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.     

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.     

Cannibalism and protective behavior of eggs in Arctic charr (Salvelinus alpinus)

From video recordings of spawning events, we quantified protective and cannibalistic behavior of Arctic charr occurring immediately after spawning. The number of fish cannibalizing on stray eggs was examined regarding (a) whether more than one male shed milt during the spawning event, that is, whether sperm competition occurred, (b) whether the sperm competition included few or many males, that is, the intensity of sperm competition, and (c) the density of fish at the spawning site. Response behavior toward egg cannibalism was also examined among females and dominant males in order to determine any parental investment toward protecting the eggs after spawning. Cannibalistic behavior was seen in almost 50% of the spawnings, and the multiple spawning events showed the highest numbers of fish cannibalizing on eggs. Both the number of males releasing milt and the number of fish approaching the spawning site were positively correlated with egg cannibalism. Sperm competition was, however, not a prerequisite for egg cannibalism. Although we also observed partial filial cannibalism, protective behavior of eggs was seen both among dominant males and females, suggesting that charr actually conduct parental care.     

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 CORTEZ DAMSELFISH STEGASTES RECTIFRAENUM

Male cortez damselfish, Stegastes rectifraenum, in a central Gulf of California population, ate a large percentage (28.3%) of the clutches they received. This high rate of filial cannibalism permitted the testing of several predictions concerning the types of clutches that should be preferentially eaten and the mating tactics females should employ to reduce cannibalism rates. Males ate clutches that were smaller than average and that were at early stages of development. Experimentally reduced clutches were consumed at higher rates than controls. When multiple clutches were present, males preferentially ate the younger, smaller clutches. Females were more likely to deposit eggs with males who were caring for other early-stage eggs and to avoid males with late-stage eggs. This pattern was accentuated in females that deposited smaller clutches. These results provide evidence that filial cannibalism represents an adaptive response to clutches that do not provide adequate benefits to warrant the costs of parental care.     

Effects of a low oxygen environment on parental effort and filial cannibalism in the male sand goby, Pomatoschistus minutus

In fish, brood cycling parental males sometimes eat some orall of their eggs, a behavior termed filial cannibalism. Wetested predictions of filial cannibalism models related to thecost of parental care in the male sand goby, Pomatoschistusminutus, by increasing the parental effort (fanning expenditure)through reduced levels of dissolved oxygen to 39% in an experimentalgroup, whereas a control group had fully saturated water. Malesshowed both full-clutch cannibalism and partial-clutch cannibalismin both treatments. Giving the males one to three females tospawn with, we found that small clutches were completely eatenmore often than were larger ones, whereas partial-clutch cannibalismwas not affected by clutch size. Although treatment did notaffect filial cannibalism, it did affect a male's energy statesuch that males in the low oxygen treatment lost more body fat,indicating a greater fanning effort. This shows that males inthe low oxygen treatment allocated more energy to the presentbrood, potentially at the expense of future reproductive success.Our study strongly suggests that filial cannibalism in malesand gobies represents a strategic life-history decision asan investment in future reproductive success, and is not triggeredby a proximate need for food necessary for the male's own survival.Furthermore, males in the low oxygen treatment built nests withlarger entrances, and were less likely to rebuild their nestsafter destruction. Presumably, this makes fanning easier butthe nest more vulnerable to predators, suggesting a trade-offbetween fanning and nest defense.     

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.     

Asynchronous hatching and brood reduction by filial cannibalism in the burying beetle Nicrophorus quadripunctatus

Despite decades of intensive research, there is still much debate about the adaptive significance of asynchronous hatching. A major obstacle in understanding the significance of this process is the difficulty involved in separating the hypotheses that explain asynchronous hatching as an adaptive trait from those that explain it as a by-product of physiological constraints on hatching or egg-laying patterns. We investigated the burying beetle Nicrophorus quadripunctatus, a species in which the parent can eliminate less-adaptive offspring (e.g., slower-growing offspring) by filial cannibalism and adjust the age structure of offspring to an adaptive pattern. The main aim of this study was to determine the age composition of offspring that survived and to determine the effect of larval growth on filial cannibalism. We investigated how the point in time at which each group of larvae hatched affects the timing of filial cannibalism by the female parent. We found that N. quadripunctatus exhibited asynchronous hatching, and reared larvae of different ages. We also found that later-hatching larvae had lower survival and growth rates; therefore, filial cannibalism plays a role in eliminating later-arriving, slower-growing, and hence less-adaptive offspring.     

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.     

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.     

A Test for Male Parental Care in a Fundulid, the Bluefin Killifish, Lucania goodei

Under field conditions, breeding male bluefin killifish, Lucania goodei, have been observed aggressively defending territories from other breeding males, non-breeding females, and minnows (mainly Notropis harperi). We performed an aquarium experiment to test whether male aggression serves to protect newly deposited eggs from predation. We allowed a male and a female to spawn in a yarn mop, removed the female, and exposed the eggs to one of four treatments (spawning male present, two minnows present, spawning mal+two minnows present, no adult fish present). Mops were censused daily for seven days. Egg predation rates were highest in the male+minnows and male only treatments. Egg predation rates in the male+minnows treatment did not differ from the predicted predation rate (sum of male only and minnows only treatments). Hence, there is no evidence for male parental care in L. goodei. In addition, we compared the egg predation rates (filial cannibalism) between males of 3 different color morphs and found no evidence for differential egg cannibalism.     

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.     

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.     

Paternity assurance before and after fertilization by male burying beetles (Nicrophorus quadripunctatus)

Parental care requires a large investment of time and energy. This can reduce future parental survival and opportunities for mating. Because males are usually more uncertain of their parentage with respect to the caring of offspring than are females, the reduction in reproductive success is thought to be greater in males. Therefore, males are under selection to ensure paternity of the offspring for which they care. Males can increase paternity before and after fertilization. Before fertilization, males can increase paternity by increasing their competitive ability for fertilization. After fertilization, males can increase paternity by cannibalizing unrelated offspring. Here, we investigated the stage at which male burying beetles, Nicrophorus quadripunctatus, increase their paternity by evaluating the number of offspring sired by a nursing male in asynchronously hatched broods in relation to hatching time. We found that nursing males assure a very high level of the paternity of hatching offspring. We also found that the paternity of non-nursing and nursing males remained constant across hatching time within a brood, indicating that it is unlikely that filial cannibalism plays a role in increasing the paternity of offspring. We concluded that ensuring paternity before fertilization is more important in increasing the paternity of offspring.     

Maternal Vibration: An Important Cue for Embryo Hatching in a Subsocial Shield Bug

Hatching care has been reported for many taxonomic groups, from invertebrates to vertebrates. The sophisticated care that occurs around hatching time is expected to have an adaptive function supporting the feeble young. However, details of the characteristics of the adaptive function of hatching care remain unclear. This study investigated the hatching care of the subsocial shield bug, Parastrachia japonensis (Heteroptera: Parastrachiidae) to verify its function. Results show that the P. japonensis mothers vibrated the egg mass intermittently while maintaining an egg-guarding posture. Then embryos started to emerge from their shells synchronously. Unlike such behaviors of closely related species, this vibrating behavior was faint, but lasted more than 6 h. To investigate the effect of this behavior on hatching synchrony and hatching success, we observed the hatching pattern and the hatching rate in control, mother-removed, and two artificial vibration groups. Control broods experienced continuous guarding from the mother. Intermittent artificial vibration broods were exposed to vibrations that matched the temporal pattern of maternal vibration produced by a motor. They showed synchronous hatching patterns and high hatching rates. However, for mother-removed broods, which were isolated from the mother, and when we provided continuous artificial vibration that did not match the temporal pattern of the maternal vibration, embryo hatching was not only asynchronous: some embryos failed to emerge from their shells. These results lead us to infer that hatching care in P. japonensis has two functions: hatching regulation and hatching assistance. Nevertheless, several points of observational and circumstantial evidence clearly contraindicate hatching assistance. A reduction in the hatching rate might result from dependence on maternal hatching care as a strong cue in P. japonensis. We conclude that the hatching care of P. japonensis regulates the hatching pattern and serves as an important cue to induce embryo hatching.     

When to care for, abandon, or eat your offspring: the evolution of parental care and filial cannibalism

Parental care and filial cannibalism (the consumption of one's own offspring) co-occur in many animals. While parental care typically increases offspring survival, filial cannibalism involves the killing of one's young. Using an evolutionary ecology approach, we evaluate the importance of a range of factors on the evolution of parental care and filial cannibalism. Parental care, no care/total abandonment, and filial cannibalism evolved and often coexisted over a range of parameter space. While no single benefit was essential for the evolution of filial cannibalism, benefits associated with adult or offspring survival and/or reproduction facilitated the evolution of cannibalism. Our model highlights the plausibility of a range of alternative hypotheses. Specifically, the evolution of filial cannibalism was enhanced if (1) parents could selectively cannibalize lower-quality offspring, (2) filial cannibalism increased egg maturation rate, (3) energetic benefits of eggs existed, or (4) cannibalism increased a parent's reproductive rate (e.g., through mate attractiveness). Density-dependent egg survivorship alone did not favor the evolution of cannibalism. However, when egg survival was density dependent, filial cannibalism invaded more often when the density dependence was relatively more intense. Our results suggest that population-level resource competition potentially plays an important role in the evolution of both parental care and filial cannibalism.     

Does time of the season influence filial cannibalism in the sand goby, <Emphasis Type="Italic">Pomatoschistus minutus</Emphasis>?

According to life-history theory, filial cannibalism by fish that breed over one season only should be more beneficial early than late in the season if they eat eggs to invest energy into later clutches. Also, filial cannibalism may be more costly late in the season if finding ripe females for replacing eaten eggs is harder then. On the other hand, offspring hatching early may have a competitive advantage over fry hatching late and hence provide higher fitness to the parent. Using data collected over three successive years, I tested if sand goby males are more prone to eat of their eggs early than late in the reproductive season. I found no difference in the amount of eggs eaten or in the frequency of males eating the whole clutch between early and late in the season. Furthermore, there was no difference in the frequency of males who ate parts of their clutches, early compared to late. This might reflect a trade-off between quality (early hatching offspring) and quantity (producing as many offspring as possible over a long reproductive season). If so, the lack of seasonal pattern of filial cannibalism found in sand gobies might be the result of opposing selection pressures.     

Filial cannibalism in fishes: Why do parents eat their offspring?

Filial cannibalism (the eating of one's own offspring) occurs in a variety of taxa, but is especially prevalent in fishes with parental care. Recent research supports a central tenet of parental-investment theory; that is, parents consume their offspring when it maximizes their lifetime reproductive success. This review outlines the theoretical framework used to explain the adaptive significance of filial cannibalism, evaluates experimental studies to test some predictions of this theory and discusses how the occurrence of filial cannibalism affects other aspects of a species' reproductive ecology.     

Non-Random Sibling Cannibalism in the Marine Gastropod Crepidula coquimbensis

Sibling cannibalism is commonly observed in marine species. For instance, intrabrood cannibalism has been documented in marine gastropods with direct development, suggesting a relationship between embryo behavior and the evolution of life history strategies. However, there has been little effort to document the factors driving sibling cannibalism in marine species. The kin selection theory suggests that the level of relatedness plays an important role in cannibalism patterns. We examined Crepidula coquimbensis, a marine gastropod that broods and encloses its brooded offspring in capsules. Encapsulated embryos show sibling cannibalism and high levels of intracapsular multiple paternity. Given these features, cannibalistic behavior may be driven by kin-relatedness. To test this hypothesis, we constructed artificial aggregations of embryos to mimic three levels of relatedness: high, medium and low. For each category of aggregation, the cannibalism rate and benefits (i.e. size at hatching of surviving offspring) were estimated. In addition, at the end of embryo development, we performed parentage analyses to determine if cannibalism was associated with the relatedness between cannibal and victim embryos. Our results show that the intensity of sibling cannibalism increased in aggregations characterized by the lowest level of relatedness. There were important benefits of cannibalism in terms of hatching cannibal size. In addition, cannibalism between embryos was not random: the variation in reproductive success between males increased over the course of the experiment and the effective number of fathers decreased. Altogether, these results suggest that polyandry may play an important role in the evolution of sibling cannibalism in C. coquimbensis and that kin selection may operate during early embryonic stages in this species.