Kazutaka Ota

Description of alternative male reproductive tactics in a shell-brooding cichlid, Telmatochromis vittatus, in Lake Tanganyika

Telmatochromis vittatus (Cichlidae) is a Tanganyikan substrate brooder which spawns in the gastropod-shell nests of a cichlid, Lamprologus callipterus. We describe male reproductive tactics of T. vittatus in and around the shell nests, where males of various sizes were found. Based on utilization patterns of the shell nests, interactions among males, and spawning behaviors, males could be categorized into four types based on reproductive tactics and in order of body size: sneaker males, satellite males, territorial males and piracy males. Size range of males in tactic groups rarely overlapped. Territorial males defended shell nests harboring multiple females, but during pair-spawning they were occasionally taken over by large piracy males that visited several nests repeatedly. Small sneaker males darted to pair-spawning territorial males and might ejaculate sperm. Satellite males did not perform parasitic spawning but pair-spawned in a single shell outside the nests. Spawning of satellite males was infrequently parasitized. The largest gonado-somatic index (GSI) was found in sneaker males followed by piracy males, territorial males and satellite males, suggesting that gonadal investment of males using the four tactics may be consistent with intensity or risk of sperm competition.

Unusual allometry for sexual size dimorphism in a cichlid where males are extremely larger than females

When males are the larger sex, a positive allometric relationship between male and female sizes is often found across populations of a single species (i.e. Rensch’s rule). This pattern is typically explained by a sexual selection pressure on males. Here, we report that the allometric relationship was negative across populations of a shell-brooding cichlid fish Lamprologus callipterus, although males are extremely larger than females. Male L. callipterus collect and defend empty snail shells in each of which a female breeds. We found that, across six populations, male and female sizes are positively correlated with not only sexual and fecundity selection indices, but also with shell sizes. Given their different reproductive behaviours, these correlations mean that males are required to be more powerful, and thus larger, to transport larger shells, while female bodies are reduced to the shell size to enable them to enter the shells. Among the three size selections (sexual selection, fecundity selection and shell size), shell size explained the allometry, suggesting that females are more strongly subject to size selection associated with shell size availability than males. However, the allometry was violated when considering an additional population where size-selection regimes of males differed from that of other populations. Therefore, sexual size allometry will be violated by body size divergence induced by multiple selection regimes.

Nest use by territorial males in a shell-brooding cichlid: the effect of reproductive parasitism

Male Telmatochromis vittatus, a substrate-brooding Tanganyikan cichlid, exhibit two parasitic reproductive tactics: takeover of spawning by larger males (“pirates”) and sneaking by smaller males (“sneakers”). Medium-sized males are territorial and pair-spawn within nests of clumped shells that harbor several resident females that are potential mates of the territory owner. To study nest use by territorial males, we analyzed the relationship between the body size of territorial males and nest quality, the number of females per nest, the distance between nests, and the frequency and intensity of reproductive parasitism. The size of males was not correlated with nest quality, the number of females, or the number of sneakers, but was negatively correlated with the frequency of intrusion by pirates and was positively correlated with the distance between nests. Territorial males effectively defended nests against sneakers but failed to defend against pirates. These results suggest that larger territorial males selected nests that have a lower risk of usurpation of spawning. We hypothesize that the risk of intrusion by pirate males affects the selection of nests by territorial males in this species.

Why are reproductively parasitic fish males so small?—influence of tactic-specific selection

Despite the wide prevalence of alternative reproductive tactics, little attention has been paid to why reproductively parasitic males are so small. In this study, we tackled this issue in a shell-brooding fish Lamprologus callipterus. Sneaky ‘dwarf males’ of this fish remain much smaller than bourgeois conspecifics throughout their life and employ a unique parasitic tactic, i.e. entering into a gastropod shell where a female is spawning, passing through the space between the female and shell wall and staying behind her to ejaculate throughout the spawning event. Here, we tested the prediction that they remain small to get past her through the shell spaces by interpopulation comparison. We showed, across populations, a negative allometry for sexual size dimorphism, an exponential increase of female size with an increase in shell size and a negative correlation between the magnitude of sexual size dimorphism and shell size. These results suggest that the inner spaces strongly regulate dwarf male size. We conclude that the small bodies of dwarf males arise from adaptation to their unique reproductive behaviour.

Changes in reproductive life-history strategies in response to nest density in a shell-brooding cichlid, Telmatochromis vittatus

To determine whether the appearance of a reproductively parasitic tactic varies, and how this variation affects territorial males of the Lake Tanganyika cichlid fish Telmatochromis vittatus, we examined the reproductive ecology of territorial males in Mtondwe and compared it with that of a neighboring Wonzye population, where nest density differs from that at Mtondwe. In Wonzye, with high nest density, male tactics change with their body size from a territorial to a non-territorial parasitic tactic called piracy in which they conquer several nests defended by territorial males and take over the nests while females are spawning. These “pirate” males could decrease the costs incurred by travelling among nests by exclusively targeting aggregations of nests in close proximity while avoiding separate nests. Territorial males in Wonzye sacrifice the potential higher attractiveness offered by large nests and instead compete for nests farther from neighbors on which pirates less frequently intrude. In contrast, the Mtondwe population had lower nest density and piracy was absent. Given that the success of piracy depends on the close proximity of nests, nest density is likely responsible for the observed variation in the occurrence of piracy between the two populations. Furthermore, in Mtondwe, territorial males competed for larger nests and were smaller than the territorial males in Wonzye. Thus, this lower nest density may free territorial males from the selection pressures for increased size caused by both defense against nest piracy and the need to develop into pirates as they grow.

A dear enemy relationship in a territorial cichlid: evidence for the threat-level hypothesis

Despite competing for resources such as space, food and mates, many territorial animals are less aggressive towards neighbours who rarely go beyond their territorial boundaries. This so-called dear enemy phenomenon is advantageous in territorial defence, but it has not been well studied in fish. In this work, we tested the ‘correct–incorrect boundary paradigm’ of the dear enemy phenomenon using the territorial cichlid fish Neolamprologus pulcher, which exhibits dear enemy relationships. When the fish was placed in a small experimental tank, in which fish established its territory, it was initially very aggressive against a neighbouring fish in an adjacent tank, but the aggression level decreased rapidly (within 4 days). When the tank containing the neighbour was shifted to the opposite side, the focal fish was more aggressive than the day before, but it exhibited less aggression than it did against a stranger placed on the shifted side. This lower level of aggression suggested that the focal fish did not regard the shifted neighbour as a stranger. Our observations provide support for the threat-level hypothesis, according to which territory owners will modulate aggression intensity based on the threat level.

Some evidence for different ecological pressures that constrain male and female body size

The dwarf morph of the Lake Tanganyika cichlid Telmatochromis temporalis uses empty snail shells as shelters and breeding sites in shell beds, in which many empty shells exist. Here, we assessed selection forces regulating body size in this fish. Field observations showed that large males tended to have a greater number of females in their territories, suggesting that sexual selection favours large males. Nonetheless, a transplant experiment suggested that male body size was limited by the ability to hide in empty shells from large piscivorous fish. In females, the number of ovarian eggs increased with body size, suggesting that fecundity selection favours large females. However, females are smaller than males. Females spawned eggs close to the apices inside the shells. The small space there would decrease the risk of egg predation by egg predators, and small body size of females may be a result of adaptation to spawn eggs in the small, safe spaces. This study provides support for the idea that male and female body sizes have been limited by different ecological pressures (predation on adult fish in males, predation on eggs in females), which has not been reported previously in any animal.

Social status-dependent nest choice of territorial males under reproductive parasitism in a Lake Tanganyika cichlid Telmatochromis vittatus

Field and laboratory studies were conducted to examine how territorial males of a Lake Tanganyika cichlid Telmatochromis vittatus balance the conflicting demands on nest choice between occupying large nests with more females and avoiding reproductive parasitism (nest piracy, which is adopted by the largest males in the population). Pirates less frequently intruded the nests farther from neighbours, perhaps due to the costs associated with travelling between nests. The field experiment showed that territorial male T. vittatus sacrificed the fitness benefits that large nests offer and instead prioritized occupying the nests farther from neighbours on which fewer pirates intruded. The field observations suggested that they adopt different strategies for nest choice according to their relative competitive ability to pirates; the large territorial males, who are size-matched to pirates and can defend their nests against them, compete for larger nests among the more-isolated nests, whereas subordinate territorial males, which are smaller than pirates and thus inferior to them, compete for the more-isolated nests among the less-isolated nests. These findings suggest that the territorial male T. vittatus chooses the more-isolated nests to avoid pirate males at the expense of occupying large nests.

Maternal Food Provisioning in a Substrate-Brooding African Cichlid

Fish demonstrate the greatest variety of parental care strategies within the animal kingdom. Fish parents seldom provision food for offspring, with some exceptions predominantly found in substrate-brooding Central American cichlids and mouth-brooding African cichlids. Here, we provide the first evidence of food provisioning in a substrate-brooding African cichlid Neolamprologus mondabu. This fish is a maternal substrate-brooding cichlid endemic to Lake Tanganyika, and feeds on benthic animals using unique techniques–individuals typically feed on the surface of sandy substrates, but also expose prey by digging up substrates with vigorous wriggling of their body and fins. Young also feed on benthos on the substrate surface, but only using the first technique. We observed that feeding induced by digging accounted for 30% of total feeding bouts in adult females, demonstrating that digging is an important foraging tactic. However, parental females fed less frequently after digging than non-parental females, although both females stayed in pits created by digging for approximately 30 s. Instead, young gathered in the pit and fed intensively, suggesting that parental females provision food for young by means of digging. We tested this hypothesis by comparing the feeding frequency of young before and after digging that was simulated by hand, and observed that young doubled their feeding frequency after the simulated digging. This suggests that parental females engage in digging to uncover food items that are otherwise unavailable to young, and provision food for them at the expense of their own foraging. This behavior was similar to what has been observed in Central American cichlids.

Bower-building behaviour is associated with increased sperm longevity in Tanganyikan cichlids.

We investigated the evolutionary relationship between spawning behaviour and sperm motility traits among Tanganyikan mouth‐brooding cichlid species that have developed diverse mating behaviours and male sexual traits. Mouth‐brooding behaviour is common among these fish, but different species demonstrate a range of spawning behaviours, bower construction, male sexual traits and timing of gamete release. We observed spawning behaviours and compared sperm motility traits of 28 Tanganyikan mouth‐brooding cichlids to elucidate the evolutionary correlations between these traits. Sperm longevity was considerably longer in bower‐building species that construct crater‐shaped spawning sites compared with species that do not build bowers. Male bower builders released sperm in the pit of the bower prior to spawning, and the time from ejaculation to fertilization was longer. Conversely, most mouth‐brooding cichlids deposited semen directly into the female buccal cavity, and spawned eggs were immediately picked up to be placed inside the cavity; thus, the time from ejaculation to fertilization was short. These observations suggest that increased sperm longevity is favoured in bower builders. Comparative phylogenetic analyses suggested that bower‐building behaviour and greater time from ejaculation to fertilization are associated with the extension of sperm longevity, whereas sperm competition rank does not play a major role. In addition, bower‐building behaviour preceded the emergence of increased sperm longevity. These results indicate that the extension of sperm longevity as a result of the emergence of bower builders may have acted as an evolutionary attractor for sperm longevity.