Tomohiro Takeyama

Niche differentiation depends on body size in a cichlid fish: a model system of a community structured according to size regularities

1. Communities of different species are often structured according to niche differentiation associated with competitive interactions. We show that similar principles may apply on an ecological time-scale when individuals of a species having a wide size variation compete for resources, using the Lake Tanganyika cichlid Lobochilotes labiatus (5-30 cm). This species has a mouth especially adapted to suck up invertebrates from rock crevices. 2. Individuals defended feeding territories against similar-sized conspecifics, but not against different-sized ones. Thus, territories of similar-sized fish rarely overlapped, but up to a total of seven individuals (of seven size-ranks) had broadly overlapping territories with dissimilar-sized individuals. Comparison with expectation from the null model demonstrated clearly that observed size ratios between adjacent size rank were determined non-randomly regardless of sexual combinations. 3. Larger individuals took larger prey types of larger average size, but more importantly used wider rock crevices from which to suck food than smaller individuals. We calculated pairwise values of Schoeners index of diet overlap C(d) and the values of Levins index of diet breadth B(d) (prey type and prey size) and the same for the width of the rock crevices used for foraging (C(r) and B(r)). C(d) remained high among all combinations of the seven ranks. In contrast, C(r) declined strongly in combinations of adjacent ranks (to 0.27), and was low or zero among further different size ranks. This shows that fish with overlapping territories divided the food resources largely through foraging site partitioning. Accordingly, B(d) did not depend on the size difference to the nearest two coinhabiting fish, whereas B(r) did. 4. We conclude that this L. labiatus community is structured non-randomly: body size-dependent effects on foraging site usage result in competition with, and territorial exclusion of, similar-sized individuals, but not of dissimilar-sized individuals that were accepted as coinhabitants. Accordingly, mean body size ratios (large/small) between two adjacent ranks were consistently approximately 1.28 [standard deviation (SD) = 0.07, n = 104], while approximately 1.34 from the null model (SD = 0.34, n = 10 400 simulations). We discuss our results as an example of Hutchinsons rule, applied originally to size ratios of different species.

Cooperatively breeding cichlid fish adjust their testis size but not sperm traits in relation to sperm competition risk

Theoretical models predict that in external fertilisers, sperm competition risk selects for larger testes and larger sperm with higher velocity, at the expense of sperm longevity. Although several empirical studies have tested this prediction within a fish species, there has been little evidence that an individual male can adjust his testis size and sperm traits according to the risk of sperm competition. Using the cooperatively breeding cichlid Julidochromis transcriptus, we examined testis size and sperm traits (sperm size, velocity and longevity) of males that were assigned to monogamous pairs (without risk of sperm competition) or cooperatively polyandrous trios composed of two males and one female (with risk); the groups were reared for breeding for 2 or more months. Our experiments showed that the polyandrous males, both siring eggs in a clutch, had larger relative testis mass than the monogamous males. However, sperm traits were unrelated to sperm competition. These results suggest that individual males of J. transcriptus can adjust their testis size but not sperm traits in response to sperm competition risk. We also examined the effect of testis investment on growth rate and the somatic condition of males. Increased investment in testes slowed growth rates, whereas testis investment did not affect somatic condition, indicating a trade-off between investment in testes and growth. We conclude that testis investment, in response to perceived sperm competition risks, occurs at the expense of growth and may be a conditional reproductive strategy that is determined by the social status (monogamous or polyandrous) of each J. transcriptus male.

Carbon and nitrogen stable isotope ratios of macroinvertebrates in the littoral zone of Lake Biwa as indicators of anthropogenic activities in the watershed

Carbon and nitrogen stable isotope ratios (δ13C and δ15N) of macroinvertebrates inhabiting littoral zones of lakes can serve as useful indicators of material loading from the watershed. We collected snails (Semisulcospira spp.) and bivalves (Unio douglasiae biwae Kobelt) from 29 littoral sites in Lake Biwa near the mouths of river tributaries with various human population density (HPD) and land-use patterns. The δ13C and δ15N signatures were determined for three potential food sources: particulate organic matter in the pelagic zone (PPOM), riverine particulate organic matter from tributaries (RPOM) and epilithic organic matter in the littoral zone (EOM). The stable isotope mixing model revealed that snails relied mainly on EOM, and bivalves on PPOM and RPOM. Multiple regression analysis showed that intersite variation in δ15N for snails was best explained by HPD, while variation in δ15N of EOM and nitrate was explained to a lesser extent by HPD. Comparison with isotope signatures of their food sources and riverine nutrients revealed that snails assimilated anthropogenic nitrogen from wastewater in the watershed. Our results also showed that the δ13C value of bivalves was marginally related to the fraction of paddy fields in the watersheds. In conclusion, the isotope signatures of macroinvertebrates inhabiting the littoral zone can be useful indicators of anthropogenic impacts from the watershed.

Living on the wedge: female control of paternity in a cooperatively polyandrous cichlid

Theories suggest that, in cooperatively breeding species, female control over paternity and reproductive output may affect male reproductive skew and group stability. Female paternity control may come about through cryptic female choice or female reproductive behaviour, but experimental studies are scarce. Here, we show a new form of female paternity control in a cooperatively polyandrous cichlid fish (Julidochromis transcriptus), in which females prefer wedge-shaped nesting sites. Wedge-shaped sites allowed females to manipulate the siring success of the group member males by spawning the clutch at the spot where the large males were just able to enter and fertilize the outer part of the clutch. Small males fertilized the inner part of the clutch, protected from the large aggressive males, leading to low male reproductive skew. Small males provided more brood care than large males. Multiple paternity induced both males to provide brood care and reduced female brood care accordingly. This is, to our knowledge, the first documented case in a species with external fertilization showing female mating behaviour leading to multiple male paternity and increased male brood care as a result.

Facial Recognition in a Group-Living Cichlid Fish.

The theoretical underpinnings of the mechanisms of sociality, e.g. territoriality, hierarchy, and reciprocity, are based on assumptions of individual recognition. While behavioural evidence suggests individual recognition is widespread, the cues that animals use to recognise individuals are established in only a handful of systems. Here, we use digital models to demonstrate that facial features are the visual cue used for individual recognition in the social fish Neolamprologus pulcher. Focal fish were exposed to digital images showing four different combinations of familiar and unfamiliar face and body colorations. Focal fish attended to digital models with unfamiliar faces longer and from a further distance to the model than to models with familiar faces. These results strongly suggest that fish can distinguish individuals accurately using facial colour patterns. Our observations also suggest that fish are able to rapidly (≤ 0.5 sec) discriminate between familiar and unfamiliar individuals, a speed of recognition comparable to primates including humans.

Male Reproductive Success in a Promiscuous Armoured Catfish Corydoras Aeneus (Callichthyidae)

Among a variety of fish mating systems, promiscuity with random-mating seems to be most prevalent. However, detailed studies of promiscuity have been rare due partly to the peculiar difficulty in examination of male mating and reproductive success in the random mating. Females of the armoured catfish Corydoras aeneus (no sexual dimorphism other than size of males > females) spawn 10–20 egg-clutches with multiple males at a time, but an entire egg clutch is inseminated by sperm of a single male. We studied mating system of this fish in aquarium. Males had neither mating territories nor monopolized females, never being aggressive against rival males. Evidence of female preference for certain male traits including size was not detected. Females mated a male in proportion to his relative courtship frequency among males. Courtship frequency was not related to male size, and male mating success was not different between small and large males. Clutch size and insemination rate were different neither between small and large males nor between frequently and less frequently courting males. Thus, the male reproductive success will not be related to the male size, but directly to courtship frequency, indicating the random mating in this fish. There seemed to be fecundity advantage with size in female, and the consequent sexual difference in energy allocation will be responsible to the sexual dimorphism. We also discuss the low male-GSI in this promiscuous fish in which sperm competition hardly occurred.

Inheritance Patterns of Lateral Dimorphism Examined through Breeding Experiments in Tanganyikan Cichlid (Julidochromis transcriptus) and Japanese Medaka (Oryzias latipes)

The asymmetry of mouth morphology, in which the mouth opens either leftward or rightward, is a unique example of antisymmetry that is widely found in fishes, such as Tanganyikan scale-eating cichlids, herbivorous cichlids, and the Japanese freshwater goby. This dimorphism is thought to be heritable in a Mendelian manner similar to that of the dominance of the lefty allele over righty, with homozygotes of lefty alleles being absent. This study aims to reveal whether this trait is inherited in the same Mendelian manner in fishes other than those examined to date, and whether the absence of the dominant homozygote is due to a lethal effect. We conducted F1 and F2 breeding experiments using the Tanganyikan cichlid Julidochromis transcriptus and Japanese medaka Oryzias latipes. For both J. transcriptus and O. latipes, the F1 generations produced by incrossing lefty parents showed a lefty:righty ratio of 2:1, whereas incrosses of righties produced only righty offspring. Test crosses between lefty and righty produced a 1:1 ratio of lefty and righty offspring. These results are consistent with the inheritance model in which righty is homozygous for a recessive righty allele and lefty is heterozygous for dominant lefty and recessive righty alleles, in agreement with previous observations. The F2 test cross also confirmed this pattern. Furthermore, no lethal effects on hatchability of O. latipes were detected, refuting the suggestion that the dominant homozygote is embryonic lethal. We conclude that mouth laterality is inherited in the same Mendelian manner in these two species, similar to that other fish species studied previously. However, the reason for absence of the dominant homozygote remains unclear.

Why egg-caring males of Isaza (Gymnogobius isaza, Gobiidae) refuse additional females: preliminary field observations

Like many other gobies, males of the Isaza goby, Gymnogobius isaza endemic to Lake Biwa, Japan, conduct parental care of eggs at nests, and females are likely to choose mates while visiting nests. The reproductive strategy should induce polygyny, but Isaza males never accept additional females in one breeding cycle. Sampling data of broods indicated that the egg mass areas were much smaller than the nest sizes, suggesting that nest size is not the limiting factor in obtaining further eggs from additional females. The brood size greatly decreased as the duration of care progressed. Few individuals including caring males ate eggs, and heterospecific egg predators were rarely observed. Sixty percent of egg masses at the middle stages of egg development were infected with aquatic fungi, some being covered with a fungus mat that drastically reduced survivorship. Infected egg masses contained more eggs than non-infected ones at the same stage, indicating that large egg masses are prone to be frequently destroyed by fungi. It is likely that the activity of parental males is lowered during the long care periods at low water temperature in early spring. Such lowered activity of caring males might be responsible for infections in large broods that would have needed more care. We propose the hypothesis that male rejection of additional females may be related to optimal brood size, which will be less susceptible to fungus infection and produce more hatching young than otherwise. This hypothesis will explain not only male avoidance of additional females but also some unique reproductive behaviors of this fish such as some females’ spawning of a portion of of the mature eggs in one nest.

Mate availability affects female choice in a fish with paternal care: female counterstrategies against male filial cannibalism

Theory predicts that individuals should adopt counterstrategies against intersexual conflict with their mating partners if the counterstrategies are effective and cost-efficient. In fishes, males with parental care often cannibalize their own offspring, which reduces the female’s fitness and creates intersexual conflicts. Males of the goby Rhinogobius flumineus cannibalize more eggs in the nest when they have access to additional females prior to spawning. Thus, it is predicted that females will strategically avoid spawning with males that have high mate availability. In the present study, we experimentally tested this prediction. When sexual pairs were placed in tanks, most females (control females; 21/22) successfully spawned inside the nest. In contrast, when a gravid female (stimulus female) that was housed in a small transparent cage was shown to the experiment pairs prior to spawning, only about half of the females (experiment females; 16/29) spawned inside the nest; the remaining females released unfertilized eggs outside of the nest. Moreover, experiment females infrequently accepted and followed males into nests, and delayed spawning more often than control females. R. flumineus females prefer males that court frequently. Indeed, experiment females that infrequently received courtship tended to spawn outside of the nest. However, infrequent courtship alone could not explain outside-nest spawning, delay in spawning, or the shorter stay of females in nests. These results imply that the presence of a stimulus female dampens female spawning with males. We suggest that R. flumineus females may strategically reject or hesitate to spawn with males that have high mate availability, and that this spawning avoidance may be a counterstrategy against male filial cannibalism.

Seasonal and site-specific variability in terrigenous particulate organic carbon concentration in near-shore waters of Lake Biwa, Japan

Identifying sources of particulate organic matter (POM) is important for clarifying fundamental mechanisms by which lake food webs are sustained. We determined carbon and nitrogen stable isotope ratios of POM in near-shore waters of Lake Biwa, a large, meso-eutrophic lake in Japan, to estimate relative contributions of terrigenous particulate organic carbon (T-POC), plankton-derived POC (P-POC) and epilithon-derived POC (E-POC) to POC in near-shore waters. Samples were collected during different months (November, February, May and July) at 29 sites located near the mouth of tributary rivers with different discharge and catchment land use. The data revealed that POC mainly consisted of P-POC and T-POC, with relative contributions varying widely over season and among locations. E-POC generally contributed little to the near-shore POC. Path analyses revealed that the concentration of riverine POC whose isotopic signatures were similar to those of rice straws increased with a larger %paddy field area in the catchment of tributary rivers, which subsequently enhanced T-POC inputs to near-shore waters through riverine transportation. Furthermore, our results suggested that T-POC contribution was influenced, with a time lag, by wave-driven turbulence and shore topography, which appear to affect sedimentation and resuspension of T-POC.