Female cannibalism and male courtship tactics in threespine sticklebacks

Summary Female threespine sticklebacks (Gasterosteus aculeatus) frequently raid male nests and eat all the eggs therein. We tested the hypothesis of Vickery et al. (1988) that females prefer to raid nests containing large numbers of eggs than ones with smaller numbers of eggs. This hypothesis is based on the finding that females spawning in nests containing many eggs will have reduced hatching success because of egg crowding. By consuming the male's eggs and forcing him to rebuild his nest, raiding females might obtain a new opportunity to spawn under better conditions. Our results were consistent with the first prediction of this hypothesis that females were more likely to spawn in nests containing fewer eggs than in nests with many eggs. However, this may be the result of males becoming less receptive to females as the number of eggs in their nests increases. Prediction 2 was that females should raid those nests containing the most eggs. Contrary to this prediction, males defending only one clutch were as likely to have their nests raided by groups of females as males defending several clutches of eggs. Female cannibalism is therefore unlikely to have evolved as a means of gaining access to a male defending a small number of eggs. We also examined the tactics used by males to counter female raids. Most raids occur when the male is courting, and nests are more vulnerable to shoals of females than to single females. Therefore, we hypothesized that males with eggs preferentially court a single female rather than large groups of females, and that males without eggs court both groups indiscriminately. We also predicted that males restrict the number of females they mate with when risk of having their nest raided is high. Our results indicate that: (1) both males with eggs and those without eggs minimize the risk of female cannibalism by courting solitary females rather than groups of females and (2) males limit the number of females that lay eggs in their nest when several potentially raiding females are present. Offprint requests to: G.J. FitzGerald     

Cannibalize or care? The role of perceived paternity in the sand goby, <Emphasis Type="Italic">Pomatoschistus minutus</Emphasis>

Parental care is a costly part of reproduction. Hence, natural selection should favor males which avoid caring for unrelated young. However, the decision to abandon or reduce care requires cues which are evaluated to give information on potential reproductive value of the offspring. The prediction that male sand gobies, Pomatoschistus minutus, care for foreign eggs as long as they were spawned in their own nest and at least some of such cues are fulfilled was tested. Egg-guarding males that had recently taken part in a spawning event were given a clutch of eggs that was sired either by themselves or another male, in either their own or another male’s aquarium. Males that had not taken part in a spawning event were used as controls and were given eggs sired by another male. We measured the amount of filial cannibalism and nest building. Control group males did not care for eggs and ate them all before rebuilding the nest. In the other treatments, there were no significant effects of paternity, though males moved to another male’s aquarium increased their clutch area threshold and completely consumed larger clutches than males that were not moved. There was no intermediate response in any treatment in the form of increased partial filial cannibalism or less well-constructed nests. Our results suggest that egg-guarding males cannot distinguish between eggs sired by themselves and those sired by other males but are able to react to cues indicating paternity state. Males do not adopt eggs to attract females in P. minutus.     

Male spottail darters (Etheostoma squamiceps) do not use chemical or positional cues to discriminate between sired and foster eggs

Filial cannibalism is hypothesized to allow nest-guarding males to recoup energy lost during nest defense. Males in many species of fishes occasionally defend broods containing both sired and foster eggs due to shifts in nest site ownership or cuckoldry. Such males are predicted to consume primarily foster eggs if the ability to discriminate among eggs exists. In a previous laboratory study, male spottail darters (Etheostoma squamiceps) consumed significantly more foster eggs than sired eggs, suggesting the existence of a mechanism for discrimination using chemical or positional cues. This discrimination mechanism in the spottail darter was tested by creating nest sites with half sired eggs and half foster eggs (n=15), or with all sired eggs with half positionally relocated (n=9). Males defended these nests for 2 days in the field, and cannibalism was determined by counting eggs lost during that interval. Neither foster eggs nor relocated sired eggs were consumed in greater numbers or percentages of the original brood sizes than the unchanged sired eggs, indicating that male spottail darters do not discriminate between foster and sired eggs by olfaction or position. Alternatively, the hypothesis that males treat all eggs in nest sites in which they have spawned as sired explains the results of both studies.     

Paternity and condition affect cannibalistic behavior in nest-tending bluegill sunfish

Theory of parental care evolution predicts that a parent should invest more in a brood when its fitness value is greater than alternative investments such as the parent's own survivorship or future broods. In fish, filial cannibalism (eating one's own offspring) is widespread and represents a challenge to parental care evolution. In this study, I investigated filial cannibalism in bluegill sunfish (Lepomis macrochirus). Bluegill are characterized by alternative mating tactics referred to as "parentals" and "cuckolders". Parentals delay maturation, construct nests, court females and provide sole parental care for the developing offspring. Cuckolders mature precociously and parasitize parentals using two tactics called "sneakers" and "satellites". I found that parentals that obtained fewer eggs during spawning appeared more likely to completely cannibalize their brood (total filial cannibalism: P=0.07), regardless of their condition. Among parentals that provided care, partial cannibalism was greater during the egg phase as compared to the fry phase of care, but it was unrelated to brood size. Throughout the care period, parentals in better condition were less likely to partially cannibalize their brood, indicating that parentals use cannibalism to replenish energy reserves. Independent of condition, parentals that were cuckolded more were more likely to eat part of their brood. This relationship was evident only after the eggs had hatched, which is consistent with data showing that parentals can use olfactory cues produced by fry but not eggs to assess their paternity. This latter result proposes that parentals may be selectively culling cuckolder offspring from their nest. These data provide empirical support for parental care theory, and the first evidence for the importance of paternity on cannibalistic behavior.Communicated by M. Abrahams     

On the evolution of nest raiding and male defensive behaviour in sticklebacks (Pisces: Gasterosteidae)

Summary We develop a model to explain the evolution of nest raiding by female sticklebacks based on enhanced female reproductive success derived by creating mating opportunities with the male whose nest has been destroyed. Our model depends critically on the shape of the function relating percentage hatch success to the number of eggs in a male's nest, and the probability that the female will later mate with the male whose nest was raided. Raiding by females will be favoured when the number of eggs in the nest is high providing high egg numbers reduces the percentage hatch rate. High probabilities of mating with the male in question also favour raiding. A second model suggests that males cannot reduce the probability of being raided by limiting the number of eggs in the nest. Instead selection should favour their increasing the number of eggs in the nest. Tests of these models are suggested and their relation to other factors which may influence the evolution of cannibalism are discussed.     

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     

Sex,cannibalism and sticklebacks

Summary Two closely related species of sticklebacks (Pisces:Gasterosteidae), breeding in the same site at the same time, showed different patterns of egg cannibalism. In Gasterosteus aculeatus the intensity of cannibalism was density-dependent and females were the most important cannibals. In G. wheatlandi cannibalism was not density-dependent and males ate more eggs than females. This study indicates that sex-specific patterns of cannibalism can differ widely between species despite their similar ecology, and it provides evidence inconsistent with a currently popular explanation for egg cannibalism.     

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.     

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.     

Role of surface chemical signals in egg cannibalism and intraguild predation in ladybirds (Coleoptera: Coccinellidae)

Summary. The eggs of some ladybirds are known to be toxic to intraguild ladybird predators. However, this defence is of little value if the eggs are killed before their toxicity becomes apparent. The results presented in this paper indicate that chemicals on the surface of the eggs of two species of ladybirds signal the relative risk of cannibalism and intraguild predation. In Adalia bipunctata and Coccinella septempunctata, 87% of the chemicals are alkanes. Each species of ladybird is less reluctant to eat their own eggs than those of the other species. This asymmetry is to be expected because there is a greater risk to ladybirds from intraguild predation than cannibalism. Similar alkanes to those on the surface of the eggs of A. bipunctata are present in tracks left by larvae and on the elytra of the adults of this species. Those in the larval tracks deter females from ovipositing in patches of prey already being attacked by their larvae and those on the elytra are used in mate recognition. That different context dependent messages could be signalled by similar chemicals is an example of semiochemical parsimony. Received 25 February 2000; accepted 22 May 2000     

Worker policing and nest mate recognition in the ant <Emphasis Type="Italic">Formica fusca</Emphasis>

A conflict over male production arises in social insects where workers are able to lay unfertilized male eggs. This happens because each female (queen or worker) is most closely related to her own sons and is thus predicted to reproduce. The conflict is modulated by worker policing where workers prevent each other from reproducing by aggression or egg cannibalism. In this study, we show that in the ant Formica fusca, worker policing occurs by egg cannibalism rather than by overt aggression among workers. Furthermore, we show that, contrary to bees, wasps and other ant species, egg discrimination in F. fusca is not based only on a universal queen signature chemical and that nest mate recognition of eggs occurs.     

Maternal nest defense reduces egg cannibalism by conspecific females in the maritime earwig <Emphasis Type="Italic">Anisolabis maritima</Emphasis>

Nest predation imposes a major cost to reproductive females, who should therefore take measures to avoid encounters with predators. However, when predators are conspecifics, avoidance can be more difficult and may be a consequence of social or aggregative behaviors. In this study, we measured the consequences of conspecific egg cannibalism on hatching success in the maritime earwig (Anisolabis maritima), which occasionally form aggregations. We hypothesized that conspecific egg cannibalism is a byproduct of aggregation, and that cannibalism rates would increase with aggregation density; however, our results do not support this. We combined field data with a lab experiment to test the effectiveness of maternal nest defense in protecting nests from a conspecific. Nests with a guard had higher hatching success and lower rates of cannibalism than unattended nests in the presence of a conspecific. We also measured body and forcep size to see whether the outcome of contests was determined by relative size. Female guards who were larger relative to the invading conspecific maintained their nest and had higher hatching success than females who were relatively smaller, suggesting that the maritime earwig is under directional selection for larger body and/or forcep size.     

Female spawning patterns and male mating success in the sand goby Pomatoschistus minutus

In June 1989 in a study conducted near Träminne Zoological Station, Finland (60° N 23° E) I investigated whether or not male mating success could be explained by female choice for male size in sand gobies (Pomatoschistus minutus). Male mating success was constrained by nest size and increased markedly with increasing nest size. I also found a negative correlation between the length of spawning females and the fullness of the nest. As large females lay more eggs, they also need to find a nest with more space available for the eggs. The size of males without eggs was the same across nest size, whereas the size of males with eggs significantly increased with increasing nest size. This is interpreted as female discrimination against males as mates in nests that are often contested. There was no correlation between a male's size and his mating success when males with no eggs in their nests were excluded. A male removal experiment, however, showed that, in a specific nest, when male size increases so does mating success, whereas, if male size decreases, mating success also decreases. It is concluded that in the sand goby females prefer to mate with larger males, especially when the male possesses a high-quality nest that he most probably will have to defend against other males.     

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.     

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     

Female sand gobies gain direct benefits by choosing males with eggs in their nests

In some fish species with paternal care, females prefer to spawn with males whose nests already contain eggs. Several hypotheses have been put forward to explain this behaviour, such as reduced risk of predation or cannibalism (the dilution effect), increased parental investment, and mate copying. This experimental study focuses on female mate choice in the sand goby, Pomatoschistus minutus. Females were found to choose males with eggs in their nests. In addition, hatching success increased with clutch size, mainly because males with larger clutches showed less filial cannibalism. Increased egg survival in large clutches may thus be explained by a combination of the dilution effect and higher parental investment. In another experiment, females did not seem to copy the observed mate choice of other females. In conclusion, female preference for males with eggs in their nests is adaptive, and can be explained by direct benefits, as more surviving offspring are produced. Received: 23 December 1995/Accepted after revision: 11 May 1996     

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.     

Mate availability accelerates male filial cannibalism in a nest brooding fish: effects of number and fecundity of females

Theoretical models predict that increased mate availability accelerates filial cannibalism by the parental male, but we do not yet fully understand how the various aspects of mate availability contribute to this effect. We examined the effects of two elements of mate availability—female fecundity and sex ratio—on filial cannibalism by the lizard goby, Rhinogobius flumineus, which is a paternal nest brooding fish. We used three types of females (stimulus-females): a single female with slim belly (not ready to spawn), a single gravid female (ready to spawn), and two gravid females. Stimulus-females were housed in a transparent cage and shown to subject males just before and after spawning with a separate female, after which males cared for the brood. A single gravid stimulus-female accelerated filial cannibalism, compared with a control-stimulus consisting of an empty cage, but only during the early care period. In contrast, a single slim-bellied stimulus-female did not accelerate cannibalism. A stimulus of two gravid females accelerated cannibalism to the same degree as a single gravid female stimulus. Our results suggest that in lizard gobies, filial cannibalism by parental males is accelerated by female quality (fecundity) in the early care period, but not by a higher number of available females (sex ratio).     

Mate compatibility,parental allocation and fitness consequences of mate choice in the sand goby <Emphasis Type="Italic">Pomatoschistus minutus</Emphasis>

Recent theory and empirical work suggests that there may be variation among females in mate preferences that is adaptive. One of the possible mechanisms maintaining variability in preferences and preferred traits is that the benefits of mate choice may depend on compatibility with potential mating partners. We examined fitness consequences of mate choice in a species of fish, the sand goby, Pomatoschistus minutus with a special focus on mate compatibility. Females were given the opportunity to establish their mate preferences in a dichotomous mate choice experiment. This information was then applied by mating the focal or control female with either the preferred or the non-preferred male. The parental performance of the males of these four mating combinations was then measured. In a separate experiment, we assessed the female differential allocation by determining the residual gonad weight of spawned females as a measure of the proportion of eggs spawned. We also estimated the amount of filial cannibalism separately for both sexes. Our results show that preferred males provided benefits in the form of an increased number of hatching eggs. This benefit was the same when the male was mated with a focal or a control female. Hence, we found no support for benefits that depend on mate compatibility. Neither did we find support for the hypothesis that females would lay a different number of eggs depending on the male status. The results also indicate that male filial cannibalism has a strong role in determining hatching success in this species.     

Parasitic common goldeneye (<Emphasis Type="Italic">Bucephala clangula</Emphasis>) females lay preferentially in safe neighbourhoods

Nest predation has been suggested as an explanation of the adaptive significance and evolution of conspecific brood parasitism, an alternative reproductive tactic pursued by females in several animal taxa. I used new nest boxes that contained only decoy eggs and were erected on lakes differing in real nest predation risk to test this hypothesis in the common goldeneye (Bucephala clangula), a hole-nesting duck. I used broken eggs to simulate predation risk of the boxes to determine if parasites having no previous experience with the boxes discriminate between seemingly safe and risky nest sites. Parasites laid eggs in the experimental boxes independently of the simulated predation risk, suggesting that they do not use broken eggs or nest disarray as indicators of predation intensity. Parasites preferred experimental boxes on lakes where real nest predation risk was low, supporting the nest predation risk hypothesis. Assuming that females in high risk areas have had experience of nest predation, they may take this into account in selecting host nests.