Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

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 A

A 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 http://dx.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 | 1:CAS:528:DC%2BD2sXhtFyqsb3I&md5=822118ad0f0a3bfc632f8f8cf2c59977CAS | open url image1

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 | 1:CAS:528:DyaL1MXjsFSjtA%3D%3D&md5=ebed36a5432cde0bf614ec49435639f6CAS | open url image1

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 | 1:CAS:528:DC%2BD28XhtValtLbM&md5=9464a42088a24c672b7ea9695d437765CAS | 16824553PubMed | open url image1

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. open url image1

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 | 1:CAS:528:DyaL2MXns1WltA%3D%3D&md5=eb498d56bfa16a9bf1525bf3f01a8575CAS | open url image1

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 | open url image1

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 | 1:CAS:528:DyaE1MXktFCltr8%3D&md5=ef9a07af78dd4daf5e1850fa50dcb828CAS | 488052PubMed | open url image1

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 | 1:CAS:528:DC%2BD3MXmsFSqtb8%3D&md5=9d79d79638e592765ea3e5052bbfd49dCAS | 11585066PubMed | open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BD1cXisVWjsLc%3D&md5=8a95072d64bf34c35c91e6227ebdf013CAS | 18022210PubMed | open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BC38Xhs1Kgu73P&md5=6aa5c36b1e89e5b5c8c467a010b0a58fCAS | 22927090PubMed | open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BD38XotVGntrY%3D&md5=520d43c6dac3f968ea3f8fabc0edfbf3CAS | 12389922PubMed | open url image1

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. open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BD3sXltleitbo%3D&md5=b32ac22ef0116b6c0654402033d6f5f7CAS | open url image1

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 | 1:CAS:528:DC%2BD3MXmslWltLY%3D&md5=85e976c2286cd09fd3515ba7e109ebbcCAS | open url image1

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 | 1:CAS:528:DC%2BD2sXhvFyqs7c%3D&md5=3017771d95503d96d7335f0c54572367CAS | open url image1

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 | open url image1

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 | 1:CAS:528:DyaK2sXjsVOqs78%3D&md5=9b2219162e0598cdc6dce009a58bd240CAS | 15093446PubMed | open url image1

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 | 1:STN:280:DC%2BD1MfhvVajuw%3D%3D&md5=54a2a88b63e8fbb37cf0822d06c1689bCAS | open url image1

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 | open url image1

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 | 1:CAS:528:DyaL3MXlvFymtLs%3D&md5=76ad6c05514e00c8814c93e5a7d99fe7CAS | open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BC3cXlsVGrsbc%3D&md5=0f2cf92a74252a20e9129d7f36e98f5eCAS | 20182790PubMed | open url image1

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 | 1:CAS:528:DyaL2MXhvVakt7Y%3D&md5=b2d55ea56d4c9c1b73284c308b75c978CAS | open url image1

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 | 1:CAS:528:DC%2BC3MXmt1ejtLk%3D&md5=3d23fac1f8f99b323bee971d7d58baa8CAS | 21589934PubMed | open url image1

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 | 1:CAS:528:DC%2BD2MXitF2gurs%3D&md5=31dd7780ba625b9da173fc6ff8c74636CAS | open url image1

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 | 1:CAS:528:DC%2BC3MXltVGktro%3D&md5=001606d8db70dbc4c17e906ab7167cbcCAS | open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BD3MXnsFKnsg%3D%3D&md5=76aecd4f4a68c1e3357c305b0d7f907cCAS | 11080341PubMed | open url image1

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 | 19757032PubMed | open url image1

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 | 1:CAS:528:DyaK2sXmtl2msg%3D%3D&md5=34907bbf5de81a8c8253b5d8966dacb0CAS | open url image1

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 | open url image1

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 | open url image1

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 | open url image1

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 | open url image1

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 | 1:CAS:528:DyaK1MXislGitb0%3D&md5=7fb1c2214ef545aa013dfdf916a80880CAS | open url image1

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 | 1:CAS:528:DC%2BD2cXltlWmt70%3D&md5=481ca22936e89aca056398a41ec91aedCAS | 15346777PubMed | open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BD3sXpt1ent7s%3D&md5=a3f8c879eaefb9a4e1fab09b96383ae1CAS | 14643784PubMed | open url image1

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 | open url image1

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 | 1:CAS:528:DyaK1cXhvV2gsLg%3D&md5=cdb3ef6e3ed6f41c26166c691392c998CAS | open url image1

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. open url image1

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 | 1:CAS:528:DC%2BC38XksVers7g%3D&md5=0a73c945e87386a30d7aea98aa06eae1CAS | 22218977PubMed | open url image1

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 | 1:CAS:528:DC%2BD1MXhtVeksrjN&md5=85d35d62b32c5d9f30be97ade9e30f6cCAS | 19504184PubMed | open url image1

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 | 1:CAS:528:DC%2BD2cXpt1aku7k%3D&md5=aa94d26a6cb2a4073b322995c6067164CAS | 15519404PubMed | open url image1



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