Ryuji Yonekura

Origin and dispersal of bluegill sunfish, Lepomis macrochirus , in Japan and Korea

The bluegill sunfish, Lepomis macrochirus, is a notorious exotic species in many freshwater ecosystems, currently expanding its distribution worldwide. In 1960, a small group of bluegills captured in the Mississippi River at Guttenberg in Iowa were imported to Japan as a gift from the mayor of Chicago to the Japanese government. The offspring of these fish were released into the wild in Japan and also in Korea. Over 40 years after this first introduction, L. macrochirus now occupies all the freshwater ecosystems of both countries. We compared invading populations of L. macrochirus in Japan and Korea with native populations in the USA, using PCR–RFLP (polymerase chain reaction–restricted fragment length polymorphism) analyses of mitochondrial DNA, to estimate the origin and dispersal of L. macrochirus in Japan and Korea. Five haplotypes of mitochondrial DNA detected in Japanese and Korean populations completely coincided with the haplotypes of the Guttenberg population. Haplotype diversity of invading populations was shown to be highest in populations established in the 1960s, while genetic variability was lower in more recently established populations. Our results suggest that all L. macrochirus in Japan and Korea have originated from the 15 fish first introduced in 1960. Low haplotype diversity in newly established populations is probably due to genetic drift arising from repeated population bottlenecks, while the high similarity of haplotypes among neighbouring populations is considered to reflect the history of transplantation by humans.

Trophic polymorphism in introduced bluegill in Japan

We demonstrate that bluegill (Lepomis macrochirus) introduced from their native North American source to Lake Biwa in Japan showed considerable trophic and morphological variations (morphs). Three morphs were found for larger bluegills, specialized in three distinct resources (i.e. plankton, benthic invertebrates and aquatic plant), and two morphs were found for smaller bluegills, specialized in two slightly different prey taxa (i.e. calanoid and cyclopoid plankton). These morphs, especially for the large size class, can be distinguished primarily by differences in midbody length and depth. The dietary specialization and morphological differentiation among individuals were considered to be a result of different requirements for efficient resource utilization, which is a unique example of trophic polymorphism occurring in an introduced fish species in a species-rich fish community.

Species diversity in native fish community in Japan : comparison between non-invaded and invaded ponds by exotic fish

The relationship between invasions by two exotic fishes (Micropterus salmoides and Lepomis macrochirus) and species diversity in native fish communities was studied in 14 Japanese farm ponds. We found that mean number of species in native fish communities was three times higher in the ponds without the exotic fish than in the ponds with them. Further, negative relationships were observed between abundance of the two exotic fish and the total abundance of native fish communities. Our results suggest that invasions by the two exotic fish caused serious depletion of native fish communities, although another process can also be considered , that is, that ponds with poor native fish communities were prone to colonization by these exotic fish.

Genetic and Physiological Characterization of the Intestinal Bacterial Microbiota of Bluegill (Lepomis macrochirus) with Three Different Feeding Habits

Bluegill (Lepomis macrochirus) in Lake Biwa, Japan, feed on benthic invertebrates (benthivorous type), aquatic plants (herbivorous type), and zooplankton (planktivorous type). To evaluate the effect of food on intestinal bacterial microbiota, we characterized and compared the intestinal microbiota of these three types of bluegill in terms of community-level physiological profile (CLPP) and genetic structure. The CLPP was analyzed using Biolog MicroPlates (Biolog, Inc., Hayward, CA, USA), and multivariate analysis of variance revealed that the CLPP of intestinal microbiota differed significantly between any pairs of the three types of bluegill. The genetic profiles were analyzed by temperature gradient gel electrophoresis of polymerase chain reaction (PCR)-amplified 16S rDNA fragments, and multidimensional scaling indicated the existence of specific intestinal bacterial structures for both the benthivorous and the planktivorous types. These results suggest that the hosts feeding habit can be one factor controlling the intestinal microbiota of fish in the natural environment.

A peculiar relationship between genetic diversity and adaptability in invasive exotic species: bluegill sunfish as a model species

A peculiar relationship exists between population genetics and invasion biology. Introduced populations often suffer a depletion of genetic variation, but they can persist and adapt to new environments. Here, we show that this relationship is observed in bluegill sunfish (Lepomis macrochirus), an invasive exotic fish in Japan. Genetic analysis using selectively neutral genetic markers reconfirmed that the bluegill introduced into Japan from the United States in 1960 had a single origin with only 15 founders. The analysis also shows that in the process of range expansion, the introduced bluegills experienced severe depletion of genetic diversity due to the founder effect and/or genetic drift. Despite such a decline in genetic diversity, the bluegill populations exhibited a divergent feeding morphology in response to the colonized environments. Such a morphological divergence can facilitate prey exploitation, thereby causing a greater negative impact on native prey resources. Further, in a trophically polymorphic bluegill population in Lake Biwa, physiological characteristics and genetic structures of the intestinal bacterial communities were associated with the difference in diet among the trophic morphs in the host bluegill population. This empirical evidence suggests that despite the severe decline in genetic diversity, the introduced bluegill populations rapidly adapted to the new environment and formed diverse functional relationships with the native bacterial community. Thus, these findings suggest that genetic variation at selectively neutral markers does not always predict adaptability and invasiveness in introduced populations.

Trophic polymorphism in bluegill sunfish (Lepomis macrochirus) introduced into Lake Biwa: evidence from stable isotope analysis

Trophic polymorphism was recently reported in introduced bluegill (Lepomis macrochirus) in Lake Biwa, Japan, where three morphs are specialized in benthic invertebrates (benthivorous type), submerged aquatic plants (herbivorous type), and zooplankton (planktivorous type). We evaluated the long-term effects of food resource utilization by these trophic morphs using stable isotope ratios, δ15N and δ13C. A significant difference in δ15N was found between the benthivorous and planktivorous types. The planktivorous type had the higher δ15N value, which corresponded with the value expected from its prey, zooplankton. The lower δ15N value of the benthivorous type would be derived from the lower δ15N values of benthic prey organisms compared to zooplankton. These results support previous findings that the benthivorous and planktivorous types have different food resource utilization. In contrast, the δ15N and δ13C values of the herbivorous type were distinctly different from the expected values, indicating that this type was unlikely to utilize aquatic plants substantially, contradicting the results of the dietary analysis.

Stress response to daily temperature fluctuations in common carp, Cyprinus carpio L.

The littoral zone of lakes and lagoons is often used by fish for feeding or reproduction. However, the large changes in temperature that are typical of natural environments, including the littoral zone, represent a potential stressor for fish. Despite the importance of this habitat, little is known about the effect of daily temperature fluctuations on the stress responses of fish. We monitored daily temperature changes in the near-shore and offshore regions of a natural lagoon between May and July 2008–2010. We observed large temperature fluctuations more frequently in the near-shore zone than the offshore zone. We then exposed common carp (Cyprinus carpio) to a temperature regime similar to that observed in the near-shore zone and measured the levels of cortisol released into the water. The rate of cortisol release increased when carp were exposed to an increase in temperature of ~0.6°C/h over a 5-h period. Conversely, there was no change in the rate of release when temperatures decreased. Our results highlight the importance of maintaining high temporal resolution when evaluating the stress response to daily fluctuations temperature.

The role of propagule pressure in the invasion success of bluegill sunfish, Lepomis macrochirus, in Japan

The bluegill sunfish, Lepomis macrochirus, is a widespread exotic species in Japan that is considered to have originated from 15 fish introduced from Guttenberg, Iowa, in 1960. Here, the genetic and phenotypic traits of Japanese populations were examined, together with 11 native populations of the USA using 10 microsatellite markers and six meristic traits. Phylogenetic analysis reconfirmed a single origin of Japanese populations, among which populations established in the 1960s were genetically close to Guttenberg population, keeping high genetic diversity comparable to the ancestral population. In contrast, genetic diversity of later‐established populations significantly declined with genetic divergence from the ancestral population. Among the 1960s established populations, that from Lake Biwa showed a significant isolation‐by‐distance pattern with surrounding populations in which genetic bottlenecks increased with geographical distance from Lake Biwa. Although phenotypic divergence among populations was recognized in both neutral and adaptive traits, PST–FST comparisons showed that it is independent of neutral genetic divergence. Divergent selection was suggested in some populations from reservoirs with unstable habitats, while stabilizing selection was dominant. Accordingly, many Japanese populations of L. macrochirus appear to have derived from Lake Biwa population, expanding their distribution with population bottlenecks. Despite low propagule pressure, the invasion success of L. macrochirus is probably because of its drastic population growth in Lake Biwa shortly after its introduction, together with artificial transplantations. It not only enabled the avoidance of a loss in genetic diversity but also formed a major gene pool that supported local adaptation with high phenotypic plasticity.

Phylogeography of the Bluegill Sunfish, Lepomis macrochirus, in the Mississippi River Basin

The Mississippi River Basin supports the richest fish fauna in eastern North America and has played a key role in the maintenance of fish biodiversity, especially as a refuge for freshwater fishes during glaciations. In this study, we investigated the phylogeography of the bluegill sunfish, Lepomis macrochirus, in eastern North America, using complete sequence of the mitochondrial ND1 gene from 369 samples collected at 15 sites. Phylogenetic analysis revealed two major lineages (northern and southern clades) in a parsimony network. A sympatric distribution of the lineages was widely observed in the Mississippi Basin. Sequence diversity in the two lineages was significantly lower in glaciated regions around the Great Lakes than in unglaciated regions. The two lineages were estimated to have diverged in the Kansan glaciation, and refugia for both existed around the Ouachita Highlands. The southern clade dispersed during the Yasmouth Interglacial, prior to the dispersal of the northern clade during the Sangamon Interglacial. In the northern clade, low genetic diversity and population fragmentation inferred by nested clade analysis (NCA) were considered due to bottleneck events in the Wisconsin glaciation, while the southern clade showed isolation by distance in a Mantel test. A difference in demographic fluctuation suggests that sympatry of the two lineages has resulted from recent secondary admixture through the range expansion of the northern clade in the post-Pleistocene. Large-scale admixture of multiple mtDNA lineages in L. macrochirus, which has not been recorded in other fishes in the Mississippi River Basin, may result from their high vagility.

Environment-KHV-carp-human linkage as a model for environmental diseases

To predict outbreaks of infectious disease and to prevent epidemics, it is essential not only to conduct pathological studies but also to understand the interactions between the environment, pathogen, host and humans that cause and spread infectious diseases. Outbreaks of mass mortality in carp caused by Cyprinid herpesvirus 3 (CyHV-3), formerly known as koi herpesvirus (KHV), disease have occurred worldwide since the late 1990s. We proposed an environment–KHV–carp–human linkage as a conceptual model for “environmental diseases” and specify research subjects that might be necessary to construct and shape this linkage.