Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T12:37:12.121Z Has data issue: false hasContentIssue false
  • English
  • Français

Sex and site-specific trends in veined rapa whelk (Rapana venosa) tributyltin bioaccumulation: considerations for biomonitoring

Published online by Cambridge University Press:  09 June 2016

Juliana M. Harding ,
Michael A. Unger ,
E. Alex Jestel  and
Roger Mann
Juliana M. Harding*
Affiliation:
Department of Fisheries Science, Virginia Institute of Marine Science, College of William & Mary, Gloucester Point, Virginia 23062, USA Department of Marine Science, Coastal Carolina University, Conway, South Carolina 29528-6054, USA
Michael A. Unger
Affiliation:
Department of Aquatic Health Sciences, Virginia Institute of Marine Science, College of William & Mary, Gloucester Point, Virginia 23062, USA
E. Alex Jestel
Affiliation:
Department of Aquatic Health Sciences, Virginia Institute of Marine Science, College of William & Mary, Gloucester Point, Virginia 23062, USA U. S. Army, Edgewood, MD 21010, USA
Roger Mann
Affiliation:
Department of Fisheries Science, Virginia Institute of Marine Science, College of William & Mary, Gloucester Point, Virginia 23062, USA
*
Correspondence should be addressed to: J. M. Harding, Department of Marine Science, Coastal Carolina University, Conway, South Carolina 29528-6054, USA email: jharding@coastal.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

The imposition of male sexual characteristics onto the female (imposex) is present in wild populations of the non-native veined rapa whelk (Rapana venosa) in Chesapeake Bay, USA but does not appear to compromise reproductive function. Cultured whelks were used to test two hypotheses: (1) Observed imposex metrics will be similar to tributyltin (TBT) water concentrations at each of three sites; (2) Male and imposex/female whelks from the same site will have similar TBT body burdens. Cultured 2-year-old whelks were transplanted to three field sites in the York River, USA at the onset of their second reproductive season. Transplant site mean TBT water concentrations ranged from 1.4 ± 0.77 to 64.2 ± 57.8 ng l−1. Imposex incidence was 100% after 28 weeks with an observed M:F:IF ratio of 81:0:92 across all sites. Imposex stages (median vas deferens scale index = 4) and reproductive output were similar across sites. The imposex severity (IS = penis length/shell length) increased with increasing TBT concentrations. The relative penis length (RPLI) and relative penis size (RPSI) indices were positively related to site-specific TBT levels. Male whelks accumulated significantly higher TBT concentrations than female whelks at the site with the highest TBT concentration. Mean TBT concentrations in whelk egg capsules were significantly higher than concentrations in male or female whelk tissue. Egg capsule deposition provides a depuration mechanism for female whelks to reduce body burden of lipophilic TBT. Sex, season and reproductive status should be considered when using gastropod bioaccumulation to monitor TBT effects.

Keywords

Rapana venosaveined rapa whelktributyltinimposexbiomonitoringbioaccumulationdepuration
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 97 , Issue 7 , November 2017 , pp. 1495 - 1504
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bryan, G., Gibbs, P., Huggett, R., Curtis, L., Bailey, D. and Dauer, D. (1989) Effects of tributyltin pollution on the mud snail, Ilyanassa obsoleta, from the York River and Sarah's Creek, Chesapeake Bay. Marine Pollution Bulletin 20, 458–462.CrossRefGoogle Scholar
Chung, E. and Kim, S. (1997) Cytological studies on testicular maturation and cyclic changes in the epithelial cells of the seminal vesicle of the male purple shell, Rapana venosa (Gastropoda: Muricidae). Malacological Review 30, 25–38.Google Scholar
Chung, E., Kim, S. and Kim, Y. (1993) Reproductive ecology of the purple shell Rapana venosa (Gastropoda: Muricidae), with special reference to the reproductive cycle, depositions of egg capsules, and hatchings of larvae. Korean Journal of Malacology 9, 1–15.Google Scholar
Chung, E., Kim, S., Park, K. and Park, G. (2002) Sexual maturation, spawning, and deposition of the egg capsules of the female purple shell, Rapana venosa (Gastropoda: Muricidae). Malacologia 44, 241–257.Google Scholar
Fernandez, M., de Luca Rebello, A., Wagener, A., Limaverde, A., Scofield, A., Pinheiro, F. and Rodrigues, E. (2005) Imposex and surface sediment speciation: a combined approach to evaluate organotin contamination in Guanabara Bay, Rio de Janeiro, Brazil. Marine Environmental Research 59, 435–452.CrossRefGoogle ScholarPubMed
Gibbs, P.E. and Bryan, G.W. (1987) TBT paints and the demise of the dog-whelk, Nucella lapillus (Gastropoda). In Proceedings of the Oceans ‘87 International Organotin Symposium, Volume 4. Piscataway, NJ: Institute of Electrical and Electronics Engineers, pp. 1482–1487.CrossRefGoogle Scholar
Gibbs, P.E. and Bryan, G.W. (1996) Reproductive failure in the gastropod Nucella lapillus associated with imposex caused by tributyltin pollution: a review. In Champ, M.A. and Seligman, P.F. (eds) Organotin: environmental fate and effects. London: Chapman and Hall Publishers, pp. 259–280.CrossRefGoogle Scholar
Gibbs, P.E., Bryan, G.W., Pascoe, P. and Burt, G. (1987) The use of the dog-whelk Nucella lapillus as an indicator of tributyltin (TBT) contamination. Journal of the Marine Biological Association of the United Kingdom 67, 507–523.CrossRefGoogle Scholar
Gibbs, P.E., Pascoe, P. and Burt, G. (1988) Sex change in the female dog-whelk Nucella lapillus, induced by tributyltin from antifouling paints. Journal of the Marine Biological Association of the United Kingdom 68, 715–731.CrossRefGoogle Scholar
Harding, J.M. (2003) Predation by blue crabs, Callinectes sapidus, on rapa whelks, Rapana venosa: possible natural controls for an invasive species? Journal of Experimental Marine Biology and Ecology 297, 161–177.CrossRefGoogle Scholar
Harding, J.M. (2006) Growth and development of veined rapa whelk Rapana venosa veligers. Journal of Shellfish Research 25, 941–946.Google Scholar
Harding, J.M. and Mann, R. (1999) Observations on the biology of the veined rapa whelk, Rapana venosa (Valenciennes, 1846) in the Chesapeake Bay. Journal of Shellfish Research 18, 9–17.Google Scholar
Harding, J.M. and Mann, R. (2005) Veined rapa whelk, Rapana venosa range extensions in the Virginia waters of the Chesapeake Bay, USA. Journal of Shellfish Research 24, 381–385.Google Scholar
Harding, J.M., Mann, R. and Kilduff, C. (2008) Influence of environmental factors and female size on reproductive output in a temperate invasive marine gastropod Rapana venosa (Muricidae: Valenciennes 1846). Marine Biology 155, 571–581.CrossRefGoogle Scholar
Harding, J.M., Mann, R., Moeller, P. and Hsia, M. (2009) Rapana venosa mortality in relation to an Alexandrium monilatum bloom in the York River, USA. Journal of Shellfish Research 28, 363–367.CrossRefGoogle Scholar
Harding, J.M., Mann, R. and Ware-Kilduff, C. (2007) The effects of female size on fecundity in a large marine gastropod Rapana venosa (Muricidae). Journal of Shellfish Research. 26, 33–42.CrossRefGoogle Scholar
Harding, J.M., Unger, M.A., Mann, R., Jestel, E.A. and Kilduff, C. (2013) Rapana venosa as an indicator species for TBT exposure over decadal and seasonal scales. Marine Biology 160, 3027–3042.CrossRefGoogle Scholar
Inoue, S., Oshima, Y., Usuki, H., Hamaguchi, M., Hanamura, Y., Kai, N., Shimasaki, Y. and Honjo, Y. (2006) Effects of tributyltin maternal and/or waterborne exposure on the embryonic development of the Manila clam, Ruditapes philippinarum . Chemosphere 63, 881–888.CrossRefGoogle ScholarPubMed
Langston, W.J., Pope, N.D., Davey, M., Langston, K.M., O’ Hara, S.C.M., Gibbs, P.E. and Pascoe, P.L. (2015) Recovery from TBT pollution in English Channel environments: a problem solved? Marine Pollution Bulletin 95, 551–564.CrossRefGoogle ScholarPubMed
Laughlin, R.B. (1996) Bioaccumulation of TBT by aquatic organisms. In Champ, M.A. and Seligman, P.F. (eds) Organotin: environmental fate and effects. London: Chapman and Hall Publishers, pp. 331–356.CrossRefGoogle Scholar
Maguire, J.R. (2000) Review of the persistence, bioaccumulation and toxicity of tributlytin in aquatic environments in relation to Canada's toxic substances management policy. Water Quality Research Journal Canada 35, 633–679.CrossRefGoogle Scholar
Mann, R. and Harding, J.M. (2000) Invasion of the North American Atlantic coast by a large predatory Asian mollusc. Biological Invasions 2, 7–22.CrossRefGoogle Scholar
Mann, R. and Harding, J.M. (2003) Salinity tolerance of larval Rapana venosa: implications for dispersal and establishment of an invading predatory gastropod on the North American Atlantic coast. Biological Bulletin 204, 96–103.CrossRefGoogle ScholarPubMed
Mann, R., Harding, J.M. and Westcott, E. (2006) Occurrence of imposex and seasonal patterns of gametogenosis in the invading veined rapa whelk Rapana venosa from Chesapeake Bay, USA. Marine Ecology Progress Series 310, 129–138.CrossRefGoogle Scholar
McClellan-Green, P., Romano, J. and Oberdorster, E. (2007) Does gender really matter in contaminant exposure? A case study using invertebrate models. Environmental Research 104, 183–191.CrossRefGoogle ScholarPubMed
McManus, G.B., Wyman, K.D., Peterson, W.T. and Wurster, C.F. (1983) Factors affecting elimination of PCBs in the marine copepod Acartia tonsa . Estuarine Coastal and Shelf Science 17, 421–430.CrossRefGoogle Scholar
Rodigari, F., Carpenter, P.D., Crecelius, E.A., Ramirez, L.M. and Unger, M.A. (2005) Tributyltin (6710)/gas chromatographic/mass spectrometric method. In Eaton, A.D., Clesceri, L.S., Rice, E.W., Greenberg, A.E. and Franson, M.A.H. (eds) Standard methods for the examination of water and wastewater. Washington, DC: APHA, AWWA and WEF Publishers, pp. S10–S16.Google Scholar
Savini, D., Harding, J.M. and Mann, R. (2002) Rapa whelk Rapana venosa (Valenciennes, 1846) predation rates on hard clams Mercenaria mercenaria (Linnaeus, 1758). Journal of Shellfish Research 21, 777–780.Google Scholar
Shi, H., Huang, C.J., Zhu, S.X., Yu, Z.J. and Xie, W.Y. (2005) Generalized system of imposex and reproductive failure in female gastropods of coastal waters of mainland China. Marine Ecology Progress Series 304, 179–189.CrossRefGoogle Scholar
Smith, B. (1971) Sexuality in the American mud snail, Nassarius obsoletus Say. Proceedings of the Malacological Society of London 39, 377–378.Google Scholar
Sternberg, R.M., Gooding, M.P., Hotchkiss, A.K. and LeBlanc, G.A. (2010) Environmental-endocrine control of reproductive maturation in gastropods: implications for the mechanism of tributyltin-induced imposex in prosobranchs. Ecotoxicology 19, 4–23.CrossRefGoogle ScholarPubMed
Stickle, W., Sharp-Dahl, J.L., Rice, S.D. and Short, J.W. (1990) Imposex induction in Nucella lima via mode of exposure to tributyltin. Journal of Experimental Marine Biology and Ecology 143, 165–180.CrossRefGoogle Scholar
Titley-O'Neal, C., MacDonald, B.A., Pelletier, E., Saint-Louis, R. and Phillip, O.S. (2011) The relationship between imposex and tributyltin (TBT) concentration in Strombus gigas from the British Virgin Islands. Bulletin of Marine Science 87, 421–435.CrossRefGoogle Scholar
Unger, M.A., Greaves, J. and Huggett, R.J. (1996) Grignard derivatization and mass spectrometry as techniques in the analysis of butyltins in environmental samples. In Champ, M.A. and Seligman, P.F. (eds) Organotin: environmental fate and effects. London: Chapman and Hall Publishers, pp. 123–134.CrossRefGoogle Scholar
Unger, M.A., MacIntyre, W.G., Greaves, J. and Huggett, R.J. (1986) GC determination of butyltins in natural waters by flame photometric detection of hexyl derivatives with mass spectrometric confirmation. Chemosphere 15, 461–470.CrossRefGoogle Scholar
Ware, C. (2002) Temporal and spatial variation in reproductive output of the veined rapa whelk (Rapana venosa) in the Chesapeake Bay . MS thesis. College of William & Mary, Gloucester Point, USA.Google Scholar
Yang, R., Zhou, Q., Liu, J. and Jiang, G. (2006) Butyltin compounds in molluscs from Chinese Bohai coastal waters. Food Chemistry 97, 637–643.CrossRefGoogle Scholar
Zar, J.H. (1996) Biostatistical analysis, 3rd edition. Englewood Cliffs, NJ: Prentice-Hall.Google Scholar
Supplementary material: PDF

Harding supplementary material S1

Harding supplementary material

Download Harding supplementary material S1(PDF)
PDF 856.2 KB
Supplementary material: PDF

Harding supplementary material S2

Harding supplementary material

Download Harding supplementary material S2(PDF)
PDF 276.1 KB
Supplementary material: PDF

Harding supplementary material S3

Harding supplementary material

Download Harding supplementary material S3(PDF)
PDF 72.2 KB
Supplementary material: PDF

Harding supplementary material S4

Harding supplementary material

Download Harding supplementary material S4(PDF)
PDF 69.6 KB
Supplementary material: PDF

Harding supplementary material S5

Harding supplementary material

Download Harding supplementary material S5(PDF)
PDF 210.2 KB