Reproductive characteristics and steroid levels in the scleractinian coral Oculina patagonica inhabiting contaminated sites along the Israeli Mediterranean coast

Marine Pollution Bulletin

Volumn 64, Issue 8, 2012, Pages 1556-1563

  Armoza Zvuloni, Rachel ^a,b,c   Kramarsky Winter, Esti ^a   Rosenfeld, Hanna ^c   Shore, Laurence S ^d   Segal, Roee ^a   Sharon, Daniel ^a   Loya, Yossi ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b The Interuniversity Institute for Marine Science Eilat   (Israel)

^c NATIONAL CENTER FOR MARICULTURE   (Israel)

^d KIMRON VETERINARY INSTITUTE   (Israel)

Author keywords

Gametogenesis; Oculina patagonica; Pollution; Reproduction; Steroid hormones; Tolerance

Indexed keywords

CHRONIC STRESS; CONTAMINATED SITES; CORAL TISSUE; GAMETOGENESIS; MEDITERRANEAN SEA; NON-INDIGENOUS; OCULINA PATAGONICA; REFERENCE SITES; REPRODUCTION; REPRODUCTIVE CHARACTERISTICS; REPRODUCTIVE POTENTIAL; SCLERACTINIAN CORALS; SHORT DURATIONS; SPECIES TOLERANCE; STEROID HORMONE;

FITS AND TOLERANCES; HORMONES; SEAWATER; TISSUE;

POLLUTION;

SEA WATER; STEROID HORMONE;

COASTAL WATER; CORAL; GAMETOGENESIS; MARINE POLLUTION; POLLUTION TOLERANCE; REPRODUCTION; STEROID;

ACUTE STRESS; ADAPTATION; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CHRONIC STRESS; CONTROLLED STUDY; CORAL; ENVIRONMENTAL EXPOSURE; FEMALE; GAMETOGENESIS; ISRAEL; LONG TERM EXPOSURE; MALE; MEDITERRANEAN SEA; NONHUMAN; OCULINA PATAGONICA; REPRODUCTIVE TOXICITY; SEA POLLUTION; SPECIES INVASION; SPECIES TOLERANCE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTHOZOA; ENVIRONMENTAL MONITORING; GAMETOGENESIS; GONADAL STEROID HORMONES; ISRAEL; MEDITERRANEAN SEA; REPRODUCTION; SEAWATER; STRESS, PHYSIOLOGICAL; WATER POLLUTANTS, CHEMICAL; WATER POLLUTION, CHEMICAL;

ISRAEL; MEDITERRANEAN COAST [ISRAEL];

ANTHOZOA; OCULINA PATAGONICA; SCLERACTINIA;

EID: 84864142724     PISSN: 0025326X     EISSN: 18793363     Source Type: Journal    
DOI: 10.1016/j.marpolbul.2012.05.020     Document Type: Article

References (71)

1. Armoza-Zvuloni R., Segal R., Kramarsky-Winter E., Loya Y. Repeated bleaching events may result in high tolerance and notable gametogenesis in stony corals: Oculina patagonica as a model. Mar. Ecol. Prog. Ser. 2011, 426:149-159.
2. Atkinson S., Atkinson M.J., Tarrant A.M. Estrogens from sewage in coastal marine environments. Environ. Health Perspect. 2003, 111:531-535.
3. Baker M.E. Albumin, steroid hormones and the origin of vertebrates. J. Endocrinol. 2002, 175:121-127.
4. Barel-Cohen K., Shore L.S., Shemesh M., Wenzel A., Mueller J., Kronfeld-Schor N. Monitoring of natural and synthetic hormones in a polluted river. J. Environ. Manage. 2006, 78:16-23.
5. Beck I.C., Bruhn R., Gandrass J., Ruck W. Liquid chromatography-tandem mass spectrometry analysis of estrogenic compounds in coastal surface water of the Baltic Sea. J. Chromatogr. A. 2005, 1090:98-106.
6. Bongiorni L., Shafir S., Angel D., Rinkevich B. Survival, growth and gonad development of two hermatypic corals subjected to in situ fish-farm nutrient enrichment. Mar. Ecol. Prog. Ser. 2003, 253:137-144.
7. Cantin N.E., Negri A.P., Willis B.L. Photoinhibition from chronic herbicide exposure reduces reproductive output of reef-building corals. Mar. Ecol. Prog. Ser. 2007, 344:81-93.
8. Celesti-Grapow L., Pysek P., Jarosik V., Blasi C. Determinants of native and alien species richness in the urban flora of Rome. Diversity Distrib. 2006, 12:490-501.
9. Cox E.F., Ward S. Impact of elevated ammonium on reproduction in two scleractinian corals with different life history patterns. Mar. Pollut. Bull. 2002, 44:1230-1235.
10. Environmental Health Department Sanitation at Public Bathing Beaches in Israel, Annual Report 2005 2005, Ministry of Health, Israel.
11. Environmental Health Department Sewage Sanitation in Israel, Annual Report 2005 2006, Ministry of Health, Israel.
12. Fabricius K.E. Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar. Pollut. Bull. 2005, 50:125-146.
13. Fine M., Loya Y. Alternate coral-bryozoan competitive superiority during coral bleaching. Mar. Biol. 2003, 142:989-996.
14. Fine M., Zibrowius H., Loya Y. Oculina patagonica: a non-lessepsian scleractinian coral invading the Mediterranean Sea. Mar. Biol. 2001, 138:1195-1203.
15. Fukushima M., Funabiki I., Hashizume T., Osada K., Yoshida W., Ishida S. Detection and changes in levels of testosterone during spermatogenesis in the freshwater planarian Bdellocephala brunnea. Zool. Sci. 2008, 5:760-765.
16. Gateno D., Israel A., Barki Y., Rinkevich B. Gastrovascular circulation in an octocoral: evidence of significant transport of coral and symbiont cells. Biol. Bull. 1998, 194:178-186.
17. Guzmán H.M., Holst I. Effects of chronic oil-sediment pollution on the reproduction of the Caribbean reef coral Siderastrea sidereal. Mar. Pollut. Bull. 1993, 26:276-282.
18. Halpern B.S., Walbridge S., Selkoe K.A., Kappel C.V., Micheli F., et al. Global map of human impact on marine ecosystems. Science 2008, 319:948-952.
19. Harrison P.L., Wallace C.C. Reproduction, dispersal and recruitment of scleractinian corals. Coral Reef Ecosystems of the World 1990, vol. 25:133-208. Elsevier, Amsterdam.
20. Herut, B., Shefer, E., Cohen, Y., 2005. Environmental quality of Israel's Mediterranean coastal waters in 2004, IOLR, Report H34/2005.
21. Hines G.A., Watts S.A. Sex steroid levels in the testes, ovaries, and pyloric caeca during gametogenesis in the sea star Asterias vulgaris. Gen. Comp. Endocrinol. 1992, 87:451-460.
22. Islam M.D., Tanaka M. Impacts of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach for management: a review and synthesis. Mar. Pollut. Bull. 2004, 48:624-649.
23. Izquierdo A., Loya A., Diaz-Valdes M., Ramos-Espla A.A. Non-indigenous species at the alicante harbor (se-spain): Oculina patagonica de angelis, 1908 and botrycapulus aculeatus (gmelin, 1791) Rapp. Comm. Int. Mer Medit. 2007, 38:506.
24. Janer G., Porte C. Sex steroids and potential mechanisms of non-genomic endocrine disruption in invertebrates. Ecotoxicology 2007, 16:145-160.
25. Johannes R.E., Wiebe W.J. A method for determination of coral tissue biomass and composition. Limnol. Oceanogr. 1970, 21:540-647.
26. Keshet, N., 2005. Water and streams monitoring, final report for 2004 of the Israeli Nature and Parks Authority and the Ministry of the Environment. 123p (in Hebrew).
27. Kirkbride-Smith A.E., Bell H.A., Edwards J.P. Effects of three vertebrate hormones on the growth, development and reproduction of the tomato moth, Lacanobia oleracea L. (Lepidoptera: Noctuidae). Environ. Toxicol. Chem. 2001, 20:1838-1845.
28. Knowlton N. The future of coral reefs. Proc. Natl. Acad. Sci. USA 2001, 98:5419-5425.
29. Kramarsky-Winter E., Downs C.A., Downs A., Loya Y. Cellular responses in the coral Stylophora pistillata exposed to eutrophication from fish mariculture. Evol. Ecol. Res. 2009, 11:1-21.
30. Kramarsky-Winter E., Fine M., Loya Y. Coral polyp expulsion. Nature 1997, 387:137.
31. Lafont R., Mathieu M. Steroids in aquatic invertebrates. Ecotoxicology 2007, 16:109-130.
32. Lesser M.P. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 1997, 16:187-192.
33. Levitan D.R., Petersen C. Sperm limitation in the sea. Trends Ecol. Evol. 1995, 10:228-231.
34. Loya Y., Lubinevsky H., Rosenfeld M., Kramarsky-Winter E. Nutrient enrichment caused by in situ fish farms at Eilat, Red Sea is detrimental to coral reproduction. Mar. Pollut. Bull. 2004, 49:344-353.
35. Loya Y., Rinkevich B. Abortion effect in corals induced by oil pollution. Mar. Ecol. Prog. Ser. 1979, 1:77-80.
36. Loya Y., Rinkevich B. Effects of oil pollution on coral reef communities. Mar. Ecol. Prog. Ser. 1980, 3:167-180.
37. Markov G.V., Tavares R., Dauphin-Villemant C., Demeneix B.A., Baker M.E., Laudet V. Independent elaboration of steroid hormone signaling pathways in metazoans. Proc. Natl. Acad. Sci. USA 2009, 106:11913-11918.
38. Mc Lusky D. The Secondary Consumers. The Estuarine Ecosystem 1989, Chapman & Hall, London, pp. 113-129.
39. Miyashita H., Nakagawa H., Kobayashi K., Hoshi M., Matsumoto M. Effects of 17β-Estradiol and Bisphenol A on the formation of reproductive organs in planarians. Biol. Bull. 2011, 220:47-56.
40. Pernet V., Anctil M. Annual variations and sex-related differences of estradiol-17β levels in the anthozoan Renilla koellikeri. Gen. Comp. Endocrinol. 2002, 129:63-68.
41. Piola R.F., Johnston E.L. Pollution reduces native diversity and increases invader dominance in marine hard-substrate communities. Diversity Distrib. 2008, 14:329-342.
42. Reitzel A.M., Tarrant A.M. Nuclear receptor complement of the cnidarian Nematostella vectensis: phylogenetic relationships and developmental expression Patterns. BMC Evol. Biol. 2009, 9:230.
43. Revelli A., Massobrio M., Tesarik J. Nongenomic actions of steroid hormones in reproductive tissues. Endocr. Rev. 1998, 19:3-17.
44. Rinkevich B., Loya Y. The reproduction of the Red Sea coral Stylophora pistillata. I. Gonads and planulae. Mar. Ecol. Prog. Ser. 1979, 1:133-144.
45. Robinson B.J., Hui J.P.M., Soo E.C., Hellou J. Estrogenic compounds in seawater and sediment from Halifax Harbour, Nova Scotia, Canada. Environ. Toxicol. Chem. 2009, 28:18-25.
46. Rodolfo-Metalpa R., Richard C., Allemand D., Ferrier-Pagès C. Growth and photosynthesis of two Mediterranean corals, Cladocora caespitosa and Oculina patagonica, under normal and elevated temperatures. J. Exp. Biol. 2006, 209:4546-4556.
47. Ronis M.J.J., Lindros K.O., Ingelmann-Sundberg M. The CYP2E family. Cytochrome P450: Metabolic and Toxicological Aspects 1996, 211-239. CRC Press, Boca Raton, FL. C. Ionnides (Ed.).
48. Rosenberg E., Falkovitz L. The Vibrio shiloi/Oculina patagonica model system of coral bleaching. Annu. Rev. Microbiol. 2004, 58:143-159.
49. Rotchell J.M., Ostrander G.K. Molecular markers of endocrine disruption in aquatic organisms. J. Toxicol. Environ. Health B 2003, 6:453-495.
50. Santos M.M., Hallers-Tjabbes C.C., Vieira N., Boon J.P., Porte C. Cytochrome P450 differences in normal and imposex-affected female whelk Buccinum undatum from the open North Sea. Mar. Environ. Res. 2002, 54:661-665.
51. Sartoretto S., Harmelin J.G., Bachet F., Bejaoui N., Zibrowius H. The alien coral Oculina patagonica De Angelis 1908 (Cnidaria; Scleractinia) in Algeria and Tunisia. Aquat. Invasions 2008, 3:173-180.
52. Segal, R., 2006. Bleaching of the coral Oculina patagonica: ecological, physiological and genetic aspects of different populations along the coast of Israel. MS Dissertation, Tel-Aviv University.
53. Slattery M., Hines G.A., Starmer J., Paul V.J. Chemical signals in gametogenesis, spawning, and larval settlement and defense of the soft coral Sinularia polydactyla. Coral Reefs 1999, 18:75-84.
54. Snyder M.J. Cytochrome P450 enzymes in aquatic invertebrates: recent advances and future directions. Aquat. Toxicol. 2000, 48:529-547.
55. Tarrant A.M. Hormonal signaling in cnidarians: do we understand the pathways well enough to know whether they are being disrupted?. Ecotoxicology 2007, 16:5-13.
56. Tarrant A.M., Atkinson S., Atkinson M.J. Estrone and estradiol-17β concentration in tissue of the scleractinian coral, Montipora verrucosa. Comp. Biochem. Physiol. 1999, 122:85-92.
57. Tarrant A.M., Atkinson M.J., Atkinson S. Uptake of estrone by a coral reef community. Mar. Biol. 2001, 139:321-325.
58. Tarrant A.M., Reitzel A.M., Blomquist C.H., Haller F., Tokarzc J., Adamskic J. Steroid metabolism in cnidarians: insights from Nematostella vectensis. Mol. Cell. Endocrinol. 2009, 301:27-36.
59. Tarrant A., Atkinson M., Atkinson S. Effects of steroidal estrogens on coral growth and reproduction. Mar. Ecol. Prog. Ser. 2004, 269:121-129.
60. Tomascik T., Sander F. Effects of eutrophication on reef-building corals III. Reproduction of the reef-building coral Porites porites. Mar. Biol. 1987, 94:77-94.
61. Twan W.H., Hwang J.S., Chang C.F. Sex steroids in scleractinian coral, Euphyllia ancora: implication in mass spawning. Biol. Reprod. 2003, 68:2255-2260.
62. Venn A.A., Quinn J., Jones R., Bodnar A. P-glycoprotein (multi-xenobiotic resistance) and heat shock protein gene expression in the reef coral Montastraea franksi in response to environmental toxicants. Aquat. Toxicol. 2009, 93:188-195.
63. Vethaak A.D., Lahr J., Schrap S.M., Belfroid A.C., Rijs G.B.J., et al. An integrated assessment of estrogenic contamination and biological effects in the aquatic environment of The Netherlands. Chemosphere 2005, 59:511-524.
64. Wang C., Croll R.P. Effects of sex steroids on gonadal development and gender determination in the sea scallop, Placopecten magellanicus. Aquaculture 2004, 238:483-498.
65. Ward S., Harrison P. Changes in gametogenesis and fecundity of acroporid corals that were exposed to elevated nitrogen and phosphorus during the ENCORE experiment. J. Exp. Mar. Biol. Ecol. 2000, 246:179-221.
66. Wu R.S.S. Eutrophication, water borne pathogens and xenobiotic compounds: environmental risks and challenges. Mar. Pollut. Bull. 1999, 39:11-22.
67. Yan H., Li Q., Liu W., Ke Q., Yu R., Kong L. Seasonal changes of oestradiol-17β and testosterone concentrations in the gonad of the razor clam Sinonovacula constricta (lamarck, 1818). J. Mollus. Stud. 2011, 77:116-122.
68. Zhang X., Gao Y., Li Q., Li G., Guo Q., Yan C. Estrogenic compounds and estrogenicity in surface water, sediments, and organisms from Yundang Lagoon in Xiamen. Chin. Arch. Environ. Contam. Toxicol. 2011, 61:93-100.
69. Zibrowius H. Oculina patagonica, scleractiniaire hermatypique introduit en Méditerrané e. Helgol. Wiss. Meeresunters. 1974, 26:153-173.
70. Zibrowius H., Ramos A. Oculina patagonica, scleractiniare exotique en Mediterranee-nouvelles observations dans le sudest de l'Espagne. Rapp PV Reun Comm Int. Explor. Sci. Mer. Mediterr. 1983, 28:297-301.
71. Zvuloni A., Mokady O., Al-Zibdah M., Bernardi G., Gaines S.D., Abelson A. Local scale genetic structure in coral populations: a signature of selection. Mar. Pollut. Bull. 2008, 56:430-438.