Skip to main content

Rapana venosa as an indicator species for TBT exposure over decadal and seasonal scales

Abstract

Imposex and decline in reproductive output in marine gastropods have been linked to tributyltin (TBT) exposure. This study describes Chesapeake Bay, USA, veined rapa whelk Rapana venosa imposex incidence and sex ratios from 1998 to 2009. Tissue TBT concentrations (ng g−1) were examined with respect to whelk sex, size, and water temperature at the time of collection, and also to egg case size, hatching success, and veliger diameter. Imposex incidence declined and population sex ratios moved closer to parity from 1998 to 2009. Observed TBT concentrations (ng g−1) were higher in James River than in Ocean View whelks with higher TBT concentrations observed in males than in females. Exponential declines in TBT concentrations from female-specific first to last clutches within a reproductive season were observed, indicating that whelks depurate TBT through egg case deposition. Egg capsule hatching success and veliger size were similar for female and imposex whelks. The R. venosa imposex levels observed in Chesapeake Bay apparently do not affect the production, release, or viability of larvae.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Amio M (1963) A comparative embryology of marine gastropods with ecological considerations. Bull Shimonoseki Univ Fish 12:15–143

    Google Scholar 

  2. Barreiro R, Gonzalez R, Quintela M, Ruiz JM (2001) Imposex, organotin bioaccumulation and sterility of female Nassarius reticulatus in polluted areas of NW Spain. Mar Ecol Prog Ser 218:203–212

    Article  CAS  Google Scholar 

  3. Bright D, Ellis D (1990) A comparative survey of imposex in northeast Pacific neogastropods (Prosobranchia) related to tributyltin contamination, and choice of a suitable bioindicator. Can J Zool 68:1915–1924

    Article  Google Scholar 

  4. Bryan G, Gibbs P, Huggett R, Curtis L, Bailey D, Dauer D (1989) Effects of tributyltin pollution on the mud snail, Ilyanassa obsoleta, from the York River and Sarah’s Creek, Chesapeake Bay. Mar Pollut Bull 20:458–462

    Article  CAS  Google Scholar 

  5. Bryan G, Burt G, Gibbs P, Pascoe P (1993) Nassarius reticulatus (Nassariidae: Gastropoda) as an indicator of tributyltin pollutin before and after TBT restrictions. J Mar Biol Assoc UK 73:913–929

    Article  CAS  Google Scholar 

  6. Burkenroad M (1931) Notes on the Louisiana conch, Thais haemastoma, Linn., in its relation to the oyster Ostrea virginica. Ecology 12:656–664

    Article  Google Scholar 

  7. Butler P (1954) The southern oyster drill. Proc Natl Shellfish Assoc 44:67–75

    Google Scholar 

  8. Carriker M (1954) Seasonal vertical movements of oyster drills. Proc Natl Shellfish Assoc 45:190–198

    Google Scholar 

  9. Carriker M (1955) Critical review of biology and control of oyster drills Urosalpinx and Eupleura. Special Scientific Report: Fisheries No. 148, US Department of the Interior, Fish and Wildlife Service

  10. Chung E, 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). Malacol Rev 30:25–38

    Google Scholar 

  11. Chung E, Kim S, 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 J Malacol 9:1–15

    Google Scholar 

  12. Chung E, Kim S, Park K, 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 

  13. D’Asaro C (1966) The egg capsules, embryogenesis, and early organogenesis of a common oyster predator, Thais haemastoma floridana (Gastropoda: Prosobranchia). Bull Mar Sci 16:884–914

    Google Scholar 

  14. Davis M (1994) Mariculture techniques for queen conch (Strombas gigas L.): Egg mass to juvenile stage. In: Appledoorn R, Rodriguez B (eds) Queen conch biology, fisheries, and mariculture. Fundacion Cientifica Los Roques, Caracas, Venezuela, pp 231–252

    Google Scholar 

  15. Dowson P, Bubb J, Lester J (1996) Persistence and degradation pathways of tributyltin in freshwater and estuarine sediments. Est Coast Shelf Sci 42:551–562

    Article  CAS  Google Scholar 

  16. Evans D, Huggett R (1991) Statistical modeling of intensive TBT monitoring data in two tidal creeks of the Chesapeake Bay. Mar Environ Res 32:169–186

    Article  Google Scholar 

  17. Evans S, Leksono T, McKinnell P (1995) Tributyltin pollution: a diminishing problem following legislation limiting the use of TBT-based anti-fouling paints. Mar Pollut Bull 30:14–21

    Article  CAS  Google Scholar 

  18. Feare C (1970) The reproductive cycle of the dog whelk (Nucella lapillus). Proc Malacol Soc Lond 39:125–137

    Google Scholar 

  19. Federighi H (1931) Studies on the oyster drill (Urosalpinx cinerea, Say). Bull Bur Fish US 47:83–115

    Google Scholar 

  20. Fernandez M, de Luca Rebello Wagener A, Limaverde A, Scofield A, Pinheiro F, Rodrigues E (2005) Imposex and surface sediment speciation: a combined approach to evaluate organotin contamination in Guanabara Bay, Rio de Janeiro, Brazil. Mar Environ Res 59:435–452

    Article  CAS  Google Scholar 

  21. Fish J, Fish S (1996) A student’s guide to the seashore, 2nd edn. Cambridge University Press, New York

    Google Scholar 

  22. Franz D (1971) Population age structure, growth, and longevity of the marine gastropod Urosalpinx cinerea Say. Biol Bull 140:63–72

    Article  CAS  Google Scholar 

  23. Gibbs PE (1996) Oviduct malformation as a sterilising effect of tributyltin (TBT) induced imposex in Ocenebra erinacea (Gastropoda: Muricidae). J Moll Stud 62:403–413

    Article  Google Scholar 

  24. Gibbs PE, Bryan GW (1987) TBT paints and the demise of the dog-whelk, Nucella lapillus (Gastropoda). In: Proc Oceans ‘87 Int Organotin symp, vol 4, IEEE, Piscataway, NJ, USA, pp 1482–1487

  25. Gibbs PE, Bryan GW (1996) Reproductive failure in the gastropod Nucella lapillus associated with imposex caused by tributyltin pollution: a review. In: Champs MA, Seligman PF (eds) Organotin: environmental fate and effects. Chapman and Hall, New York, pp 259–280

    Google Scholar 

  26. Gibbs PE, Bryan GW, Pascoe P, Burt GR (1987) The use of the dog-whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. J Mar Biol Ass UK 67:507–523

    Article  CAS  Google Scholar 

  27. Gibbs PE, Pascoe PL, Burt GR (1988) Sex change in the female dog whelk Nucella lapillus induced by tributyltin from antifouling paints. J Mar Biol Assoc UK 68:715–731

    Article  Google Scholar 

  28. Gibbs PE, Bryan GW, Pascoe PL, Burt GR (1990) Reproductive abnormalities in female Ocenebra erinacea (Gastropoda) resulting from tributyltin induced imposex. J Mar Biol Assoc UK 70:639–656

    Article  Google Scholar 

  29. Gibbs PE, Bryan GW, Pascoe PL (1991a) TBT-induced imposex in the dogwhelk, Nucella lapillus: geographical uniformity of the response and effects. Mar Environ Res 32:79–87

    Article  CAS  Google Scholar 

  30. Gibbs PE, Spencer B, Pascoe P (1991b) The American oyster drill, Urosalpinx cinerea (Gastropoda): evidence of decline in an imposex-affected population (R. Blackwater, Essex). J Mar Biol Assoc UK 71:827–838

    Article  Google Scholar 

  31. Harding JM (2006) Growth and development of veined rapa whelk Rapana venosa veligers. J Shellfish Res 25:941–946

    Article  Google Scholar 

  32. Harding JM, Mann R (1999) Observations on the biology of the veined rapa whelk, Rapana venosa (Valenciennes, 1846) in the Chesapeake Bay. J Shellfish Res 18:9–17

    Google Scholar 

  33. Harding JM, Mann R, Ware-Kilduff C (2007) The effects of female size on fecundity in a large marine gastropod Rapana venosa (Muricidae). J Shellfish Res 26:33–42

    Article  Google Scholar 

  34. Harding JM, Mann R, Kilduff C (2008) Influence of environmental factors and female size on reproductive output in a temperate invasive marine gastropod Rapana venosa (Muricidae: Valenciennes 1846). Mar Biol 155:571–581

    Article  Google Scholar 

  35. Harding JM, Trapiani CM, Walton W, Frick M, Mann R (2011) Sea turtles as potential dispersal vectors for non-indigenous species: the veined rapa whelk as an epibiont of loggerhead turtles. Southeast Nat 10:233–244

    Article  Google Scholar 

  36. Huggett RJ, Evans DA, MacIntyre WG, Unger MA, Seligman PF, Hall LW Jr (1996) Tributyltin concentration in waters of the Chesapeake Bay. In: Champ MA, Seligman PF (eds) Tributyltin: environmental fate and effects. Chapman and Hall, New York, pp 485–502

    Google Scholar 

  37. Ide I, Witten E, Fisher J, Kalbfus W, Zellner A, Stroben E, Watermann B (1997) Accumulation of organotin compounds in the common whelk Buccinum undatum and the red whelk Neptunea antiqua in association with imposex. Mar Ecol Prog Ser 152:197–203

    Article  CAS  Google Scholar 

  38. Jestel EA (2002) Imposex as an indicator of butyltin exposure in the veined rapa whelk (Rapana venosa): a Chesapeake Bay invader. MS thesis, Virginia Institute of Marine Science, The College of William & Mary, Gloucester Point

  39. Knickmeyer R, Steinhart H (1990) Seasonal variations and sex related differences of organochlorines in whelks (Buccinum undatum) from the German bight. Chemosphere 20:109–122

    Article  CAS  Google Scholar 

  40. Limaverde A, Wagener A, Fernandez M, Scofield A, Coutinho R (2007) Stramonita haemastoma as a bioindicator for organotin contamination in coastal environments. Mar Environ Res 64:384–398

    Article  CAS  Google Scholar 

  41. Luckenbach MW, O’Beirn FX, Taylor J (1999) An introduction to culturing oysters in Virginia. Virginia Institute of Marine Science, Gloucester Point

    Google Scholar 

  42. Mann R, Harding JM (2000) Invasion of the North American Atlantic coast by a large predatory Asian mollusc. Biol Inv 2:7–22

    Article  Google Scholar 

  43. Mann R, Harding JM (2003) Salinity tolerance of larval Rapana venosa: implications for dispersal and establishment of an invading predatory gastropod on the North American Atlantic coast. Biol Bull 204:96–103

    Article  CAS  Google Scholar 

  44. Mann R, Harding JM, Westcott E (2006) Occurrence of imposex and seasonal patterns of gametogenesis in the invading veined rapa whelk Rapana venosa from Chesapeake Bay, USA. Mar Ecol Prog Ser 310:129–138

    Article  Google Scholar 

  45. Mensink B, Everaarts JM, Kralt H, ten Hallers-Tjabbes C, Boon J (1996) Tributyltin exposure in early life stages induces the development of male sexual characteristics in the common whelk Buccinum undatum. Mar Environ Res 42:151–154

    Article  CAS  Google Scholar 

  46. Mensink BP, Kralt H, Vethaak AD, ten Hallers-Tjabbes CC, Koeman JH, van Hattum B, Boon JP (2002) Imposex induction in laboratory reared juvenile Buccinum undatum by tributyltin (TBT). Environ Toxicol Pharmacol 11:49–65

    Article  CAS  Google Scholar 

  47. Nicholson G, Evans S (1997) Anthropogenic impacts on the stocks of the common whelk (Buccinum undulatum (L.). Mar Environ Res 44:305–314

    Article  CAS  Google Scholar 

  48. Oehlmann J, Stroben E, Fioroni P (1992) The rough tingle Ocenebra erinacea (Gastropoda: Muricidae): an exhibitor of imposex in comparison to Nucella lapillus. Helgolander Meeresun 46:311–328

    Article  Google Scholar 

  49. Pearce JB, Thorson G (1967) The feeding and reproductive biology of the red whelk, Neptunea antiqua (L.) (Gastropoda, Prosobranchia). Ophelia 4:277–314

    Article  Google Scholar 

  50. Poloczanska ES, Ansell AD (1999) Imposex in the whelks Buccinum undatum and Neptunea antiqua from the west coast of Scotland. Mar Environ Res 47:203–212

    Article  CAS  Google Scholar 

  51. Power A, Keegan B (2001a) The significance of imposex levels and TBT contamination in the red whelk Neptunea antiqua (L.) from the offshore Irish Sea. Mar Pollut Bull 42:761–772

    Article  CAS  Google Scholar 

  52. Power A, Keegan B (2001b) Seasonal patterns in the reproductive activity of the red whelk, Neptunea antiqua (Mollusca: Prosobranchia) in the Irish Sea. J Mar Biol Assoc UK 81:243–250

    Google Scholar 

  53. Rodigari F, Carpenter PD, Crecelius EA, Ramirez LM, Unger MA (2005) Tributyltin (6710)/Gas chromatographic/mass spectrometric method. In: Eaton AD, Clesceri LS, Rice EW, Greenberg AE, Franson MAH (eds) Standard methods for the examination of water and wastewater. APHA, AWWA and WEF

  54. Roller R, Stickle W (1988) Intracapsular development of Thais haemastoma canaliculata (Gray) (Prosobranchia: Muricidae) under laboratory conditions. Am Malacol Bull 6:189–197

    Google Scholar 

  55. Roller R, Stickle W (1989) Temperature and salinity effects on the intracapsular development, metabolic rates, and survival to hatching of Thais haemastoma canaliculata (Gray) (Prosobranchia: Muricidae) under laboratory conditions. J Exp Mar Biol Ecol 125:235–251

    Article  Google Scholar 

  56. Saglam H, Duzgunes E (2007) Deposition of egg capsule and larval development of Rapana venosa (Gastropoda: Muricidae) from the south-eastern Black Sea. J Mar Biol Assoc UK 87:953–957

    Article  Google Scholar 

  57. Sakai A, Allendorf F, Holt J, Lodge D, Molofsky J, With K, Baughman S, Cabin R, Cohen J, Ellstrand N, McCauley D, O’Neil P, Parker I, Thompson J, Weller S (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  58. Savini D, Harding JM, Mann R (2002) Rapa whelk Rapana venosa (Valenciennes, 1846) predation rates on hard clams Mercenaria mercenaria (Linnaeus, 1758). J Shellfish Res 21:777–779

    Google Scholar 

  59. Smith B (1971) Sexuality in the American mud snail, Nassarius obsoletus Say. Proc Malacol Soc Lond 39:377–378

    Google Scholar 

  60. Spence SK, Bryan GW, Gibbs PE, Masters D, Morris L, Hawkins SJ (1990) Effects of TBT contamination on Nucella populations. Funct Ecol 4:425–432

    Article  Google Scholar 

  61. Spight TM, Emlen J (1976) Clutch sizes of two marine snails with a changing food supply. Ecology 57:1162–1178

    Article  Google Scholar 

  62. Sternberg RM, Gooding MP, Hotchkiss AK, LeBlanc GA (2010) Environmental-endocrine control of reproductive maturation in gastropods: implications for the mechanism of tributyltin-induced imposex in prosobranchs. Ecotoxicology 19:4–23

    Article  CAS  Google Scholar 

  63. Stickle W, Zhang Z (2003) Long term trends in imposex in six populations of Stramonita haemastoma. Bull Mar Sci 72:685–694

    Google Scholar 

  64. Stickle W, Sharp-Dahl J, Rice S, Short J (1990) Imposex induction in Nucella lima (Gmelin) via mode of exposure to tributyltin. J Exp Mar Biol Ecol 143:165–180

    Article  Google Scholar 

  65. Strand J, Jacobsen J (2002) Imposex in two sublittoral neogastropods from the Kattegat and Skagerrak: the common whelk Buccinum undatum and the red whelk Neptunea antiqua. Mar Ecol Prog Ser 244:171–177

    Article  Google Scholar 

  66. Tallmark B (1980) Population dynamics of Nassarius reticulatus (Gastropoda, Prosobranchia) in Gullmar Fjord, Sweden. Mar Ecol Prog Ser 3:51–62

    Article  Google Scholar 

  67. ten Hallers-Tjabbes C, Everaarts J, Mensink B, Boon J (1996) The decline of the North Sea Whelk (Buccinum undatum L.) between 1970 and 1990: a natural or human-induced event? Mar Ecol 17:333–343

    Article  CAS  Google Scholar 

  68. Tester M, Ellis D (1995) TBT controls and recovery of whelks from imposex. Mar Pollut Bull 30:90–91

    Article  CAS  Google Scholar 

  69. Titley-O’Neal CP, Munkittrick KR, MacDonald BA (2011) The effects of organotin on female gastropods. J Environ Monit 13:2360–2388

    Article  Google Scholar 

  70. Unger MA (2007) Elizabeth River tributyltin monitoring program (1999–2006). Virginia Institute of Marine Science, Gloucester Point

    Google Scholar 

  71. Unger MA, MacIntyre WG, Greaves J, Huggett RJ (1986) GC determination of butyltins in natural waters by flame photometric detection of hexyl derivatives with mass spectrometric confirmation. Chemosphere 15:461–470

    Article  CAS  Google Scholar 

  72. Unger MA, MacIntyre WG, Huggett RJ (1988) Sorption behavior of tributyltin on estuarine and freshwater sediments. Environ Toxicol Chem 7:907–915

    Article  CAS  Google Scholar 

  73. Unger MA, Greaves J, Huggett RJ (1996) Grignard derivatization and mass spectrometry as techniques in the analysis of butyltins in environmental samples. In: Champ MA, Seligman PF (eds) Tributyltin: environmental fate and effects. Chapman and Hall, New York, pp 123–134

    Google Scholar 

  74. Valentinsson D (2002) Reproductive cycle and maternal effects on offspring size and number in the neogastropod Buccinum undatum (L.). Mar Biol 140:1139–1147

    Article  Google Scholar 

  75. Waite M, Waldock M, Thaine J, Smith D, Milton S (1991) Reductions in TBT concentrations in UK estuaries following legislation in 1986 and 1987. Mar Environ Res 32:89–111

    Article  Google Scholar 

  76. Ware C (2002) Temporal and spatial variation in reproductive output of the veined rapa whelk (Rapana venosa) in the Chesapeake Bay. MS thesis, Virginia Institute of Marine Science, The College of William & Mary, Gloucester Point

  77. Westcott E (2001) A descriptive study of the reproductive biology of the veined rapa whelk (Rapana venosa) in the Chesapeake Bay. MS thesis, Virginia Institute of Marine Science, The College of William & Mary, Gloucester Point

  78. Williamson M (1996) Biological invasions. Chapman and Hall, New York

    Google Scholar 

  79. Zar JH (1996) Biostatistical analysis. Prentice Hall, New Jersey

    Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge all the people who contributed whelks to our bounty program (1998–2009), especially the watermen. The bounty program was made possible through funding from the Virginia Institute of Marine Science/College of William & Mary, The Virginia Marine Resources Commission, National Oceanic and Atmospheric Administration, and the Virginia General Assembly. Their support is appreciated. Courtney Harris Burge, Karen Caposella, Emily Chandler, Meredith Fagan, Stephanie Gera, James Green, Rebecca Green, Meghan Harris, Stephanie Haywood, Rhonda Howlett, David Kerstetter, Adriana Picariello, Erin Reilly, Matthew Robinson, Melissa Southworth, George Vadas, and Erica Westcott assisted with whelk collection and processing. Melissa Southworth, Meghan Harris, Meredith Fagan, and Erin Reilly assisted with laboratory analyses and data entry. Ellen Travelstead, George Vadas, and James Greene assisted with TBT analyses. This manuscript includes data from the M.S. theses of Catherine Ware Kilduff and E. Alex Jestel (both School of Marine Science, College of William & Mary, Williamsburg, VA). This is contribution number 3295 from the Virginia Institute of Marine Science.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Juliana M. Harding.

Additional information

Communicated by J. P. Grassle.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Harding, J.M., Unger, M.A., Mann, R. et al. Rapana venosa as an indicator species for TBT exposure over decadal and seasonal scales. Mar Biol 160, 3027–3042 (2013). https://doi.org/10.1007/s00227-013-2292-7

Download citation

Keywords

  • Shell Length
  • Penis Length
  • Ocean View
  • Rapa Whelk
  • Benthic Juvenile