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A decadal study of biometric and imposex indices in two gastropods

Published online by Cambridge University Press:  20 June 2019

J. M. Ruiz
Affiliation:
Grupo BIOCOST, Centro de Investigacións Científicas Avanzadas (CICA), Depto. Biología, Facultade de Ciencias, Campus da Zapateira, Universidade da Coruña, 15071 Coruña,Spain
B. Carro
Affiliation:
Grupo BIOCOST, Centro de Investigacións Científicas Avanzadas (CICA), Depto. Biología, Facultade de Ciencias, Campus da Zapateira, Universidade da Coruña, 15071 Coruña,Spain
N. Albaina
Affiliation:
Grupo BIOCOST, Centro de Investigacións Científicas Avanzadas (CICA), Depto. Biología, Facultade de Ciencias, Campus da Zapateira, Universidade da Coruña, 15071 Coruña,Spain
L. Couceiro
Affiliation:
Grupo BIOCOST, Centro de Investigacións Científicas Avanzadas (CICA), Depto. Biología, Facultade de Ciencias, Campus da Zapateira, Universidade da Coruña, 15071 Coruña,Spain
M. Quintela
Affiliation:
Grupo BIOCOST, Centro de Investigacións Científicas Avanzadas (CICA), Depto. Biología, Facultade de Ciencias, Campus da Zapateira, Universidade da Coruña, 15071 Coruña,Spain
R. Barreiro
Affiliation:
Grupo BIOCOST, Centro de Investigacións Científicas Avanzadas (CICA), Depto. Biología, Facultade de Ciencias, Campus da Zapateira, Universidade da Coruña, 15071 Coruña,Spain
Corresponding
E-mail address:

Abstract

We have monitored tributyltin (TBT) pollution in Galicia (NW Spain) for more than a decade by means of assessing gastropod imposex in populations of Nucella lapillus (N ≥ 34) and Tritia reticulata (N ≥ 18) at regular intervals. Several thousand specimens were processed to obtain their shell height (SH), penis length (PL) and vas deferens sequence (VDS); imposex indices (including the VDS index, VDSI) were subsequently calculated. The regional mean SH of both females and males has not changed significantly in either species throughout the study. This also applies to the mean male PL in N. lapillus, but male T. reticulata penises surprisingly enlarged. On the contrary, the regional mean female PL (MFPL) and all imposex indices significantly decreased in both snails. Results confirm previous conclusions based on the chemical analyses of tissues and partial imposex observations. In addition, the close correlations between MFPL and VDSI show some potential applications to TBT biomonitoring.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

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References

Bailey, SK and Davies, IM (1991) Continuing impact of TBT, previously used in mariculture, on dogwhelk (Nucella lapillus L.) populations in a Scottish sea loch. Marine Environmental Research 32, 187199.CrossRefGoogle Scholar
Barreiro, R, Quintela, M and Ruiz, JM (1999) Aphally and imposex in Nucella lapillus from Galicia (NW Spain): incidence, geographical distribution and consequences for the biomonitoring of TBT contamination. Marine Ecology Progress Series 185, 229238.CrossRefGoogle Scholar
Barreiro, R, González, R, Quintela, M and Ruiz, JM (2001) Imposex, organotin bioaccumulation and sterility of female Nassarius reticulatus in polluted areas of NW Spain. Marine Ecology Progress Series 218, 203212.CrossRefGoogle Scholar
Barroso, CM and Moreira, MH (1998) Reproductive cycle of Nassarius reticulatus in the Ria de Aveiro, Portugal: implications for imposex studies. Journal of the Marine Biological Association of the United Kingdom 78, 12331246.CrossRefGoogle Scholar
Barroso, CM, Moreira, MH and Bebianno, MJ (2002) Imposex, female sterility and organotin contamination of the prosobranch Nassarius reticulatus (L.) from the Portuguese coast. Marine Ecology Progress Series 230, 127135.CrossRefGoogle Scholar
Barroso, CM, Moreira, MH and Richardson, CA (2005) Age and growth of Nassarius reticulatus in the Ria de Aveiro, NW Portugal. Journal of the Marine Biological Association of the United Kingdom 85, 151156.CrossRefGoogle Scholar
Bryan, GW, Burt, GR, Gibbs, PE and Pascoe, PL (1993) Nassarius reticulatus (Nassariidae: Gastropoda) as an indicator of tributyltin pollution before and after TBT restrictions. Journal of the Marine Biological Association of the United Kingdom 73, 913929.CrossRefGoogle Scholar
Bryan, GW, Gibbs, PE, Hummerstone, LG and Burt, GR (1986) The decline of the gastropod Nucella lapillus around South-West England: evidence for the effect of tributyltin from antifouling paints. Journal of the Marine Biological Association of the United Kingdom 66, 611640.CrossRefGoogle Scholar
Bryan, GW, Gibbs, PE, Burt, GR and Hummerstone, LG (1987) The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: long-term field and laboratory experiments. Journal of the Marine Biological Association of the United Kingdom 67, 525544.CrossRefGoogle Scholar
Bryan, GW, Gibbs, PE, Hummerstone, LG and Burt, GR (1989) Uptake and transformation of 14C-labelled tributyltin chloride by the dog-whelk, Nucella lapillus: importance of absorption from the diet. Marine Environmental Research 28, 241245.CrossRefGoogle Scholar
Cacciatore, F, Brusa, RB, Noventa, S, Antonini, C, Moschino, V, Formalewicz, M, Gion, C, Berto, D, Gabellini, M and Marin, MG (2018) Imposex levels and butyltin compounds (BTs) in Hexaplex trunculus (Linnaeus, 1758) from the northern Adriatic Sea (Italy): ecological risk assessment before and after the ban. Ecotoxicology and Environmental Safety 147, 688698.CrossRefGoogle ScholarPubMed
Castro, IB and Fillmann, G (2012) High tributyltin and imposex levels in the commercial muricid Thais chocolata from two Peruvian harbor areas. Environmental Toxicology and Chemistry 31, 955960.CrossRefGoogle ScholarPubMed
Crothers, JH (1985) Dog-whelks: an introduction to the biology of Nucella lapillus (L.). Field Studies 6, 291360.Google Scholar
de Azevedo, D, Rocha-Barreira, CD, Matthews-Cascon, H and Castro, IB (2012) Pugilina morio L., a new imposex exhibitor from South American estuarine environments: approach for a non-lethal method to evaluate imposex. Bulletin of Environmental Contamination and Toxicology 89, 786792.CrossRefGoogle Scholar
Galante-Oliveira, S, Oliveira, I, Santos, JA, Pereira, MD, Pacheco, M and Barroso, CM (2010) Factors affecting RPSI in imposex monitoring studies using Nucella lapillus (L.) as bioindicator. Journal of Environmental Monitoring 12, 10551063.CrossRefGoogle ScholarPubMed
Galante-Oliveira, S, Oliveira, I, Ferreira, N, Santos, JA, Pacheco, M and Barroso, C (2011) Nucella lapillus L. imposex levels after legislation prohibiting TBT antifoulants: temporal trends from 2003 to 2008 along the Portuguese coast. Journal of Environmental Monitoring 13, 304312.CrossRefGoogle ScholarPubMed
Gibbs, PE (1993) Phenotypic changes in the progeny of Nucella lapillus (Gastropoda) transplanted from an exposed shore to sheltered inlets. Journal of Molluscan Studies 59, 187194.CrossRefGoogle Scholar
Gibbs, PE (1999) Biological effects of contaminants: use of imposex in the dogwhelk (Nucella lapillus) as a bioindicator of tributyltin (TBT) pollution. International Council for the Exploration of the Sea (Techniques in Marine Environmental Sciences), TIMES 24, 37 pp.Google Scholar
Gibbs, PE (2005) Male genital defect (Dumpton syndrome) in the dog-whelk Nucella lapillus (L.) (Neogastropoda): Mendelian inheritance inferred, based on laboratory breeding experiments. Journal of the Marine Biological Association of the United Kingdom 85, 143150.CrossRefGoogle Scholar
Gibbs, PE, Bryan, GW, Pascoe, PL and Burt, GR (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, 507523.CrossRefGoogle Scholar
Guomundsdottir, LO, Ho, KKY, Lam, JCW, Svavarsson, J and Leung, KMY (2011) Long-term temporal trends (1992–2008) of imposex status associated with organotin contamination in the dogwhelk Nucella lapillus along the Icelandic coast. Marine Pollution Bulletin 63, 500507.CrossRefGoogle Scholar
Harding, JM, Unger, MA, Mann, R, Jestel, EA and Kilduff, C (2013) Rapana venosa as an indicator species for TBT exposure over decadal and seasonal scales. Marine Biology 160, 30273042.CrossRefGoogle Scholar
Huet, M, Fioroni, P, Oehlmann, J and Stroben, E (1995) Comparison of imposex response in three prosobranch species. Hydrobiologia 309, 2935.CrossRefGoogle Scholar
Kim, NS, Hong, SH, Shin, KH and Shim, WJ (2017) Imposex in Reishia clavigera as an indicator to assess recovery of TBT pollution after a total ban in South Korea. Archives of Environmental Contamination and Toxicology 73, 301309.CrossRefGoogle ScholarPubMed
Laranjeiro, F, Sanchez-Marin, P, Oliveira, IB, Galante-Oliveira, S and Barroso, C (2018) Fifteen years of imposex and tributyltin pollution monitoring along the Portuguese coast. Environmental Pollution 232, 411421.CrossRefGoogle ScholarPubMed
Minchin, A and Davies, IM (1998) Effect of Sample Handling on Imposex Measurement in the Dogwhelk Nucella lapillus (L.). Aberdeen: FRS Marine Laboratory, no. 4/98, 10 pp.Google Scholar
Morley, NJ (2006) Parasitism as a source of potential distortion in studies on endocrine disrupting chemicals in molluscs. Marine Pollution Bulletin 52, 13301332.CrossRefGoogle ScholarPubMed
Nicolaus, EEM and Barry, J (2015) Imposex in the dogwhelk (Nucella lapillus): 22-year monitoring around England and Wales. Environmental Monitoring and Assessment 187, 736.CrossRefGoogle ScholarPubMed
OSPAR (2003) Joint Assessment and Monitoring Program. Guidelines for Contaminant-Specific Biological Effects Monitoring: Technical Annex 3 (TBT-Specific Biological Effects Monitoring). London: OSPAR Commission (SIME 03/3/8), 40 pp.Google Scholar
OSPAR (2004) Proposal for Assessment Criteria For TBT-Specific Biological Effects. London: OSPAR Commission (ASMO 04/3/3), 3 pp.Google Scholar
Pope, N (1998) The Bioavailability of Sediment-Bound Tributyltin (TBT) (PhD thesis). University of Plymouth, Plymouth, UK.Google Scholar
Rato, M, Ferreira, N, Santos, J and Barroso, C (2009 a) Temporal evolution of imposex in Nassarius reticulatus (L.) along the Portuguese coast: the efficacy of EC regulation 782/2003. Journal of Environmental Monitoring 11, 100107.CrossRefGoogle ScholarPubMed
Rato, M, Russel-Pinto, F and Barroso, C (2009 b) Assessment of digenean parasitism in Nassarius reticulatus (L.) along the Portuguese coast: evaluation of possible impacts on reproduction and imposex expression. Journal of Parasitology 95, 327336.CrossRefGoogle ScholarPubMed
Ruiz, JM, Barreiro, R and González, JJ (2005) Biomonitoring organotin pollution with gastropods and mussels. Marine Ecology Progress Series 287, 169176.CrossRefGoogle Scholar
Ruiz, JM, Albaina, N, Carro, B and Barreiro, R (2015) A combined whelk watch suggests repeated TBT desorption pulses. Science of the Total Environment 502, 167171.CrossRefGoogle ScholarPubMed
Ruiz, JM, Carro, B, Albaina, N, Couceiro, L, Quintela, M and Barreiro, R (2017) Bi-species imposex monitoring in Galicia (NW Spain) shows contrasting achievement of the OSPAR Ecological Quality Objective for TBT. Marine Pollution Bulletin 114, 715723.CrossRefGoogle ScholarPubMed
Ruiz, JM, Quintela, M and Barreiro, R (1998) Ubiquitous imposex and organotin bioaccumulation in gastropods Nucella lapillus (L.) from Galicia (NW Spain): a possible effect of nearshore shipping. Marine Ecology Progress Series 164, 237244.CrossRefGoogle Scholar
Schøyen, M, Green, NW, Hjermann, , Tveiten, L, Beylich, B, Øxnevad, S and Beyer, J (2019) Levels and trends of tributyltin (TBT) and imposex in dogwhelk (Nucella lapillus) along the Norwegian coastline from 1991 to 2017. Marine Environmental Research 144, 18.CrossRefGoogle ScholarPubMed
Shi, H, Huang, C, Zhu, S, Yu, X and Xie, WY (2005) Generalized system of imposex and reproductive failure in female gastropods of coastal waters of mainland China. Marine Ecology Progress Series 304, 179189.CrossRefGoogle Scholar
Smith, BS (1971) Sexuality in the American mud snail, Nassarius obsoletus Say. Proceedings of the Malacological Society of London 39, 377378.Google Scholar
Son, MH and Hughes, RN (2000) Sexual dimorphism of Nucella lapillus (Gastropoda: Muricidae) in North Wales, UK. Journal of Molluscan Studies 66, 489498.CrossRefGoogle Scholar
Stroben, E, Oehlmann, J and Fioroni, P (1992) The morphological expression of imposex in Hinia reticulata (Gastropoda: Buccinidae): a potential indicator of tributyltin pollution. Marine Biology 113, 625636.CrossRefGoogle Scholar
Tallmark, B (1980) Population dynamics of Nassarius reticulatus (Gastropoda: Prosobranchia) in Gullmar Fjord, Sweden. Marine Ecology Progress Series 3, 5162.CrossRefGoogle Scholar
Vasconcelos, P, Moura, P, Barroso, CM and Gaspar, MB (2011) Size matters: importance of penis length variation on reproduction studies and imposex monitoring in Bolinus brandaris (Gastropoda: Muricidae). Hydrobiologia 661, 363375.CrossRefGoogle Scholar
Wilson, JG, Minchin, D, McHugh, B, McGovern, E, Tanner, CJ and Giltrap, M (2015) Declines in TBT contamination in Irish coastal waters 1987–2011, using the dogwhelk (Nucella lapillus) as a biological indicator. Marine Pollution Bulletin 100, 289296.CrossRefGoogle Scholar
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