Early Filial Cannibalism in Fish Revisited: Endocrinological Constraint, Costs of Parental Care, and Mating Possibility.

AbstractOffspring desertion by parents generally occurs at an early stage of parental care, which is thought to minimize the costs of parental care prior to desertion. This study investigated the effects of endocrinological constraints on early total filial cannibalism by male Rhabdoblennius nitidus in the field, a paternal brooding blennid fish with androgen-dependent brood cycling. In brood reduction experiments, cannibal males showed low levels of plasma 11-ketotestosterone (11-KT) relative to noncannibals and also similar levels of 11-KT to males in the parental care phase. Since 11-KT regulates male courtship intensity, males with decreased courtship activity would exhibit total filial cannibalism. However, there is a possibility that a transient increase in 11-KT levels at the early stage of parental care delays total filial cannibalism. In contrast, total filial cannibalism could occur before a decline to the lowest 11-KT levels, at which point males might still be able to exhibit courtships, possibly to reduce the costs of parental care. To understand how much and when caregiving males exhibit mating and parental care behaviors, it is important to consider not only the presence of endocrinological constraints but also its intensity and flexibility.

Tetrodotoxin Profiles in Xanthid Crab Atergatis floridus and Blue-Lined Octopus Hapalochlaena cf. fasciata from the Same Site in Nagasaki, Japan.

The xanhid crab Atergatis floridus and the blue-lined octopus Hapalochlaena cf. fasciata have long been known as TTX-bearing organisms. It has been speculated that the TTX possessed by both organisms is exogenously toxic through the food chain, since they are reported to have geographic and individual differences. The source and supply chain of TTX for both of these organisms, however, remain unclear. On the other hand, since crabs are one of the preferred prey of octopuses, we focused our attention on the relationship between the two species living in the same site. The aim of this study was to determine TTX concentrations and TTX profiles of A. floridus and H. cf. fasciata, collected simultaneously in the same site, and examine the relationship between them. Although there were individual differences in the TTX concentration in both A. floridus and H. cf. fasciata, the toxin components commonly contained 11-norTTX-6(S)-ol in addition to TTX as the major components, with 4-epiTTX, 11-deoxyTTX, and 4,9-anhydroTTX as the minor components. The results suggest that octopuses and crabs in this site acquire TTX from common prey, including TTX-producing bacteria and/or may have a predator-prey relationship.

Evidence of sperm removal behaviour in an externally fertilizing species and compensatory behaviour for the risk of self-sperm removal.

The removal of rival sperm from a female's sperm storage organ acts as a strong sperm competition avoidance mechanism, which has been reported only in internally fertilizing species and not at all in externally fertilizing species. This study demonstrated for the first time that nest-holding males of Bathygobius fuscus, an externally fertilizing marine fish, remove the sperm of rival sneaker males from the spawning nest by exhibiting tail-fanning behaviour within the nest. Males showed tail-fanning behaviour when semen was artificially injected into the nest but not when seawater was injected, and in open nests this behaviour resulted in higher paternity rates for the focal male. The sperm removal behaviour entails the risk of removing their own sperm; therefore, additional sperm release behaviour is likely necessary to benefit from the sperm removal effect. Consistent with this, males increased post-fanning sperm release behaviour more in the semen than in the seawater injection treatment. Moreover, males who had removed sperm for a longer time spent more time releasing sperm after the removal, suggesting that the additional sperm release behaviour compensated for the loss of their own sperm. These results suggest that sperm removal behaviour is not restricted to internally fertilizing organisms and deserves further investigation in this and other species.

Effect of the administration of prolactin-releasing peptide2 on feeding activity in the intertidal blenny Rhabdoblennius nitidus (Günther, 1861).

Prolactin-releasing peptide2 (PrRP2) was administered intraperitoneally to male intertidal blenny Rhabdoblennius nitidus, a species with male uniparental care of eggs, to investigate the effect on their feeding activity. A significant inhibitory effect on appetite was observed in the breeding season, but not in the nonbreeding season. These results suggest that PrRP2 and PrRP2 receptors are more active during the breeding season. The presence of a mechanism to inhibit feeding activity while parents take care of their offspring may be important for the success of parental care.

Male parental assistance in embryo hatching of barred-chin blenny Rhabdoblennius nitidus.

Most teleostean embryos develop and hatch without parental assistance, though some receive parental care. We focused on a paternal brood-care species, the barred-chin blenny (Rhabdoblennius nitidus [Günther, 1861]). As hatching approached, fanning behavior by the male parent drastically increased and then embryos hatch. In the absence of the male parent, most embryos failed to hatch. However, the hatching rate was greatly assisted by introducing an artificial water current, suggesting that paternal assistance other than for aeration is required for successful embryo hatching. Next, we analyzed genes for the hatching enzyme and egg-envelope protein, which were successfully cloned from barred-chin blenny, and found the expression patterns differed from those of other euteleosts. Generally, high choriolytic enzyme swells the intact egg envelope, and then low choriolytic enzyme solubilizes the swollen envelope. The expression levels of both the enzymes, but especially the latter, were much lower in barred-chin blenny that is known in most other oviparous species. In addition, the main component of the egg envelope was changed into ChgHm and choriogenin L (ChgL) in barred-chin blenny, whereas ChgH and ChgL for other euteleosts. These in barred-chin blenny would result in ineffective egg-envelope digestion because the posthatching egg envelopes were observed to be swollen but not solubilized. Male parental assistance by fanning until hatching may compensate for this insufficiency. Our study illustrates an example of the evolution of parent-embryo interaction built on a novel relationship: Degradation of the hatching enzyme/egg-envelope digestion system, accompanied by male parental hatching assistance.

Filial Cannibalism by Male Fish as an Infanticide to Restart Courtship by Self-Regulating Androgen Levels.

Parental care is costly for animal parents [1-3], who often desert, abort, or kill their offspring and sometimes even eat them-so-called filial cannibalism [1, 4]. A primary adaptive hypothesis for filial cannibalism centers on the expected nutritional benefits from eating offspring (the energy-based [EB] hypothesis [5-7]). However, many empirical studies are inconsistent with the EB hypothesis [8, 9]. One notable case is total filial cannibalism observed in some fishes. The caregiving males of these species eat all eggs and restart reproduction when tending a small number of eggs, as predicted by the EB hypothesis; but, this is puzzling because they can potentially court females even while tending eggs and increase the eggs by additional matings. Here we show that brood termination known as total filial cannibalism in blenniid fish Rhabdoblennius nitidus males is an endocrinological necessity to restart courtship behavior for subsequent mating. Males exhibit androgen-dependent brood cycling, and they are normally incapable of exhibiting courtships during the parental phase [10]. Egg manipulation experiments demonstrated that egg presence in the nest is a key stimulus regulating male androgen levels; they cannot restart courtship until removing all eggs. Furthermore, surprisingly, eggs were sometimes spit out without being consumed, and the occurrence of cannibalization and removal of all eggs was not associated with male condition. These results strongly suggest that the egg cannibalistic and removal behaviors that have been regarded as total filial cannibalism in this species are infanticide or embryocide rather than cannibalism, which serve to increase the males' androgen levels.

Male coercive mating in externally fertilizing species: male coercion, female reluctance and explanation for female acceptance.

Male coercive mating exerts a strong evolutionary pressure on mating-related traits of both sexes. However, it is extremely rare in externally fertilizing species probably because the male mating behaviour is incomplete until females release their eggs. Here we showed that males of the externally fertilizing fish Rhabdoblennius nitidus coercively confine females to the nests until spawning, and investigated why females accept male coercive mating. The females entered the males' nests following male courtship displays, but they usually tried to escape when there were no eggs because males tended to cannibalize all the eggs when there were few. Most males that used small, tight nests acquired new eggs but with experimentally enlarged nests, 90% of the males without eggs failed to confine the females. Spawning tended to occur during the early/late spawning period in nests with no eggs (i.e. male coercive mating). In the nests where the first eggs were deposited in the early period, subsequent matings with other females were more likely to occur, whereas in the late period, most parental care of the eggs failed without additional matings. The females that spawned in the late period may have been compelled to accept male coercive mating due to time constraints.

Large- and small-size advantages in sneaking behaviour in the dusky frillgoby Bathygobius fuscus.

Sneaking tactic, a male alternative reproductive tactic involving sperm competition, is generally adopted by small individuals because of its inconspicuousness. However, large size has an advantage when competition occurs between sneakers for fertilization of eggs. Here, we suggest that both large- and small-size advantages of sneaker males are present within the same species. Large sneaker males of the dusky frillgoby Bathygobius fuscus showed a high success rate in intruding into spawning nests because of their advantage in competition among sneaker males in keeping a suitable position to sneak, whereas small sneakers had few chances to sneak. However, small sneaker males were able to stay in the nests longer than large sneaker males when they succeeded in sneak intrusion. This suggests the possibility of an increase in their paternity. The findings of these size-specific behavioural advantages may be important in considering the evolution of size-related reproductive traits.

Alternative male mating behaviors dependent on relative body size in captive oval squid Sepioteuthis lessoniana (Cephalopoda, Loliginidae).

We observed the reproductive behavior of the oval squid Sepioteuthis lessoniana in captivity. The male used three different mating behaviors: male-parallel (MP), male-upturned (MU) and sneaking. Male competition over females frequently occurred before and during the female egg-laying period, and the outcome of most fights depended on male body size. Larger males guarded their partners from other males and performed MP mating during the egg-laying period of the paired females. In contrast, there was no pairing and mate guarding in MU mating and sneaking, which were adopted by smaller subordinate males as alternative tactics outside female egg-laying period and during the period, respectively. MP matings were 95% successful, but more than half of MU matings were unsuccessful. Higher mating success in MP mating was achieved through pairing, whereas males in MU mating were less successful because mating attempts without pair formation were often foiled by escape of the female. Sneaking was successful in all cases but occurred less frequently. Spermatophores were attached at the opening of the oviduct in MP mating, whereas they were attached around the female buccal membrane in MU mating and sneaking. Considering the route of egg transportation, higher fertilization success can be expected in MP mating because of the advantageous location of the attached spermatophores. Our results suggest that MP mating is used by larger, paired males during the female egg-laying period, and that MU mating and sneaking are alternative tactics adopted by smaller, subordinate males. These alternative mating behaviors would be conditional strategy dependent on relative body size, because some individual males displayed both MP and MU mating behaviors.