Yoichi Yusa

Predatory Potential of Freshwater Animals on an Invasive Agricultural Pest, the Apple Snail Pomacea canaliculata (Gastropoda: Ampullariidae), in Southern Japan

The apple snail Pomacea canaliculata is an invasive species and a serious pest of rice in many Asian countries. We studied predatory activities of various animals living in Japanese freshwater habitats, by keeping each individual of a potential predator species with 36 snails of various sizes for three days in the aquarium. Forty-six species were tested, and 26 in eight classes fed on small snails. A species of leech, crabs, the common carp, turtles, the mallard duck and the Norway rat attacked even adult snails of 20–30 mm in shell height. These findings will be helpful in identifying effective predators for biological control of the pest snail. In addition, most of the animals attacking snails are reported to be common in rivers or ponds, but few live in modernized paddy fields having little connections with natural water systems. This may be a reason why this snail maintains large populations in paddy fields but not in other freshwater habitats.

Density-dependent growth and reproduction of the apple snail, Pomacea canaliculata: a density manipulation experiment in a paddy field

To examine density dependence in the survival, growth, and reproduction of Pomacea canaliculata, we conducted an experiment in which snail densities were manipulated in a paddy field. We released paint-marked snails of 15–20 mm shell height into 12 enclosures (pens) of 16 m2 at one of five densities – 8, 16, 32, 64, or 128 snails per pen. The survival rate of released snails was 95% and was independent of snail density. The snail density had a significant effect on the growth and egg production of individual snails. This density dependence may have been caused by reduced food availability. The females at high density deposited fewer and smaller egg masses than those at low density, and consequently produced fewer eggs. The females at densities 8 and 16 deposited more than 3000 eggs per female, while the females at density 128 oviposited only 414 eggs. The total egg production per pen was, however, higher at higher snail density. The survival rates of juvenile snails were 21%–37% and were independent of adult density. The juvenile density was positively correlated with the total egg production per pen and hence was higher at higher adult density. However, the density of juveniles larger than 5 mm in shell height, i.e., juveniles that can survive an overwintering period, was not significantly different among density treatments. These results suggest that snail density after the overwintering period is independent of the density in the previous year. Thus, density dependence in growth and reproduction might regulate the population of P. canaliculata in paddies.

Insights from an Integrated View of the Biology of Apple Snails (Caenogastropoda: Ampullariidae)

ABSTRACT Apple snails (Ampullariidae) are among the largest and most ecologically important freshwater snails. The introduction of multiple species has reinvigorated the field and spurred a burgeoning body of research since the early 1990s, particularly regarding two species introduced to Asian wetlands and elsewhere, where they have become serious agricultural pests. This review places these recent advances in the context of previous work, across diverse fields ranging from phylogenetics and biogeography through ecology and developmental biology, and the more applied areas of environmental health and human disease. The review does not deal with the role of ampullariids as pests, nor their control and management, as this has been substantially reviewed elsewhere. Despite this large and diverse body of research, significant gaps in knowledge of these important snails remain, particularly in a comparative framework. The great majority of the work to date concerns a single species, Pomacea canaliculata, which we see as having the potential to become a model organism in a wide range of fields. However, additional comparative data are essential for understanding this diverse and potentially informative group. With the rapid advances in genomic technologies, many questions, seemingly intractable two decades ago, can be addressed, and ampullariids will provide valuable insights to our understanding across diverse fields in integrative biology.

Adaptive evolution of sexual systems in pedunculate barnacles

How and why diverse sexual systems evolve are fascinating evolutionary questions, but few empirical studies have dealt with these questions in animals. Pedunculate (gooseneck) barnacles show such diversity, including simultaneous hermaphroditism, coexistence of dwarf males and hermaphrodites (androdioecy), and coexistence of dwarf males and females (dioecy). Here, we report the first phylogenetically controlled test of the hypothesis that the ultimate cause of the diverse sexual systems and presence of dwarf males in this group is limited mating opportunities for non-dwarf individuals, owing to mating in small groups. Within the pedunculate barnacle phylogeny, dwarf males and females have evolved repeatedly. Females are more likely to evolve in androdioecious than hermaphroditic populations, suggesting that evolution of dwarf males has preceded that of females in pedunculates. Both dwarf males and females are associated with a higher proportion of solitary individuals in the population, corroborating the hypothesis that limited mating opportunities have favoured evolution of these diverse sexual systems, which have puzzled biologists since Darwin.

A snail with unbiased population sex ratios but highly biased brood sex ratios

Extraordinary sex ratio patterns and the underlying sex–determining mechanisms in various organisms are worth investigating, particularly because they shed light on adaptive sex–ratio adjustment. Here, we report an extremely large variation in the brood sex ratio in the freshwater snail, Pomacea canaliculata. In eight rearing series originating from three wild populations, sex ratios were highly variable among broods, ranging continuously from almost exclusively males to almost exclusively females. However, sex ratios were similar between broods from the same mating pair, indicating that sex ratio is a family trait. Irrespective of the large variations, the average sex ratios in all rearing series were not significantly different from 0.5. We argue that Fishers adaptive sex–ratio theory can explain the equal average sex ratios, and the results, in turn, directly support Fishers theory. Polyfactorial sex determination (in which sex is determined by three or more genetic factors) is suggested as the most likely mechanism producing the variable brood sex ratio.

Predator-driven biotic resistance and propagule pressure regulate the invasive apple snail Pomacea canaliculata in Japan.

Species richness in local communities has been considered an important factor determining the success of invasion by exotic species (the biotic resistance hypothesis). However, the detailed mechanisms, especially the role of predator communities, are not well understood. We studied biotic resistance to an invasive freshwater snail, Pomacea canaliculata, at 31 sites in an urban river basin (the Yamatogawa) in western Japan. First, we studied the relationship between the richness of local animal species and the abundance of P. canaliculata, demonstrating a negative relationship, which suggests that the intensity of biotic resistance regulates local snail populations. This pattern was due to the richness of native predator communities rather than that of introduced species or non-predators (mainly competitors of the apple snail). Local snail abundance was also affected by immigration of snails from nearby rice fields (i.e. propagule pressure), where few predators occur. Second, we assessed short-term predation pressure on the snail by means of a tethering experiment. Predation pressure was positively correlated with the number of individual predators and negatively correlated with snail abundance. The introduced crayfish Procambarus clarkii was responsible for the variance in predation pressure. These results indicate that the predator community, composed of both native and introduced species, is responsible for resistance to a novel invader even in a polluted urban river.

Mating group size and evolutionarily stable pattern of sexuality in barnacles

Barnacles, marine crustaceans, have various patterns of sexuality depending on species including simultaneous hermaphroditism, androdioecy (hermaphrodites and dwarf males), and dioecy (females and dwarf males). We develop a model that predicts the pattern of sexuality in barnacles by two key environmental factors: (i) food availability and (ii) the fraction of larvae that settle on the sea floor. Populations in the model consist of small individuals and large ones. We calculate the optimal resource allocation toward male function, female function and growth for small and large barnacles that maximizes each barnacles lifetime reproductive success using dynamic programming. The pattern of sexuality is defined by the combination of the optimal resource allocations. In our model, the mating group size is a dependent variable and we found that sexuality pattern changes with the food availability through the mating group size: simultaneous hermaphroditism appears in food-rich environments, where the mating group size is large, protandric simultaneous hermaphroditism appears in intermediate food environments, where the mating group size also takes intermediate value, the other sexuality patterns, androdioecy, dioecy, and sex change are observed in food-poor environments, where the mating group size is small. Our model is the first one where small males can control their growth to large individuals, and hence has ability to explain a rich spectrum of sexual patterns found in barnacles.

Dwarf Males of Octolasmis warwickii (Cirripedia: Thoracica): The First Example of Coexistence of Males and Hermaphrodites in the Suborder Lepadomorpha

In the lepadomorph barnacle Octolasmis warwickii, individuals are often found attached to the scutum of conspecifics living externally on the crab hosts. To test whether these conspecific-attached individuals are dwarf males, as are known to occur in other suborders of barnacles, we compared the pattern of attachment, size-frequency distribution, and reproductive status of the conspecific-attached (Con-A) and crab-attached (Crab-A) individuals. Con-As were smaller than Crab-As. There was a positive relationship between the body size of Crab-As and the number of individuals on them. Con-As had longer penises than Crab-As of the same body size, and their testes were better developed. The four largest Con-As examined were brooding eggs. These results indicate that Con-As of O. warwickii are dwarf males, with a potential to become hermaphroditic. This represents the first known example of coexistence of males and hermaphrodites in the suborder Lepadomorpha. The mating group size of O. warwickii was smaller than in its hermaphroditic congeners but larger than in barnacles with dwarf males and females, which supports the current theories that group size is important for the evolution of sexuality patterns in barnacles.

Diverse, Continuous, and Plastic Sexual Systems in Barnacles

Barnacles (Crustacea: Thoracica) show diverse sexual systems, including simultaneous hermaphroditism, androdioecy (hermaphrodites + males), and dioecy (females + males). When males occur, they are always much smaller (called dwarf males) than conspecific hermaphrodites or females. Ever since Darwin made this discovery, many scientists have been fascinated by such diversity. In this study, we provide an overview of (1) the diversity of sexual systems in barnacles, (2) the continuity between different sexual systems in some genera or species, and (3) the plasticity in sexual expression in several species. First, although most barnacles are hermaphroditic, both theoretical and empirical studies suggest that females and dwarf males tend to occur in species with small mating groups. Low sperm competition among hermaphrodites and little chance to act as a male are both associated with small group sizes and identified as the forces promoting the evolution of dwarf males and pure females, respectively. Second, in some groups of barnacles, the distinction between hermaphrodites and dwarf males is unclear because of the potential of dwarf males to become hermaphrodites. As many barnacle species tend toward protandric simultaneous hermaphroditism (develop male function first and then add female function without discarding male function), the dwarf males in such cases are best described as potential hermaphrodites that arrest growth and emphasize male function much earlier because of attachment to conspecifics. This is presumably advantageous in fertilizing the eggs of the host individuals. The distinction between hermaphrodites and females may also be obscured in some species. Third, sex allocation and penial morphology are plastic in some species. We also report the results of a transplanting experiment on small individuals of the pedunculate barnacle Octolasmis angulata, which suggests that individuals transplanted onto conspecifics developed longer and broader penises than did control individuals. Overall, the diversity, continuity, and plasticity in the sexual systems of barnacles are sources of important insights into the evolution and maintenance of the diversity of sexual systems.

Alarm response of hatchlings of the apple snail, Pomacea canaliculata (Gastropoda: Ampullariidae), to aqueous extracts of other individuals

We examined how hatchlings of the freshwater snail, Pomacea canaliculata, responded to aqueous extracts of conspecific hatchlings. Three, 3-day-old hatchlings were macerated in deionized water (1 mg hatchling per 1 ml water). When 0.5 ml of the aqueous extract was added to a test tube containing 10 hatchlings of the same age and 50 ml of water, the hatchlings in the water began to crawl out of the water within 5 min. The proportion of hatchlings that crawled out of the water approached 0.6–0.9 after 1 h, but gradually decreased to 0.4 after 24 h. The relatedness between the live and the macerated hatchlings had no significant influence on the response. Hatchlings of egg masses obtained either in the laboratory or in the wild responded similarly to aqueous extracts of hatchlings from either egg mass. This suggests that the conditions under which the egg masses were incubated or the conditions that their parents had experienced had no effect on the hatchlings’ response. When compared with experiments reported on other aquatic animals, we consider the behavior of the hatchlings to be an alarm response of escaping from predators.