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Malformations of the Endangered Chinese Sturgeon, Acipenser Sinensis, and Its Causal Agent

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Malformations of the Endangered Chinese Sturgeon, Acipenser Sinensis, and Its Causal Agent Malformations of the endangered Chinese sturgeon, Acipenser sinensis, and its causal agent Jianying Hua,1, Zhaobin Zhanga, Qiwei Weib, Huajun Zhena, Yanbin Zhaoa, Hui Penga, Yi Wana, John P. Giesyc,d,e, Luoxin Lib, and Bo Zhangf aCollege of Urban and Environmental Sciences, Peking University, Beijing 100871, China; bKey Laboratory of Freshwater Biodiversity Conservation and Utilization, Yangtze River Fisheries Research Institute, Chinese Academy of Fisheries Science, Ministry of Agriculture of China, Jingzhou, Hubei 434000, China; cDepartment of Veterinary Biomedical Sciences and Toxicology Center, University of Saskatchewan, 44 Campus Drive, Saskatoon, SK, Canada S7N 5B3; dDepartment of Zoology, Center for Integrative Toxicology, Michigan State University, East Lansing, MI 48824; eDepartment of Biology and Chemistry, Research Centre for Coastal Pollution and Conservation, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, SAR, China; and fKey Laboratory of Cell Proliferation and Differentiation, Center of Developmental Biology and Genetics, College of Life Sciences, Peking University, Beijing 100871, China Edited by Derek Muir, Environment Canada, Burlington, ON, Canada, and accepted by the Editorial Board April 8, 2009 (received for review September 20, 2008) The anadromous Chinese sturgeon (Acipenser sinensis) is endan- decreased (7), and intersex has been observed (5). These ob- gered and listed among the first class of protected animals in China. servations have indicated that synthetic chemicals may be having The possible causes for the decline of this species are the effects of adverse effects that could contribute to the population declines synthetic chemicals, and loss of critical habitat. Chinese sturgeon in observed for this endangered species. Chinese sturgeon are the Yangtze River have accumulated triphenyltin (TPT) to 31–128 exposed to relatively great concentrations of synthetic com- ng/g wet weigh (ww) in liver, which is greater than the concen- pounds, including musk fragrances and organochlorines, which trations of tributyltin (<1.0 ng/g ww). Maternal transfer of TPT has possibly affect the fertilization and, therefore, affect populations resulted in concentrations of 25.5 ؎ 13.0 ng/g ww in eggs of wild (8). However, until now, there has been no direct evidence that Chinese sturgeon, which poses a significant risk to the larvae exposure to synthetic compounds was related to adverse effects on naturally fertilized or hatched in the Yangtze River. The incidence the Chinese sturgeon population. Thus, it has been difficult to make of deformities in fry was 7.5%, with 1.2% of individuals exhibiting appropriate management policies for the protection of Chinese ocular abnormal development, and 6.3% exhibited skeletal/mor- sturgeon. phological deformations. The incidences of both ocular and skel- Both triphenyltin (TPT) and tributyltin (TBT) have been used etal/morphological deformations were directly proportional to the extensively in paints to prevent fouling of ship hulls and fishnets. TPT concentration in the eggs of both the Chinese sturgeon and the In addition to the fact that TPT concentrations measured in Siberian sturgeon (Acipenser baerii) in controlled laboratory stud- marine fish were unexpectedly greater than those of TBT ies. The rates of deformities in the controlled studies were consis- because of the trophic magnification of TPT (9, 10), TPT tent with the rates caused at the similar concentrations in eggs continues to be used as a contact fungicide to treat crops in collected from the field. Thus, TPT is the causal agent to induce the China. TPT acetate and TPT hydroxide are registered for use in malformation of larvae of Chinese sturgeon. The incidence of China especially as molluscicides to eliminate the golden apple deformed larvae of Chinese sturgeon is an indicator of overall snail (Pomacea canaliculata) in paddy fields where it has seri- population-level effects of TPT on Chinese sturgeon, because TPT ously threatened aquatic crops. Based on a questionnaire among at environmentally relevant concentrations can result in signifi- the pesticide companies that registered TPT pesticides, Ϸ200 cantly decrease both quality and quantity of eggs and spawning tons of TPT pesticides are manufactured in China. Although all frequency of fish. of the TPT usage in agriculture in Taiwan was completely prohibited in 1999, 27% of the surveyed farmers are still using teratogenesis ͉ fish ͉ triphenyltin ͉ Yangtze River TPT acetate illegally after the ban (11). Ocular and morphological malformations have been observed in embryos and larvae of European minnows (Phoxinus phoxi- uman activities have contributed to extinctions of species, nus) and zebrafish (Danio rerio) after in ovo exposure of TPT and can be a contributing factor to decreases in populations. H (12, 13) and in the offspring of medaka (Oryzias latipes) mater- In particular, some pesticides can adversely affect endangered nally exposed to TBT and TPT (14, 15). Also, TBT and TPT can species (1–3). Sturgeons belong to one of the most ancient inhibit reproduction (14, 15). Therefore, in the present study, the groups of the Osteichthyes. Because of their desirability as food, following questions were addressed. (i) Is TPT accumulated by their long-life, and changes in their habitats, populations of Chinese sturgeon and then transferred to the eggs? (ii) Can the sturgeon have declined globally. All extant sturgeon species are malformation be observed in wild Chinese sturgeon population? listed as ‘‘protected’’ under the Convention on the International (iii) Can the malformations observed in larvae and fry of wild Trade of Endangered Species. Among the 25 extant sturgeon Chinese sturgeon be caused by TPT under controlled laboratory species, the Chinese sturgeon (Acipenser sinensis) is an anadro- conditions? Nanoinjection techniques were used to accurately mous fish that has survived at the edge of extinction, and is listed determine the effects of known concentrations including envi- among the first class of protected animals in China (4). ronmentally relevant concentrations of TPT on both Chinese The Chinese sturgeon inhabits the East China and Yellow sturgeon and Siberian sturgeon eggs. Seas, and spawns in the Yangtze River. Loss of critical spawning habitat because of construction of the Three-Gorges Dam and Gezhouba Dam on the Yangtze River is thought to have Author contributions: J.H., Q.W., Y.W., and J.P.G. designed research; Z.Z., H.Z., Y.Z., H.P., contributed to a steep population decline (4, 5). To save this and L.L. performed research; B.Z. contributed new reagents/tools; and J.H. wrote the paper. endangered species, in the 1980s, the Chinese government began The authors declare no conflict of interest. an artificial propagation program. However, this program has This article is a PNAS Direct Submission. D.M. is a guest editor invited by the Editorial Board. 1 not resulted in the recovery of the Chinese sturgeon population. To whom correspondence should be addressed. E-mail: [email protected]. SCIENCES Also, the female:male sex ratio has changed from 0.79 in This article contains supporting information online at www.pnas.org/cgi/content/full/ ENVIRONMENTAL 1981–1993 (5) to 5.9 in 2003–2004 (6), the motility of sperm has 0809434106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0809434106 PNAS ͉ June 9, 2009 ͉ vol. 106 ͉ no. 23 ͉ 9339–9344 Downloaded by guest on September 27, 2021 Table 1. Concentrations of BTs and PTs in different tissues (ng/g ww) of the Chinese sturgeon Tissue Lipid, % Value MBT DBT TBT BTs MPT DPT TPT PTs Liver, n ϭ 8 12.2 Ϯ 7.4 Min 9.1 11.8 Ͻ1.0 20.9 Ͻ2.0 5.8 30.8 37.6 Max 1,115 257 Ͻ1.0 1,373 104 324 128 468 Mean Ϯ SD 293 Ϯ 366 72.1 Ϯ 81.0 — 365 Ϯ 447 33.3 Ϯ 30.9 66.3 Ϯ 105 68.0 Ϯ 31.2 168 Ϯ 134 Heart, n ϭ 7 4.2 Ϯ 1.7 Min 5.2 7.6 Ͻ1.0 14.6 Ͻ2.0 1.9 28.3 31.2 Max 12.5 15.9 3.8 28.6 4.4 6.4 73.5 79.6 Mean Ϯ SD 9.3 Ϯ 3.0 10.8 Ϯ 2.9 1.4 Ϯ 1.5 21.4 Ϯ 5.7 1.5 Ϯ 1.3 3.6 Ϯ 1.7 53.0 Ϯ 15.8 58.1 Ϯ 16.9 Muscle, n ϭ 8 1.9 Ϯ 1.2 Min 1.5 2.2 Ͻ1.0 4.1 Ͻ2.0 0.7 17.7 18.4 Max 8.3 7.5 4.3 20.2 Ͻ2.0 3.3 56.7 58.8 Mean Ϯ SD 3.7 Ϯ 2.3 4.6 Ϯ 1.7 1.3 Ϯ 1.4 9.6 Ϯ 4.8 — 1.8 Ϯ 0.8 38.2 Ϯ 14.9 40.0 Ϯ 15.4 Gill, n ϭ 6 2.4 Ϯ 0.6 Min 12.3 3.1 Ͻ1.0 18.0 Ͻ2.0 Ͻ1.0 7.6 8.1 Max 23.8 14.6 Ͻ1.0 37.7 Ͻ2.0 8.2 42.6 45.4 Mean Ϯ SD 18.2 Ϯ 4.7 7.7 Ϯ 3.9 — 25.9 Ϯ 7.5 — 2.4 Ϯ 3.2 25.5 Ϯ 13.0 27.9 Ϯ 14.3 Roe, n ϭ 15 33.7 Ϯ 9.8 Min Ͻ1.5 2.2 Ͻ1.0 3.4 Ͻ2.0 Ͻ1.0 7.8 9.1 Max 10.8 10.8 Ͻ1.0 15.8 Ͻ2.0 2.4 53.5 55.6 Mean Ϯ SD 5.9 Ϯ 3.7 4.0 Ϯ 2.0 — 9.9 Ϯ 4.0 — 1.3 Ϯ 0.8 25.6 Ϯ 13.0 26.9 Ϯ 13.4 Gonad, n ϭ 6 3.6 Ϯ 1.7 Min 3.4 4.0 Ͻ1.0 8.2 Ͻ2.0 Ͻ1.0 7.1 7.9 Max 20.0 14.0 Ͻ1.0 34.0 Ͻ2.0 2.4 32.6 35.0 Mean Ϯ SD 8.8 Ϯ 6.7 8.9 Ϯ 4.2 — 17.7 Ϯ 10.5 — 1.0 Ϯ 0.7 16.6 Ϯ 9.3 17.6 Ϯ 9.8 Adipose, n ϭ 566Ϯ 18 Min Ͻ1.5 Ͻ1.0 Ͻ1.0 Ͻ3.5 Ͻ2.0 Ͻ1.0 Ͻ1.0 Ͻ4.0 Max 3.6 5.3 Ͻ1.0 6.2 Ͻ2.0 2.5 37.3 39.9 Mean Ϯ SD 1.3 Ϯ 1.3 1.9 Ϯ 2.1 — 3.2 Ϯ 2.7 — 0.9 Ϯ 0.9 15.8 Ϯ 17.7 16.7 Ϯ 18.3 Intestine, n ϭ 7 2.8 Ϯ 1.6 Min Ͻ1.5 2.8 Ͻ1.0 3.5 Ͻ2.0 Ͻ1.0 6.1 6.6 Max 20.1 9.7 Ͻ1.0 26.7 Ͻ2.0 1.5 16.3 17.6 Mean Ϯ SD 12.4 Ϯ 6.1 6.3 Ϯ 2.3 — 18.7 Ϯ 8.0 — 0.6 Ϯ 0.4 11.5 Ϯ 4.4 12.1 Ϯ 4.5 Stomach, n ϭ 5 1.3 Ϯ 0.4 Min Ͻ1.5 4.3 Ͻ1.0 6.1 Ͻ2.0 Ͻ1.0 5.5 5.5 Max 4.4 8.5 Ͻ1.0 11.3 Ͻ2.0 Ͻ1.0 15.1 15.1 Mean Ϯ SD 2.3 Ϯ 1.3 6.5 Ϯ 1.8 — 8.9 Ϯ 2.4 — — 10.1 Ϯ 4.0 10.1 Ϯ 4.0 Pancreas, n ϭ 2 6.8 Min 2.6 6.4 Ͻ1.0 9.0 Ͻ2.0 Ͻ1.0 22.3 23.1 Max 10.2 8.3 Ͻ1.0 18.5 Ͻ2.0 5.1 22.6 27.4 Kidney, n ϭ 1 31.5 — 33.5 36.9 4.0 74.4 12.5 40.0 70.0 122 Gallbladder, n ϭ 1 23.0 — 9.0 5.7 Ͻ1.0 14.7 4.4 7.1 11.0 22.4 Spleen, n ϭ 1 ND — 11.2 13.6 Ͻ1.0 24.8 3.4 2.1 40.4 46.0 ND, not determined.
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