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.     

Age structure of juvenile Amur sturgeon Acipenser schrenckii and kaluga Huso dauricus in the Fuyuan reach of the Amur River,Northeast China

Amur sturgeon Acipenser schrenckiii Brandt 1869 and kaluga Huso dauricus (Georgi 1775) are critically endangered species with populations showing significant decline from historical levels due to overexploitation, yet little is known about their population structure. Adults are not often captured in the Fuyuan reach of the Amur River, Heilongjiang Province, Northeast China, and the government prioritizes juvenile sturgeon management. This study was conducted to determine the age and length/weight relationships of juvenile Amur sturgeon and kaluga in the Fuyuan reach of the Amur River. We estimated age using pectoral fin spine sections obtained from 65 juvenile Amur sturgeon and 50 juvenile kaluga. We compared the age estimates from two readers, and found 100% between‐reader agreement in 67.7% of the Amur sturgeon and 64.0% of the kaluga. The majority of differences in estimated age were within 1 year. Length/weight relationships (LWR) were calculated, and the LWR of the Amur sturgeon and kaluga were W = 0.0025L3.106 (r² = 0.966）and W = 0.0022L3.175 (r² = 0.989), respectively. Our study provides the age structure and LWR in juveniles of two sturgeon species.     

New data about distribution of lower Amur grayling <Emphasis Type="Italic">Thymallus tugarinae</Emphasis> and Baikal-Lena grayling <Emphasis Type="Italic">Thymallus</Emphasis> sp. (Thymallidae) in the basins of the upper Amur River and Zeya River

New findings of lower Amur grayling (Lower Amur grayling) Thymallus tugarinae and Baikal-Lena grayling Th. sp. (Th. baicalolenensis) in the basins of the upper Amur River and Zeya River are reported for 2010?2014. Lower Amur grayling has been registered in the tributaries of Argun River and in the middle stream of Ingoda River. Baikal-Lena grayling has been found for the first time in the headstream of Ingoda River. New data about the distribution of this species in the basin of upper stream of Zeya River are reported; particularly, Baikal-Lena grayling has been found in Okonon Lake; this is the first finding of a representative of Thymallidae family in the alpine lakes of the watershed area of Amur River. In the basins of upper Amur River and Zeya River, the summer ranges of upper Amur grayling Th. grubii grubii and lower Amur grayling overlap to some extent; on the other hand, the ranges of Baikal-Lena grayling and lower Amur grayling are disjoint. During the summer period, upper Amur grayling and Baikal-Lena grayling together inhabit the basin of upper stream of Zeya River, but only Baikal-Lena grayling has been found in the headstream of Zeya River. In the basin of upper Amur River (the headstream of Ingoda River), the joint range of these species is still unknown; the sympatric zone is located in Dzhermoltai River (the basin of Onon River).     

Unidirectional hybridization of kaluga <Emphasis Type="Italic">Acipenser dauricus</Emphasis> Georgi, 1775 and Amur sturgeon <Emphasis Type="Italic">Acipenser schrenckii</Emphasis> Brandt, 1869, inferred from the mitochondrial DNA genotyping of their natural hybrids

In 2009 through 2011, among 730 individuals of kaluga and Amur sturgeon collected in the lower reaches of the Amur River and the Amursky Liman, 17 morphologically intermediate individuals (hybrids) with the body length of 56 to 202 cm (median, 81 cm) were identified, including 11 individuals (4.6%) found in 2009, three individuals (1.6%) found in 2010, and three individuals (1.1%), in 2011. In 16 hybrids, 819 bp of the mtDNA control regions were sequences and 11 haplotypes were identified. Since all these haplotypes were from the mtDNA lineages of kaluga, it was concluded that hybridization occurred in one direction, kaluga (♀) × Amur sturgeon (♂). This asymmetry could be caused by the large size differences between these species. Since the earlier examined morphologically typical Amur sturgeons showed the absence of alien haplotypes (Shedko et al., 2015), the absence of the mtDNA introgression is claimed. This can be caused by low viability or sterility of the backcross females (kaluga (♀) × Amur sturgeon (♂)) × Amur sturgeon (♂). The samples of hybrids and typical kaluga individuals demonstrated no differences in the frequency spectra of the mtDNA haplotypes. However, haplotype and nucleotide diversity in the first sample was somewhat higher than in the second one (0.950 versus 0.927 and 0.0054 versus 0.0044, respectively). The data obtained will be useful for population monitoring of kaluga and Amur sturgeon, Amur River endemics, which are classified as critically endangered by the IUCN Red List of Threatened Species.     

Distribution of Masu Salmon <Emphasis Type="Italic">Oncorhynchus masou</Emphasis> (Salmonidae) in Amur River Basin

The presented data on the distribution of the masu salmon Oncorhynchus masou in the Amur River Basin are collected in 1976–2015. In the analyzed region the species’ spawning range includes the lower part of the Amur River basin from the rivers flowing into the Amur estuary to the basins of the Anyui and Amgun’ Rivers in their middle courses. The information on the catch of a masu salmon specimen in the Khor River Basin (approximately 1300 km from the Amur River mouth) in 2015 is presented. It is assumed that the total Amur population does not exceed several thousand of adult anadromous fish.     

Comparative Ontogenetic Behavior and Migration of Kaluga, Huso Dauricus, and Amur Sturgeon, Acipenser Schrenckii, from the Amur River

We conducted laboratory experiments with kaluga, Huso dauricus, and Amur sturgeon, Acipenser schrenckii, to develop a conceptual model of early behavior. We daily observed embryos (first life phase after hatching) and larvae (period initiating exogenous feeding) to day-30 (late larvae) for preference of bright habitat and cover, swimming distance above the bottom, up- and downstream movement, and diel activity. Day-0 embryos of both species strongly preferred bright, open habitat and initiated a strong, downstream migration that lasted 4 days (3 day peak) for kaluga and 3 days (2 day peak) for Amur sturgeon. Kaluga migrants swam far above the bottom (150cm) on only 1 day and moved day and night; Amur sturgeon migrants swam far above the bottom (median 130cm) during 3 days and were more nocturnal than kaluga. Post-migrant embryos of both species moved day and night, but Amur sturgeon used dark, cover habitat and swam closer to the bottom than kaluga. The larva period of both species began on day 7 (cumulative temperature degree-days, 192.0 for kaluga and 171.5 for Amur sturgeon). Larvae of both species preferred open habitat. Kaluga larvae strongly preferred bright habitat, initially swam far above the bottom (median 50–105cm), and migrated downstream at night during days 10–16 (7-day migration). Amur sturgeon larvae strongly avoided illumination, had a mixed response to white substrate, swam 20–30cm above the bottom during most days, and during days 12–34 (most of the larva period) moved downstream mostly at night (23-day migration). The embryo–larva migration style of the two species likely shows convergence of non-related species for a common style in response to environmental selection in the Amur River. The embryo–larva migration style of Amur sturgeon is unique among Acipenser yet studied.     

Distribution,abundance, and size structure of Amur kaluga <Emphasis Type="Italic">Acipenser dauricus</Emphasis> and Amur sturgeon <Emphasis Type="Italic">A. schrenckii</Emphasis> in the Lower Amur and Amur Estuary

Distribution, population structure, and abundance of Amur kaluga Acipenser dauricus and Amur sturgeon A. schrenckii in the Lower Amur and Amur Estuary have been considered based on the materials of two surveys performed in 2011. Both species occur along almost the entire length of the Lower Amur and in major part of the Amur Estuary. The density of their aggregations has significantly decreased in most regions of the river if compared to the 1960s. In the Amur Estuary, A. dauricus and A. schrenckii are most abundant in freshwater and light salted water bodies of its western part. In 2011, the abundance and biomass of A. dauricus and A. schrenckii in the Lower Amur and Amur Estuary was 345000 specimens and 7110 tons and 289000 specimens and 1946 tons, respectively.     

New species of grayling <Emphasis Type="Italic">Thymallus tugarinae</Emphasis> sp. nova (Thymallidae) from the Amur River Basin

Data on a new species, low Amur grayling Thymallus tugarinae sp. nova, inhabiting tributaries of the lower and middle current of the Amur River, are presented. This species has been earlier equated with the Amur grayling T. grubii, described by Dybowski (1869) from the rivers Onon and Ingoda (the Upper Amur Basin). The new species differs from other representatives of the genus in the body coloration, the pattern on the upper fin, and certain morphological characters. On most of the Amur Basin, the grayling from the Lower Amur is sympatric with T. grubii and in its tributary Bureya River, also with the Bureya grayling T. burejensis. Individuals with intermediate traits are unknown, pointing to reproductive isolation. These data are supported by the results of molecular-genetic analysis (Froufe et al., 2003, 2005; Knizhin et al., 2004).     

Biological specific features of the Lower Amur grayling Thymallus tugarinae (Salmoniformes: Thymallidae): 1. Age composition

We consider age composition of samples of the Lower Amur grayling Thymallus tugarinae inhabiting water bodies of the lower and middle course of the Amur and several rivers of the northwestern part of Sakhalin Island and the southern coast of the Sea of Okhotsk. Age composition of the Lower Amur grayling from the studied samples is not similar because of several reasons. In rivers of the Amur basin, the species has a maximal age of 6+.     

Biological features of Low Amur grayling Thymallus tugarinae (Salmoniformes: Thymallidae): 2. Growth

We present the results of analysis of the group growth of the Low Amur grayling Thymallus tugarinae from 18 rivers of the Low Amur basin, tributaries of the Bureya and Ussuri rivers. We made use of the published data on the fishes of Sakhalin Island. The dwarf and fast-growing forms are not revealed among the investigated groups of this species. The parameters of growth of the Low Amur grayling in the investigated rivers are different, which is determined by the different conditions of feeding migration connected with the geographical location of the streams, their hydrological features, density of populations, etc. The anthropogenic factor influence is essential. Growth rate of T. tugarinae is lower compared with the other Amur species of graylings.     

Discrimination of interspecific hybrids in natural populations of Amur sturgeon fish by means of multilocus RAPD-PCR markers

A RAPD-PCR analysis of a sample of Amur sturgeon fish (46 individuals) is performed. An estimate of the genetic state of native populations of Amur sturgeon Acipenser schrenckii (Brandt, 1869) and kaluga fish Huso dauricus (Georgi, 1775) is given. Genetic evidence for the hybrid origin of two phenotypical hybrids is obtained. Estimates of the genetic distances between the species and the hybrids proved to be at the level of interspecific distances. It is shown that an Exact Test for differentiation of the populations is the most effective means of discriminating the two species, while multidimensional scaling (MDS) is the most effective means of discriminating the hybrids. It is concluded that the populations of sturgeon fish in the Amur River have maintained a substantial level of genetic diversity; the presence of hybrids in these populations is judged to be one of the risk factors. Multilocus RAPD-PCR markers are acknowledged as a convenient and reliable tool for conducting genetic monitoring of populations of Amur sturgeon fish for the purpose of preserving the gene pool of the fish.     

Age and growth of kaluga Acipenser dauricus from the estuary of the Amur and its lagoon

Age composition and the rate of growth of kaluga Acipenser dauricus from the estuary of the Amur and the Amur lagoon have been analyzed. Differences in the distribution of juvenile and mature individuals of kaluga in the river estuary and the lagoon were revealed. Males are dominant among mature individuals aged 18–26 years, and females are dominanat at an age 27–43 years. Females and males of the same age do not differ in length and body weight. A decrease in the rate of linear and gravimetric growth of mature individuals at the modern stage (2005–2008) compared to the period of 1965–1982 was revealed. Juvenile individuals of kaluga from the near-estuarine part of the Amur and its lagoon are inferior in the rate of growth to fish of the same age caught in the river channel, 500 km to the south.     

Across Siberia and over Europe: Phylogenetic relationships of the freshwater fish genus Rhodeus in Europe and the phylogenetic position of R. sericeus from the River Amur

We present the phylogenetic relationships of the freshwater fish genus Rhodeus from 45 localities in Europe and three localities in the Amur basin using the mitochondrial cytochrome b sequence. The study aims to (1) test the colonisation history between Europe and East Asia and (2) to reconstruct the evolutionary history of Rhodeus in Europe. Our analyses revealed five monophyletic clades which correspond to four species: R. sericeus in the Amur basin, R. meridionalis in the River Vardar, R. colchicus in western Caucasus and two sister lineages in most of Europe which together represent R. amarus. The reconstructed colonisation scenario assumes a continuous distribution of Rhodeus from Europe through Siberia until East Asia during Pliocene, depletion of the Siberian population in late Pliocene, isolation of the population in River Vardar during early Pleistocene, refuges during late Pleistocene glaciations in the Danubian basin, in the lowlands of western Black Sea and in western Caucasus Mountains and a post-glacial expansion from the Danubian refuge towards western Europe and from the Black Sea refuge across Eastern Europe.     

Realization of the project for Acipenser oxyrhynchus oxyrhynchus restoration in the basin of the Neman River

The results of the works on the international project for the Baltic sturgeon restoration in the basin of the Neman River are considered. The mutual goal of the project is the restoration of the Baltic sturgeon population in its whole former area in the Baltic Sea. Successful works on the restoration of the Baltic sturgeon population are conducted in the Oder and the Vistula basins. The stockings of the Neman River with the sturgeon fry were started from 2012 year. It is contemplated that the sturgeon stockings of the main rivers of the Baltic Sea will enable to restore local sturgeon populations in these river basins. Till the beginning of the XXI century it was supposed that the Atlantic sturgeon Acipenser sturio had inhabited the Baltic Sea, but numerous genetic analysis of the samples of the sturgeon bones from the archeological finds in the museums showed that the Baltic Sea had been inhabited with Acipenser oxyrhynchus and its population still inhabits several rivers in Canada. This discovery permitted to start the creation of the Baltic sturgeon broodstock. Sturgeon fry from the eggs imported from Canada were used for stocking at the first stage of the project. Later it is contemplated to use the fry from the broodstocks in Germany and Poland. Sturgeon fry hatched from Canadian eggs in Poland and reared in Lithuania was used for the Neman River stocking. The fry were tagged and released in the Neris and the Sventoji Rivers in the Neman River basin. The sturgeon migrated into the Curonian lagoon where the monitoring of the catches was fulfilled. The results of sturgeon catches monitoring are discussed.     

Seasonal variation in diet of juvenile Amur sturgeon Acipenser schrenckii in the lower reaches of the Songhua River,Northeast China

We investigated seasonal variation in the diet of hatchery-reared juvenile Amur sturgeon Acipenser schrenckii in the Tongjiang reach of the Songhua River, Northeast China. The results indicated that Amur sturgeon fed mainly on Chironomidae and Ephemeroptera and secondarily on unspecified bony fish, Odonata, and Trichoptera. Diet changed throughout the year, with autumn 2017 and spring 2018 dominated by Ephemeroptera larvae, while summer 2018 prey comprised primarily Chironomidae larvae. Unspecified bony fish were observed at greater frequency in autumn 2017. Amur sturgeon captured in summer contained a greater quantity of Trichoptera larvae compared to those from autumn and spring sampling. Results were consistent with previous reports of Amur sturgeon diet in other areas of its native distribution and suggested that they may be opportunistic feeders throughout the year, although larval Chironomidae and Ephemeroptera appear to be important prey. These results represent the first reported diet composition data for juvenile Amur sturgeon in the lower Songhua River. Results of the study form part of a comprehensive investigation of feeding habits of juvenile Amur sturgeon that provides basic data for study of the biological characteristics of the species.     

On the diversity of fishes in mountain lakes of the Amur basin

Results of the study of 11 lakes situated in the mountainous part of the Amur River basin are reported. Six fish species, namely, blunt-snouted lenok Brachymystax tumensis, Baikal-Lena grayling Thymallus baicalolenensis, Siberian stone loach Barbatula toni, Lagowski’s minnow Rhynchocypris lagowskii, Czekanowski’s minnow Rh. czekanowskii, and Amur sculpin Cottus szanaga, were found in five lakes. Four species were found in one lake (Lake Pereval’noe, basin of the Amgun’ River), and two species were found in each of the remaining lakes. Lenok and Amur sculpin were the most common species. The fauna of Lake Okonon (basin of the river Zeya) was the most specific and did not have analogs among the lake faunas; Czekanowski’s minnow and Baikal black grayling were found in this lake. The lenok ecotype that formed in the mountain lakes differed from the river lenok in some regards. The potential pathways of formation and protection of mountain lake ichthyocenoses of the Amur basin are discussed.     

Biology, fisheries, and conservation of sturgeons and paddlefish in China

This paper reviews five of the eight species of acipenseriforms that occur in China, chiefly those of the Amur and Yangtze rivers. Kaluga Huso dauricus and Amur sturgeon Acipenser schrenckii are endemic to the Amur River. Both species still support fisheries, but stocks are declining due to overfishing. Acipenseriformes of the Yangtze River are primarily threatened by hydroelectric dams that block free passage to spawning and feeding areas. The Chinese paddlefish Psephurus gladius now is rare in the Yangtze River system, and its spawning activities were severely limited by completion of the Gezhouba Dam in 1981. Since 1988, only 3–10 adult paddlefishes per year have been found below the dam. Limited spawning still exists above the dam, but when the new Three Gorges Dam is complete, it will further threaten the paddlefish. Artificial propagation appears to be the only hope for preventing extinction of P. gladius, but it has yet to be successfully bred in captivity. Dabry's sturgeon A. dabryanus is a small, exclusively freshwater sturgeon found only in the Yangtze River system. It is concentrated today in reaches of the main stream above Gezhouba Dam. The fishery has been closed since 1983, but populations continue to decline. Acipenser dabryanus has been cultured since the 1970s, and holds promise for commercial aquaculture; availability of aquacultural methods offers hope for enhancing natural populations. The Chinese sturgeon A. sinensis occurs in the Yangtze and Pearl rivers and seas of east Asia. There is still disagreement about the taxonomy of the Pearl and Yangtze River populations. The Yangtze River population is anadromous. Adults begin spawning at about age 14 years (males) and 21 years (females), and adults spend over 15 months in the river for reproduction. Spawning sites of A. sinensis were found every year since 1982 below the Gezhouba Dam, but it seems that insufficient suitable ground is available for spawning. Since 1983, commercial fishing has been prohibited but more measures need to be taken such as establishing protected areas and characterizing critical spawning, summering and wintering habitats.     

Multiple species of grayling (Thymallus sp.) found in sympatry in a remote tributary of the Amur River

Large-scale phenotypic and genetic studies of the salmonid genus Thymallus (grayling) in the Palaearctic suggest that most major phylogeographic lineages represent good biological species. Evaluating such a premise in areas involved in palaeo-hydrological dynamics where multiple species are found in sympatry should serve to assess the level of reproductive isolation, the traditional sine qua non of species recognition. Molecular sequence (mtDNA) and microsatellite (nDNA, seven loci) analysis of grayling in the upper Bureya River watershed support the occurrence of three distinctive species of grayling living in sympatry in this large oligotrophic tributary of the Amur River. One of these lineages is primarily found throughout the Lena River basin and is recognized as Baikal-Lena grayling Thymallus baicalolenensis; the second, the upper Amur grayling Thymallus grubii is found over large areas of the Amur catchment including the entire headwater region; and the third, the Bureya grayling Thymallus burejensis is endemic to the study area. A limited number of hybrids were identified, primarily between Baikal-Lena grayling T. baicalolenensis and Bureya grayling T. burejensis with little to no signs of introgression among non-hybrid individuals. Morphological distinctiveness among populations of these species living in sympatry was greater than between populations living in allopatry, suggesting character displacement. Divergence estimates among taxa range up to 6.2 MY, and allopatric origins for all three species’ is suggested. To our knowledge, this is the first data-based confirmation of three species of grayling living in sympatry.     

Amur sleeper (Perccottus glenii Dubowski, 1877) spreading in the Danube River Basin

Whereas earlier Amur sleeper (Perccottus glenii) findings in the Danube River were only single specimens, data reported in this study represent the first record on establishment of a local population. An overview of the spread of the Amur sleeper in the Danube River basin is also presented.     

Macrozoobenthic Communities of the Piedmont and Lowland Watercourses of the Lower Amur Region

On the basis of 120 original stations, macrozoobenthic communities of rivers from two adjacent areas of the Lower Amur Region (Khabarovsk krai) have been described. Rivers basins are characterized by contrasting landscape conditions: the Anyuy River basin in the piedmonts of the Sikhote-Alin mountain range and the Simmi River basin on the Amur Lowland. About 250 taxa of macroinvertebrates have been found; 16 types of communities have been described. The principal differences in both benthic fauna and macrozoobenthic communities in the basins of the Anyuy River (cold-water rheophilic fauna as well as ritral and crenal communities predominate) and the Simmi River (warm-water limnophilic fauna and phytal communities predominate) are shown. We discuss the reasons for these differences, specific features of the fauna and communities of the whole region, and the biogeographical position of the region.