Ventilation or nest defense—parental care trade-offs in a fish with male care

Brood guarding animals face many critical trade-offs. Sand goby males (Pomatoschistus minutus) build nests with larger openings during low oxygen conditions, presumably to enhance ventilation. However, this may make the nest easier for egg predators to detect and harder for guarding males to defend. Manipulating oxygen level and predator presence (a small crab) for small and large males, we found support for a parental trade-off between fanning and nest defense. An increased fanning activity resulted in less time for guarding. Small males and males in low oxygen showed a higher fanning expenditure than large males and males in high oxygen, but surprisingly, filial cannibalism did not differ between these groups. Males built larger nest openings in low than high oxygen. However, males in both high and low oxygen treatments reduced their nest opening size in the presence of a predator, again indicating an important trade-off between ventilation and nest defense.     

Allopaternal care in the fathead minnow,Pimephales promelas: females prefer males with eggs

Summary Some species of fishes with exclusive male parental care exhibit the phenomenon of allopaternal care; that is, some males acquire and care for other males' eggs. We conducted a series of experiments to investigate the dynamics and evolution of allopaternal care in one such species, the fathead minnow (Pimephales promelas). In choosing a nest site, a newly reproductive male tended to take over the nest site of a parental male by evicting the resident male, rather than occupy a physically identical empty nest site. The new male generally cared for the old male's eggs, and in most cases, daily egg survival improved under the new male's care. When males were given a choice among unguarded nest sites, they preferred to occupy nest sites already containing eggs. When eggs were randomly assigned to nesting males, females preferred to spawn with males who had eggs in their nest sites. Thus, it appears that female preference for males with eggs led to the evolution of allopaternal care in the fathead minnow.     

The presence of eggs in the nest and female choice in common freshwater gobies (Rhinogobius brunneus)

In many species of fishes with paternal care, females prefer to spawn with males who are already guarding eggs. We studied the effect of egg presence on female mate choice in common freshwater gobies, Rhinogobius brunneus sp. OR. In our tests, females did not prefer males with eggs, suggesting egg presence per se may not act as a cue to attract females. We also examined the effects of brood size on paternal care and offspring survival to look for possible benefits females could obtain when choosing males with eggs. Both fanning by egg-guarding males and egg survival increased with brood size. The presence of neighboring males did have a significantly negative effect on males' parental activity, which subsequently results in a lower level of egg survival than in solitary egg-guarding males. This result provides a partial explanation for the result of eggs not attracting females to mate.     

Sex change limited by paternal care: a test using four Mediterranean labrid fishes,genus Symphodus

Four species of the Mediterrnean wrasse (genus Symphodus) were investigated under natural conditions near Calvi, Corsica, France, to test the idea that extensive male mating-investment limits the extremes of male reproductive success, and thus reduces selection for protogynous sex change. The four species differ in the extent to which males build nests and care for the eggs, and this sort of paternal care can detract from time spent in mating. In S. ocellatus and S. roissali larger males construct an elaborate nest, ventilate the eggs, and engage in territorial defense. The spawning rates for these males are relatively low and variable due to long periods spent in nest construction and egg tending. They also suffer a large amount of interference from smaller males, which may be due to the predictability of nest location. Sex change appears to be absent. S. tinca males construct only a rudimentary nest, do not ventilate the eggs, and experience much less spawning interference. Large males are relatively more successful in mating in this species, and sex change appears to occasionally occur. The large males of S. melanocercus spawn at a much higher rate than small males, due in part to the fact that they do not construct or defend nests and thus are able to spawn on a daily basis. Sex change appears to be common in this species. Thus, the species that shows the greatest sexual difference in changes of expected fertility with size is also the species that shows the strongest expression of sex change. Studies such as this can begin to indicate the actual costs of changing sex.     

Effects of costs and benefits of brood care on filial cannibalism in the sand goby

This study tested experimentally whether clutch size and the cost of care affect filial cannibalism in the sand goby, Pomatoschistus minutus. Evolutionary models of filial cannibalism suggest that egg eating has evolved as a way for the male parent to prolong his breeding season. These models assume that eggs function as an alternative energy source for the constrained parent. I manipulated clutch size by allowing males to mate with either one or two females, representing a small and a large clutch, respectively. The addition of a small male shore crab, a common egg predator, increased the cost of care. I quantified fat reserves as a measure of the condition of guarding males. Males who did not build nests had lower fat reserves than males who built nests, suggesting that males with low energy reserves do not start breeding. Males with small clutches lost their nest to the crab more often than males with large clutches. Neither filial cannibalism nor the amount of eggs eaten were affected by the treatments. Males who consumed eggs had a higher fat percentage than males who did not eat eggs. The result that males with small clutches lost their nests to the crabs supports the idea that eggs are defended only if the benefit from continued care will outweigh the cost and that males therefore are sensitive to the trade-off between present and future reproductive success. Received: 15 May 1997 / Accepted after revision: 15 November 1997     

Paternal care and egg survival both increase with clutch size in the fathead minnow,Pimephales promelas

Summary In some species of fishes with paternal care, females prefer to spawn with males who are already defeding eggs; moreover, in many species, paternal care increases with the number of eggs that a male is defending. If egg survival depends on the level of paternal care, and is largely independent of egg number, then egg survival should increase with clutch size. This result would provide a potential adaptive mechanism for female preference for males with eggs. I examined the effects of clutch size on paternal care and egg survival in the fathead minnow, Pimephales promelas, and found that both increased with male clutch size.     

Allopaternal care in the fathead minnow,Pimephales promelas: stepfathers discriminate against their adopted eggs

Summary Some species of fishes with exclusive male parental care exhibit the phenomena of allopaternal care and female preference for males with eggs. In these species, newly reproductive males adopt and care for the eggs of other males, apparently as a part of their mating strategy. Assuming that adoption is adaptive, I would expect males to discriminate between adopted eggs and eggs that they sired themselves. Specifically, I predicted that adopted eggs would receive less care and suffer heavier mortality than sired eggs. I examined the allocation of care and egg survival for adopted and sired eggs in the fathead minnow, Pimephales promelas, and corroborated both predictions.     

Reduced disease in offspring: A benefit of coloniality in sunfish

Summary Increased disease and parasitism are a well-documented cost of group living for colonial birds and mammals, but we now show that disease in offspring of fish may be reduced by nesting in colonies. The aquatic fungusSaprolegnia sp., which is a common cause of egg mortality among freshwater fishes, is more prevalent in the nests of solitary than colonial male bluegill sunfish (Lepomis macrochirus). Moreover, fungal infection decreases with nest density in colonies. This may be due in part to a behavioural advantage since colonial males can devote less time to defending eggs and more time to fanning them, which reduces fungal infection. In addition, we demonstrate experimentally that solitary nests become infected at higher rates than colonial nests, even in the absence of parental males. This suggests that colonies are encountered by spores at a lower rate and/or that the large number of nests in colonies dilutes the number of fungal spores per nest. Through one or all of these mechanisms, egg mortality in colonial nests is lowered significantly. Therefore, in some cases, disease may select for group living.     

Egg mimicry and allopaternal care: two mate-attracting tactics by which nesting striped darter (Etheostoma virgatum) males enhance reproductive success

In a variety of fish species with paternal care of offspring, females prefer to spawn in nests that already contain eggs. This female preference has been hypothesized to explain egg thievery in male sticklebacks, allopaternal care of eggs in minnows, and the evolution of egg-mimicking body features in male cichlids and darters. Here we employ microsatellite-based parentage analyses to evaluate the reproductive success of striped darter (Etheostoma virgatum) males that appear to utilize two of these functionally related tactics to entice females to spawn in their nests. In an isolated population (Clear Creek, Ky.), we observed that breeding males develop conspicuous white spots on their pectoral fins. If these spots are egg mimics, as we suspect, then this represents the fourth independent evolutionary origin of egg mimicry documented to date in darters, the first based on pigmentation (as opposed to physical structures), and the first in which the egg mimics vary greatly in number among males. From direct counts of microsatellite genotypes in clutches of embryos, at least 3.8 females contributed to the progeny within a typical nest, and females tended to spawn preferentially with males that were larger and displayed more egg-mimic spots. In another population (Hurricane Creek, Tenn.) without egg mimics, the multi-locus genetic data document that allopaternal care is common, especially among the smallest males who sometimes tend nests containing their own as well as an earlier sire's offspring. Thus, these foster males had adopted egg-containing nests and then successfully spawned with subsequent females. Overall, the genetic data on paternity and maternity, in conjunction with field observations, suggest that egg mimicry and allopaternal care are two mate-attracting reproductive tactics employed by striped darter males to exploit female preferences for spawning in nests with 'eggs'. Electronic Publication     

Egg adoption can explain joint egg-laying in common eiders

Hypotheses regarding the evolution and maintenance of intraspecific nest parasitism were tested with data collected during a 3-year study of common eiders (Somateria mollissima) breeding near Churchill, Manitoba. The nest parasitism rate was highest (42.4% of nests) during the year with the highest nest density and the best environmental conditions, and lowest (20.2% of nests) in the year with the lowest nest density and the poorest environmental conditions. Over the nesting season, parasitic eggs were laid at the same time as normally laid eggs. Most parasitic eggs (>75%) were laid before the host female laid her third egg. The majority of the parasitic eggs were the first or second egg produced by the parasitic female. When a parasitic egg was laid before or on the same day as the host female initiated her clutch, the probability of her first egg being depredated before incubation was significantly lowered. First- and second-laid eggs suffered a high rate of predation probably because nesting females do not attend their clutch until their second or third egg is laid. Hypotheses that some females use intraspecific nest parasitism to parasitize the parental care of other females were inconsistent with these data. Egg adoption is a likely explanation for the prevalence of females incubating parasitic eggs in this population. Received: 30 September 1997 / Accepted after revision: 6 May 1998     

Courtship in fast water currents by a male stream goby ( Rhinogobius brunneus) communicates the parental quality honestly

The stream goby Rhinogobius sp. DA (dark color type) shows exclusive paternal care of the eggs. Males court females in the stream current and previous field observations suggest that females favor males that perform their courtship display in faster water currents, and that such males may have high parental ability because of good physical condition. To validate these observations we examined female choice under controlled laboratory conditions. Mate choice experiments indicated clearly that females preferred males that courted in the faster currents, whereas neither sexually different morphological traits, such as body size, nor the water current alone were important. The experiments with food supply treatments indicated that only males of high physical condition are able to court in the fast currents. Furthermore, males that courted in the fast currents achieved good egg survival, whereas males that were unable to court in the currents did not, due to cannibalism of their egg clutch. Thus, the maximum speed of the water current in which a male courts should be indicative of his quality and of the subsequent survival of eggs under his care. We conclude that Rhinogobius sp. DA females utilize the male courtship display in the water current as an honest indicator of parental quality.Communicated by K. LindströmAn erratum to this article can be found at     

Filial cannibalism in a nest-guarding fish: females prefer to spawn in nests with few eggs over many

In fish, fecundity correlates with female body size and egg-tending males often eat small broods. Therefore, small females may prefer to spawn in nests that already contain many eggs, to ensure the brood is as large as possible. In contrast, large females may prefer nests with few eggs, if high egg number or density has a negative effect on egg survival, or if there are drawbacks of spawning last in a nest. To test the hypothesis that female body size affects nest (and male mate) choice, using the sand goby (Pomatoschistus minutus), we allowed small and large females to choose between two males that were matched in size — one guarding a small clutch and the other a large clutch, respectively. We recorded where females spawned (measure of female preference), the combined brood size, male courtship, egg care and nest building. We also quantified the effect of brood size and egg density on egg survival in a separate data set. Although the combined broods did not exceed the small brood sizes that are at risk of being eaten, both small and large females preferred to spawn in nests with smaller clutch sizes. This preference could not be explained by more courtship or male parental effort, nor by reduced survival of larger or denser broods. Instead, our result might be explained by females avoiding the danger of cannibalism of young eggs by males or the risk of reduced egg health associated with being near the nest periphery.     

Brood defense and filial cannibalism in the spottail darter (<Emphasis Type="Italic">Etheostoma squamiceps)</Emphasis>: the effects of parental status and prior experience

Male spottail darters (Etheostoma squamiceps) defend nest sites in which females deposit eggs over the course of several weeks. In laboratory experiments, I tested three predictions of the hypothesis that the presence of eggs increases the value of a nest site to male spottail darters: (1) males should preferentially defend nests with eggs over empty nests, and males that sired the eggs should (2) spend more time defending them and (3) consume less of their broods than should alloparent males. Parent males were tested using eggs they were guarding in the field; alloparents included males that were not defending eggs immediately prior to the experiment (inexperienced), and males that were defending eggs in the field when captured but were given eggs sired by a different male (experienced). In choice experiments in which males were offered nest sites differing only in the presence of eggs, males preferred to defend nest sites with eggs regardless of parental status. Parent males spent significantly more time defending eggs and consumed less of their broods than did inexperienced alloparent males. Experienced alloparent males were similar to parent males in brood defense but had levels of filial cannibalism similar to inexperienced males, suggesting that prior experience may influence brood defense but not egg consumption.     

Offspring recognition and the influence of clutch size on nest fostering among male sand gobies, Pomatoschistus minutus

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 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.     

Tactics of parasitic American coots: host choice and the pattern of egg dispersion among host nests

Summary I examined the tactics adopted by a conspecific brood parasite, the American coot (Fulica americana), and the degree to which these tactics reflect sources of mortality for parasitic eggs. Only 8% of parasitic eggs produced independent offspring, compared to a 35% success rate for non-parasitic eggs, and most mortality was due to egg-rejection by hosts or the consequences of laying eggs too late in the host's nesting cycle. Parasites usually laid parasitically before initiating their own nests and usually parasitized immediate neighbours. Parasites did not remove host eggs before laying their own egg, and egg disappearance in general was not more common at parasitized nests. I found no evidence for non-random host choice, either on the basis of stage of the host's nesting cycle or the host's brood size. The absence of adaptive host choice is likely a consequence of the fact that, due to host limitation, only a small proportion of parasites had meaningful variation among potential hosts to choose from. The pattern of egg dispersion among host nests by individual parasites appears to be a compromise between constraints imposed by host limitation and the increased success obtained from spreading eggs among nests. Most females laying fewer than five parasitic eggs laid them in a single host nest while females laying five or more eggs normally parasitized two or more hosts. An examination of egg rejection and survival rates showed that parasites would maximize success by laying a single egg per host nest, and the pattern of laying several eggs per host nest is likely a consequence of host limitation. However, no egg that was the fifth laid, or later, parasitic egg in a host nest was ever successful and this probably explains why most females laying five or more eggs parasitized more than one host.     

Dynamics of biparental care in the dampwood termite,Zootermopsis nevadensis (Hagen): response to nitrogen availability

Summary Studies were conducted on the dampwood termite, Zootermopsis nevadensis, to examine the behavioral roles of the reproductive pair during the nest-founding period and to determine the effect of nitrogen availability on their reproduction and division of labor. Nitrogen has been hypothesized to be an important limiting nutrient for founding pairs. One nitrogenous reserve, uric acid-nitrogen, was examined in reproductives and in nutrient-receiving and nutrient-gathering colony members; it was found in highest amounts in the reproductives (i.e., alates, de-alates, and primary reproductives). Young pairs may use these nitrogenous reserves to increase their chances for reproduction. In support of this hypothesis, founding pairs that were fed a diet supplemented with uric acid-nitrogen had a significantly greater probability of producing at least one offspring than did pairs fed an unsupplemented diet. Females that were fed a nitrogen-poor diet restricted their total activity while their mates sustained a high activity during colony initiation. When fed a nitrogen-rich diet, females collected pulp more often than their mates, while males collected more water, though only in the period prior to egg laying. In all pairs, males transferred proctodeal pellets (food derived from the hindgut intestine) to their mates significantly more often than females to males, and females fed on proctodeal pellets significantly more often than did their mates. The male-female asymmetries in pellet transfer and feeding were not significant in the stage after egg deposition. Once eggs and larvae were present in the nest, a male and female spend an equal percentage of time caring for eggs and feeding larvae. Proctodeal pellets examined in reproductives were found to be rich in proteins. This suggests that in the pre-egg period, the male provides nitrogen-rich substances to the female as a form of paternal investment.     

Mate guarding in the swallowHirundo rustica

Summary The importance of mate guarding by males in the monogamous swallowHirundo rustica was studied by temporarily detaining the males. Mate guarding reduced the frequency of extra-pair copulations and of sexual chases involving female mates. Males participated in sexual chases more frequently if they had a non-fertile female. Neighbouring males of ‘widowed’ females increased their own mate guarding presumably in response to the experimentally increased rate of sexual chases. Neighbouring males with a fertile female increased their mate guarding more than did males with a non-fertile female. Addition of eggs to swallow nests in the post-fledging period of the first brood induced mate guarding by male nest owners. These males also copulated more frequently with their mates than did control males. Neighbouring male swallows responded to the increased mate guarding by showing sexual interest in the guarded females. removal of eggs from swallow nests during the laying period, leaving only one egg in the nest, resulted in reduced nest attendance by females. Male mates responded by increasing their mate guarding intensity as compared to controls, and neighbouring males showed an increased sexual interest in these females.     

Effects of nest site concealment on hatching success,reproductive success,and paternal behavior of the threespine stickleback,Gasterosteus aculeatus

Summary Male sticklebacks (Gasterosteus aculeatus) actively competed for a limited number of clay flowerpots as nest sites in circular wading pools. Males nesting in pots spawned earlier and more often, had higher mean and lower variance for hatching success (number of fry per gram of estimated clutch weight), and suffered fewer stolen fertilizations, nest raids, and territorial encounters than did males nesting outside pots, and in pools without pots (Table 2). Males nesting in pots had the more even temporal distribution of fanning bouts and interfanning intervals; the durations of fanning bouts and interfanning intervals were less variable for these males (Table 2).In replicate aquaria, one male nested on each side of a glass partition and both males spawned approximately simultaneously. Flowerpots were provided to one, both, or neither male. Males with pots had higher mean hatching success, fewer territorial encounters, and the more even temporal distribution of fanning bouts and interfanning intervals (Table 4).Thus it appears that nest site concealment, in the form of clay flowerpots, affected male hatching success, reproductive success, and parental behavior, even when physical contact between males was prevented. These data suggest that a causal relationship may exist between the paternal fanning regime and the subsequent hatching success. Furthermore, these data suggest that males which nest in high concealment increase their reproductive success, and that females which spawn with these males reduce the variance of their hatching success as well as increase their mean hatching success.     

Factors affecting the allocation of paternal care in waterbugs (Belostoma flumineum Say)

Summary Male giant waterbugs (Belostoma flumineum Say) brood eggs oviposited on their dorsa by conspecific females. Laboratory observations indicate that viable egg pads are occasionally discarded before hatching. Theory predicts that such behavior should occur only if the costs incurred by brooding exceed the benefits of hatching the egg pad. We studied the effects of egg pad size, time invested in brooding, and egg viability upon the continuation of paternal care in the giant waterbug. We found that smaller egg pads are less likely to hatch than larger ones, and males appear to be less likely to discard egg pads as temporal investment increases. However, the inviability of eggs did not appear to affect the probability of an egg pad being discarded. Males of this species appear to have evolved a decision-making process involving the continuation of paternal care. Offprint requests to: K.C. Kruse     

Parental care and mate attraction in the Florida flagfish, <Emphasis Type="Italic">Jordanella floridae</Emphasis>

Theory suggests that there is a trade-off between mate attraction and investment in parental care. Yet, under some circumstances, such as in species with uniparental male care, it is conceivable that males who provide more care also attract more females, and hence avoid this cost. We tested these two alternative hypotheses using the Florida flagfish, Jordanella floridae, which is a highly sexually dimorphic species with male parental care. We predicted that if components of male care behavior primarily serve offspring survival, they should display these behaviors more in the presence of eggs than without eggs. We also predicted that males should show a trade-off between display, and other activities directed to other fish, and care behaviors. Alternatively, if care has a positive effect on mating success, we expected males to show care even in the absence of eggs, and that they should display more care in the presence of females. We found that care behavior mostly depended on the presence of eggs, males increased care when they guarded eggs, and there was a negative relationship between rates of interaction and care behavior. Most care was exhibited in the absence of other fish while the presence of males and females both had a negative effect on care behavior. There was no difference in care behavior with males or females present. Only nest-visitation rates were highest in the presence of females, suggesting that this behavior is used as part of the courtship. These results support the idea that male care in this species is primarily influenced by natural selection. Males did, however, display fanning and other egg-directed behaviors even in the absence of eggs. The level of these behaviors was constant and independent of display behavior. Hence, it seems that care may be used in mate attraction before the male has received his first clutches.