Noboru Okuda

Filial cannibalism by mouthbrooding males of the cardinal fish, Apogon doederleini, in relation to their physical condition

SynopsisPaternal brood cannibalism was observed in a population ofApogon doederleini in Shikoku Island, Japan. Of 361 egg masses mouthbrooded by males, 47 disappeared within a day of spawning. A stomach check with a syringe ascertained that they had been consumed by the males. The frequency of this cannibalism increased as the breeding season advanced. As males completed 4–7 breeding cycles in a breeding season and spent 80% of the time mouthbrooding without taking ordinary food, their physical condition deteriorated greatly late in the breeding season. We concluded that parental physical condition is an important factor in the occurrence of brood cannibalism.

Sex Roles Are Not Always Reversed When the Potential Reproductive Rate Is Higher in Females

Sex roles were examined in a cardinalfish, Apogon notatus, in which males alone mouthbrood the eggs received from a single female. Before spawning, a male and female formed a pair, within which the female is more active in courtship and attacks against conspecifics. Females had a higher potential for reproduction and on average produced more than twice as many clutches as those mouthbrooded by a male in a season by changing mates after spawning. Animals in which mating competition is more intense among females and, ultimately, sexual selection is more strongly acting on females are defined as sex‐role reversed. Sex‐role reversal is expected where the operational sex ratio (OSR) is female biased. In A. notatus, however, the OSR was male biased throughout the breeding season. This was due primarily to a higher mortality in females. The theory predicts that sexual selection operates more strongly on the sex toward which the OSR is biased. The facts that the variance in reproductive success was greater in males and the males developed a sexual trait suggest that sexual selection is acting more strongly on males than on females. Accordingly, this fish is not sex‐role reversed.

Is the relationship between body size and trophic niche position time-invariant in a predatory fish? First stable isotope evidence.

Characterizing relationships between individual body size and trophic niche position is essential for understanding how population and food-web dynamics are mediated by size-dependent trophic interactions. However, whether (and how) intraspecific size-trophic relationships (i.e., trophic ontogeny pattern at the population level) vary with time remains poorly understood. Using archival specimens of a freshwater predatory fish Gymnogobius isaza (Tanaka 1916) from Lake Biwa, Japan, we assembled a long-term (>40 years) time-series of the size-dependence of trophic niche position by examining nitrogen stable isotope ratios (δ 15N) of the fish specimens. The size-dependence of trophic niche position was defined as the slope of the relationship between δ 15N and log body size. Our analyses showed that the slope was significantly positive in about 60% of years and null in other years, changing through time. This is the first quantitative (i.e., stable isotope) evidence of long-term variability in the size-trophic relationship in a predatory fish. This finding had implications for the fish trophic dynamics, despite that about 60% of the yearly values were not statistically different from the long-term average. We proposed hypotheses for the underlying mechanism of the time-varying size-trophic relationship.

Female mating strategy and male brood cannibalism in a sand-dwelling cardinalfish

I investigated male and female sexual strategies of a cardinalfish, Apogon niger, which breeds in sandy areas at sporadic coral colonies. Males mouthbrood an egg mass received from one female at a time. Because of the lengthy mouthbrooding period, the interspawning interval was shorter for females than for males. Females moved between coral colonies to find mates more extensively than did males, and more frequently deserted mates after spawning. The females shortened their interspawning intervals by changing mates, especially in the late breeding season, when their mobility was highest. Their mobility was positively correlated with their disappearance rate, suggesting that mate search increases mortality. This may reduce competition between females for males, resulting in an unbiased rather than female-biased operational sex ratio. Males, on the other hand, practised filial cannibalism of entire broods, which might allow them partially to compensate for the lack of food during the mouthbrooding period. The reproductive loss entailed by filial cannibalism could be effectively offset if males remate soon afterwards. However, cannibal males took a long time to remate because few females were available. Filial cannibalism was less frequent than in a boulder-dwelling congener in which males have easy access to mates. Low mate availability may inhibit male A. niger from committing filial cannibalism. Copyright 1999 The Association for the Study of Animal Behaviour.

Determinate growth in a paternal mouthbrooding fish whose reproductive success is limited by buccal capacity

The life history of the paternal mouthbrooding cardinal fish Apogon doederleini was investigated in the temperate waters of Japan, with particular reference to its growth and reproductive rate. Both males and females almost ceased to grow at age 3 years, although living to 7 years of age. Their growth pattern, represented by the relative size at sexual maturity to the asymptotic size and the von Bertalanffy growth coefficient, was among the most determinate in ectothermic vertebrates. Brood size just before hatching increased in proportion to the second power of the body size of the brooding male, and correlated more positively with the males than the females body size, suggesting that it was limited by the males buccal capacity. The estimated total number of broods hatched in a breeding season showed a weak or no correlation with the body size or age in either sex. Using life-history parameters based on data of A. doederleini, a simulation model of energy allocation without considering sexual interaction revealed that the optimal growth pattern shows an indeterminate growth that differs greatly from the actual growth pattern of A. doederleini. This suggests that there are some brooding constraints to size-advantage of reproductive success in this species. The possible mechanism of such reproductive constraint is discussed.

Mate availability influences filial cannibalism in fish with paternal care

In fish with paternal care, males often eat their offspring (i.e. filial cannibalism). This is regarded as a male’s adaptive strategy to maximize lifetime reproductive success by enhancing his own survivorship or the survivorship of the remaining offspring at the cost of current reproductive success. Although the parental energy reserve has been considered a primary factor influencing filial cannibalism, the possibility that mate availability may also be an important factor has been overlooked. When many mates are available, males may receive a surplus of eggs, which can be treated as an energy reserve and reallocated to future breeding attempts. We present a game theoretical model for the evolution of filial cannibalism, incorporating intrinsic parental condition and extrinsic breeding system components which determine mate availability. The model predicts that filial cannibalism is favoured under the following conditions: (1) the male’s energy reserve is low; (2) mate search efficiency is high; (3) the population density is high; (4) the sex ratio is female biased; (5) the male care period is long; and (6) the female’s refractory period is short. Conditions 2–6 facilitate filial cannibalism through an increase in mate availability.  2002 The Association for the Study of Animal Behaviour

Vertical heterogeneity of a forest floor invertebrate food web as indicated by stable-isotope analysis

Diverse populations of invertebrates constitute the food web in detritus layers of a forest floor. Heterogeneity in trophic interactions within such a species-rich community food web may affect the dynamic properties of biological communities such as stability. To examine the vertical heterogeneity in trophic interactions among invertebrates in litter and humus layers, we studied differences in species composition and variations in carbon and nitrogen stable-isotope ratios (δ13C and δ15N) using community-wide metrics of the forest floors of temperate broadleaf forests in Japan. The species composition differed between the two layers, and the invertebrates in the litter layer were generally larger than those in the humus layer, suggesting that these layers harbored separate food webs based on different basal resources. However, the δ13C of invertebrates, an indicator of differences in the basal resources of community food webs, did not provide evidence for separate food webs between layers even though plant-derived organic matter showed differences in stable-isotope ratios according to decomposition state. The minimum δ15N of invertebrates also did not differ between layers, suggesting sharing of food by detritivores from the two layers at lower trophic levels. The maximum and range of δ15N were greater in the humus layer, suggesting more trophic transfers (probably involving microorganisms) than in the litter layer and providing circumstantial evidence for weak trophic interactions between layers at higher trophic levels. Thus, the invertebrate community food web was not clearly compartmentalized between the detrital layers but still showed a conspicuous spatial (vertical) heterogeneity in trophic interactions.

Stable nitrogen isotopic composition of amino acids reveals food web structure in stream ecosystems

The stable N isotopic composition of individual amino acids (SIAA) has recently been used to estimate trophic positions (TPs) of animals in several simple food chain systems. However, it is unknown whether the SIAA is applicable to more complex food web analysis. In this study we measured the SIAA of stream macroinvertebrates, fishes, and their potential food sources (periphyton and leaf litter of terrestrial C3 plants) collected from upper and lower sites in two streams having contrasting riparian landscapes. The stable N isotope ratios of glutamic acid and phenylalanine confirmed that for primary producers (periphyton and C3 litter) the TP was 1, and for primary consumers (e.g., mayfly and caddisfly larvae) it was 2. We built a two-source mixing model to estimate the relative contributions of aquatic and terrestrial sources to secondary and higher consumers (e.g., stonefly larva and fishes) prior to the TP calculation. The estimated TPs (2.3–3.5) roughly corresponded to their omnivorous and carnivorous feeding habits, respectively. We found that the SIAA method offers substantial advantages over traditional bulk method for food web analysis because it defines the food web structure based on the metabolic pathway of amino groups, and can be used to estimate food web structure under conditions where the bulk method cannot be used. Our result provides evidence that the SIAA method is applicable to the analysis of complex food webs, where heterogeneous resources are mixed.

Stable isotope analysis indicates trophic differences among forest floor carabids in Japan

Differences in trophic niches among carabid beetles (Coleoptera: Carabidae) co‐occurring on the forest floors of warm temperate forests in central Japan were studied using carbon (δ13C) and nitrogen (δ15N) stable isotope analyses. Different carabid species showed similar δ15N values, which were higher than those of their possible invertebrate prey (herbivores and detritivores) collected from the litter layer, indicating that these species were consumers in the same trophic level. In contrast, δ13C values differed among carabid species, indicating interspecific differences in prey animals. The variation in the δ13C value was larger in summer than in autumn. In summer, δ13C values indicated that some carabids depended highly on either grazing (low δ13C values) or detrital sources (high δ13C values) within the food chain [Chlaenius posticalis Motschulsky and Haplochlaenius costiger (Chaudoir), respectively], although other species with intermediate δ13C values likely depended on both. The latter group of species comprised mostly two dominant genera (Carabus and Synuchus). Although congeners might have similar feeding habits, the stable isotope ratios indicated trophic niche differences between adults of different species and between adults and larvae of the same genus.

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.