Decline of unionid mussels enhances hybridisation of native and introduced bitterling fish species through competition for breeding substrate

1. Bitterling fishes (Subfamily: Acheilognathinae) spawn in the gills of living freshwater mussels and obligately depend on the mussels for reproduction. On the Matsuyama Plain, Japan, populations of unionid mussels—Pronodularia japanensis, Nodularia douglasiae, and Sinanodonta lauta—have decreased rapidly over the past 30 years. Simultaneously, the population of a native bitterling fish, Tanakia lanceolata, which depends on the three unionids as a breeding substrate, has decreased. Furthermore, a congeneric bitterling, Tanakia limbata, has been artificially introduced, and hybridisation and genetic introgression occur between them. Here, we hypothesised that decline of the unionids has enhanced this invasive hybridisation through competition for the breeding substrate.
2. Three study sites were set in three streams on the Matsuyama Plain. We collected adult bitterling fishes (native T. lanceolata, introduced T. limbata, and foreign Rhodeus ocellatus ocellatus) once a week from April to October 2013 to measure their densities in streams and to examine seasonal differences in female ovipositor length, which elongates in the breeding season. Simultaneously, we set quadrats and captured unionids and measured environmental conditions. Each unionid individual was kept separately in its own aquarium to collect ejected bitterling eggs/larvae. Tanakia eggs and larvae were genotyped using six microsatellite markers and the mitochondrial cytochrome b gene.
3. Introduced T. limbata was more abundant, had a longer breeding period, and produced more juveniles than native T. lanceolata. Hybrids between the two species occurred at all sites, and in total 101 of the 837 juveniles genotyped were hybrids. The density of P. japanensis was low, at most 0.42 individuals/m². Nodularia douglasiae and S. lauta have nearly or totally disappeared from these sites. Hybrid clutches of Tanakia species occurred more frequently where the local density of P. japanensis was low. Mussels were apparently overused and used simultaneously by three species of bitterlings.
4. Decline of freshwater unionid populations has enhanced hybridisation of native and invasive bitterling fishes through increasing competition for breeding substrate. We showed that rapid decline of host mussel species and introduction of an invasive congener have interacted to cause a rapid decline of native bitterling fish.
5. Degradation of habitat and the introduction of invasive species interact to cause a cascade of extinctions in native species. In our study, obligate parasite species are threatened because the host species are disappearing, which means there is a serious threat of coextinction.

     

The costs and benefits in an unusual symbiosis: experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe

Interspecific symbiotic relationships involve a complex network of interactions, and understanding their outcome requires quantification of the costs and benefits to both partners. We experimentally investigated the costs and benefits in the relationship between European bitterling fish (Rhodeus sericeus) and freshwater mussels that are used by R. sericeus for oviposition. This relationship has hitherto been thought mutualistic, on the premise that R. sericeus use mussels as foster parents of their embryos while mussels use R. sericeus as hosts for their larvae. We demonstrate that R. sericeus is a parasite of European mussels, because it (i) avoids the cost of infection by mussel larvae and (ii) imposes a direct cost on mussels. Our experiments also indicate a potential coevolutionary arms race between bitterling fishes and their mussel hosts; the outcome of this relationship may differ between Asia, the centre of distribution of bitterling fishes, and Europe where they have recently invaded.     

A possible evolutionary lag in the relationship between freshwater mussels and European bitterling

The coevolutionary dynamics between European bitterling Rhodeus amarus and freshwater unionid mussels, which the former parasitize by laying eggs on their gills, were tested. In a series of experiments fish preferences and mussel responses were compared in parasites and hosts of recent (Europe) and ancient (Asia) sympatry. Rhodeus amarus readily oviposited on the gills of all mussel species tested. Fish that laid their eggs on the gills of Asian Anodonta woodiana, however, suffered a dramatic reduction in reproductive success compared to fish that oviposited on the gills of European mussels: Unio pictorum , Unio tumidus , Anodonta anatina and Anodonta cygnea . This difference was the result of egg ejection behaviour by mussels rather than the unsuitability of the internal gill environment for European bitterling embryo development. The ejection response of mussels with a long sympatry with European bitterling was considerably more pronounced than that of mussels with a substantially shorter sympatry. The data support a coevolutionary arms race between bitterling and mussels and point to an evolutionary lag in the relationship between R. amarus and its European mussel hosts.     

No evidence for host specialization or host-race formation in the European bitterling (Rhodeus amarus), a fish that parasitizes freshwater mussels

Coevolutionary relationships between parasites and hosts can elevate the rate of evolutionary changes owing to reciprocal adaptations between coevolving partners. Such relationships can result in the evolution of host specificity. Recent methodological advances have permitted the recognition of cryptic lineages, with important consequences for our understanding of biological diversity. We used the European bitterling (Rhodeus amarus), a freshwater fish that parasitizes unionid mussels, to investigate host specialization across regions of recent and ancient sympatry between coevolving partners. We combined genetic data (12 microsatellite and 2 mitochondrial markers) from five populations with experimental data for possible mechanisms of host species recognition (imprinting and conditioning). We found no strong evidence for the existence of cryptic lineages in R. amarus, though a small proportion of variation among individuals in an area of recent bitterling–mussel association was statistically significant in explaining host specificity. No other measures supported the existence of host‐specific lineages. Behavioural data revealed a weak effect of conditioning that biased behavioural preferences towards specific host species. Host imprinting had no effect on oviposition behaviour. Overall, we established that populations of R. amarus show limited potential for specialization, manifested as weak effects of host conditioning and genetic within‐population structure. Rhodeus amarus is the only species of mussel‐parasitizing fish in Europe, which contrasts with the species‐rich communities of bitterling in eastern Asia where several host‐specific bitterling occur. We discuss costs and constraints on the evolution of host‐specific lineages in our study system and more generally.     

Phylogeny, host-parasite relationship and zoogeography

Phylogeny is the evolutionary history of a group or the lineage of organisms and is reconstructed based on morphological, molecular and other characteristics. The genealogical relationship of a group of taxa is often expressed as a phylogenetic tree. The difficulty in categorizing the phylogeny is mainly due to the existence of frequent homoplasies that deceive observers. At the present time, cladistic analysis is believed to be one of the most effective methods of reconstructing a phylogenetic tree. Excellent computer program software for phylogenetic analysis is available. As an example, cladistic analysis was applied for nematode genera of the family Acuariidae, and the phylogenetic tree formed was compared with the system used currently. Nematodes in the genera Nippostrongylus and Heligmonoides were also analyzed, and the validity of the reconstructed phylogenetic trees was observed from a zoogeographical point of view. Some of the theories of parasite evolution were briefly reviewed as well. Coevolution of parasites and humans was discussed with special reference to the evolutionary relationship between Enterobius and primates.     

An indirect effect of biological invasions: the effect of zebra mussel fouling on parasitisation of unionid mussels by bitterling fish

Invasive species represent a major threat with both direct and indirect effects on natural ecosystems, including effects on established and coevolved relationships. In a series of experiments, we examined how the interaction between two native species, a unionid mussel (Unio pictorum) and the European bitterling (Rhodeus amarus), a fish that parasitises unionids, was affected by the non-native zebra mussel (Dreissena polymorpha). The zebra mussel fouls hard substrates, including shells of living unionids, and its presence is often associated with a decrease in population density of native unionid mussels. Bitterling lay their eggs into live unionids and the embryos develop inside their gills. Using a range of zebra mussel densities, we demonstrated that zebra mussel fouling had a negative effect on the number of bitterling eggs inside the mussel host, with abundances of 5–10 zebra mussels (shell size 15–25 mm) per unionid critical for bitterling ability to utilise the host. In a further experiment, we found that bitterling did not discriminate between unfouled unionids and those fouled with five zebra mussels. Most ovipositions into fouled hosts, however, were unsuccessful as eggs failed to reach the unionid gills. We discuss implications of such unsuccessful ovipositions for bitterling recruitment and population dynamics.     

云丘山地区灌木群落优势种数量关系

以68个灌木样方的重要值矩阵和2×2列联表为基础,结合实地调查,应用方差比率法、χ2检验、Pearson相关系数及Spearman秩相关系数法,对云丘山地区灌木群落的20个优势种、190个种对的关联性进行了定量研究。方差比率法结果表明,20个优势种总体间关联为显著正相关,云丘山地区的灌木群落处于较稳定的状态;χ2检验、Pearson相关系数、Spearman秩相个关系数结果表明,大部分种对的种间关联未达到显著程度,种间联结较为松散,群落结构及其种类组成将逐渐趋于完善和稳定;根据这20个优势种对环境的适应方式和主导生态因素辅助以PCA排序,可将它们划分为两种生态种组。以上结果揭示了该地区主要优势物种与环境的相互关系。     

入侵种西花蓟马与其它昆虫的种间竞争

西花蓟马Frankliniella occidentalis作为一种重要的入侵害虫,在全球范围的入侵过程中,为获取更多资源以建立自己的种群,势必会和处于同一营养级的昆虫发生种间竞争。本文对近年来有关西花蓟马与其它种蓟马、粉虱及叶螨等昆虫种间竞争的研究进行了综述,分析了温度、CO 2、寄主植物、农药和天敌等主要因素在竞争取代中的作用,并对今后的研究方向以及种间竞争的研究方法进行了讨论,以期为揭示西花蓟马在我国的种群动态和变化规律奠定基础。     

Density‐dependent effects of non‐native brown trout Salmo trutta on the species–area relationship in stream fish assemblages

The spatial scale and density‐dependent effects of non‐native brown trout Salmo trutta on species richness of fish assemblages were examined at 48 study sites in Mamachi Stream, a tributary of Chitose River, Hokkaido, Japan. The density of age ≥1 year S. trutta was high in the upstream side of the main stem of Mamachi Stream. Fish species richness increased with increasing area of study sites (habitat size), but the increasing magnitude of the species richness with area decreased with increasing age of ≥1 year S. trutta density. The relationships between age ≥1 year S. trutta, however, and presence–absence of each species seemed to be different among species. Species richness was also determined by location and physical environmental variables, i.e. it was high on the downstream side and in structurally complex environments.     

天龙山木本群落种间关系的研究

采用χ^2检验方法和相关分析等方法对山西天龙山木本植物群落进行了种间关系分析．结果表明木本植物群落的种间关系以正相关为主,但是负关联的比重也较大,而且还有一定的独立格局存在,表明物种间的关系不大稳定,群落正处于发展演替之中,同时也表明物种对环境资源的竞争并不激烈,物种资源比较丰富。     

Convict cichlids benefit from close proximity to another species of cichlid fish

The coexistence of species with overlapping resource use is often thought to involve only negative fitness effects as a consequence of interspecific competition. Furthermore, the scarce empirical research on positive species interactions has predominantly focused on sessile organisms. Here, I experimentally assessed the effect of close proximity of a potential brood predator and competitor on reproductive success of a neotropical cichlid fish. I demonstrate that convict cichlid (Archocentrus nigrofasciatus) broods have a higher survival rate near territories of the Nicaragua cichlid (Hypsophrys nicaraguensis), and that escape from predation and nest takeovers is the most likely explanation for the decreased offspring mortality.     

草地物种多样性对群落可入侵性影响的研究进展

综述草地群落入侵实验中物种多样性和群落可入侵性关系的研究进展。目前物种多样性与群落可入侵性主要出现了对立的关系模式,被普遍接受的解释机制为尺度依赖。但其它研究中出现了更为复杂的关系,提出物种特性、植物更新、种间关系变化和群落构建机制等其它因素可能是导致物种多样性与群落可入侵性出现复杂关系的原因。建议未来研究中应注意的几个问题,即物种多样性与群落可入侵性关系在不同营养级适用性,与群落构建机制变化间的联系和时间尺度对物种多样性与群落可入侵性关系的影响。     

Indirect interactions between two aphid species in relation to ant attendance

The influence of foraging by the ant, Lasius niger, on the population growth of two aphid species, Lachnus tropicalis and Myzocallis kuricola, on chestnut trees, Castanea crenata, was examined. The ant-tending effect was divergent depending on the aphid density per ant: it was positive when there were few aphids per ant, but negative when there were many aphids per ant. In addition, the density of one aphid species also influenced the ant-tending effect on the other aphid. Furthermore, the influences were asymmetrical: an increase in L. tropicalis density per ant reversed the ants effect on this species and on M. kuricola, while an increase in M. kuricola per ant did not significantly influence the ants effect on L. tropicalis. Thus, the ant seems to stabilize the L. tropicalis population density and keep this species from extinction, while the ants effect on M. kuricola depends on the density of L. tropicalis and may lead M. kuricola to extermination. This change in the ant-tending effect corresponds to the previously detected density-dependent change in predation activity of the ants on aphids. In contrast, the density-dependent change in the protection effect of the ants against natural enemies does not explain the results.     

凉水保护区红松与主要伴生树种的空间关系

空间关系是影响森林生长与群落演替的重要因素,种间关系是其重要组成部分,研究空间关系有利于了解森林群落的生长更新、功能作用与演替进程。利用移动窗口法对凉水自然保护区10.4 hm²样地不同径级的红松与主要伴生树种做空间相关性研究,并进行多尺度比较,得到不同尺度下不同径级红松与主要伴生树种个体的空间关系特征。研究结果表明:(1)红松与伴生树种的相互关系复杂多样,多种相互关系并存,表现出阔叶红松林群落结构的复杂性与稳定性。大径级红松压制同径级伴生树种,二者呈极显著负相关,但其对小径级伴生树种有庇荫作用,二者呈极显著正相关。(2)红松与主要伴生树种的相互关系在不同尺度、径级上均有极显著差异。尺度越大,红松与主要伴生树种的相关系数变化速率越小;伴生树种的径级越大,红松与主要伴生树种的相关系数变化速率越大。(3)红松与伴生树种的相关性具有尺度特征,主要表现在大尺度(≥60 m)范围上,在小尺度(＜60 m)上相关性较弱。红松与伴生树种在相同径级与不同径级的结合方式上表现出不同的空间关系。同径级的红松与伴生树的种间关系多表现为负相关,不同径级的红松与伴生树种种间关系多表现为正相关。(4)以种间关系确定样方最小面积,凉水保护区临界样地面积为60 m×60 m。该研究集中于不同尺度下不同径级的红松与伴生树种的种间关系,解释优势种红松与伴生树种在森林的空间关系以及群落结构特征,为东北地区阔叶红松林的森林管理提供参考意见。     

Evidence of phenotypic plasticity in the response of unionid mussels to turbidity

1. Increases in total suspended solids (TSS) reduce feeding and reproductive success of unionid mussels, but mussels in turbid rivers are less affected than those in clear rivers, probably due to differences in gill and palp morphology. This study was designed to determine whether the differences observed between adult mussels in populations from turbid versus clear rivers are due to phenotypic plasticity.
2. Parasitic larvae (glochidia) of Lampsilis siliquoidea (Fatmucket) obtained from a low turbidity river (TSS < 5 mg/L) were transformed on Ambloplites rupestris (Rock Bass) in the laboratory to obtain juvenile mussels for rearing under clear and turbid conditions in the laboratory (i.e. nominally 0 versus 50 mg/L suspended river sediment). Juveniles obtained were reared under these contrasting conditions until age 3–4 weeks, when they were examined in a feeding experiment under a range of TSS concentrations (0, 5, 10, 15, 20, 25 mg/L).
3. The clearance rate (volume cleared of particles per unit time) of algae by juveniles from both rearing conditions was similar for the no-TSS control and declined with increased TSS. The rate of decline was, however, lower in the group reared under turbid conditions, which is consistent with reports for adult mussels.
4. Our results indicate that differences in the clearance rate response to high TSS observed in mussels in clear and turbid rivers are probably driven in part by phenotypic plasticity. This finding provides a mechanism to explain how freshwater mussels thrive under turbid conditions as well as informs conservation efforts involving reintroduction of mussels in this highly imperilled taxon.

     

芦芽山植物群落种间关系的研究

通过采用 2× 2列联表的 Fisher精确检验、Pearson相关分析和 Sperman秩相关分析等方法对芦芽山植物群落的种间关系进行了分析。结果表明 ,研究物种关联程度大小时 ,Sperman检验的灵敏性要高于 Pearson相关 ,使用 Sperman秩相关分析得出的结果较好 ,分层对种间关联性进行的研究发现 ,极显著相关和显著相关种对多发生于各层的优势种及次优势种间 ,并依层次不同而不同 ,其中草本层极显著相关种对最多 ,灌木层次之 ,乔木层最少     

Genetic relationship between parasitized and non-parasitized Haloxyion ammodendron in the Alxa Desert

Haloxylon ammodendron (C. A. Mey.) Bunge is a host for the holoparasitic plant Cistanche deserticola Y. C. Ma, the original source of medicinal material known as Herba Cistanchis. The inter-simple sequence repeat marker was used to assess the genetic variations and relationships among six accessions of H. ammodendron with a total of 120 individuals collected from three localities in the Alxa Desert, Inner Mongolia, China. At each locality, individuals both parasitized (PP) by C. deserticola and non-parasitized (NP) were sampled. The results showed that Nei's gene diversity and Shannon's index of PP accessions were higher, but were not significantly different, from those of NP accessions. An unweighted pair-group method arithmetic average dendrogram showed two clusters, one that included all PP accessions, and the other the NP accessions. Genetic differentiation therefore existed between PP and NP accessions, which might be attributed to low gene flow between the NP and PP groups (Nm< 1). However, the relationship between genetic distance and geographic distance within each group, although not statistically significant in this study, might be associated with high gene flow in both the NP and PP groups.     

Presence of an invasive species reverses latitudinal clines of multiple traits in a native species

Understanding the processes driving formation and maintenance of latitudinal clines has become increasingly important in light of accelerating global change. Many studies have focused on the role of abiotic factors, especially temperature, in generating clines, but biotic factors, including the introduction of non‐native species, may also drive clinal variation. We assessed the impact of invasion by predatory fire ants on latitudinal clines in multiple fitness‐relevant traits—morphology, physiological stress responsiveness, and antipredator behavior—in a native fence lizard. In areas invaded by fire ants, a latitudinal cline in morphology is opposite both the cline found in museum specimens from historical populations across the species’ full latitudinal range and that found in current populations uninvaded by fire ants. Similarly, clines in stress‐relevant hormone response to a stressor and in antipredator behavior differ significantly between the portions of the fence lizard range invaded and uninvaded by fire ants. Changes in these traits within fire ant‐invaded areas are adaptive and together support increased and more effective antipredator behavior that allows escape from attacks by this invasive predator. However, these changes may mismatch lizards to the environments under which they historically evolved. This research shows that novel biotic pressures can alter latitudinal clines in multiple traits within a single species on ecological timescales. As global change intensifies, a greater understanding of novel abiotic and biotic pressures and how affected organisms adapt to them across space and time will be central to predicting and managing our changing 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.