Structure of the ovipositor and ovary and the features of reproduction in Amur bitterling <Emphasis Type="Italic">Rhodeus sericeus</Emphasis> (Cyprinidae: Acheilognatinae)

Biological characteristics of sexually mature individuals of Amur bitterling Rhodeus sericeus from the Amur River basin are described. Sexual maturity is reached in the first year of life in males and in the second year in females. The development of ovipositors is observed during sexual maturation of the females and their preparation to spawning. The base of the ovipositor is formed by the conical organ. Based on the structure of the conical organ, including a special distribution of collagenous and muscular fibrils, well developed blood system, and numerous mucous cells in the internal epithelial layer, this organ is used for temporal storage of oocytes during the spawning period and for their movement along the ovipositor. Owing to a well developed net of blood vessels, presence of muscular wall, and numerous collagenous fibrils in the connective tissue, a stable position of the ovipositor is reached during the spawning. Based on secretion of numerous mucous cells of the external epithelial layer of the ovipositor, this organ is inserted into the excretory siphon of the mollusk during egg deposition. The spawning in Amur bitterling is in batches, and it is multiple. The oocytes of three generations can be seen in the ovary. The oocyte possesses a thin zona radiata. Based on the presence of a dense gelatinous layer in the basal part of the chorion, the egg is attached to the internal hemibranches of bivalves. The observations of free embryos of Amur bitterling in the left internal hemibranches of bivalves Sinanodonta likharevi, Nodularia amurensis, N. schrencki, and N. middendorffi show that the symbiotic relationships can be characterized as obligate.     

Comparison of biology of the Sakhalin sturgeon, Amur sturgeon, and kaluga from the Amur River, Sea of Okhotsk, and Sea of Japan biogeographic Province

Three Acipenseridae species live in the rivers and marine waters of the Khabarovsk Territory, Russia: Sakhalin sturgeon, Acipenser mikadoi, Amur sturgeon, A. schrenckii, and kaluga, Huso dauricus. We review the general biology and life history of each species, including their historic and current distributions, and examine current paleogeographic theories to outline the possible origin and evolution of these three species in the Amur River, Sea of Okhotsk, and Sea of Japan biogeographic province. Apparently, these species have evolved during distinct geologic time periods, which has reinforced the reproductive isolation of these species although hybridization does occur. They have convergently adapted to the unique environmental conditions of the Amur River and Russian Maritime regions, and yet developed behavioral adaptations to reduce competition between species. Sakhalin sturgeon is the least studied species among anadromous sturgeon in the world. This species is highly migratory and spends the majority of its life in the ocean only returning to natal rivers to spawn. Amur sturgeon and kaluga are distributed throughout the Amur River basin and the estuary and share many life history traits. They are both represented by distinct morphs. Additionally, we present size and weight relationships to estimate the growth of Amur sturgeon and kaluga. All three species have suffered declines in abundance due to over fishing and their contemporary distributions have contracted compared to their historic ranges. We identify gaps in knowledge and suggest further research useful for guiding management of each species.     

Predicting distributions of seven bitterling fishes in northern Kyushu,Japan

The distributions of seven bitterling species and subspecies—Tanakia lanceolata, T. limbata, Acheilognathus tabira nakamurae, A. rhombeus, Rhodeus ocellatus kurumeus, R. ocellatus ocellatus, and R. atremius atremius—in northern Kyushu were predicted using generalized linear models (GLMs) in order to provide information helpful for conserving native bitterlings and preventing the expansion of alien bitterling species. Predictions were made according to the following procedure: (1) a set of GLMs for each species was formulated using environmental data from 710 sites that were derived using digital maps and GIS software, from which the best fit model for each species was selected using the Akaike information criterion for predicting the fish occurrence, (2) model performance was evaluated based on the receiver-operating characteristics (ROC) analysis using occurrence and environmental data from 362 sites, and (3) potential distributions of the bitterling were analyzed using the best fit models and environmental data for 1,272 sites, of which 200 data points without occurrence data were prepared. The best fit models revealed that 4–6 environmental factors were important in predicting seven bitterling distributions, which was supported by the area under the ROC curve (AUC) values of these fishes ranging from 0.753 to 0.927. The AUC values in model evaluation were significantly greater than 0.5 for six fishes, suggesting the moderate accuracies of these best fit models for predicting the fish distributions. These predictive models can be used for evaluating potential native bitterling richness and the potential distribution expansion of an alien subspecies.     

The use of microsatellite loci for identification of sturgeon species (Acipenseridae) and hybrid forms

The genetic polymorphism of ten sturgeon species that inhabit the territory of the Russian Federation (Russian sturgeon, Siberian sturgeon, Amur sturgeon, Sakhalin sturgeon, Persian sturgeon, ship sturgeon, sterlet, stellate sturgeon, beluga, and kaluga) was examined at five microsatellite loci (Afug41, Afug51, An20, AoxD161, AoxD165) (in total, 3821 individuals). The examined loci were successfully amplified with the same primer set in all species tested and demonstrated a high level of variation. Alleles specific to different species have been identified, which allows them to be used to identify species of sturgeon and their food products. In addition, the possibility of identifying hybrid forms was demonstrated. The assignment test performed in the STRUCTURE software program showed a high probability of correctly assigning each individual to its species based on genotyping with five microsatellite loci examined (96–98%, on average). However, for Russian and Persian sturgeon, the rate of proper species assignment was considerably lower (75 and 84%, respectively).

     

Hypoxia tolerance of three native and three alien species of bitterling inhabiting Lake Kasumigaura,Japan

Differences in hypoxia tolerance among three native and three alien bitterling species were examined by means of field surveys and aquarium experiments. I caught fish in minnow traps and measured environmental factors such as dissolved oxygen and current velocity once a month between June and November 2006 at 30 points around Lake Kasumigaura, Japan. In addition, aquarium experiments were carried out to compare aquatic surface respiration thresholds among the bitterling species. Much more individuals of an alien species, Rhodeus ocellatus ocellatus, was caught at the least oxygen range than expected in the field, and showed the highest hypoxia tolerance in the laboratory experiments. Another alien bitterling, Acheilognathus rhombeus, also showed higher hypoxia tolerance than the three native bitterling species. Lake Kasumigaura is well known for eutrophication and water masses with low dissolved oxygen have often been observed there. Differences in hypoxia tolerance among bitterling species might have affected bitterling assemblage structure in Lake Kasumigaura, which is currently characterized by the dominance of R. o. ocellatus.     

Fossil wood of <Emphasis Type="Italic">Sequoioxylon burejense</Emphasis> sp. nov. (Taxodiaceae) from the Upper Cretaceous of the Zeya-Bureya Basin (Russian Far East)

A new species Sequoioxylon burejense Blokhina et M. Afonin (Taxodiaceae), identified on the basis of anatomical features of fossil wood from the Middle Maastrichtian (Upper Cretaceous) of the Zeya-Bureya Basin, Amur Region, Russian Far East, is described. The new species is characterized by mixed anatomical features of the modern representatives of the tribe Sequoieae. Cretaceous wood of Taxodiaceae was found in the Amur Region for the first time.     

Reproductive Ecology and Host Utilization of Four Sympatric Bitterling (Acheilognathinae,Cyprinidae) in a Lowland Reach of the Harai River in Mie,Japan

Bitterling are fishes that use freshwater mussels for oviposition. The reproductive ecology and pattern of mussel utilization of four sympatric species of bitterling, Acheilognathus rhombeus, A. tabira tabira, Tanakia lanceolata, and T. limbata, were investigated in a lowland river with seven sympatric mussel species. Three bitterling species are spring spawners with overlapping spawning seasons. A. rhombeus is an autumn-spawning species and is temporally isolated in its reproduction from the other species. Ovipositor length during oviposition of T. limbata and T. lanceolata was short, while those of A. tabira tabira and A. rhombeus were long. Most T. limbata inhabited near-shore areas, whereas the two other spring-spawning species were distributed across the entire river. All bitterling species used Inversidens brandti, Obovalis omiensis and Inversiunio jokohamensis as spawning hosts, but not the other mussel species available. T. lanceolata, A. tabira tabira and A. rhombeus showed spawning preferences for O. omiensis and I. brandti. However, T. limbata did not show clear preferences for any of the mussel species they used. A. t. tabira showed a significant preference for large I. brandti in offshore areas, while the other spring-spawning bitterling showed a preference for mussels inshore. These results are discussed in the context of reproductive resource partitioning.     

Contribution to the knowledge of the leaf-rollers (Lepidoptera,Tortricidae) of the Lower Amur Area

A list of 94 species of Tortricidae from the Lower Amur Area is presented, 14 species being recorded for Khabarovsk Terr. for the first time. Three species, Endotheina quadrimaculana, Argyroploce arbutella, and Dichrorampha obscuratana, are new to the Russian Far East. Two species monophagous on Quercus, Tortrix sinapina and Hedya inornata, have been found in the relict oak forests of the Lower Amur Area. Individual variation of the male genitalia within the Dichrorampha simpliciana species-group is revealed, and doubts are cast on the species rank of D. cancellatana and D. okui.     

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 zebra mussel (<Emphasis Type="Italic">Dreissena polymorpha</Emphasis>) impacts European bitterling (<Emphasis Type="Italic">Rhodeus amarus</Emphasis>) load in a host freshwater mussel (<Emphasis Type="Italic">Unio pictorum</Emphasis>)

The European bitterling, Rhodeus amarus, is a non-indigenous fish species in British fresh waters. It lays its eggs in unionid mussels which themselves are vulnerable to fouling by the non-indigenous zebra mussel, Dreissena polymorpha. Observations from an unmanipulated natural system showed that only 27% of zebra mussel-fouled Unio pictorum hosted bitterling, while 47% of unfouled U. pictorum hosted bitterling. We conducted a field experiment in the River Great Ouse catchment, Cambridgeshire, England in May–June 2007 and 2008 to quantify the impact of zebra mussels on bitterling load in host mussels. Zebra mussel-fouled unionids were significantly less likely to host bitterling than unfouled unionids. The number of unionids hosting bitterling did not differ significantly whether the zebra mussels fouling the unionid were alive or dead. Bitterling appeared to discriminate against zebra mussel-fouled unionids less as the 2007 breeding season advanced, potentially because preferred unfouled unionids had a higher bitterling load, and were therefore relatively lower quality hosts than at the start of the breeding season.     

FISH-mapping of 18S ribosomal RNA genes and telomeric sequences in the Japanese bitterlings Rhodeus ocellatus kurumeus and Tanakia limbata (Pisces,Cyprinidae) reveals significant cytogenetic differences in morphologically similar karyotypes

The Japanese rose bitterling, Rhodeus ocellatus kurumeus, and the oily bitterling, Tanakia limbata, were cytogenetically studied by silver (Ag)- and chromomycin A₃ (CMA₃)-staining, by C-banding and by mapping of the 18S ribosomal genes and of the (TTAGGG) _n telomeric sequence. These two representative species of related genera of the subfamily Acheilognathinae show very similar chromosome complements. Nevertheless, significant differences in the chromosomal distribution of nucleolus organizer regions (NORs) and interstitial telomeric sequences were observed. Whereas R. ocellatus kurumeus shows a single NOR-bearing chromosome pair, T. limbata is characterized by a higher number of variable NORs. Multiple telomeric sequence sites were found at the pericentromeric regions of several chromosomes in the rose bitterling. No telomeric sequence sites were detected near centromeres, but they were found to be scattered along the NORs in the oily bitterling. Two karyoevolutive trends might have been identified in the subfamily.     

A new host record of <Emphasis Type="Italic">Ichthyoxenus amurensis</Emphasis> (Crustacea: Isopoda: Cymothoidae) from the Amur bitterling <Emphasis Type="Italic">Rhodeus sericeus</Emphasis> (Cypriniformes: Cyprinidae)

Ichthyoxenus amurensis (Crustacea: Isopoda: Cymothoidae) was found in the body cavity of the Amur bitterling, Rhodeus sericeus (Cypriniformes: Cyprinidae), from Primorsky, Russia, in August 2003. A total of 13 individuals of I. amurensis were obtained from nine of 29 fish specimens (prevalence = 31.0%). Rhodeus sericeus is a new host for I. amurensis. In the body cavity of R. sericeus, I. amurensis was found within a thin-walled membranous sac, and the intestines of the host were malformed as a result of infection. There was no significant difference in the standard length of infected and uninfected R. sericeus.     

Fossil wood of Piceoxylon burejense sp. nov. (Pinaceae) from the Upper Cretaceous of Zeya-Bureya Basin, Amur Region (Russian Far East)

A new species, Piceoxylon burejense sp. nov. (Pinaceae), is described from the Middle Maastrichtian (Upper Cretaceous) of the Zeya-Bureya Basin, Amur Region (Russian Far East) based on the fossil wood anatomy. The new species is characterized by a combination of anatomical wood features of the modern genera Picea and Larix. The fossil wood of Pinaceae was found in the Cretaceous deposits of the Amur Region for the first time.     

The lateral line receptor array of cyprinids from different habitats

The lateral line system of teleost fishes consists of an array of superficial and canal neuromasts (CN). Number and distribution of neuromasts and the morphology of the lateral line canals vary across species. We investigated the morphology of the lateral line system in four diurnal European cyprinids, the limnophilic bitterling (Rhodeus sericeus), the indifferent gudgeon (Gobio gobio), and ide (Leuciscus idus), and the rheophilic minnow (Phoxinus phoxinus). All fish had lateral line canals on head and trunk. The total number of both, CN and superficial neuromasts (SN), was comparable in minnow and ide but was greater than in gudgeon and bitterling. The ratio of SNs to CNs for the head was comparable in minnow and bitterling but was greater in gudgeon and ide. The SN‐to‐CN ratio for the trunk was greatest in bitterling. Polarization of hair cells in CNs was in the direction of the canal. Polarization of hair cells in SNs depended on body area. In cephalic SNs, hair cell polarization was dorso‐ventral or rostro‐caudal. In trunk SNs, it was rostro‐caudal on lateral line scales and dorso‐ventral on other trunk scales. On the caudal fin, hair cell polarization was rostro‐caudal. The data show that, in the four species studied here, number, distribution, and orientation of CNs and SNs cannot be unequivocally related to habitat. J. Morphol. 275:357–370, 2014. © 2013 Wiley Periodicals, Inc.     

The reproductive ecology of two subspecies of the bitterling Rhodeus atremius (Cyprinidae, Acheilognathinae)

The reproductive ecology of two endangered subspecies of the bitterling Rhodeus atremius was investigated in two rivers in Okayama and Fukuoka Prefectures, Japan. Several other bitterling species, R. ocellatus, Tanakia limbata, T. lanceolata, Acheilognathus tabira and A. rhombeus, are also found in these rivers. Spawning of both R. atremius subspecies was recorded between late March and August 2007, peaking between April and July. Females of R. atremius began to mature at small body size (minimum 25 mm). They had small clutch sizes (maximum 16 eggs) and developed a short ovipositor (mean 13.6 mm), which was used to deposit a bulb-shaped egg of comparatively large size (3.2 mm³, major and minor axes 2.8 and 1.5 mm). Clutch size, ovipositor length and egg size appear to be a function of female body size. Both the body size and ovipositor length of R. atremius with ripe ova and the size and shape of the eggs varied seasonally. Rhodeus a. suigensis achieved maturity at a smaller body size, had a longer ovipositor and produced smaller eggs, with the minor axis being wider relative to the major axis than those of R. a. atremius. Rhodeus atremius may be adapted for depositing small numbers of eggs in a much shallower position inside the gills of smaller host mussels than other bitterling species.     

A morphological and genetic analysis of the European bitterling species complex

Bitterling fishes lay their eggs on the gills of living freshwater mussels and are valuable models in behavioural and evolutionary ecology. We used morphological and genetic data to resolve the taxonomic relationships of bitterling in Europe. Previous studies have suggested the European bitterling is either a single species with a wide but discontinuous geographic distribution, or a complex of species. Morphometric and meristic data identified differences between three putative species; with a clear distinction between the eastern Asian Rhodeus sericeus, western European bitterling Rhodeus amarus, and colchian bitterling, Rhodeus colchicus. Polymorphism in the mitochondrial DNA control region was predominantly due to insertion/deletion events, making phylogenetic inference difficult, but the single haplotype found in R. sericeus populations was detected at low frequency (one of 24 individuals) in R. amarus and R. colchicus populations. Eight control region haplotypes were found in R. amarus populations, which were distinct from the two haplotypes in a R. colchicus population. Cytochrome b data produced a phylogeny with strongly‐supported differentiation between a clade of two R. sericeus haplotypes and a clade of six R. amarus/colchicus haplotypes. The star‐like topology of the R. amarus/colchicus haplotypes in a minimum spanning network suggested a rapid radiation in this clade. Our results are consistent with an hypothesis of relatively ancient divergence of R. sericeus from R. amarus/colchicus and more recent and rapid differentiation between R. amarus and R. colchicus. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 337–347.     

The role of local adaptation in shaping fish‐mussel coevolution

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Breeding habitat and nest‐site selection by an obligatory “nest‐cleptoparasite”, the Amur Falcon Falco amurensis

The selection of a nest site is crucial for successful reproduction of birds. Animals which re‐use or occupy nest sites constructed by other species often have limited choice. Little is known about the criteria of nest‐stealing species to choose suitable nesting sites and habitats. Here, we analyze breeding‐site selection of an obligatory “nest‐cleptoparasite”, the Amur Falcon Falco amurensis. We collected data on nest sites at Muraviovka Park in the Russian Far East, where the species breeds exclusively in nests of the Eurasian Magpie Pica pica. We sampled 117 Eurasian Magpie nests, 38 of which were occupied by Amur Falcons. Nest‐specific variables were assessed, and a recently developed habitat classification map was used to derive landscape metrics. We found that Amur Falcons chose a wide range of nesting sites, but significantly preferred nests with a domed roof. Breeding pairs of Eurasian Hobby Falco subbuteo and Eurasian Magpie were often found to breed near the nest in about the same distance as neighboring Amur Falcon pairs. Additionally, the occurrence of the species was positively associated with bare soil cover, forest cover, and shrub patches within their home range and negatively with the distance to wetlands. Areas of wetlands and fallow land might be used for foraging since Amur Falcons mostly depend on an insect diet. Additionally, we found that rarely burned habitats were preferred. Overall, the effect of landscape variables on the choice of actual nest sites appeared to be rather small. We used different classification methods to predict the probability of occurrence, of which the Random forest method showed the highest accuracy. The areas determined as suitable habitat showed a high concordance with the actual nest locations. We conclude that Amur Falcons prefer to occupy newly built (domed) nests to ensure high nest quality, as well as nests surrounded by available feeding habitats.     

Polymorphism of microsatellite markers in Russian common carp (<Emphasis Type="Italic">Cyprinus carpio</Emphasis> L.) breeds

Using five microsatellite loci, genotyping and genetic diversity estimates were obtained for nine samples representing seven common carp breeds most widespread in Russia. For comparison, the samples of Amur wild common carp (Cyprinus carpio haematopterus) and a sample of European Hungarian carp were used. In the samples examined (n = 148) a total of 78 alleles were revealed. The highest mean allele number per locus (7.3) was identified in Amur wild common carp, while the lowest number was found in Cherepets carps (4.0). In different breeds, the observed heterozygosities varied from 0.819 (Altai carp) to 0.651 (Cherepets scaly carp). Three out of five microsatellite loci (MFW-24, MFW-28, and MFW-19) revealed a high level of population differentiation. In the dendrogram of genetic differences, all breeds clustered into two groups. One of these groups was composed of the two strains of Ropsha carp, Stavropol carp, Amur wild common carp, and the two samples of Cherepets carp. The second cluster included Altai carp (Priobskii and Chumysh populations), two Angelinskii carp breeds (mirror and scaly), and Hungarian carp. The pairs of breeds/populations/strains, having common origin, were differentiated. Specifically, these were two populations of Altai carp, two strains of Ropsha carp, as well as the breeds of Angelinskii and Cherepets carps. The reasons for genetic differentiation of Russian common carp breeds, as well as the concordance of the evolutionary histories of these breeds, some of which originated from the European breeds, while the others contain substantial admixture of the Amur wild common carp, are discussed.     

Genetic diversification of the Kanehira bitterling Acheilognathus rhombeus inferred from mitochondrial DNA,with comments on the phylogenetic relationship with its sister species Acheilognathus barbatulus

The Kanehira bitterling, Acheilognathus rhombeus, is a freshwater fish, discontinuously distributed in western Japan and the Korean Peninsula. Unusually among bitterling it is an autumn-spawning species and shows developmental diapause. Consequently, the characterization of its evolutionary history is significant not only in the context of the fish assemblage of East Asia, but also for understanding life-history evolution. This study aimed to investigate the phylogeography of A. rhombeus and its sister species Acheilognathus barbatulus, distributed in China, using a mitochondrial analysis of the ND1 gene from 311 samples collected from 50 localities in Japan and continental Asia. Phylogenetic analysis revealed that A. barbatulus is included in A. rhombeus and genetically closer to Japanese A. rhombeus than to Korean A. rhombeus. Divergence of Korean A. rhombeus and A. barbatulus from Japanese A. rhombeus was estimated to be from the late Pliocene (3.44 Mya) and the early Pleistocene (1.98 Mya), respectively. Each event closely coincided with the time of the Japan Sea opening. Japanese A. rhombeus comprised seven lineages: three in Honshu and four in Kyushu. One lineage in central Kyushu was genetically closer to the Honshu lineages than to other lineages in northern Kyushu. Divergence of Japanese lineages was estimated to be from the early to middle Pleistocene (0.55–0.93 Mya), during a period of geological and paleoclimatic change, including volcanic activity. Population expansion in the late Pleistocene (<0.10 Ma) was suggested in many of the lineages, which accords with other freshwater fishes. Biogeographically the ancestral A. rhombeus/A. barbatulus was likely to have repeatedly colonized Japan from the continent through land bridges in the late Pliocene and the early Pleistocene. However, the close genetic relationship between Japanese A. rhombeus and A. barbatulus suggests another possibility, with the second colonization occurring in reverse, from Japan to China. The small genetic distance between them indicates that the colonization occurred later than colonization events of other freshwater fishes, including other bitterling species.