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J. Appl. Ichthyol. 24 (Suppl. 1) (2008), 29–35 Received: December 20, 2006 2008 The Authors Accepted: September 5, 2007 Journal compilation 2008 Blackwell Verlag, Berlin doi: 10.1111/j.1439-0426.2008.01087.x ISSN 0175–8659

A review on genetic studies in and their trade control in By B. Zhu, Y. Que, Z. Yang and J. Chang

Department of conservation biology, Institute of Hydroecology, Ministry of Water Resources & Chinese Academy of Sciences, Wuhan, Hubei, China

Summary Eight species of are native in China, Eight native species of Acipenseriformes mainly inhabit three mainly distributed in the Xinjiang Area and the geographical in China: the Yangtze system, the Amur and Amur. dauricus and schrenckii are shared system and the Xinjiang area. All populations in with in the Amur system, and A. baerii and China have suffered from various anthropogenic impacts, A. ruthenus with Kazakhstan and Russia in the River. pushing them to rarity or extirpation in most of their historical A. nudiventris occurs in the River, which is a tributary of range. Sturgeon aquaculture in China has become popular Lake Balkhash in Kazakhstan. The remaining three species, since 1998 with eleven species and hybrids presently being A. sinensis, A. dabryanus and Psephurus gladius are endemic to cultured. In this paper, we firstly review the development and China; particularly distributed in the Yangtze River and Sea of current status of aquaculture with sturgeons and paddlefish in China (Wei et al., 1997). Like other sturgeon species, all stocks China. Secondly, we present some of the main conclusions that of sturgeon populations in China have suffered from overfish- can be drawn from previous conservation genetic and phylo- ing, poaching, barriers to migration, loss of spawning habitat genetic studies in native sturgeon species. The sturgeon trade and the deterioration of water quality. However, the combi- control in China is also reported in this review. Considering nation of the various anthropogenic factors have different the outcome of all previous studies, we conclude, firstly, in impacts for each species, and are also particular to each river sturgeon aquaculture, capture breeding program is the key to system. Overexploitations and poaching for caviar production establish a sustainable sturgeon culture industry in China, are responsible for the significant decline in Amur stocks of which will also help sturgeon conservation. Secondly, in H. dauricus and A. schrenckii during the last 20 years. For )1 conservation genetics, the influence of restocking and release instance, the maximum output was 452 tonnes year and its programmes on native populations need to be assessed much average value was 346 tonnes during the 1980s, while the )1 more comprehensively in order to avoid admixture and maximum output was 243 tonnes year and its average value hybridization among genetically different spawning stocks. was 181 tonnes during the 1990s, which was only half of that This holds especially for and Amur sturgeon. in the 1980s (Qu et al., 1997; Feng et al., 2004). Acipencer Thirdly, in trade control, considering the current endangered sinensis, A. dabryanus and P. gladius were once the major status of this species, catch quotas should be based on the commercial fishes in the Yangtze, but habitat alteration and results of scientific investigations rather than on official the closing of Gezhouba have led to a collapse of their statistics of harvest records. Finally, species identification abundance during the last decades. Although the capture of methods based on the combination of mitochondrial and these species are strictly prohibited since 1983; they were listed nuclear markers are still unsufficiently developed in China and as a state protected species class I in 1988; their survival in the in need of rapid attention. They are the first step in structuring wild is further threatened by the construction of Jinshajiang and implementing a successful conservation programme and First Hydroelectric Project and the Three Gorges Project, provide the necessary tools for effective international trade which will disrupt spawning grounds and alter hydrological control. conditions dramatically. Few studies have been conducted on A. baerii, A. ruthenus and A. nudiventris in China because the wild populations are believed to be very small and their catches Introduction are rare (Wei et al., 2004). Once widely distributed and highly abundant in the northern Sturgeon aquaculture can be used as a tool not only for Hemisphere (Billard and Lecointre, 2001), sturgeon species economic development to meet the demand for products from today exist as fragmented populations occupying limited these species, but also for restocking (Burtsev et al., 2002; geographic areas, showing an alarming decline in adult Chebanov et al., 2002). Scientific research on sturgeon aqua- abundance. According to the International Union for the culture in China was in its infancy before 1970s. Only a few Conservation of Nature and Natural Resources (IUCN), most fragmentary scientific studies were performed on the reproduc- of the species are threatened or endangered because of various tive biology. Due to market demands and the economic benefits, human activities. Some populations are rare or even extinct in sturgeon aquaculture was aggressively promoted from the their original habitats. Therefore, due to the critical status of beginning of 1990s, mainly for restocking programmes in the these species, as well as their high economic value and Yangtze and Amur river systems (Chang and Cao, 1999; Sun significance in phylogenetic evolution, Acipenseriformes have et al., 2003). For example, A. schrenckii was firstly artificially been of critical concern to these involved in species conserva- reproduced in China in 1957 (Zhang, 1985), A. sinensis in 1971, tion (Rosenthal et al., 2006). and A. dabryanus in 1976 (Anonymous, 1988). Meanwhile, a

www.blackwell-synergy.com 30 B. Zhu et al. large number of fertilized sturgeon eggs or of prolarvae of other were 11 sturgeon species ⁄ hybrids being cultured in China non-indigenous species, including P. spathula, A. stellatus, around the year 2000 (Sun et al., 2003). Besides the Chinese A. gueldenstaedtii and a hybrid called Bester (H. huso · native species, P. spathula, H. huso, A. stellatus, A. gue- A. ruthenus), were also imported from Russia, Germany, France ldenstaedtii and Bester hybrids (H. huso · A. ruthenus) were and Hungary (Sun et al., 2003). It is believed that China has also raised (Wei and Yang, 2003). At present, sturgeon become one of the largest sturgeon aquaculture country in the aquaculture operations in China occur in about 70% of the world by the year 2000 (Wei and Yang, 2003). Hopefully, provinces, including Anhui, Chongqing, Guangxi, Guizhou, artificial breeding and aquaculture will contribute to a reduction Hainan, , Henan, Hunan, Jiangxi, Liaoning, of fishing pressure and will be able to effectively support Shandong, Shanxi, Sichuan and Yunnan. A series of culture rehabilitation programmes for wild stocks. experiments showed that aquaculture of sturgeons could be Sturgeons were and are of large interest to many researchers successfully in the warmer waters of South China with great world wide because of their special position in economic potential (Zhuang et al., 2002). Therefore, most evolution and the great public interest in these species. Modern sturgeon farms are located in the delta and the molecular genetic techniques play a key role as tools in Yangtze delta. Investigations in 39 major sturgeon farms sturgeon preservation strategies and in trade control (Wolf producing fingerlings in China estimated an overall number in et al., 1999; Ludwig et al., 2002a and Ludwig, 2006, 2008). An standing stock of 17.86 million for all sturgeon species and increasing number of studies relate to molecular phylogenetics hybrids (Wei et al., 2004). The authors also predicted from the and evolution (Krieger et al., 2000, 2008; Ludwig et al., 2000, farms surveyed that approximately 6000 tonnes of sturgeons 2001, 2003; Krieger and Fuerst, 2002), and point to the with an average size of 0.75 kg should be ready for the importance of genetic variation for conservation management markets, assuming a 50% survival rate of farmed fingerlings. (May et al., 1997; Wirgin et al., 1997; Mcquown et al., 2000; Jenneckens et al., 2001; Ludwig et al., 2002b; Schrey and Heist, 2007). The genetic studies on native sturgeon species of Yangtze River China were initiated in the 1980s. Most of these studies were As Chinese sturgeon, Chinese paddlefish and DabryÕs sturgeon focused on species preservation, population stabilizing and are listed nationally as Class I state protected , people controlled propagation (Anonymous, 1988). After the 1990s, who are permitted to culture them have also the obligation to with the development of molecular markers, studies concen- restock these to natural waters or preserve them in captivity. trated on conservation genetics and phylogenetics. Important Commercial use of these species is strictly prohibited. The results on genetics were derived for A. sinensis, A. dabryanus, populations of Chinese paddlefish and DabryÕs sturgeon P. gladius, A. schrenckii and H. dauricus, and were applied in dramatically declined since the construction. conservation management (Deng and Deng, 1997; Wei et al., The latest catch of a Chinese paddlefish was reported in the 1997; Zhuang et al., 1997; Zhu et al., 2006; Peng et al., 2007). branch of the Yangtze River in January 2003. Several Due to the rareness of A. baerii, A. ruthenus and A. nudiventris, attempts on artificial reproduction of Chinese paddlefish were few genetic data are available for these species from the . not successful. Meantime, very few DabryÕs sturgeon are being Genetic studies on sturgeons in China have until recently still held in captivity and are maintained by artificial breeding as a been in the initial state. Numerous problems, such as popu- tool for conservation. lation structure and species identification, have not yet been Acipencer sinensis cultured at the Chinese Sturgeon Institute resolved adequately or have not been employed until now. In (CSI) and the Yangtze River Fisheries Research Institute this paper, we review the development and current status of (YFI) originated from captive broodstock artificially fertilized sturgeon aquaculture and paddlefish in China, as well as the eggs from wild broodfish (Wei and Yang, 1998; Chang and main genetic and phylogenetic research results for native Cao, 1999). The two institutes received special licenses on a species. The trade control in sturgeon specimens and caviar yearly basis to capture a few specimens of multiple spawners products in China is also addressed. for use in restocking programmes and for specific research projects. With improvements in cultivation techniques, facility design and rearing techniques, the number of wild spawners Status of sturgeon aquaculture in China actively caught for restocking purposes has decreased, while The conflict between limited natural population abundances the fry production has noticeable increased. Two institutes and the great economic interest in sturgeon products is one of (CSI and YFI) received special licenses from the Fisheries the driving forces to push the development of the sturgeon Bureau of Ministry of Agriculture (FB of MOA) to capture aquaculture in China. After the first attempt of controlled Chinese sturgeon spawners for artificial propagation with a reproduction, the successful culture of A. schrenckii in 1957 quota of 20 spawners in 1999, 26 spawners in 2000 and 14 (Zhang, 1985), promoted the development of sturgeon aqua- spawners in 2001. Fry production was about 1 000 000, culture techniques. Cultivation was based on the collection of 2 000 000 and 800 000 in 1999, 2000 and 2001, respectively mature broodfish in relevant spawning grounds and the (Wei et al., 2004). In recent years, the central government injection of pituitary hormones for final maturation and these (MOA) granted permits to several hatcheries and companies to methods were gradually improved during the 1990s and raise Chinese sturgeons to try to complete the life cycle in applied for other species from China (Chen and Zhou, 1992; captivity in case the species becomes extinct in the wild. This Wei et al., 1997; Chang and Cao, 1999; Zhuang et al., 2002; threat is real because of the anticipated additional impact of Sun et al., 2003). Late in the 1990s, fry and fertilized eggs of the Three Gorges Project on the remaining population. Some adventive sturgeons and hybrids were imported and intro- fry were sent to farms that had been licensed for grow-out of duced to farms in different provinces. Techniques for mass the species. Since 1998, a total of eleven farms and companies rearing of juveniles were tested on a commercial scale and were in China have been granted permits for aquaculture of the gradually developed until 1996, while sturgeon farming in Chinese sturgeon. Although there have been many discussions China increased in popularity since 1998. As a result, there on the potential exploitation and commercial use of Chinese A review on genetic studies in sturgeons 31 sturgeon because of successful rearing in experimental aqua- volume to Hong Kong and Japan increased to 123 tonnes in culture facilities, commercial utilization of these reared fish has 2001, which included , and not been permitted. . Besides these species, only the cultivation of P. spathula has also widely developed ( and Lin, 1999), the output depending on the successful breeding since 2002 (Wang et al., Amur River 2004). In recent years, aquaculture of Russian sturgeon has In the Heilongjiang Province, A. schrenckii and H. dauricus are declined because the yellow colour and coarse meat of this the only two commercially important species from which species is not well accepted by consumers in China and caviar is still produced. Historically, landings of these two worldwide. species have not been recorded separately from others so that only the total yield can be reported. From 1957 to 1977, the landings ranged 13–100 tonnes year)1, with an average of Trade control of sturgeon products in China 43.3 tonnes. In 1978, the industry expanded the sturgeon Sturgeon aquaculture is a new developing industry in China. fisheries as foreign traders came to China to purchase caviar at The cultured sturgeons have been used for many diversified high prices. Sturgeon catches for all species reached a peak of products, such as fins, pharmaceutical products and leather, 452 tonnes in 1987 and averaged 322.2 tonnes annually but have also been sold as whole live fish. Generally, caviar between 1987 and 1991. Sturgeon landings declined thereafter and meat are the major products derived and marketed from and averaged 176.2 tonnes year)1 between 1992 and 1996. sturgeon processing in China. The caviar is exported and the From 1997 to 1999, landings were recorded with 136, 149 and meat is mainly consumed domestically. In order to protect the 141 tonnes respectively (Feng et al., 2004; Wang and Chang, sturgeon resources in China, the Centre Government has taken 2006). There is a lack of scientific information on the current measures to restrict sturgeon production. According to the status of the sturgeons in the Chinese part of the Amur River. ÔWild Animals Protection LawÕ promulgated in 1988, the Many data on fisheries were collected by the Fisheries permits for the export and import of sturgeons, their caviar, Department of the local government, however, these data are specimens and parts thereof, are issued by the China CITES usually scattered and insufficient for a rigid scientific analysis. Management Authority after approval by the FB of MOA in Nevertheless, available catch figures indicate a significant China (Wang and Chang, 2006). Harvest quotas for sturgeons decline in stocks of H. dauricus and A. schrenckii over the last (for caviar production and for specimens destined for prop- decade. It is anticipated that H. dauricus may soon be near agation) are based on the sturgeon quota established for caviar . production. In accordance with the provisions of CITES, Two major sturgeon propagation stations on the Chinese China has implemented effective management measures over side of the Amur Rivers were set up at Qingdeli in 1988 and at caviar trade since 1998. The export quotas for Chinese caviar Fuyuan in 1998. As of 2005, about 8.45 million fry (according were 6.27, 5.94, and 5.65 tonnes for the years 1998, 1999 and to the FB of Heilongjiang Province) have been released into 2000 respectively. Generally, the quotas declined gradually and the Heilongjiang River. From 1988 to 1998, the Qindeli Farm have been maintained at the level around 5.9 tonnes since 2001 released a total of 3.6 million fry of A. schrenckii. In 1998, the (Wei et al., 2004). Fuyuan station released about 80 000 fry. In 2001, 20 000 and 130 000 Amur sturgeon fingerlings were released into the Amur River by the Fuyuan Sturgeon Propagation Domestic trade Station. It was the first time that H. dauricus, a critically Live sturgeons are sold in most provincial capitals and in large endangered species, was released into the Amur. Although the cities of China, with plenty of huge fish markets, such as in captive breeding of Amur sturgeon was successful in 2002 (Qu Guangdong, Shanghai, Xinjiang and Beijing. Among all the et al., 2002), the majority of the cultured specimens of cultured sturgeons, A. schrenckii dominates the domestic A. schrenckii and H. dauricus have still been obtained under markets. For instance, its amount in Guangzhou was controlled propagation using wild spawners caught in the 20 000 individuals day)1, while it was 10 000–15 000 individ- Amur River. Survey data revealed that 25.8 million and 43.3 uals day)1 in Shanghai and 12 000–16 000 individuals day)1 million fertilized eggs and fry of Amur sturgeon or Kalu- in Beijing (Wang et al., 2004) during the breeding seasons. ga ⁄ Amur hybrids were produced in Heilongjiang in 2001 and 2002 respectively (Wei et al., 2004). Most fertilized eggs were quickly transported to provinces in the South of China for International trade incubation. Some fry in the southern hatcheries were main- Sturgeons and paddlefish are highly prized for their caviar; one tained for grow-out and some were sold to other fish farms. of the most valuable wildlife products in international trade The author also indicated that the Amur sturgeon is now the (De Meulenaer and Raymaker, 1996; Ludwig, 2008). There is most commonly farmed sturgeon species in China, accounting little caviar consumed on the domestic markets, although for 70.8% of the total number of cultured specimens. caviar processing in China started in the early 1950s. Caviar is mainly exported to Germany, the USA and Japan. Although there are eight native species in China, only caviar from wild Exotic species Amur populations of A. schrenckii and H. dauricus are traded Most of the introduced (non-native) sturgeon species in China (exported) legally. Six companies were licensed to export are owned by private companies and organizations. There is caviar from these species, which are located along the Amur unfortunately no official data reporting on their production (Wang and Chang, 2006). The caviar trade is strictly executed figures or total output except the data for sturgeon meat by the quotas from China CITES Management Authority. produced for export. All we know is that seven and a half According to official statistics, the volume of exported caviar tonnes of Siberian sturgeon and Russian sturgeon were reached a peak of 26 metric tonnes (mt) in 1987. Since 1992, exported to Singapore and Hong Kong in 2000. The exported the caviar production has declined gradually, fluctuating 32 B. Zhu et al. between 6.46 and 12.7 mt, with an annual average production from year 1995 to 1997. Similar results in this study also of 9.16 mt. The export reached the minimum of about 2000 kg indicated that low genetic variability did exist in A. sinensis. of A. schrenckii and H. dauricus in 2003, but the export rose Mitochondrial control region sequences were obtained from slightly up to about 2600 kg in 2005 (Cui et al., 2006). 106 adult sturgeons that were collected at the spawning site of Furthermore, some private corporations also have got the the Yangtze River between years 1995 and 2000. Analysis of caviar from cultured sturgeons in China, for instance, 500 kg molecular variance (AMOVA) indicated that 98.7% of the caviar was successfully produced by Tianxia Sturgeons Culti- genetic variability occurred within each yearÕs spawning vating Corporation in 2006; and thereafter, 343 kg caviar were population. Moreover, the authors also reported the ratio of obtained from the culture of A. gueldenstaedtii and A. baerii effective female population size was 0.77–0.93 (Zhang et al., and this was exported to the Occident, Japan and Hongkong 2003), which indicated that the remnant Chinese sturgeon by Tianhai Aquiculture Food Corporation in 2007 (pers. population was still characterized by a relative large effective comm.). female population size, providing still a good potential for recovery of this species in the future, provided sufficient spawning habitats will be maintained as made available. Status of sturgeon genetic studies in China Recently, large numbers of microsatellites were used in the The important results on sturgeon genetic research in China studies (Zhu et al., 1999, 2005; Shao et al., 2002). Four were achieved during two time periods. The first period microsatellites were employed to evaluate the recruitment happened before the 1980s, focusing on ecological genetics. effects of controlled propagation and release programmes in During this period, certain preliminary outcomes were nature. The parentage analysis revealed a low proportion (5– achieved, such as reproductive ecology and hatchery opera- 10%) of artificially propagated individuals among juveniles in tions providing the basic knowledge for implementing the of the Yangtze River (Zhu et al., 2002). The advanced genetic research and programmes. Research during present rate of release of artificially produced larvae may not the period after 1980s mainly focused on conservation biology, be adequate to maintain the population of A. sinensis, as the especially on conservation genetics addressing the endangered natural spawning area has been dramatically reduced in size. status of native sturgeons. Many important results have also Zhu et al. (2006) detected the genetic variation within and been achieved on the genetic structure of variation within wild among three annual spawning runs of the Chinese sturgeon by stocks (Zhang et al., 1999a,b, 2000a; Zhu et al., 1999, 2002, six microsatellites. In this study, a new method called 2005; Liang et al., 2002), controlled reproduction and hybrid- unsupervised self-organizing mapping was employed to extract ization (Zhuang et al., 1997; Chang and Cao, 1999; Xiao et al., information of the genetic structure of the population. A 1999; Pan et al., 2001) and on molecular phylogenetics and complex genetic structure was detected in the annual spawning evolution (Song et al., 1997; Zhang et al., 1999c,d, 2001; Wang runs. Meanwhile these genetically differentiated spawning et al., 2005; Peng et al., 2007). During this period, the studies stocks may occur sympatrically on a small geographic scale. identified a lower genetic variation in sturgeons compared to These results further suggested that the current supportive other bony fishes, yet little influence on the natural stocks by breeding of A. sinensis may require a careful identification of controlled reproduction and release and some basic phyloge- broodstocks for the artificial propagation in order to avoid netic relationships within Acipenseriformes. In this part, we admixture and hybridization among these genetically different will focus in detail on the native species which are now spawning stocks. frequently studied in genetics.

Chinese paddlefish and DabryÕs sturgeon Chinese sturgeon The rareness of the Chinese paddlefish makes genetic studies Genetic investigation about A. sinensis can be divided into the very difficult. Cytogenetic studies revealed that P. gladius is two following periods: (i) 1958–1970s, studies focused on possibly tetraploid, which is a similar ploidy level as in ecological genetics of the species and (ii) from the 1970s until Polyodon spathula (Dingerkus and Howell, 1976). In contrast, now, focused on conservation genetics. In the first period, A. dabryanus, A. sinensis and A. schrenckii are octoploid some basic data such as spawning sites, reproductive strategies species (Zhang et al., 1999d). However, these results are still and the mobility of offspring were obtained (Anonymous, not helping to resolve the unclear ploidy status of Acipenser- 1988; Chang and Cao, 1999). Although these data could only formes (Birstein and Vasiliev, 1987; Blacklidge and Bidwell, provide certain preliminary results in genetics, they could be 1993; Fontana, 1994; Song et al., 1997; Ludwig et al., 2001). beneficial to boost research for conservation of A. sinensis.In Although the wild populations are very rare, several genetic the second period, development of molecular markers and studies were performed focusing on the phylogenetic relation- their application is becoming popular, especially on the genetic ships of these species. Zhang et al. (1999d) used 13 RAPD variation of wild stocks and assessment of artificial reproduc- primers to probe the relationship among seven species includ- tion. ing P. gladius and A. dabryanus. The result revealed that Allozyme electrophoresis technique is based on the differ- P. gladius is the most closely related species to P. spathula, and ence of mobility of enzymes from different alleles of the same A. dabryanus can be considered phylogenetically to be the gene. Zhang et al. (1999b) reported that the activity of 11 sister species of A. sinensis. Other studies based on mtDNA proteins were detectable and 26 loci were screened, among supported these results (Zhang et al., 2000a, 2001; Peng et al., which only one locus was polymorphic. The percentage of 2007). polymorphic loci and heterozygosity was 0.039 and 0.004 respectively. Later, random amplified polymorphic DNA (RAPD) was also used to detect genetic variation in this Amur sturgeon and Kaluga species. Zhang et al. (2000a) screened the nuclear genomes via Quite a few (cyto)genetic reports dealing with the Amur RAPD analysis in 70 samples collected in the Yangtze River sturgeon were published previously (Song et al., 1997; Zhang A review on genetic studies in sturgeons 33 et al., 1999a; Ludwig et al., 2001; Robles et al., 2004, 2005). conservation. Unfortunately, most sturgeon farms in China Chen et al. (2004) reported that the Sox 9 gene has been could not establish sustained captive breeding programmes to widely expressed in the early eight stages, which indicated a built consistent brood stocks because of economic restrictions. conserved function of Sox 9 in the cartilage development At present, none of the sturgeon species complete their life among . Very recently, sex specific cDNA expres- cycle in a hatchery except for Amur sturgeon. Development of sion differences between female and male gonads in adult sustainable sturgeon aquaculture for both commercial and individuals of A. schrenckii were obtained (Chen et al., 2006). conservation purposes is hindered by a shortage of higher-age However, it is not clear whether the difference also exist in parental stock that can serve as a founder population in sex development and polarization at the beginning. No captivity. Preserving sufficient higher-age fish annually and gender specific genetic differences were observed in European developing captive breeding populations of A. sinensis, sturgeon, Acipenser sturio (Hett and Ludwig, 2005; Hett A. schrenckii and H. dauricus should become a national et al., 2005). Due to the different outcome by different species priority in fisheries science and management. Furthermore, the of Acipenseriformes, it is valuable to promote research about introduction of millions of fry of exotic sturgeon species and sex specific cDNA expression. Only unsatisfactory knowledge their hybrids to China will negatively impact native sturgeon has yet been gained for H. dauricus. Propagation biology of species because little efforts are presently undertaken to H. dauricus was analysed by Pan et al. (2001), who reported prevent escapement. There is an urgent need to improve that ovaries grew big as weight increased. However, egg management to maintain sturgeon biodiversity and sturgeon production was less than in A. schrenckii. In addition, Liang ecosystems. We believe that hatcheries should be very cautious et al. (2002) performed microsatellite investigations on with open-water rearing of sturgeons in net cages because of H. dauricus in samples from the Heilongjiang River. The the high risk for escapement and biological pollution and authors found relatively low genetic variation in this species. alternative and save culture methods should be employed even One hundred and sixty-nine DNA bands were amplified using if cage culture greatly reduces rearing costs. eleven microsatellites. Overall 47.93% of the loci were polymorphic. Acknowledgements We greatly appreciate the review and many subsequent Discussion and conclusion editorial suggestions of Arne Ludwig. We are grateful to Prof. There are eight indigenous species of Acipenseriformes in Qu Qiuzhi in Heilongjiang River Fishery Research Institute China, all of which are endangered resulting from various and Prof. Wei Qiwei in Yangtze River Fisheries Research human activities. All these species are protected as class 1 or Institute, who provided the source data about the sturgeon class II animals under the Chinese endangered species act. Of aquaculture. The research was funded by the National Natural all native species so far only five have been often used in Science Foundation of China (NSFC 30490234) and China genetic studies. These studies focused on genetic variation, three Gorges Project Corporation (no. 0799511). phylogenetic and evolution aspects and breeding programmes. Not only traditional methods but also molecular methods such as RAPD, mtDNA and microsatellites were widely used in References genetic studies in sturgeon. However, a scientific stock Anonymous (The Yangtze Aquatic Resources Survey Group), 1988: assessment for the Amur sturgeon or Chinese sturgeon based The biology of the sturgeon in Yangtze River and their artificial propagation. Sichuan Scientific and Technical Publishing House, on genetic diversity and on the population structure is still Chengdu. lacking. Little was known about the genetic influence or risks Billard, R.; Lecointre, G., 2001: Biology and conservation of sturgeon associated with restocking ⁄ rehabitation programmes on the and paddlefish. Biol. Fisher. 10, 355–392. wild populations. In comparison to the identification trials on Birstein, V. J.; Vasiliev, V. P., 1987: Tetraploid–octoploid relationships the origin of caviar products in European and North American and karyological evolution in order Acipenseriformes (Pisces), karyotypes, nucleoli and nucleolus-organizer regions in four countries, our molecular identification efforts on native reared acipenserid species. Genetica 73, 3–12. stocks presently commercially utilized in agriculture is far Blacklidge, K. H.; Bidwell, C. A., 1993: Three ploidy levels indicated behind, and this will impede progress in sturgeon aquaculture, by genomes quantification in Acipenseriformes of . trade control of black caviar and also the development of J. Hered. 84, 427–430. Burtsev, I. A.; Nikolaev, A. I.; Maltsev, S. A.; Igumnova, L. V., 2002: adequate strategies in conservation genetics. Formation of domesticated broodstocks as a guarantee of Commercial farming of sturgeons has become popular since sustainable hatchery reproduction of sturgeon for sea ranching. 1998. There are eleven species and hybrids presently cultured J. Appl. Ichthyol. 18, 655–658. in China, including imported species and hybrids. Acipenser Chang, J.; Cao, W., 1999: History and prospective of conservation on schrenckii and Amur hybrids are presently the major objects of the Chinese sturgeon in the Yangtze River. Acta Hydrobiol. Sinica 23, 712–720. commercial culture. Sturgeon aquaculture is practiced in about Chebanov, M. S.; Karnaukhov, G. I.; Galich, E. V.; Chmir, Y. N., 20 provinces, with major centres in the region of the Pearl 2002: Hatchery stock enhancement and conservation of sturgeon, River delta, the Yangtze delta as well as in the Fujian and with an emphasis on the Azov Sea populations. J. Appl. Ichthyol. Hubei provinces. The quantity of sturgeons produced by 18, 463–469. Chen, S.; Zhou, X., 1992: Studies on the artificial spawning of aquaculture in China appears to be the largest in the world as Acipenser schrenckii. Heilongjiang Fish. 4, 8–12. of the year 2000. However, there have not been any national or Chen, J.; Yuan, H.; Wang, B.; Liang, B.; Zhang, S., 2004: cDNA governmental programmes with a certain guaranteed invest- cloning, mRNA transcription of Sox 9 gene at early developmen- ment to preserve native sturgeons via aquaculture as a tool and tal stages in Amur Sturgeons (Acipenser schrenckii). Zool. Res. 25, very limited sturgeon culture facilities are employed for 527–533. Chen, J.; Wang, B.; Wu, W.; Lian, G.; Zhang, S., 2006: Cloning and conservation purposes in China. Successful breeding of stur- screening of differentially expressed genes from testis and ovary of geon in captivity is the key to establishing a sustainable Amur sturgeon. J. Fish. Sci. China 13, 8–12. sturgeon culture industry, which will also help sturgeon 34 B. Zhu et al.

Cui, E.; He, J. X.; Zheng, W. Z., 2006: The status analysis and Qu, Q.; Sun, D.; Ma, G.; Wu, W.; Qiu, L.; Wang, B., 2002: A note development suggestion on Sturgeons in China. Chin. Aquac. 6, report on artificial reproduction of Amur sturgeon, Acipenser 8–10. schrencki. J. Fish. Sci. China 9, 277–279. De Meulenaer, T.; Raymaker, C., 1996: Sturgeons of the Robles, F.; Herra´n, R.; Ludwig, A.; Rejo´n, C.; Rejo´na, M.; Garrido- and investigation of the international trade in Caviar. TRAFFIC Ramosa, M., 2004: Evolution of ancient satellite DNAs in International, Cambridge. sturgeon genomes. Gene 338, 133–142. Deng, X.; Deng, Z., 1997: Progress in the conservation biology of Robles, F.; de la Herra´n, R.; Ludwig, A.; Ruiz-Rejo´n, C.; Ruiz-Rejo´n, Chinese sturgeon. Zool. Res. 18, 113–120. M.; Garrido-Ramos, M. A., 2005: Genomic organization and Dingerkus, G.; Howell, W. M., 1976: Karyotypic analysis and evidence evolution of the 5S ribosomal DNA in the ancient fish sturgeon. of tetraploidy in the North American paddlefish, Polyodon Genome 48, 18–28. spathula. Science 194, 842–843. Rosenthal, H.; Pourkazemi, M.; Bruch, R., 2006: The 5th international Feng, G.; Zhang, P.; Zhang, L.; Zhang, T.; Huang, X.; Zhao, F., 2004: symposium on sturgeons: a conference with major emphasis on Status quo and prospects of sturgeon aquaculture in China. Mar. conservation, environmental mitigation and sustainable use of the Fish. 4, 317–320. sturgeon resources. J. Appl. Ichthyol. 22(Suppl. 1), 1–11. Fontana, F., 1994: Chromosomal nucleolar organizer regions in four Schrey, A. W.; Heist, E. J., 2007: Stock structure of sturgeon species as markers of karyotype evolution in Acipens- analyzed with microsatellite loci. J. Appl. Ichthyol. 23, 521–524. eriformes (Pisces). Genome 37, 888–892. Shao, Z.; Zhao, N.; Zhu, B.; Zhou, F.; Chang, J., 2002: Applicability Hett, A. K.; Ludwig, A., 2005: SRY-related (Sox) genes in the genome of microsatellite primers developed from shovelnose structure in of European (Acipenser sturio). Genome 48, Chinese sturgeon. Acta Hydrobiol. Sinica 6, 577–584. 181–186. Song, S.; Liu, H.; Sun, D.; Fan, Z., 1997: The karyotype and cellular Hett, A. K.; Pitra, C.; Jenneckens, I.; Ludwig, A., 2005: Character- DNA contents of Amur sturgeon (Acipenser schrencki). Hereditas ization of the Sox9 gene in European Atlantic sturgeon (Acipenser 19, 5–8. sturio). J. Hered. 96, 150–154. Sun, D.; Qu, Q.; Ma, G., 2003: The status of sturgeon culture in China. Jenneckens, I.; Meyer, J. N.; Rstgen-Schwark, G. H.; Debus, M. L.; J. Dalian Fish. Univ. 18, 216–221. Wedekind, H.; Ludwig, A., 2001: A fixed allele at microsatellite Wang, Y.; Chang, J., 2006: Status and conservation of sturgeons in locus LS-39 exhibiting species-specificity for the black caviar Amur River, China: a review based on surveys since the year 2000. producer, Acipenser stellatus. J. Appl. Ichthyol. 17, 39–42. J. Appl. Ichthyol. 22(Suppl. 1), 44–52. Krieger, J.; Fuerst, A., 2002: Evidence for a slowed rate of molecular Wang, Y.; Hu, M.; Cao, K., 2004: Preliminary discussion on evolution in the order Acipenseriformes. Mol. Biol. Evol. 19, 891– development and industrialization of the sturgeons in Yangtze 897. River. Beij. Aquac. 3, 8–10. Krieger, J.; Fuerst, A.; Cavender, T. M., 2000: Phylogenetic relation- Wang, D.; Wei, W.; Wang, C.; Luo, X., 2005: PCR-RFLP analysis of ships of the North American Sturgeons (Order Acipenseriformes) mitochondrial DNA in thirteen species of Acipenseriformes. J. based on mitochondrial DNA sequences. Mol. Biol. Evol. 16, 64– Fish. Sci. China 12, 383–389. 72. Wei, Q.; Yang, D., 1998: Strategy of conservation of sturgeons and Krieger, J.; Hett, A. K.; Fuerst, P. A.; Artyukhin, E.; Ludwig, A., paddlefish in the Yangtze River, the 21 CenturyÕs Ecological 2008: The molecular phylogeny of the order Acipenseriformes Environment and Conservation in Large Hydroelectric Projects revisited. J. Appl. Ichthyol. 24, (Suppl 1), 36–45. on the Yangtze River. The Chinese Environment Press, Beijing, Liang, L. Q.; Sun, X. W.; Dong, C. Z.; Yin, J. S., 2002: PCR analysis pp. 208–216. on genetic diversity of five species of Acipenseridae and Huso. J. Wei, Q.; Yang, D., 2003: Conservation and management of sturgeons Fish. Sci. China 9, 273–276. and paddlefish in China and their industrialization. Freshw. Fish. Ludwig, A., 2006: A sturgeon view on conservation genetics. Eur. J. 33, 3–7. Wildl. Res. 52, 3–8. Wei, Q.; Ke, F.; Zhang, J.; Zhuang, P.; Luo, J.; Zhou, R.; Yang, W., Ludwig, A., 2008: Identification of Acipenseriformes species in trade. 1997: Biology, fisheries, and conservation of sturgeons and J. Appl. Ichthyol. 24, (Suppl 1), 2–19. paddlefish in China. Environ. Biol. Fish. 48, 241–255. Ludwig, A.; May, B.; Debus, L.; Jenneckens, I., 2000: Heteroplasmy in Wei, Q.; He, J.; Yang, D.; Zheng, W.; Li, L., 2004: Status of sturgeon the mtDNA control region of sturgeon (Acipenser, Huso and aquaculture and sturgeon trade in China: a review based on two ). Genetics 156, 1933–1947. recent nationwide surveys. J. Appl. Ichthyol. 20, 321–332. Ludwig, A.; Belfiore, N. M.; Pitra, C.; Svirsky, V.; Jenneckens, I., Wirgin, I. I.; Stabile, J. E.; Waldman, J. R., 1997: Molecular analysis in 2001: Genome duplication events and functional reduction of the conservation of sturgeons and paddlefish. Environ. Biol. Fish. ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus). 48, 385–398. Genetics 158, 1203–1215. Wolf, C.; Hu¨bner, P.; Lu¨thy, J., 1999: Differentiation of sturgeon Ludwig, A.; Debus, L.; Jenneckens, I., 2002a: A molecular approach species by PCR–RFLP. Food Res. Int. 32, 699–705. for trading control of black caviar. Int. Rev. Hydrobiol. 87, 661– Wu, Y.; Lin, J., 1999: American paddlefish and its aquaculture. 674. Freshw. Fish. 1, 38–39. Ludwig, A.; Debus, L.; Lieckfeldt, D.; Wirgin, I.; Benecke, N.; Xiao, H.; Chang, J.; Liu, Y., 1999: Evaluation on status of artificial Jenneckens, I.; Williot, P.; Waldman, J. R.; Pitra, C., 2002b: propagation and releasing of Chinese sturgeon in the Yangtze When the American sea sturgeon swam east. Nature 419, 447– River. ACTA Hydrobiol. Sinica 23, 572–576. 448. Zhang, J., 1985: Fishery resources of Heilongjiang Province. The Ludwig, A.; Congiu, L.; Pitra, C.; Fickel, J.; Gessner, J.; Fontana, F.; haoxian Nationality Publishing House of Heilongjiang, Mudanji- Patarnello, T.; Zane, L., 2003: Nonconcordant evolutionary ang, pp. 352–389. history of maternal and paternal lineages in . Zhang, S.; Deng, H.; Wang, D.; Zhang, Y.; Wu, Q., 1999a: Mol. Ecol. 12, 3253–3264. Mitochondrial DNA length variation and heteroplasmy in Chi- May, B.; Krueger, C. C.; Kincaid, H. 1997: Genetic variation at nese sturgeon (Acipenser sinensis). Acta Genet. Sinica 26, 489–496. microsatellite loci in sturgeon: primer sequence homology in Zhang, S.; Deng, H.; Wei, Q.; Wang, D.; Wu, Q., 1999b: The Acipenser and Scaphirhynchus. Can. J. Fish. Aquat. Sci. 54, preliminary evidence for low genetic diversity in Chinese sturgeon 1542–1547. (Acipenser sinensis) revealed by protein electrophoresis. Zool. Res. Mcquown, E. C.; Sloss, B. L.; Sheehan, R. J.; Rodzen, J.; Trnah, G. J.; 2, 93–98. May, B., 2000: Microsatellite analysis of genetic variation in Zhang, S.; Deng, X.; Wang, D.; Wu, Q., 1999c: Studies on random sturgeon: new primer sequences for scaphirhynchus and acipenser. amplified polymorphic DNA in the relationship of 7 species in Trans. Am. Fish. Soc. 129, 1380–1388. Acipenseriforme. Prog. Nat. Sci. 9, 818–823. Pan, W. Z.; Yin, J. S.; Zhao, C. G.; Ye, G. F., 2001: Preliminary study Zhang, S.; Yan, Y.; Deng, H.; Wang, D.; Wei, Q.; Wu, Q., 1999d: on artificial progation of Huso dauricus and its hybridization with Genome size, ploidy characters of several species of sturgeons and acipenser Schrenckii. Chin. J. Fish. 14, 3–6. paddlefish with comment on cellular evolution of Acipenserifor- Peng, Z.; Ludwig, A.; Wang, D.; Diogo, R.; Wei, Q.; He, S., 2007: Age mes. Acta Zool. Sinica 45, 200–206. and biogeography of major clades in sturgeons and paddlefishes Zhang, S.; Deng, H.; Yan, Y.; Wang, D.; Wu, Q., 2000a: Random (Pisces: Acipenseriformes). Mol. Phylogenet. Evol. 42, 854–862. amplified polymorphic DNA (RAPD) and genetic diversity of Qu, Q.; Ma, G.; Sun, D., 1997: The sturgeons and the general situation Chinese sturgeon (Acipenser Sinensis). Oceanol. Limnol. Sinica of sturgeon developments in China. Chin. J. Fish. 9, 78–84. 31, 1–7. A review on genetic studies in sturgeons 35

Zhang, S.; Wu, Q.; Zhang, Y., 2001: On the taxonomic status of Zhu, B.; Zhao, N.; Shao, Z.; Lek, S.; Chang, J., 2006: Genetic Yangtze sturgeon, Asian and American based on population structure of Chinese sturgeon (Acipenser sinensis)in mitochondrial control region sequences. Acta Zool. Sinica 47, the Yangtze River revealed by artificial neural network. J. Appl. 632–639. Ichthyol. 22(Suppl. 1), 82–88. Zhang, S.; Wang, D.; Zhang, Y., 2003: Mitochondrial DNA variation, Zhuang, P.; Ke, F.; Wei, Q.; He, X.; Cen, Y., 1997: Biology and life effective female population size and population history of the history of DabryÕs sturgeon, Acipenser dabryanus, in the Yangtze endangered Chinese sturgeon, Acipenser sinensis. Conser. Genet. River. Environ. Biol. Fish. 48, 257–264. 4, 673–683. Zhuang, P.; Kynard, B.; Zhang, L.; Zhang, T.; Zhang, Z.; Li, D., 2002: Zhu, B.; Chang, J.; Tan, X.; Yu, G.; Xiao, C.; Wu, Z., 1999: Overview of biology and aquaculture of Amur sturgeon (Aci- Applicability of microsatellite DNA primers of for penser schrenckii) in China. J. Appl. Ichthyol. 18, 659–664. the parentage analyzing of Chinese sturgeon. ACTA Hydrobiol. Sinica 23, 547–553. AuthorÕs addresss: Zhu Bin, Department of conservation biology, Zhu, B.; Zhou, F.; Cao, H.; Shao, Z.; Zhao, N.; May, B.; Chang, J., Institute of Hydroecology, Ministry of Water 2002: Analysis of genetic variation in the Chinese sturgeon, Resources & Chinese Academy of Sciences, Acipenser sinensis: estimating the contribution of artificially Wuhan, Hubei 430079, China. produced larvae in a wild population. J. Appl. Ichthyol. 18, E-mail: [email protected] 301–306. The authors have not declared any conflict of interests. Zhu, B.; Liao, X.; Shao, Z.; Rosenthal, H.; Chang, J., 2005: Isolation and characterization of microsatellites in Chinese sturgeon, Acipenser sinensis. Mol. Ecol. Notes 5, 888–892.