First record of a morphologically abnormal and highly metal-contaminated Spotback Skate Atlantoraja castelnaui (Rajiformes: Arhynchobatidae) from southeastern Rio de Janeiro, Brazil

Main Article Content

Rachel Ann Hauser-Davis
https://orcid.org/0000-0002-9451-471X
Márcio L.V. Barbosa-Filho
https://orcid.org/0000-0002-1162-3575
Lucia Helena S. de S. Pereira
https://orcid.org/0000-0003-0347-8213
Catarina A. Lopes
https://orcid.org/0000-0002-1191-2852
Sérgio C. Moreira
https://orcid.org/0000-0002-3550-9515
Rafael C.C. Rocha
https://orcid.org/0000-0002-6495-7093
Tatiana D. Saint’Pierre
https://orcid.org/0000-0002-7619-5620
Paula Baldassin
https://orcid.org/0000-0002-1140-302X
Salvatore Siciliano
https://orcid.org/0000-0002-0124-8070

Abstract

This paper reports the first record of a morphologically abnormal and highly metal-contaminated Spotback Skate Atlantoraja castelnaui (Ribeiro, 1907) (Elasmobranchii, Rajidae) in Rio de Janeiro, Brazil. Incomplete fusion of the right pectoral fin with the head was observed, while a radiography indicated muscle sheaf discontinuity near the rostrum.  Extremely high contamination by several elements, including teratogenic As, Hg and Cd in the individual was detected.  The observed morphological deformity may be due to high concentrations of teratogenic elements in the environment, possibly playing a role in abnormal embryonic development in egg cases exposed to high environmental concentrations of these contaminants.  Atlantoraja castelnaui is the least biologically understood member of the genus Atlantoraja, and this paper furthers both morphological observations and ecotoxicological assessments on this species. 

Article Details

How to Cite
[1]
Rachel Ann Hauser-Davis, Márcio L.V. Barbosa-Filho, Lucia Helena S. de S. Pereira, Catarina A. Lopes, Sérgio C. Moreira, Rafael C.C. Rocha, Tatiana D. Saint’Pierre, Paula Baldassin and Salvatore Siciliano 2020. First record of a morphologically abnormal and highly metal-contaminated Spotback Skate Atlantoraja castelnaui (Rajiformes: Arhynchobatidae) from southeastern Rio de Janeiro, Brazil. Journal of Threatened Taxa. 12, 11 (Aug. 2020), 16510–16520. DOI:https://doi.org/10.11609/jott.5903.12.11.16510-16520.
Section
Communications

References

Ahlstrom, E.H. & Bigelow, H.B. (1963). Fishes of the Western North Atlantic. Part Four. Soft-Rayed Bony Fishes: Orders Isospondyli and Giganturoidei: Argentinoids, Stomiatoids, Pickerels, Bathylaconids, Giganturids. Yale, 599pp.

Alavi-Yeganeh, M.S, S. Razavi & J.P. Egan (2019). Taillessness and skeletal deformity in striped piggy Pomadasys stridens (Osteichthyes: Haemulidae) from the Persian Gulf. Diseases of Aquatic Organisms 132: 209–213. https://doi.org/10.3354/dao03322 DOI: https://doi.org/10.3354/dao03322

ANVISA (2013). RESOLUÇÃO - RDC N- 42, DE 29 DE AGOSTO DE 2013. Available at: http://bvsms.saude.gov.br/bvs/saudelegis/anvisa/2013/rdc0042_29_08_2013.html

ATSDR (2017). Lead Toxicity: What Are Possible Health Effects from Lead Exposure? Available at: https://www.atsdr.cdc.gov/csem/csem.asp?csem=34&po=10

Azevedo-Silva, C.E., A. Azeredo, A.C.L. Dias, P. Costa, J. Lailson-Brito, O. Malm, J.R.D. Guimarães & J.P.M Torres (2009). Organochlorine compounds in sharks from the Brazilian coast. Marine Pollution Bulletin 58: 294–298. https://doi.org/0.1016/j.marpolbul.2008.11.003

Barbini, S.A. & L.O. Lucifora (2012). Feeding habits of a large endangered skate from the south-west Atlantic: The spotback skate, Atlantoraja castelnaui. Marine and Freshwater Research 63: 180–188. https://doi.org/10.1071/MF11170 DOI: https://doi.org/10.1071/MF11170

Bengtsson, B.E. & G. Lithner (1988). Vertebral defects in fourhorn sculpin, Myoxocephalus quadricornis L., exposed to heavy metal pollution in the Gulf of Bothnia. Journal of Fish Biology 33: 517–529. https://doi.org/10.1111/j.1095-8649.1988.tb05496.x DOI: https://doi.org/10.1111/j.1095-8649.1988.tb05496.x

Braga, E.S., J.S. Azevedo, L. Kuniyoshi & D.I.T. Fávaro (2019). Zn, Co, Cr, As, and genotoxic effects in the ichthyofauna species from polluted and non-polluted/protected estuaries of the São Paulo Coast, Brazil. Anais da Academia Brasileira de Ciências 91: e20190066. https://doi.org/10.1590/0001-3765201920190066 DOI: https://doi.org/10.1590/0001-3765201920190066

Casarini, L.M., U.L. Gomes & O.B.G. Tomas (1996). Would be Santos harbour dredged material dumping a reason of teratogeny on Raja agassizi?. In: Abstracts of the VII Congresso Latino-Americano sobre Ciências do Mar Caderno de Resumos 7: 152–153. (SBEEL: Santos, Brazil.)

Cheng, S.H., A.W.K. Wai, C.H. So & R.S.S. Wu (2000). Cellular and molecular basis of cadmium-induced deformities in zebrafish embryos. Environmental Toxicology and Chemistry 19: 3024–3031. https://doi.org/10.1002/etc.5620191223 DOI: https://doi.org/10.1002/etc.5620191223

China (2005). GB2762-2005 - National Food Safety Standard Maximum Levels of Contaminants in Food. Available at: https://apps.fas.usda.gov/newgainapi/api/report/downloadreportbyfilename?filename=Maximum%20Levels%20of%20Contaminants%20in%20Foods%20_Beijing_China%20-%20Peoples%20Republic%20of_12-11-2014.pdf

Codex Alimentarius Commission (2009). Report of the 32nd session of the Codex Committee on Nutrition and Foods for Special Dietary Uses (ALINORM 09/32/REP). Available at: https://www.usda.gov/codex

Dawson, D.A., E.F. Stebler, S.L. Burks & J.A. Bantle (1988). Evaluation of the developmental toxicity of metal-contaminated sediments using short-term fathead minnow and frog embryo-larval assays. Environmental Toxicology and Chemistry 7: 27–34.

de Moura, J.F., A. Merico, R.C. Montone, J. Silva, T.G. Seixas, J.M. Godoy, T.D. Saint’Pierre, R.A. Hauser-Davis, A.P.M. Di Beneditto, E.C. Reis, D.V. Tavares, L.S. Lemos & S. Siciliano (2015). Assessment of trace elements, POPs, 210Po and stable isotopes (15N and 13C) in a rare filter-feeding shark: The megamouth. Marine Pollution Bulletin 95: 402–406. https://doi.org/10.1016/j.marpolbul.2015.03.038 DOI: https://doi.org/10.1016/j.marpolbul.2015.03.038

Dulvy, N.K. & J.D. Reynolds (1997). Evolutionary transitions among egg-laying, live-bearing and maternal inputs in sharks and rays. Proceedings of the Royal Society B: Biological Sciences 264: 1309–1315. https://doi.org/10.1098/rspb.1997.0181 DOI: https://doi.org/10.1098/rspb.1997.0181

Dulvy, N.K. & J.D. Reynolds (2002). Predicting extinction vulnerability in skates. Conservation Biology 16: 440–450. https://doi.org/10.1046/j.1523-1739.2002.00416.x DOI: https://doi.org/10.1046/j.1523-1739.2002.00416.x

Ebert, D.A. & J. Sulikowski (2009). Biology of Skates. In: Noakes, D.L.G. (series ed.) Developments in Environmental Biology of Fishes. Springer-Verlag, Heidelberg, 244pp. DOI: https://doi.org/10.1007/978-1-4020-9703-4

Eisler, R. (1988a). Contaminant Hazard Reviews Arsenic Hazards to Fish, Wildlife, and Invertabrates: A Synoptic Review. Contaminant Hazard Reviews, U.S. Department of the Interior, Fish and Wildlife Service 85(1.12) 92pp.

Eisler, R. (1988b). Lead hazards to fish, wildlife, and invertebrates: A synoptic review. Contaminant Hazard Reviews, U.S. Department of the Interior, Fish and Wildlife Service 85(1.14) 134pp.

Ferrante, M., A.M. Pappalardo, V. Ferrito, V. Pulvirenti, C. Fruciano, A. Grasso, S. Sciacca, C. Tigano & C. Copat (2017). Bioaccumulation of metals and biomarkers of environmental stress in Parablennius sanguinolentus (Pallas 1814) sampled along the Italian coast. Marine Pollution Bulletin 122: 288–296. https://doi.org/10.1016/j.marpolbul.2017.06.060 DOI: https://doi.org/10.1016/j.marpolbul.2017.06.060

Figueiredo, J.L., N.A. Menezes (2015). Manual de peixes marinhos do sudeste do Brasil. São Paulo: Museu de Zoologia, USP, 105pp. https://doi.org/10.5962/bhl.title.109986 DOI: https://doi.org/10.5962/bhl.title.109986

Flik, G., X.J.H.X. Stouthart, F.A.T. Spanings, R.A.C. Lock, J.C. Fenwick & S.E.W. Bonga (2002). Stress response to waterborne Cu during early life stages of carp Cyprinus carpio. Aquatic Toxicology 56: 167–176. https://doi.org/10.1016/S0166-445X(01)00202-8 DOI: https://doi.org/10.1016/S0166-445X(01)00202-8

Frenzilli, G., M. Bernardeschi, P. Guidi, V. Scarcelli, P. Lucchesi, L. Marsili, M.C. Fossi, A. Brunelli, G. Pojana, A. Marcomini & M. Nigro (2014). Effects of in vitro exposure to titanium dioxide on DNA integrity of Bottlenose Dolphin (Tursiops truncatus) fibroblasts and leukocytes. Marine Environmental Research 100: 67–73. https://doi.org/10.1016/j.marenvres.2014.01.002 DOI: https://doi.org/10.1016/j.marenvres.2014.01.002

Gao, Y., P. Baisch, N. Mirlean, F.M.R. da Silva Júnior, N. Van Larebeke, W. Baeyens & M. Leermakers (2018). Arsenic speciation in fish and shellfish from the North Sea (Southern bight) and Açu Port area (Brazil) and health risks related to seafood consumption. Chemosphere 191: 89–96. https://doi.org/10.1016/j.chemosphere.2017.10.031 DOI: https://doi.org/10.1016/j.chemosphere.2017.10.031

Hallare, A.V., M. Schirling, T. Luckenbach, H.R. Köhler & R. Triebskorn (2005). Combined effects of temperature and cadmium on developmental parameters and biomarker responses in zebrafish (Danio rerio) embryos. Journal of Thermal Biology 30: 7–1. https://doi.org/10.1016/j.jtherbio.2004.06.002 DOI: https://doi.org/10.1016/j.jtherbio.2004.06.002

González-Doncel, M., M. Larrea, S. Sánchez-Fortún & D.E. Hinton (2003). Influence of water hardening of the chorion on cadmium accumulation in Medaka (Oryzias latipes) eggs. Chemosphere 52: 75–83. https://doi.org/10.1016/S0045-6535(03)00227-3 DOI: https://doi.org/10.1016/S0045-6535(03)00227-3

Gonzalez, H.O., J.A. Roling, W.S. Baldwin & L.J. Bain (2006). Physiological changes and differential gene expression in Mummichogs (Fundulus heteroclitus) exposed to arsenic. Aquatic Toxicology 77: 43–52. https://doi.org/10.1016/j.aquatox.2005.10.014 DOI: https://doi.org/10.1016/j.aquatox.2005.10.014

Guo, W.D., M.H. Hu, Y.P. Yang, Z.B. Gong & Y.Wu (2003). Characteristics of ecological chemistry of rare earth elements in fish from Xiamen Bay. Oceanologia Et Limnologia Sinica 34: 241–248.

Hirano, S. & K.T. Suzuki (1996). Exposure metabolism and toxicity of rare earths and related compounds. Environmental Health Perspectives 104: 85–95. https://doi.org/10.1289/ehp.96104s185 DOI: https://doi.org/10.1289/ehp.96104s185

Hiraoka, Y. & H. Okuda (1983). Characteristics of vertebral abnormalities of Medaka as a water pollution indicator. Hiroshima Journal of Medical Sciences 32: 261–266

Holcombe, G.W., D.A. Benoit, E.N. Leonard & J.M. McKim (1976). Long-term effects of lead exposure on three generations of brook trout (Salvelinus fontinalis). Journal of the Fisheries Research Board of Canada 33: 1731–1741. https://doi.org/10.1139/f76-220 DOI: https://doi.org/10.1139/f76-220

Holsbeek, L., C.R. Joiris, V. Debacker, I.B. Ali, P. Roose, J.P. Nellissen, S. Gobert, J.M. Bouquegneau & M. Bossicart (1999). Heavy metals, organochlorines and polycyclic aromatic hydrocarbons in sperm whales stranded in the southern North Sea during the 1994/1995 winter. Marine Pollution Bulletin 38: 304–313. https://doi.org/10.1016/S0025-326X(98)00150-7 DOI: https://doi.org/10.1016/S0025-326X(98)00150-7

Holsbeek, L., U. Siebert & C.R. Joiris (1998). Heavy metals in dolphins stranded on the French Atlantic coast. Science of the Total Environment 217: 241–249. https://doi.org/10.1016/S0048-9697(98)00177-6 DOI: https://doi.org/10.1016/S0048-9697(98)00177-6

Hozbor, N., A. Massa & C.M. Vooren, (2004). Atlantoraja castelnaui. The IUCN Red List of Threatened Species 2004: e.T44575A10921544.

Hu. Z., S. Haneklaus, G. Sparovek & E. Schnug (2006). Rare earth elements in soils. Communications in Soil Science and Plant Analysis 37: 1381–1420. https://doi.org/10.1080/00103620600628680 DOI: https://doi.org/10.1080/00103620600628680

Huang, P., J. Li, S. Zhang, C. Chen, Y. Han, N. Liu, Y. Xiao, H. Wang, M. Zhang, Q. Yu, Y. Liu & W. Wang (2011). Effects of lanthanum cerium and neodymium on the nuclei and mitochondria of hepatocytes: Accumulation and oxidative damage. Environmental Toxicology and Pharmacology 31: 25–32. https://doi.org/10.1016/j.etap.2010.09.001 DOI: https://doi.org/10.1016/j.etap.2010.09.001

Jagoe, C.H. & T.A. Haines (1985). Fluctuating asymmetry in fishes inhabiting acidified and unacidified lakes. Canadian Journal of Zoology 63: 130–138. https://doi.org/10.1139/z85-022 DOI: https://doi.org/10.1139/z85-022

Jezierska, B., K. Ługowska & M. Witeska (2009). The effects of heavy metals on embryonic development of fish (a review). Fish Physiology and Biochemistry 36: 625–640. https://doi.org/10.1007/s10695-008-9284-4 DOI: https://doi.org/10.1007/s10695-008-9284-4

Jha, A.M. & A.C. Singh (1995). Clastogenicity of lanthanides: induction of chromosomal aberration in bone marrow cells of mice in vivo. Mutation Research - Genetic Toxicology and Environmental Mutagenesis 341 193–197. https://doi.org/10.1016/0165-1218(95)90009-8 DOI: https://doi.org/10.1016/0165-1218(95)90009-8

Kessabi, K., A. Annabi, A.I.H. Hassine, I. Bazin, W. Mnif, K. Said & I. Messaoudi (2013). Possible chemical causes of skeletal deformities in natural populations of Aphanius fasciatus collected from the Tunisian coast. Chemosphere 90: 2683–2689. https://doi.org/10.1016/j.chemosphere.2012.11.047 DOI: https://doi.org/10.1016/j.chemosphere.2012.11.047

Kessabi, K., A. Kerkeni, K. Saïd & I. Messaoudi (2009). Involvement of Cd bioaccumulation in spinal deformities occurrence in natural populations of mediterranean killifish. Biological Trace Element Research 128: 72–81. https://doi.org/10.1007/s12011-008-8255-z DOI: https://doi.org/10.1007/s12011-008-8255-z

Laveuf, C. & S. Cornu (2009). A review on the potentiality of Rare Earth Elements to trace pedogenetic processes. Geoderma 154: 1–12. https://doi.org/10.1016/j.geoderma.2009.10.002 DOI: https://doi.org/10.1016/j.geoderma.2009.10.002

Lemos, S.L., J.F. de Moura, R.A. Hauser-Davis, R.C. de Campos & S. Siciliano (2013). Small cetaceans found stranded or accidentally captured in southeastern Brazil: Bioindicators of essential and non-essential trace elements in the environment. Ecotoxicology and Environmental Safety 97:166-175. https://doi.org/10.1016/j.ecoenv.2013.07.025 DOI: https://doi.org/10.1016/j.ecoenv.2013.07.025

Mayfield, D.B. & A. Fairbrother (2015). Examination of rare earth element concentration patterns in freshwater fish tissues. Chemosphere 120: 68–74. https://doi.org/10.1016/j.chemosphere.2014.06.010 DOI: https://doi.org/10.1016/j.chemosphere.2014.06.010

Mejía-Falla, P.A., A.F. Navia & L.A. Muñoz (2011). First record of morphological abnormality in embryos of Urotrygon rogersi (Jordan & Starks, 1895) (Myliobatiformes: Urotrygonidae) in the Tropical Eastern Pacific. Latin American Journal of Aquatic Research 39: 184–188. https://doi.org/10.3856/vol39-issue1-fulltext-19

Messaoudi, I., T. Deli, K. Kessabi, S. Barhoumi, A. Kerkeni & K. Saïd (2009). Association of spinal deformities with heavy metal bioaccumulation in natural populations of grass goby Zosterisessor ophiocephalus Pallas 1811 from the Gulf of Gabès (Tunisia). Environmental Monitoring and Assessment 156: 551–560. https://doi.org/10.1007/s10661-008-0504-2 DOI: https://doi.org/10.1007/s10661-008-0504-2

Moermond, C.T.A., J. Tijink, A.P. Van Wezel & A.A. Koelmans (2001). Distribution speciation and bioavailability of lanthanides in the Rhine-Meuse estuary the Netherlands. Environmental Toxicology and Chemistry 20: 1916–1926. https://doi.org/10.1002/etc.5620200909 DOI: https://doi.org/10.1002/etc.5620200909

Moreira, R.A., U.L. Gomes & M.R. de Carvalho (2011). Morphological description of Dipturus mennii (Chondrichthyes: Elasmobranchii: Rajidae) and its differentiation from Dipturus trachyderma. Zoologia 28: 97–111. https://doi.org/10.1590/S1984-46702011000100014 DOI: https://doi.org/10.1590/S1984-46702011000100014

Munkittrick, K.R. & D.G. Dixon (1989). Effects of natural exposure to copper and zinc on egg size and larval copper tolerance in white sucker (Catostomus commersoni). Ecotoxicology and Environmental Safety 18: 15–26. https://doi.org/10.1016/0147-6513(89)90088-2 DOI: https://doi.org/10.1016/0147-6513(89)90088-2

Oddone, M.C., A.F. Amorim & P.L. Mancini (2008). Reproductive biology of the spotback skate, Atlantoraja castelnaui (Ribeiro, 1907) (Chondrichthyes, Rajidae), in southeastern Brazilian waters. Revista de Biología Marina y Oceanografía 43: 327–334.

Osman, A.G.M., S. Wuertz, I.A. Mekkawy, H.J. Exner & F. Kirschbaum (2007). Lead induced malformations in embryos of the African catfish Clarias gariepinus (Burchell 1822). Environmental Toxicology 22: 375–389. https://doi.org/10.1002/tox.20272 DOI: https://doi.org/10.1002/tox.20272

Redling, K. (2006). Rare Earth Elements in Agriculture with Emphasis on Animal Husbandry. DVG-Service, Munich, 326pp.

Ribeiro, A.M. (1907). Fauna Brasiliense. Peixes. II. Desmobranchios. Archivos do Museu Nacional do Rio Janeiro 14:129–212

Ribeiro-Prado, C.C., M.C. Oddone, M.M.B. Gonzalez, A.F. Amorim & C. Capapé (2008). Morphological abnormalities in skates and rays (Chondrichthyes) from off southeastern Brazil. Arquivos de Ciências do Mar 41: 21–28

Rim, K.T., K.H. Koo & J.S. Park (2013). Toxicological evaluations of rare earths and their health impacts to workers: A literature review. Safety and Health at Work 4: 12–26. https://doi.org/10.5491/SHAW.2013.4.1.12 DOI: https://doi.org/10.5491/SHAW.2013.4.1.12

Rossouw, G.J. (1987). Function of the liver and hepatic lipids of the lesser sand shark, Rhinobatos annulatus (Müller & Henle). Comparative Biochemistry and Physiology - Part B: Biochemistry & Molecular Biology 86: 785–790. https://doi.org/10.1016/0305-0491(87)90225-2 DOI: https://doi.org/10.1016/0305-0491(87)90225-2

Ruelas-Inzunza, J., Z. Šlejkovec, D. Mazej, V. Fajon, M. Horvat & M. Ramos-Osuna (2018). Bioaccumulation of As, Hg, and Se in tunas Thunnus albacares and Katsuwonus pelamis from the Eastern Pacific: tissue distribution and As speciation. Environmental Science and Pollution Research 25: 19499–19509. https://doi.org/10.1007/s11356-018-2166-0 DOI: https://doi.org/10.1007/s11356-018-2166-0

Sandheinrich, M.B. & J.G. Wiener (2011). Methylmercury Freshwater Fish: Recent Advances in Assessing Toxicity and Environmentally Relevant Exposures, pp. 169–190. In: Beyer, W.N. & J.P. Meador (eds.). Environmental Contaminants in Biota CRC Press/Taylor and Francis, Boca Raton, FL, 768pp.

Slooff, W. (1982). Skeletal anomalies in fish from polluted surface waters. Aquatic Toxicology 2: 157–173. https://doi.org/10.1016/0166-445X(82)90013-3 DOI: https://doi.org/10.1016/0166-445X(82)90013-3

Somasundaram, B., P.E. King & S. Shackley (1984). The effects of zinc on postfertilization development in eggs of Clupea harengus L. Aquatic Toxicology 5: 167–178. https://doi.org/10.1016/0166-445X(84)90007-9 DOI: https://doi.org/10.1016/0166-445X(84)90007-9

Stouthart, A.J.H.X., F.A.T. Spanings, R.A.C. Lock & S.E.W. Bonga (1995). Effects of water pH on chromium toxicity to early life stages of the common carp (Cyprinus carpio). Aquatic Toxicology 32: 31–42. https://doi.org/10.1016/0166-445X(94)00079-6 DOI: https://doi.org/10.1016/0166-445X(94)00079-6

Sun, P.L., W.E. Hawkins, R.M. Overstreet & N.J. Brown-Peterson (2009). Morphological deformities as biomarkers in fish from contaminated rivers in Taiwan. International Journal of Environmental Research and Public Health 6: 2307–2331. https://doi.org/10.3390/ijerph6082307 DOI: https://doi.org/10.3390/ijerph6082307

Taylor, H.E., R.C. Antweiler, D.A. Roth, C.N. Alpers & P. Dileanis (2012). Selected trace elements in the Sacramento River, California: Occurrence and distribution. Archives of Environmental Contamination and Toxicology 62: 557–569. https://doi.org/10.1007/s00244-011-9738-z DOI: https://doi.org/10.1007/s00244-011-9738-z

Weis, J.S. & P. Weis (1977). Effects of heavy metals on development of the killifish, Fundulus heteroclitus. Journal of Fish Biology 11: 49–54. https://doi.org/10.1111/j.1095-8649.1977.tb04097.x DOI: https://doi.org/10.1111/j.1095-8649.1977.tb04097.x

Woodworth, J. & D. Pascoe (1982). Cadmium toxicity to rainbow trout, Salmo gairdneri Richardson: a study of eggs and alevins. Journal of Fish Biology 21: 47–57. https://doi.org/10.1111/j.1095-8649.1982.tb02822.x DOI: https://doi.org/10.1111/j.1095-8649.1982.tb02822.x

Yang, X., D. Yin, H. Sun, X. Wang, L. Dai, Y. Chen, M. Cao (1999). Distribution and bioavailability of rare earth elements in aquatic microcosm. Chemosphere 39: 2443–2450. https://doi.org/10.1016/S0045-6535(99)00172-1 DOI: https://doi.org/10.1016/S0045-6535(99)00172-1

Zhang, H., H. Cao, Y. Meng, G. Jin & M. Zhu (2012). The toxicity of cadmium (Cd2+) towards embryos and pro-larva of soldatov’s catfish (Silurus soldatovi). Ecotoxicology and Environmental Safety 80: 258–265. https://doi.org/10.1016/j.ecoenv.2012.03.013 DOI: https://doi.org/10.1016/j.ecoenv.2012.03.013