 1966). In addition, males clean eggs and remove dead eggs and debris from the nest (Breder and Rosen, 1966). In many species, males guard nest sites in which several females can deposit their eggs (Gross and Sargent, 1985).
There is evidence (direct or indirect) for both natural and sexual selection for care. Egg fanning has been shown to increase egg survivorship in fishes (see Östlund and Ahnesjö, 1998). There is also indirect evidence that males may use care behavior to attract mates. In the three-spined stickleback, males fan when courting females, hence the term courtship fanning (Sevenster, 1961), and courtship fanning is performed even in the absence of eggs. In many species of fish, males are still actively mating with additional females after having received their initial broods. Clearly, in this situation the quality of care can be more directly assessed. This could be one explanation for why female preference for already mated males is so frequently observed in fishes (Jamieson, 1995). Furthermore, one explanation for the evolution of a preference for eggs in the nest is that the presence of eggs signals male parental quality (Sargent, 1988). In addition, increased egg numbers are also predicted to increase a male's investment in his current reproduction (Sargent and Gross, 1993). In view of these findings, it is conceivable that a whole suite of parental behaviors may act in mate attraction and that paternal care in fishes therefore may be under sexual selection.
In the present study, we examine the conflicting predictions of parental care theory: (1) there should be a trade-off between parental investment and mate attraction (i.e., investment in future mating opportunities), and (2) care itself may be used in mate attraction (as is expected if there is sexual selection for care). We experimentally manipulated the perceived future mating potential of sand goby, Pomatoschistus minutus, males in order to test whether there is a trade-off between mate attraction (future mating opportunities) and egg survival (current reproductive success). Future mating opportunities were altered by manipulating nest size and the presence of females. In sand gobies, nest size is a physical constraint on male mating success (Lindström, 1992). According to the traditional view, in which there is a conflict between allocating time and resources to mate attraction and care, we expect to see males allocate less time to care when the potential for mating is high. There should also be a negative relationship between investment in mate attraction and egg survival. In fishes with male parental care, filial cannibalism (i.e., when a male consumes his own viable offspring) is a common phenomenon (FitzGerald and Whoriskey, 1992), and it has been suggested that this is a strategy to alleviate energetic costs of the current reproductive effort (Kvarnemo et al., 1998; Marconato and Bisazza, 1988; Mrowka, 1987; Rohwer, 1978). Hence, we would predict more filial cannibalism when mate attraction effort is high.
Alternatively, if care functions in mate attraction, then we expect males to increase care and care-related behavior in response to increased future mating opportunities. As a result of increases in care, these males should also have greater hatching success. We may also expect to see reduced filial cannibalism because future mating opportunities are higher when males display high-quality care and because there is not so great a trade-off between current reproductive success for expected future reproductive success.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sand gobies were collected in shallow brackish water (30 to 50 cm) in natural breeding habitats, near Tvärminne Zoological Station (Southern Finland) using a beach seine. Females and males were stocked in separate holding tanks (100 l) with continuous flow through of seawater. During this time, the fishes were fed ad lib live mysid shrimp and frozen Chironomidae larvae. The experiment was run during the sand goby breeding season in June and early July of 2001. The experimental tanks (60 l) were placed in a greenhouse. Each tank had a continuous flow through of seawater. Hence, light, temperature, and salinity followed natural conditions. The bottom of each tank was covered with a 4-cm layer of fine sand.
Each tank received a flower pot as an artificial nest site. We provided two nest size treatments: large (diameter, 10 cm) or small (diameter, 4 cm). Sand goby females lay their eggs in a single layer on the ceiling of the nest, and a large flower pot can simultaneously contain the spawn from as many as eight females, whereas a small nest only has space for the spawn of, on average, two females. Hence, a male guarding a large nest would, merely from a nest size point of view, have a much higher expected future mating success (Lindström, 1992). Each nest had a sheet of transparent plastic fitted on the inside onto which the females would attach their eggs. By removing the sheet, we could photograph the eggs using a Minolta RD-175 digital camera fitted with a 50-mm 1:1 macro lens and later count the number of eggs. After we completed photographing, the sheet was carefully placed back, and males quickly resumed parental duties and did not seem to be disturbed by the procedure.
One male (ranging in total length from 42–59 mm) was added to each tank, and once the male had completed building his nest (as detailed below), he was given a female (total length from 45–55 mm) with whom to spawn. After the female had spawned, she was removed and released. After spawning, males were assigned to treatments such that half of the large and small nest tanks were assigned to the "female presence" treatment and the other half to the "female absence" treatment. One end of the tanks (10 cm) was screened off by using a fine mesh divider. The nest was in the back of the other half, and the nest opening was facing the screen. In the female-presence treatment, on the day of spawning two ripe females were put into the small compartment, where they stayed to the end of the experiment, after which they were released back into nature. Hence, the male could view the females and be in chemical contact with them but could not spawn with them. During the experiment each fish was fed eight frozen Chironomid larvae at the end of every day.
The experimental setup corresponded to a factorial design with nest size and female-presence treatments, each with two levels and equal numbers of replicates (n = 12) in all treatment combinations. Males and females were randomly assigned to treatments.
Male behavior was recorded for 30 min by using a VHS video recorder on day 2 after spawning. For males in the female-present treatment, this was the day after the stimulus females were added. At this stage males still accept additional mates and are actively courting. Also, by making the observations on day 2, we characterized the initial behavioral response to the treatment conditions. After videotaping, the eggs were photographed, and this provided an estimate of the initial egg numbers. To quantify reproductive success, eggs were photographed again as hatching approached at the age of 9–11 days (when the eyes of the embryos were clearly pigmented and movement was visible).
Data analyses
Male behavior was analyzed from the videotapes by using an event recorder written specifically for this purpose (Delphi 5). The mutually exclusive behavior recorded included (1) inside the nest (where the male typically cleans the eggs and rubs his belly against them); (2) fanning; (3) resting at the mouth of the nest; (4) nest building, that is, when a male orients himself with his tail close to the nest and uses his tail to produce a jet of sand onto the nest, partially burying the flower pot; (5) courtship (for a description of these behaviors, see Kangas and Lindström, 2001); and (6) outside the nest without displaying or building. From these, we calculated the total time and frequency of each activity. For example, we calculated the total time spent fanning as well as the frequency of fanning bouts. In addition, nest time was calculated as the sum of all activities inside the nest (including behaviors 1, 2, and 3). Total time spent in each behavior is presented as a proportion of the total observation time, and the units for frequencies are per second.
Generally, we analyzed these data by using two-way ANOVA. We used parametric statistical methods whenever our data fulfilled the requirements of these analyses. For variables that could not be transformed to fulfill these requirements we used nonparametric factorial methods (Meddis, 1984).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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To evaluate whether the pattern of male parental care in sand gobies is consistent with the traditional view of parental care (that parental and mating effort are traded off against each other) or whether there is evidence that parental investment is also used in mate attraction, we compared patterns of paternal care (fanning and other time in the nest), courtship, nest building, and egg hatching success among our treatments. The total time spent fanning was affected by both treatments. Males fanned more in big nests (two-factor ANOVA on log-transformed proportional fanning time; nest size effect, F1,44 = 17.51, p <.001) and also more in the presence of females (female effect, F1,44 = 8.15, p =.007; interaction effect, F1,44 = 0.002, p =.961) (Figure 1A). Similarly, the frequency of fanning bouts depended on treatment. Fanning bout frequency was higher in big nests and in the presence of females (two-factor ANOVA, nest effect, F1,44 = 22.97, p <.001; female effect, F1,44 = 10.44, p =.002; interaction effect, F1,44 = 0.09, p =.764) (Figure 1B). Individual fanning bouts lasted on average 12.7 s (SD = 6.7, n = 48), but there was no treatment effect on the length of fanning bouts (two-factor ANOVA, all effects F1,44 < 1.89, p >.170).
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Overall, in the absence of females, males spent more time inside the nest (nonparametric ANOVA, female effect, H1 = 13.91, p <.001). However, there was also an interaction between female presence and nest size such that males with small nests spent similar amounts of time in the nest with and without females present (interaction effect, H1 = 337.64, p <.001) (Figure 2). Nest size did not independently affect the time a male spent in the nest (H1 = 0.69, p >.05).
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Only males with females present courted. Hence, we analyzed this behavior only for the female-present treatments. Males guarding big nests spent more time courting than did males with small nests (Mann-Whitney U = 115.50, p =.012) (Figure 3). Males often interrupted their courtship to build on their nests. However, in contrast to courtship, nest building also occurred in the absence of females. The frequency of nest building was higher in the presence of females (nonparametric two factor ANOVA, female effect, H1 = 8.54, p =.004) (Figure 4). Nest construction frequency was also higher for large than for small nests (nest size effect, H1 = 4.56, p =.032; interaction, H1 = 0.69, p =.406) (Figure 4).
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All males lost some eggs. On average 427 eggs (SD = 352, n = 48) disappeared from a male's clutch during the brood cycle. This corresponds to 50.3% (SD = 41.1, n = 48) of the initial egg mass. These lost eggs were most likely eaten by the guarding male, as filial cannibalism is a common phenomenon in fishes (FitzGerald and Whoriskey, 1992
) and occurs in the sand goby (Lindström and Hellström, 1993). Complete clutch cannibalism was a function of both nest size and the presence of females (logistic regression, nest size coefficient = -2.71 ± 0.67; t = 2.65, p =.008; female-presence coefficient = -1.79 ± 0.91, t = 1.98, p =.048; log-likelihood, G = 12.00, df = 3, p =.007); it was most common in small nests and in the absence of females (Figure 5). Males who lost only part of their clutch lost on average 228 eggs (SD = 234, n = 31), which corresponds to 23.3% (SD = 22.7, n = 31) of the clutch. The number of eggs lost in partially cannibalized clutches increased with initial clutch size (completely consumed clutches excluded, rS =.365, n = 31, p <.05) (Figure 6). The number of eggs consumed in partially cannibalized clutches was, however, not affected by treatment (completely consumed clutches excluded, nest size effect, F1,27 = 0.32, p =.578; female effect, F1,27 = 0.22, p =.639; interaction, F1,27 = 1.45, p =.238). Completely lost clutches were smaller, with an average initial egg number of 795 (SD = 210, n = 17), whereas partially lost clutches initially contained on average 976 eggs (SD = 275, n = 31; t test, t = 2.35, df = 46, p =.023).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In the present study, we are among the first to show that males increase their care and care-related behavior in response to increases in apparent mating opportunities. Males increased care in the presence of females and when guarding big nests, whereas they prematurely terminated care in small nests in the absence of females. Hence, care behavior is flexible and used differently by males, depending on mating opportunities. Much of parental care theory has assumed that there is a trade-off between mate attraction and parental effort (Clutton-Brock, 1991
). Our results did not support this view. Instead, our findings provide support for the hypothesis that the evolution of male parental care in fishes may result from sexual selection and increased mating success associated with higher levels of care.
Males increased fanning in big nests and in the presence of females. Fanning is an important part of fish parental care and is thought to function in aerating eggs (Coleman and Fischer, 1991; Reebs et al., 1984; van Iersel, 1953) and potentially in removing debris and waste products from the eggs. Some fraction of the increased fanning effort in big nests is likely to be explained by an increased effort needed to circulate a large water volume compared with a small volume. However, males also increased fanning in the presence of females, and this increase cannot be explained by the requirements of the eggs, as all males on average guarded the same number of eggs. Males showed more fanning in the presence of females, even if they spent less time in their nest. Had there been a trade-off between care and mate attraction, we would have expected to see a decrease in fanning effort in the presence of females. Thus, fanning appears to serve functions other than egg aeration. Fanning during courtship (courtship fanning) was originally observed in the three-spined stickleback and was originally analyzed as displacement behavior (Sevenster, 1961). In the 15-spined stickleback, females seem to prefer males with higher fanning rates (Östlund and Ahnesjö, 1998). Our results suggest that male sand gobies used fanning as part of their courtship, and hence, they increased fanning in the presence of females. Similarly, it is possible that males maintained higher fanning levels in big nests because these males can accept eggs from many more females than in small nests.
Parallel to changes in fanning, we found that males increased the frequency of nest building in the presence of females and when guarding big nests. Big nests may require more construction and maintenance in order to signal the same level of quality. More importantly we did not find a trade-off between mate attraction and nest maintenance; that is, males did more nest construction in the presence of females than they did in the absence of females. As in the case of fanning, this suggests that nest building is not only for nest maintenance. This finding is especially interesting in light of recent studies of female preference for nest quality. These studies have suggested that the quality of the nest may reflect male quality and that females hence should use nest quality as a mate choice cue (Barber et al., 2001; Borgia, 1985; Jones and Reynolds, 1999b; Kvarnemo et al., 1998; Östlund-Nilsson, 2001; Soler et al., 1998). Jones and Reynolds (1999a) showed in the common goby, P. microps, that females preferred males guarding well built nests (with a thick sand cover). The present study is the first to show that males change their nest-building behavior in response to perceived mating opportunities. Thus, nest building may also be used as part of the courtship sequence aimed at attracting mates and may therefore be under sexual selection.
As several investigators have suggested (Östlund-Nilsson, 2000; Sargent and Gebler, 1980) a well-built nest may function better as protection against nest and egg predators. It is conceivable that the males in the female-present treatment may have viewed the females as potential egg predators and, hence, increased their nest-building rate. This would be an alternative explanation to the "nest building as courtship" hypothesis above. However, previous studies that have explicitly examined nest-building behavior in the presence of egg predators have not found an effect on nest building (Jones and Reynolds, 1999c; Svensson O, Kvarnemo C, unpublished data). Jones and Reynolds (1999b) also found that males exposed to egg predators (small shore crabs) spent less time fanning and more time attacking the crab. This result is also distinct from the present finding that there is a positive correlation between egg care and behavior directed toward the female. Hence, we conclude that it is unlikely that the males in the present study viewed the females as potential egg predators but instead that they were perceived as potential mating partners and that the observed changes in male behavior are intended to increase mate attraction.
Finally, courtship depended on nest size. Males with large nests courted more than did males with small nests. This may be because a large nest has a higher potential reproductive success, and males try to capitalize on this potential. Previous research has suggested that courtship intensity may be an indicator of male and care quality (Forsgren, 1997; Knapp and Kovach, 1991). In the present study, we show that courtship intensity is modified with respect to resource quality. Thus, males shift their allocation toward mate attraction apparently in response to the increased reproductive potential associated with having a large nest. They simultaneously increase their parental effort in the same manner. This similarity between patterns of courtship and parental behavior lends support to the idea that the higher levels of fanning and nest building not only are a result of higher need for such activities in large nests but also are in fact used to attract mates.
All males lost eggs during their brood cycle, and filial cannibalism is likely the main source of egg loss in the present study (FitzGerald and Whoriskey, 1992). Generally, filial cannibalism is thought to be a response to (1) limited foraging opportunities while nesting, and (2) the high energetic costs (manifest as loss of male body weight, see DeMartini, 1987; Marconato et al., 1993; Mrowka and Schierwater, 1988; and fat reserves, see Lindström, 1998). Therefore, consuming some of one's own offspring may be a means for an individual to sustain itself through the parental phase (Rohwer, 1978). Indeed, males who consume eggs have been shown to maintain their body condition during the brood cycle (Lindström and Sargent, 1997). In addition, mate attraction is likely to be energetically costly, and hence, we would expect that males who exhibit high rates of courtship might also consume eggs. Generally, we expect males to consume a fraction of their clutches to defray these energetic costs or to consume their entire clutch if the cost of continued care outweighs its benefits (Lindström and Sargent, 1997).
Thus, we expected males who exhibited high rates of parental care, nest building, and courtship activity to have the greatest levels of egg loss. In the present study, such males corresponded to males with big nests and females present. Furthermore, we expected smaller clutches that may not be of sufficient value to warrant care to experience greater rates of complete clutch loss. Our first expectation was not met; instead, the pattern we found was that males with large nests and females present had higher egg survival, as they showed lower levels of total filial cannibalism. Partial cannibalism increased with initial egg numbers, as predicted by energy-based theory (Sargent, 1992), but it was not related to nest size or female presence. Consistent with our second expectation, completely consumed clutches were smaller than were partially eaten clutches. However, there was also an effect of nest size and female presence on the frequency of whole clutch loss; males guarding small nests in the absence of females frequently terminated their brood cycles prematurely.
A small nest certainly limits the potential egg number a male can guard and results in a lower expected fitness value (Lindström, 1992). In our experiment, males were allowed to mate with only a single female before the experiment begun. One mate is less than a male would expect under natural conditions (average male mating success in this population is 2.8 females, SD = 1.3, n = 17; Jones et al., 2001), although the number of expected mates depends on nest size (Lindström, 1992). Thus, the absolute numbers of eggs received by all experimental males was low. We think that the combination of a small brood in a small nest with no potential mates around implies fitness benefits that are too low for continued investment, and thus, these broods tend to be consumed.
The behavioral responses of male sand gobies to the presence of females that we have documented will result in more aeration of the eggs, a better-built nest, and fewer cannibalized eggs. In the present study, we have no evidence that there are any direct consequences of fanning or nest building activity for egg survivorship; however, there is evidence from other studies to support this (Jones and Reynolds, 1999b; Östlund and Ahnesjö, 1998). If increases in parental behavior translate into higher offspring survival or quality, as would be expected (Andersson, 1994), then females who base mating decisions on these signals will indeed experience direct benefits. Females may, for example, base mating decisions on traits that indicate a male's willingness and ability to provide care (Hoelzer, 1989; Kunzler and Bakker, 2000; Tallamy, 2000), but it has also been suggested that care and care-related behavior, such as nest building (the extended phenotype, see Dawkins, 1982), may function as indicators of male quality (Barber et al., 2001; Soler et al., 1998). The present study shows that females that choose males who have high potential for multiple mating, for example, males guarding large nests, can expect more care for their eggs. Notably, the choice of male need not be made based on male traits alone but also the male's potential to obtain additional mates. A crucial test of the sexually selected care hypothesis is that females show a preference for males who show elevated levels of care. Such a test will have to involve experimental manipulation of male care behavior.
In conclusion, the present study supports the idea that male parental care is under sexual selection and that it may have evolved or been elaborated through selection for increased mating success. Our results clearly show that males increase parental behavior, nest building, and egg survival in the presence of potential mates. Furthermore, there appears to be no trade-off between parental care and mate attraction. Future studies should test the controversial proposal, implicit in some models of sexual selection for care (see Kirkpatrick, 1985), that males with a high investment in mate attraction have higher egg survival because of care behavior than do males who only invest in care.
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ACKNOWLEDGEMENTS |
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We would like to thank Topi Lehtonen for his help in the field and the Tvärminne Zoological Station for facilities and technical support. Financial support for this study was provided by the Finnish Academy (K.L.) and CIMO (C.P.).
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