Spawning behaviour and acoustic communication in Atlantic cod

Cannibalism of small numbers of offspring by a parent has been proposed as an adaptive parental strategy, by providing energy to support parental care. There are few empirical studies, however, to support this hypothesis. The beaugregory damselfish, Stegastes leucostictus , is a marine teleost that does not actively ventilate its eggs by fanning them. Partial cannibalism is common in this species, but in field studies was found to be unrelated to ration level. Filial cannibalism differed from predation in the pattern of egg eating; filial cannibalism was characterised by a random pattern of egg loss from a clutch rather than an aggregated distribution. Embryos developed quicker and had higher survival rates when they were at low densities and in nest sites where oxygen levels were high, and experimental reduction of oxygen levels increased rates of filial cannibalism. Here I present a hypothesis for filial cannibalism in the beaugregory damselfish; males cannibalise egg clutches in order to reduce clutch density and improve oxygen supply to the remaining embryos. I use a model of filial cannibalism to demonstrate how oxygen mediated cannibalism may be adaptive, and discuss the evolution of filial cannibalism in the beaugregory damselfish and other teleosts.     

Adaptive filial cannibalism in the beaugregory damselfish

Cannibalism of small numbers of offspring by a parent has been proposed as an adaptive parental strategy, by providing energy to support parental care. There are few empirical studies, however, to support this hypothesis. The beaugregory damselfish, Stegastes leucostictus, is a marine teleost that does not actively ventilate its eggs by fanning them. Partial cannibalism is common in this species, but in field studies was found to be unrelated to ration level. Filial cannibalism differed from predation in the pattern of egg eating; filial cannibalism was characterised by a random pattern of egg loss from a clutch rather than an aggregated distribution. Embryos developed quicker and had higher survival rates when they were at low densities and in nest sites where oxygen levels were high, and experimental reduction of oxygen levels increased rates of filial cannibalism. Here I present a hypothesis for filial cannibalism in the beaugregory damselfish; males cannibalise egg clutches in order to reduce clutch density and improve oxygen supply to the remaining embryos. I use a model of filial cannibalism to demonstrate how oxygen mediated cannibalism may be adaptive, and discuss the evolution of filial cannibalism in the beaugregory damselfish and other teleosts.     

The evolution of filial cannibalism and female mate choice strategies as resolutions to sexual conflict in fishes

Filial cannibalism (the consumption of one's own viable offspring) is common among fish with paternal care. In this study, I use a computer simulation to study simultaneous evolution of male filial cannibalism and female mate choice. Under certain conditions, selection on parental males favors filial cannibalism. When filial cannibalism increases a male's probability to raise the current brood successfully, filial cannibalism also benefits the female. However, when egg eating is a male investment into future reproduction, a conflict between female and male interests emerges. Here I investigate how female discrimination against filial cannibals affects evolution of filial cannibalism and how different female choice criteria perform against filial cannibalism. The introduction of discriminating females makes the fixation of filial cannibalism less likely. I introduced three different female choice criteria: (1) females who could discern a male's genotype, that is, whether the male was going to eat eggs as an investment in future reproductive events; (2) energy-choosing females that preferred to mate with males who had enough energy reserves to live through the current brood cycle without consuming eggs; and (3) females that preferred to mate with already mated males, that is, males with eggs in their nest. Genotype choice never coexisted with filial cannibals at fixation and filial cannibals were unable to invade a population with genotype-choosing females. Energy choice was successful only when males had high energy reserves and were less dependent on filial cannibalism as an alternative energy source. The egg choosers frequently coexisted with the cannibals at fixation. When the female strategies were entered simultaneously, the most frequent outcome for low mate sampling costs was that both the cannibals and the egg choice was fixed and all other strategies went extinct. These results suggest that sexual conflicts may not always evolve toward a resolution of the conflict, but sometimes the stable state retains the conflict. In the present case, this was because the egg-preference strategy had a higher fitness than the other female strategies. The outcome of this simulation is similar to empirical findings. In fish with paternal care, male filial cannibalism and female preference for mates with eggs commonly co-occur.     

Parents benefit from eating offspring: density-dependent egg survivorship compensates for filial cannibalism

Abstract Why should animals knowingly consume their own young? It is difficult to imagine many circumstances in which eating one's own young (i.e., filial cannibalism) actually increases an individual's fitness; however, filial cannibalism commonly co‐occurs with parental care in fishes. The evolutionary significance of filial cannibalism remains unclear. The most commonly accepted explanation is that filial cannibalism is a mechanism by which caring males gain energy or nutrients that they reinvest into future reproduction, thereby increasing net reproductive success. There is mixed support for this hypothesis and, at best, it can only explain filial cannibalism in some species. A recent alternative hypothesis suggests that filial cannibalism improves the survivorship of remaining eggs by increasing oxygen availability, and thus increases current reproductive success. This theory has received little attention as of yet. We evaluated the hypothesis of oxygen‐mediated filial cannibalism in the sand goby by examining the effect of oxygen and egg density on the occurrence of filial cannibalism, evaluating the effects of partial clutch cannibalism on the survivorship of remaining eggs, and comparing potential costs and benefits of filial cannibalism related to the net number of eggs surviving. Indeed, we found that oxygen level and egg density affected the occurrence of cannibalism and that simulated partial clutch cannibalism improved survivorship of the remaining eggs. Additionally, because increased egg survivorship, stemming from partial egg removal, compensated for the cost of cannibalism (i.e., number of eggs removed) at a range of cannibalism levels, filial cannibalism potentially results in no net losses in reproductive success. However, oxygen did not affect egg survivorship. Thus, we suggest a more general hypothesis of filial cannibalism mediated by density‐dependent egg survivorship.     

Cuckoldry incites cannibalism: male fish turn to cannibalism when perceived certainty of paternity decreases

Perceived certainty of paternity is expected to influence a male's behavior toward his offspring: if he is uncertain of his reproductive success with a current brood due to the presence of cuckolders, it may benefit him to invest instead in future reproduction. A decrease in perceived certainty of paternity incites filial cannibalism (the eating of one's own offspring) in some teleost fishes that provide parental care; however, no work has demonstrated that cannibalism increases proportionately with increased levels of cuckoldry. Here we show for the first time in a fish with no parental care that as the number of cuckolders at a spawning event increases, so does the probability that a male will cannibalize eggs. In field observations of Telmatherina sarasinorum, a small fish endemic to Sulawesi, Indonesia, males increased filial cannibalism behavior threefold in the presence of one cuckolder and nearly sixfold in the presence of two or more cuckolders. This suggests that males may use detection of cuckolders as an indication that the paternity of current offspring has been compromised.     

Filial cannibalism improves survival and development of beaugregory damselfish embryos

Cannibalism of small numbers of offspring by a parent has been proposed as an adaptive parental strategy, by providing energy to support parental care. However, there are few empirical studies to support this hypothesis. We conducted field and laboratory experiments to investigate partial filial cannibalism in Stegastes leucostictus, a coral reef fish with paternal care. Partial cannibalism was shown to be common, and males were found to remove developing embryos from throughout a clutch in a random pattern, rather than in the more aggregated pattern seen during embryo predation. Males that received a diet supplement grew faster than control males, but did not engage in less cannibalism. Also, males did not concentrate cannibalism on early embryonic stages with the highest energetic value. Experimental reduction of embryo densities was found to significantly increase embryo development rate and survival from egg deposition to hatching, and experimental reduction of oxygen levels significantly increased rates of partial filial cannibalism by males. Artificial spawning sites with low oxygen levels were avoided by spawning females, and cannibalism rates by males were higher. We propose that partial filial cannibalism serves as an adaptive parental strategy to low oxygen levels in S. leucostictus by increasing the hatching success of embryos.     

Have your cake and eat it too: male sand gobies show more parental care in the presence of female partners

Traditionally, male parental effort and mate attraction effortare expected to be in conflict as they compete for the sameresource budget. However, the quality of care provided by themale may be of a direct benefit to females and may provide animportant mate choice cue. In a laboratory experiment, we examinedhow males modified their parental behavior with respect to matingopportunity by allowing male sand gobies to mate with a singlefemale either in a big or small nest (a constraint on futuremating potential). We then exposed half of these males to thevisual stimulus from additional females and recorded male eggfanning and nest building (two components of care), courtshipbehavior, and reproductive success through out the brood cycle.We found that males fanned longer and more frequently and didmore nest construction in the presence of females and in bignests. Males guarding large nests courted females more thandid males guarding small nests. All males consumed eggs duringthe brood cycle, but complete clutch cannibalism was most frequentwhen males were guarding small nests in the absence of females.The pattern of filial cannibalism that we observed suggeststhat males prematurely terminated care when their reproductivepotential was low, that is, when there was little nest spacefor additional mating and no mates present. We found no supportfor a trade-off between mate attraction and parental care. Indeed,taken together our results suggest that males may use parentalcare as a courtship strategy and that males who invest in mateattraction also have higher parental effort.     

Expected future reproductive success and paternal behaviour in the sand goby, Pomatoschistus minutus (Pisces, Gobiidae)

We studied egg care and guarding behaviour in the paternal sand goby, Pomatoschislus minutus , in relation to egg number and age. A male's expected reproductive success is assumed to increase with larger egg masses and older eggs. Non-shareable care, i.e. fanning, was higher in larger and older egg masses. Egg age explained 65% and egg mass size 22% of the total variation in the amount of fanning performed by a male. Contrary to expectation, egg removal did not affect a male's fanning behaviour, Males that were approached stayed longer in the nest when they guarded larger egg masses. Males with older eggs were also more reluctant to leave the nest. The time since a male had been chased away from his nest until he returned decreased as the season progressed. The results are discussed in relation to tradeoffs between present and future reproductive events.     

Paternity and paternal effort in the pumpkinseed sunfish

Theoretical models suggest that males should adjust their parentaleffort according to paternity when parental effort is costly,paternity varies among clutches, and males have a cue to assesspaternity. To date, nearly all tests of this theory have beenconducted using birds as model organisms. In this study we examinedthese three factors and the relationship between paternity andmale parental care in a fish system. In the pumpkinseed sunfish(Lepomis gibbosus), parental care is provided exclusively bymales (parentals), but some males (sneakers) parasitize othersby sneaking fertilizations. Parental males significantly lostweight during the parental care period. Clutch size and amountof parental effort did not affect a male's probability of obtainingmore eggs. Paternity was variable among broods. The proportionof young sired by a parental male was not associated with frequencyof fanning eggs or defense of hatched young, but was positivelycorrelated with levels of nest defense during the egg stage.Egg survivorship might restrict an adjustment of fanning behavior,and a general decline in parental behavior (with brood age)might explain the lack of adjustment once the eggs hatch. Parentalmales did not adjust their care when we experimentally manipulatedone possible cue of paternity. Together, these results indicatethat male pumpkinseeds do adjust their care in relation to paternity,but the cues used to assess paternity are not clear.     

Filial cannibalism in teleost fish

This review summarizes information on filial cannibalism (the act of eating one's own offspring) in teleost fish. Cannibalistic parents can either consume their whole brood (total filial cannibalism), or eat only some of the eggs in the nest (partial filial cannibalism). Offspring consumption has been argued to be adaptive under the assumption that offspring survival is traded against feeding, and that offspring can act as an alternative food source for the parents. The evidence supporting the basic predictions formulated under these assumptions is summarized for both total and partial filial cannibalism. These two forms of cannibalism differ significantly since the former represents an investment only in future reproductive success, whereas the latter can affect both present and future reproductive success. Despite a few inconsistencies in the data from laboratory and field studies, the energy-based explanation appears valid for both forms of cannibalism. Alternative non-energy-based explanations are considered, but they are unable to account for the wide distribution of this behaviour in teleosts. The intersexual conflict arising from attempts of the non-cannibal sex to minimize the cost of filial cannibalism is also discussed, together with the potential effect of this behaviour on the operational sex ratio at a population level.     

Dietary carotenoid availability influences a male's ability to provide parental care

Despite convincing evidence that carotenoid availability canhave positive physiological effects, we still lack informationon the functional consequences of carotenoid limitation at thebehavioral level. Given the role carotenoids play in mitigatingoxidative stress produced during physical activity and as immunostimulants,one behavioral function on which they may have a significantimpact is an individual's capacity to provide parental care.We tested this hypothesis using three-spined sticklebacks (Gasterosteusaculeatus), a species in which males provide obligate and intensivepaternal care. Males were fed either high or low (but biologicallyrealistic) levels of carotenoids and monitored throughout incubation,during which we quantified 2 key aspects of parental care: theirability to fan their eggs under normoxic and hypoxic conditions(when both the costs and requirements of fanning increase) andtheir ability to defend their nest against a simulated conspecificmale. High-carotenoid diet males fanned their eggs at a significantlyhigher rate during hypoxic (but not normoxic) conditions andhad higher clutch hatching success than males fed the low-carotenoiddiet. There was no evidence that they defended their nest moreaggressively. Furthermore, low-carotenoid diet males also appearedto engage in cannibalization of their clutch. These resultsdemonstrate that dietary carotenoid availability can affecta male's ability to provide parental care, and we discuss thepotential mechanisms and implications of this finding.     

Effects of among-offspring relatedness on the origins and evolution of parental care and filial cannibalism

Parental care is expected to increase the likelihood of offspring survival at the cost of investment in future reproductive success. However, alternative parental behaviours, such as filial cannibalism, can decrease current reproductive success and consequently individual fitness. We evaluate the role of among-offspring relatedness on the evolution of parental care and filial cannibalism. Building on our previous work, we show how the evolution of care is influenced by the effect of among-offspring relatedness on both the strength of competition and filial cannibalism. When there is a positive relationship between among-offspring competition and relatedness, parental care will be favoured when among-offspring relatedness is relatively low, and the maintenance of both care and no-care strategies is expected. If the relationship between among-offspring competition and relatedness is negative, parental care is most strongly favoured when broods contain highly related offspring. Further, we highlight the range of conditions over which the level of this among-offspring relatedness can affect the co-occurrence of different care/no care and cannibalism/no cannibalism strategies. Coexistence of multiple strategies is independent of the effects of among-offspring relatedness on cannibalism but more likely when among-offspring relatedness and competition are positively associated.     

What makes a nest-building male successful? Male behavior and female care in penduline tits

Why do females increase parental effort when caring for theoffspring of attractive males? First, attractive males may bepoor fathers so that their females are compelled to increasetheir own contribution in order to fledge some young (the partner-compensationhypothesis). Second, females mated to attractive males may bewilling to increase their parental effort to reap high indirectbenefits for their offspring, and in turn males can decreasetheir own contribution (the differential allocation hypothesis[DAH]). We investigated these hypotheses in the penduline titRemiz pendulinus, a small passerine bird that has sequentialpolygamy by both sexes and strict uniparental care either bythe male or the female. We focused on two sexually selectedmale traits: nest size and nest-building behavior. We show thatmale care is unrelated to nest-building behavior, whereas femalesare more likely to care for the offspring of those males thatspend more time nest building. Females also more likely carefor the offspring of males that build large nests. Consequently,the reproductive success of males increases with nest size andnest-building behavior. Our results are consistent with theDAH and suggest that nest-building behavior and nest size areunder postmating sexual selection in penduline tits.     

Parental fish change their cannibalistic behaviour in response to the cost-to-benefit ratio of parental care

Partial filial cannibalism, the act of cannibalizing some offspring, has been explained as a response to the high energetic cost of care. I tested this hypothesis by manipulating the cost-to-benefit ratio of care in the scissortail sergeant, Abudefduf sexfasciatus, a tropical damselfish with male care. Background egg mortality was lower than the incidence of cannibalism, confirming that males did not just dispose of dead eggs. Investment in the current brood affected future investment, because males forced to skip a brood cycle put more effort into courtship during the following cycle and obtained larger broods than did unmanipulated males. Any factor influencing the cost-to-benefit ratio of parental care should also affect the incidence of cannibalism. I reduced the cost of care by supplementary feeding and reduced the benefit of care by simulating a decrease in paternity certainty through simulated intrusions by non-nesting males. Supplementary feeding significantly reduced partial filial cannibalism by parental males, a result compatible with the hypothesis that eggs are consumed to cover the energetic costs of parental care. Cannibalism decreased regardless of whether males were fed with conspecific eggs or crabmeat. Cannibalism was only reduced but not fully eliminated by supplementary feeding, and residual levels of cannibalism after feeding were similar to the background rate of egg mortality. Simulated intrusions by non-nesting males led to an increase in filial cannibalism and a decrease in parental effort.     

Filial Cannibalism in the Biparental Fish Cichlasoma nigrofasciatum (Pisces: Cichlidae) in Response to Early Brood Reductions

Filial cannibalism (eating one's own offspring) may enhance a parent's lifetime reproductive success if the costs associated with this behaviour are outweighed by its benefits. An organism might limit its parental care to relatively high quality offspring and eat the others. Or, an organism capable of repeated breeding in the same season might eat the survivors of a brood that was reduced by predators, and breed again. In this study, we manipulated brood size of convict cichlids by removing 0 % (control), 33 % (ER 33) or 66 % (ER 66) of the eggs spawned. The results show that smaller broods are more likely to be cannibalized by their parent(s) than are larger broods. Furthermore, pairs with reduced broods were preparing to respawn; female gonad weights were significantly higher in the brood-reduction groups than in the control group. In a second experiment, we show that the behaviour of the parents differed significantly between experimental groups; the ER 66 group performed less parental care than the control group. Moreover, females invested more parental effort than males. The results suggest that filial cannibalism may be a tactic used by parental convict cichlids to enhance their lifetime reproductive success.     

The effect of brood size and age on partial filial cannibalism in the scissortail sergeant

Within the size range found in the field for the scissortail sergeant Abudefduf sexfasciatus , there was no correlation between the number of cannibalized eggs and total brood size. Very small broods were fully cannibalized. In a manipulation experiment, males were provided with broods of one of three standardized sizes: at the two extremes and in the middle of the range of naturally occurring broods. Brood size had no effect on partial filial cannibalism, but parental effort increased with increasing brood size. Field correlates and the manipulation experiment showed that the cost of cannibalism in terms of current reproductive success decreased significantly with increasing brood size. Contrary to expectations, there was no relationship between male size and the incidence of cannibalism. No preference for younger eggs was found either from field correlates or from a manipulative experiment in which males were provided with an equal number of young and old eggs at the beginning of the parental phase.     

Do Male Desert Gobies Compromise Offspring Care to Attract Additional Mating Opportunities?

Males often play a critical role in offspring care but the time and energy invested in looking after young can potentially limit their ability to seek out additional mating opportunities. Recent studies, however, suggest that a conflict between male parental effort and mating effort may not always be inevitable, especially if breeding occurs near the nest, or if parental behaviours are under sexual selection. Accordingly, we set out to experimentally investigate male care and courtship in the desert goby Chlamydogobius eremius, a nest-guarding fish with exclusive paternal care. Despite courtship occurring near the nest, we found that when egg-tending males were given the opportunity to attract additional females, they fanned their eggs less often, engaged in shorter fanning bouts, and spent more of their time outside their nests courting. Our findings highlight the importance of understanding the circumstances under which reproductive tradeoffs are expected to occur and how these, in turn, operate to influence male reproductive decisions.     

Costs of egg ventilation for male common gobies breeding in conditions of low dissolved oxygen

This study examines the effects of harsh environmental conditions on life history trade-offs in parental care in a marine fish, the common goby, Pomatoschistus microps. We compared male parental care and hatching success over two sequential brood cycles in fish breeding in conditions of either low dissolved oxygen or normal levels of oxygen. Males compensated for a low oxygen environment by increasing the time they spent fanning water over their eggs, as well as their fanning tempo. They also increased the frequency of egg-directed activities and decreased nest-building activities. Males in the low oxygen treatment lost more weight than control fish during the first spawning, and were more likely to abandon care during the second spawning. Males that completed care under low oxygen conditions did not differ from control males in the hatching success of their offspring or the size of young at hatching, but hatching started on average 1 day later. Thus, greater parental allocations to offspring while breeding in a harsh environment led to reduced future allocations. Copyright 1999 The Association for the Study of Animal Behaviour.     

Filial cannibalism as a conditional strategy in males of a paternal mouthbrooding fish

Filial cannibalism is widespread in a variety of animal species and has been generally accepted as an adaptive behavior. Within a population, some individuals adopt filial cannibalism and others do not, in spite of its adaptiveness. There is little knowledge of how such a polymorphic trait is maintained in nature. To understand the underlying mechanism of cannibalistic polymorphism, we conducted a long-term field study that involved monitoring of the reproductive experience of marked individuals in the paternal mouthbrooding cardinalfish, Apogon doederleini, in which parental males sometimes cannibalize their entire broods. We assumed that filial cannibalism can be described as one of three possible strategies: alternative, mixed or conditional. Individual cannibalistic tendencies, represented by the number of entire brood cannibalism performed by each individual in one breeding season, showed a random distribution within the study population. Moreover, the individual cannibalistic tendencies were not consistent between two successive seasons. These results suggest that filial cannibalism is phenotypically plastic, thus eliminating the alternative strategy as a possible mechanism. Comparison of variance in reproductive success between cannibals and non-cannibals showed that observations were not in accordance with those expected in the case that males adopt filial cannibalism stochastically, that is, as a mixed strategy. Our previous studies have indicated that filial cannibalism is affected by male status, such as age, somatic condition and mate availability. In conclusion, filial cannibalism by male A. doederleini is carried out as a conditional strategy.     

You eat what you are: personality‐dependent filial cannibalism in a fish with paternal care

Many animal parents invest heavily to ensure offspring survival, yet some eventually consume some or all of their very own young. This so‐called filial cannibalism is known from a wide range of taxa, but its adaptive benefit remains largely unclear. The extent to which parents cannibalize their broods varies substantially not only between species, but also between individuals, indicating that intrinsic behavioral differences, or animal personalities, might constitute a relevant proximate trigger for filial cannibalism. Using a marine fish with extensive paternal care, the common goby (Pomatoschistus microps), we investigated the influence of animal personality on filial cannibalism by assessing (1) behavioral consistency across a breeding and a nonbreeding context; (2) correlations between different breeding (egg fanning; filial cannibalism) and nonbreeding (activity) behaviors, and, in a separate experiment; (3) whether previously established personality scores affect filial cannibalism levels. We found consistent individual differences in activity across contexts. Partial filial cannibalism was independent of egg fanning but correlated strongly with activity, where active males cannibalized more eggs than less active males. This pattern was strong initially but vanished as the breeding season progressed. The incidence of whole clutch filial cannibalism increased with activity and clutch size. Our findings indicate that filial cannibalism cannot generally be adjusted independently of male personality and is thus phenotypically less plastic than typically assumed. The present work stresses the multidimensional interaction between animal personality, individual plasticity and the environment in shaping filial cannibalism.