Investigating lethal and sublethal effects of the trace metals cadmium, cobalt, lead, nickel and zinc on the anemone Aiptasia pulchella, a cnidarian representative for ecotoxicology in tropical marine environments
Pelli L. Howe A , Amanda J. Reichelt-Brushett A B and Malcolm W. Clark AA Marine Ecology Research Centre, School of Environment, Science and Engineering, Southern Cross University, PO Box 417, Lismore, NSW 2480, Australia.
B Corresponding author. Email: amanda.reichelt-brushett@scu.edu.au
Marine and Freshwater Research 65(6) 551-561 https://doi.org/10.1071/MF13195
Submitted: 22 July 2013 Accepted: 18 October 2013 Published: 7 May 2014
Abstract
The zooxanthellate sea anemone Aiptasia pulchella is found throughout the tropical and subtropical oceans of the Indo-Pacific and is easily maintained in aquaria, posing potential suitability as a standard tropical marine test organism for use in ecotoxicology. To gain an understanding of the sensitivity of A. pulchella to trace metals, 96-h static-renewal toxicity tests were conducted. Values of 96-h LC50 between 946 and 1196 µg L–1 were estimated for cadmium, between 595 and 1146 µg L–1 for zinc, 8060 and 12 352 µg L–1 for lead and 2209 and 5751 µg L–1 for nickel. In addition, preliminary assessment of rapid tentacle retraction was made. Six-hour EC50 values of 355 and 979 µg L–1 for cadmium, between 384 and 493 µg L–1 for zinc, between 2340 and 2584 µg L–1 for nickel, and 2610 µg L–1 for lead, were estimated for ‘severe’ tentacle retraction. Cobalt concentrations up to 1547 µg L–1 caused extreme zooxanthellae loss, but no more than 10% mortality and no rapid ‘severe’ tentacle retraction. The present study has provided important baseline information, enabling comparison of the acute sensitivity of A. pulchella to trace metals with other marine invertebrates, and guiding the development of sublethal endpoints.
Additional keywords: cnidaria, toxicity tests, trace metals, tropical marine ecotoxicology.
References
ANZECC and ARMCANZ (2000). ‘Australian and New Zealand Water Quality Guidelines for Fresh and Marine Water Quality.’ (Australian and New Zealand Environment and Conservation Council and Agriculture and Resource Management Council of Australia and New Zealand: Canberra.)Cantin, N. E., Negri, A. P., and Willis, B. L. (2007). Photoinhibition from chronic herbicide exposure reduces reproductive output of reef-building corals. Marine Ecology Progress Series 344, 81–93.
| Photoinhibition from chronic herbicide exposure reduces reproductive output of reef-building corals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFyqsb3I&md5=822118ad0f0a3bfc632f8f8cf2c59977CAS |
Chan, H. M. (1988). Accumulation and tolerance to copper, cadmium, lead and zinc by the green mussel Perna viridis. Marine Ecology Progress Series 48, 295–303.
| Accumulation and tolerance to copper, cadmium, lead and zinc by the green mussel Perna viridis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXjsFSjtA%3D%3D&md5=ebed36a5432cde0bf614ec49435639f6CAS |
Chapman, P. M., McDonald, B. G., Kickham, P. E., and McKinnon, S. (2006). Global geographic differences in marine metal toxicity. Marine Pollution Bulletin 52, 1081–1084.
| Global geographic differences in marine metal toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtValtLbM&md5=9464a42088a24c672b7ea9695d437765CAS | 16824553PubMed |
Chen, C., Soong, K., and Chen, C. A. (2008). The smallest oocytes among broadcast-spawning actiniarians and a unique lunar reproductive cycle in a unisexual population of the sea anemone, Aiptasia pulchella (Anthozoa: Actiniaria). Zoological Studies 47, 37–45.
Dykens, J. A., and Shick, J. M. (1984). Photobiology of the symbiotic sea anemone, Anthopleura elegantissima: defenses against photodynamic effects, and seasonal photoacclimatization. The Biological Bulletin 167, 683–697.
| Photobiology of the symbiotic sea anemone, Anthopleura elegantissima: defenses against photodynamic effects, and seasonal photoacclimatization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXns1WltA%3D%3D&md5=eb498d56bfa16a9bf1525bf3f01a8575CAS |
El-Sheekh, M. M., El-Naggar, A. H., Osman, M. E. H., and El-Mazaly, E. (2003). Effect of cobalt on growth, pigments and the photosynthetic electron transport in Monoraphidium minutum and Nitzchia perminuta. Brazilian Journal of Plant Physiology 15, 150–166.
| Effect of cobalt on growth, pigments and the photosynthetic electron transport in Monoraphidium minutum and Nitzchia perminuta.Crossref | GoogleScholarGoogle Scholar |
Engel, D. W., and Fowlert, B. A. (1979). Factors influencing cadmium accumulation and its toxicity to marine organisms. Environmental Health Perspectives 28, 81–88.
| Factors influencing cadmium accumulation and its toxicity to marine organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXktFCltr8%3D&md5=ef9a07af78dd4daf5e1850fa50dcb828CAS | 488052PubMed |
Gilbert, A. L., and Guzman, H. M. (2001). Bioindication of carbonic anhydrase activity in anemones and corals. Marine Pollution Bulletin 42, 742–744.
| Bioindication of carbonic anhydrase activity in anemones and corals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmsFSqtb8%3D&md5=9d79d79638e592765ea3e5052bbfd49dCAS | 11585066PubMed |
Goh, B. P. L. (1991). Mortality and settlement success of Pocillopora damicornis larvae during recovery from low levels of nickel. Pacific Science 45, 276–286.
| 1:CAS:528:DyaK3MXlslKqs74%3D&md5=44abefc264fa58d047213c72c62d500bCAS |
Goh, B. P. L., and Chou, L. M. (1992). Effect of low levels of zinc on zooxanthellae cells in culture. In Richmond, Robert (Ed.) ‘7th International Coral Reef Symposium, Guam’. pp. 367–372. (University of Guam Press.)
Gopalakrishnan, S., Thiliagam, H., and Raja, P. V. (2008). Comparison of heavy metal toxicity in life stages (spremiotoxicity, egg toxicity, embryotoxicity and larval toxicity) of Hydroides elegans. Chemosphere 71, 515–528.
| Comparison of heavy metal toxicity in life stages (spremiotoxicity, egg toxicity, embryotoxicity and larval toxicity) of Hydroides elegans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisVWjsLc%3D&md5=8a95072d64bf34c35c91e6227ebdf013CAS | 18022210PubMed |
Greenwood, J. G., and Field, D. R. (1983). Acute toxicity of zinc and cadmium to zoeae of three species of portunid crabs (crustacea: brachyura). Comparative Biochemistry and Physiology – Part C 75, 141–144.
| Acute toxicity of zinc and cadmium to zoeae of three species of portunid crabs (crustacea: brachyura).Crossref | GoogleScholarGoogle Scholar |
Heyward, A. J. (1988). Inhibitory effects of copper and zinc sulphates on fertilisation in corals. In ‘6th International Coral Reef Symposium’Australia’. (Ed. J. H. Choat.) pp. 299–303.
Howe, P. L., Reichelt-Brushett, A. J., and Clark, M. W. (2012). Aiptasia pulchella: a tropical cnidarian representative for laboratory ecotoxicological research. Environmental Toxicology and Chemistry 31, 2653–2662.
| Aiptasia pulchella: a tropical cnidarian representative for laboratory ecotoxicological research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Kgu73P&md5=6aa5c36b1e89e5b5c8c467a010b0a58fCAS | 22927090PubMed |
Hughes, R., Reichelt-Brushett, A. J., and Newman, L. J. (2005). Identifying suitable invertebrate species from a unique habitat for ecotoxicological testing. Australasian Journal of Ecotoxicology 11, 85–92.
| 1:CAS:528:DC%2BD28XitFOksbw%3D&md5=4c764af7bd0c4c49f4e2c52a8fbf52deCAS |
Hunt, J. W., Anderson, B. S., Phillips, B. M., Tjeedema, R. S., and Puckett, H. M. (2002). Acute and chronic toxicity of nickel to marine organisms: implications for water quality criteria. Environmental Toxicology and Chemistry 21, 2423–2430.
| Acute and chronic toxicity of nickel to marine organisms: implications for water quality criteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVGntrY%3D&md5=520d43c6dac3f968ea3f8fabc0edfbf3CAS | 12389922PubMed |
Jokiel, P. L., and York, R. H. (1982). Solar ultraviolet photobiology of the reef coral Pocillopora damicornis and symbiotic zooxanthellae. Bulletin of Marine Science 32, 301–315.
Jones, R. (1997). Zooxanthellae loss as a bioassay for assessing stress in corals. Marine Ecology Progress Series 149, 163–171.
| Zooxanthellae loss as a bioassay for assessing stress in corals.Crossref | GoogleScholarGoogle Scholar |
Jones, R., Muller, J., Haynes, D., and Schrieber, U. (2003). Effects of herbicides diuron and atrazine on corals of the Great Barrier Reef, Australia. Marine Ecology Progress Series 251, 153–167.
| Effects of herbicides diuron and atrazine on corals of the Great Barrier Reef, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltleitbo%3D&md5=b32ac22ef0116b6c0654402033d6f5f7CAS |
King, C. K., and Riddle, M. J. (2001). Effects of metal contaminants on the development of the common Antarctic sea urchin Sterechinus neumayeri and comparisons of sensitivity with tropical and temperate echinoids. Marine Ecology Progress Series 215, 143–154.
| Effects of metal contaminants on the development of the common Antarctic sea urchin Sterechinus neumayeri and comparisons of sensitivity with tropical and temperate echinoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmslWltLY%3D&md5=85e976c2286cd09fd3515ba7e109ebbcCAS |
Kwok, K. W. H., Leung, K. M. Y., Lui, G. S. G., Chu, V. K. H., Lam, P. K. S., Morritt, D., Maltby, L., Brock, T. C. M., Van den Brink, P. J., Warne, M. St. J., and Crane, M. (2007). Comparison of tropical and temperate freshwater animal species’ acute sensitivities to chemicals: implications for deriving safe extrapolation factors. Integrated Environmental Assessment and Management 3, 49–67.
| Comparison of tropical and temperate freshwater animal species’ acute sensitivities to chemicals: implications for deriving safe extrapolation factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvFyqs7c%3D&md5=3017771d95503d96d7335f0c54572367CAS |
Liao, C. M., and Lin, M. C. (2001). Toxicokinetics and acute toxicity of waterborne zinc in abalone (Haliotis diversicolor supertexta Lischke). Bulletin of Environmental Contamination and Toxicology 66, 597–602.
| 1:CAS:528:DC%2BD3MXisFOmtrs%3D&md5=9e44437aacffa7576ecf0de5b8d99c13CAS | 11443329PubMed |
Loganathan, P., and Hedley, M. J. (1997). Downward movement of cadmium and phosphorus from phosphatic fertilizers in a pasture soil in New Zealand. Environmental Pollution 95, 319–324.
| Downward movement of cadmium and phosphorus from phosphatic fertilizers in a pasture soil in New Zealand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsVOqs78%3D&md5=9b2219162e0598cdc6dce009a58bd240CAS | 15093446PubMed |
Main, W. P. L., Ross, C., and Bielmyer, G. K. (2010). Copper accumulation and oxidative stress in the sea anemone, Aiptasia pallida, after waterborne copper exposure. Comparative Biochemistry and Physiology. Part C Toxicology & Pharmacology 151, 216–221.
| Copper accumulation and oxidative stress in the sea anemone, Aiptasia pallida, after waterborne copper exposure.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MfhvVajuw%3D%3D&md5=54a2a88b63e8fbb37cf0822d06c1689bCAS |
Markich, S., and Camilleri, C. (1997). Investigation of metal toxicity to tropical biota: recommendations for revision of the Australian water quality guidelines. Supervising Scientist, Australian Government. Canberra.
Markich, S. J., Warne, M. S. J., Westbury, A.-M., and Roberts, C. J. (2002). A complitation of data on the toxicity of chemicals to species in Australasia. Part 3: metals. Australasian Journal of Ecotoxicology 8, 1–72.
| 1:CAS:528:DC%2BD3sXovFWmsw%3D%3D&md5=130c603e2fbfd8874da997141b2d95b7CAS |
Martin, M., Osborne, K. E., Billig, P., and Glickstein, N. (1981). Toxicities of ten metals to Crasstostrea gigas and Mytilus edulis embyros and Cancer magistar larvae. Marine Pollution Bulletin 12, 305–308.
| Toxicities of ten metals to Crasstostrea gigas and Mytilus edulis embyros and Cancer magistar larvae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlvFymtLs%3D&md5=76ad6c05514e00c8814c93e5a7d99fe7CAS |
McClurg, T. P. (1984). Effects of fluoride, cadmium and mercury on the estuarine prawn Penaeus indicus. Water SA 10, 40–45.
| 1:CAS:528:DyaL2cXpsl2hug%3D%3D&md5=0e639f5ec5c69f7bbf40f49a1bec1ceaCAS |
Mohammed, E. H., Wang, G., and Jiang, J. (2010). The effects of nickel on the reproductive ability of three different marine copepods. Ecotoxicology 19, 911–916.
| The effects of nickel on the reproductive ability of three different marine copepods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsVGrsbc%3D&md5=0f2cf92a74252a20e9129d7f36e98f5eCAS | 20182790PubMed |
Muller-Parker, G. (1984). Photosynthesis-irradiance responses and photosynthetic periodocity in the sea anemone Aiptasia pulchella and its zooxanthellae. Marine Biology 82, 225–232.
| Photosynthesis-irradiance responses and photosynthetic periodocity in the sea anemone Aiptasia pulchella and its zooxanthellae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhvVakt7Y%3D&md5=b2d55ea56d4c9c1b73284c308b75c978CAS |
Negri, A. P., and Hoogenboom, M. O. (2011). Water contamination reduces the tolerance of coral larvae to thermal stress. PLoS ONE 6, e19703.
| Water contamination reduces the tolerance of coral larvae to thermal stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmt1ejtLk%3D&md5=3d23fac1f8f99b323bee971d7d58baa8CAS | 21589934PubMed |
Negri, A. P., Vollhardt, C., Humphrey, C., Heyward, A. J., Jones, R., Eaglesham, G., and Fabricius, K. (2005). Effects of the herbicide diuron on the early life history stages of coral. Marine Pollution Bulletin 51, 370–383.
| Effects of the herbicide diuron on the early life history stages of coral.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitF2gurs%3D&md5=31dd7780ba625b9da173fc6ff8c74636CAS |
Negri, A. P., Flores, F., Rothig, T., and Uthicke, S. (2011). Herbicides increase the vulnerability of corals to rising sea surface temperatures. Limnology and Oceanography 56, 471–485.
| Herbicides increase the vulnerability of corals to rising sea surface temperatures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltVGktro%3D&md5=001606d8db70dbc4c17e906ab7167cbcCAS |
Nicol, J. A. C. (1959). Digestion in sea anemones. Journal of the Marine Biological Association of the United Kingdom 38, 469–476.
| Digestion in sea anemones.Crossref | GoogleScholarGoogle Scholar |
Ong, E. S., and Din, Z. B. (2001). Cadmium, copper, and zinc toxicity to the clam, Donax faba, and the blood cockle, Anadara granosa. Bulletin of Environmental Contamination and Toxicology 66, 86–93.
| Cadmium, copper, and zinc toxicity to the clam, Donax faba, and the blood cockle, Anadara granosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnsFKnsg%3D%3D&md5=76aecd4f4a68c1e3357c305b0d7f907cCAS | 11080341PubMed |
Pérez, S., and Beiras, R. (2010). The mysid Siriella armata as a model organism in marine ecotoxicology: comparative acute toxicity sensitivity with Daphnia magna. Ecotoxicology 19, 196–206.
| The mysid Siriella armata as a model organism in marine ecotoxicology: comparative acute toxicity sensitivity with Daphnia magna.Crossref | GoogleScholarGoogle Scholar | 19757032PubMed |
Peters, E. C., Gassman, N. J., Firman, J. C., Richmond, R. H., and Power, E. A. (1997). Ecotoxicology of tropical marine ecosystems. Environmental Toxicology and Chemistry 16, 12–40.
| Ecotoxicology of tropical marine ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtl2msg%3D%3D&md5=34907bbf5de81a8c8253b5d8966dacb0CAS |
Prato, E., Bianolino, F., and Scardicchio, C. (2006). Test for acute toxicity of copper, cadmium, and mercury in five marine species. Turkish Journal of Zoology 30, 285–290.
| 1:CAS:528:DC%2BD28Xht1WgtrrL&md5=3455c3a7b5387ff597a427bfe0455e89CAS |
Rajkumar, J. S. I., John Milton, M. C., Ulthiralingam, M., Azhaguraj, R., Ganesh, J., and Ambrose, T. (2011). Toxic effect and bioaccumulation of cadmium, copper, lead and zinc in post larval stages of Penaeus monodon. International Journal of Development Research 1, 1–5.
| 1:CAS:528:DC%2BC2cXlsVWqsbs%3D&md5=2622705580275c962207c7aa1b7f2989CAS |
Ramakritinan, C. M., Chandurvelan, R., and Kumaraguru, A. K. (2012). Acute toxicity of metals: Cu, Pb, Cd, Hg and Zn on marine molluscs Cerithedia cingulata, and Modiolus phillipinnarum. Indian Journal of Geo-Marine Sciences 41, 141–145.
| 1:CAS:528:DC%2BC3sXivFKqsrk%3D&md5=2d1ab207f92d9df08c10436f26fbf3c3CAS |
Reichelt-Brushett, A. J. (2012). Risk assessment and ecotoxicology: limitations and recommendations for ocean disposal of mine waste in the coral triangle. Oceanography 25, 40–51.
| Risk assessment and ecotoxicology: limitations and recommendations for ocean disposal of mine waste in the coral triangle.Crossref | GoogleScholarGoogle Scholar |
Reichelt-Brushett, A. J., and Harrison, P. L. (1999). The effect of copper, zinc and cadmium on fertilisation success of gametes from scleractinian reef corals. Marine Pollution Bulletin 38, 182–187.
| The effect of copper, zinc and cadmium on fertilisation success of gametes from scleractinian reef corals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXislGitb0%3D&md5=7fb1c2214ef545aa013dfdf916a80880CAS |
Reichelt-Brushett, A. J., and Harrison, P. L. (2004). Development of a sublethal test to determine the effects of copper and lead on scleractinian coral larvae. Archives of Environmental Contamination and Toxicology 47, 40–55.
| Development of a sublethal test to determine the effects of copper and lead on scleractinian coral larvae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlWmt70%3D&md5=481ca22936e89aca056398a41ec91aedCAS | 15346777PubMed |
Reichelt-Brushett, A. J., and Harrison, P. L. (2005). The effect of selected trace metals on the fertilisation success of several scleractinian coral species. Coral Reefs 24, 524–534.
| The effect of selected trace metals on the fertilisation success of several scleractinian coral species.Crossref | GoogleScholarGoogle Scholar |
Reichelt-Brushett, A. J., and McOrist, G. (2003). Trace metals in the living and non-living components of scleractinian corals. Marine Pollution Bulletin 46, 1573–1582.
| Trace metals in the living and non-living components of scleractinian corals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1ent7s%3D&md5=a3f8c879eaefb9a4e1fab09b96383ae1CAS | 14643784PubMed |
Rotmann, S., and Thomas, S. (2012). Coral tissue thickness as a bioindicator of mine-related turbidity stress on coral reefs at Lihir Island, Papua New Guinea. Oceanography 25, 52–63.
| Coral tissue thickness as a bioindicator of mine-related turbidity stress on coral reefs at Lihir Island, Papua New Guinea.Crossref | GoogleScholarGoogle Scholar |
Thompson, J. H., Jr, Shinn, E. A., and Bright, T. J. (1980). Chapter 16: effects of drilling muds on seven species of reef building corals as measured in the field and laboratory. Elseveier Oceanography Series 27 (Part A), 433–453.
Thongra-ar, W. (1997). Toxicity of cadmium, zinc and copper on sperm cell fertilisation of sea urchin, Diadema setosum. Journal of the Science Society of Thailand 23, 297–306.
| Toxicity of cadmium, zinc and copper on sperm cell fertilisation of sea urchin, Diadema setosum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhvV2gsLg%3D&md5=cdb3ef6e3ed6f41c26166c691392c998CAS |
US Environmental Protection Authority (EPA) (2002). Short-term methods for estimating the chronic toxicity of effluents and receiving waters to freshwater organisms. Environmental Monitoring and Support Laboratory. Available at http://water.epa.gov/scitech/methods/cwa/wet/disk3_index.cfm [accessed 14 October 2013].
US Environmental Protection Authority (EPA) (2013) ‘ECOTOX Database. Vol. 2013.’ Available at www.ecotox.gov [accessed 20 August 2013].
van Dam, R. A., Harford, A. J., Houston, M. A., Hogan, A. C., and Negri, A. P. (2008). Tropical marine toxicity testing in Australia: a review and recommendations. Australasian Journal of Ecotoxicology 14, 55–88.
Veron, J. E. N. (1986) ‘Corals of Australia and the Indo-Pacific.’ (University of Hawaii Press: Singapore.)
Vijayavel, K., and Richmond, R. H. (2012). The preparation of the rice coral Montipora capitata nubbins for application in coral-reef ecotoxicology. Ecotoxicology 21, 925–930.
| The preparation of the rice coral Montipora capitata nubbins for application in coral-reef ecotoxicology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksVers7g%3D&md5=0a73c945e87386a30d7aea98aa06eae1CAS | 22218977PubMed |
Wang, Q., Liu, B., Yang, H., Wang, X., and Lin, Z. (2009). Toxicity of lead, cadmium and mercury on embryogenesis,survival, growth and metamorphosis of Meretrix meretrix larvae. Ecotoxicology 18, 829–837.
| Toxicity of lead, cadmium and mercury on embryogenesis,survival, growth and metamorphosis of Meretrix meretrix larvae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVeksrjN&md5=85d35d62b32c5d9f30be97ade9e30f6cCAS | 19504184PubMed |
Wu, J. P., and Chen, H. C. (2004). Effects of cadmium and zinc on oxygen consumption, ammonium excretion, and osmoregulation of white shrimp (Litopenaeus vannamei). Chemosphere 57, 1591–1598.
| Effects of cadmium and zinc on oxygen consumption, ammonium excretion, and osmoregulation of white shrimp (Litopenaeus vannamei).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpt1aku7k%3D&md5=aa94d26a6cb2a4073b322995c6067164CAS | 15519404PubMed |