Abstract
Imposex is a phenomenon widely associated with environmental exposure to organotin compounds which were quite common components of antifouling paints applied on boats and ship hulls. Here we study the incidence of imposex in neogastropods and its relation with water quality and maritime traffic in the coastal strip of Santa Marta, Colombia. Imposex was determined via specialized indexes and related to the organisms’ size, somatic conditions, variables of water quality and maritime traffic, in a space–time assessment. There was evidence of imposex in five species Plicopurpura patula, Vasula deltoidea, Stramonita haemastoma, S. floridana, and Gemophos auritulus. Purpura patula and Vasula deltoidea species were found in all sampling sites. The results have proved that imposex is highly influenced by the maritime traffic variable, with greater prevalence during the dry season, and with P. patula being more sensitive than V. deltoidea.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Batista-Andrade JA, Caldas SS, Batista RM, Castro IB, Fillmann G, Primel EG (2018) From TBT to booster biocides: levels and impacts of antifouling along coastal areas of Panama. Environ Pollut. https://doi.org/10.1016/j.envpol.2017.11.063
Bayraktarov E, Pizarro V, Wild C (2014) Spatial and temporal variability of water quality in the coral reefs of Tayrona National Natural Park, Colombian Caribbean. Environ Environ Monit Assess. https://doi.org/10.1007/s10661-014-3647-3
Brio FD, Commendatore M, Castro IB, Costa PG, Fillmann G, Bigatti G (2016) Distribution and bioaccumulation of butyltins in the edible gastropod Odontocymbiola magellanica. Mar Biol Res. https://doi.org/10.1080/17451000.2016.1169296
Castro ÍB (2019) Improper environmental sampling design bias assessments of coastal contamination. Trends Environ Anal Chem. https://doi.org/10.1016/j.teac.2019.e00068
Castro ÍB, Fillmann G (2012) High tributyltin and imposex levels in the commercial muricid Thais chocolata from two Peruvian harbor areas. Environ Toxicol Chem. https://doi.org/10.1002/etc.1794
Castro ÍB, Perina FC, Fillmann G (2012) Organotin contamination in South American coastal areas. Environ Monit Assess. https://doi.org/10.1007/s10661-011-2078-7
Castro ÍB, Iannacone J, Santos S, Fillmann G (2018) TBT is still a matter of concern in Peru. Chemosphere. https://doi.org/10.1016/j.chemosphere.2018.04.097
CIOH (2012) Guía Náutica Turística de Colombia. Centro de Investigaciones Oceanográficas e Hidrográficas del Caribe, Cartagena
Crowe TP, Thompson RC, Bray S, Hawkins SJ (2000) Impacts of anthropogenic stress on rocky intertidal communities. J Aquat Ecosyst Stress Recovery 7:273–297
Davies RB (1987) Hypothesis testing when a nuisance parameter is present only under the alternative. Biometrika. https://doi.org/10.1093/biomet/74.1.33
DIMAR (2018) Dirección General Marítima de Colombia. Radicado No. MD-DIMAR-SUBMERC-ATRANC en relación a la entrega de información
Dobson S, Cabridenc R (1990) Tributyltin Compounds. U.N.E Programme, New York
Dudley N (2008) Guidelines for applying protected area management categories. IUCN, Gland
El Ayari T, El Menif NT (2019) First record of imposex in Euthria cornea (Neogastropoda: Buccinidae) collected from the complex lagoon-channel of Bizerta. Thalass Int J Mar Sci. https://doi.org/10.1007/s41208-018-0089-7
El Ayari T, Abidli S, Lahbib Y, González PR, García JI, Trigui-El Menif N (2015) The effect of size and epibiotic barnacles on imposex in Stramonita haemastoma collected from the northern coast of Tunisia. Mar Biol Res. https://doi.org/10.1080/17451000.2014.914223
Elith J, Leathwick J (2017) Boosted Regression Trees for ecological modeling. R Doc
Fernández MA, de Wagener ALR, Limaverde AM, Scofield AL, Pinheiro FM, 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. https://doi.org/10.1016/j.marenvres.2004.07.001
GANP (2020) Global Alliance of National Parks. Obtenido de Tayrona National Park. Available at https://national-parks.org/colombia/tayrona. Accessed on 4 Mar 2020
Gibbs PE, Bryan GW, Pascoe PL, Burt GR (1987) The use of the dog-whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. J Mar Biol Assoc U K. https://doi.org/10.1017/s0025315400027260
Guisande C, Lise AV, Felpeto AB (2013) Tratamiento de datos con R, Statistica y SPSS. Ediciones Díaz de Santos, Madrid
Hernández S, Stotz WB (2004) Reproductive biology of the “Copey” snail Melongena melongena (Linnaeus, 1758) in Cispata Bay on the Caribbean coast of Colombia. J Shellfish Res 23:849–855
Horiguchi T, Kojima M, Hamada F, Kajikawa A, Shiraishi H, Morita M, Shimizu M (2006) Impact of tributyltin and triphenyltin on ivory shell (Babylonia japonica) populations. Environ Health Perspect. https://doi.org/10.1289/ehp.8047
IDEAM (2020) Instituto de Hidrología, Meteorología y Estudios Ambientales. Available at https://www.ideam.gov.co/web/tiempo-y-clima/clima. Accessed on 3 Mar 2020
INVEMAR-GEO (2015) Variabilidad oceanográfica y climática en la bahía de Santa Marta, ensenada de Gaira y zona de puertos (Caribe colombiano) y su relación con la dinámica sedimentaria del carbón. Actividad GEO—BPIN INVEMAR, Santa Marta
Jenner MG (1979) Pseudohermaphroditism in Ilyanassa obsoleta (Mollusca: Neogastropoda). Science. https://doi.org/10.1126/science.472758
Jones MRL, Ross PM (2018) Recovery of the New Zealand muricid dogwhelk Haustrum scobina from TBT-induced imposex. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2017.11.034
Laranjeiro F, Sánchez-Marín P, Oliveira IB, Galante-Oliveira S, Barroso C (2018) Fifteen years of imposex and tributyltin pollution monitoring along the Portuguese coast. Environ Pollut. https://doi.org/10.1016/j.envpol.2017.09.056
Lima AFA, Castro ÍB, Rocha-Barreira C (2006) Imposex induction in Stramonita haemastoma floridana (Conrad, 1837) (Mollusca: Gastropoda: Muricidae) submitted to an organotin-contaminated diet. Braz J Oceanogr. https://doi.org/10.1590/s1679-87592006000100008
Márquez F, Gonzalez R, Bigatti G (2011) Combined methods to detect pollution effects on shell shape and structure in Neogastropods. Ecol Ind. https://doi.org/10.1016/j.ecolind.2010.05.001
Mattos Y, Stotz WB, Romero MS, Bravo M, Fillmann G, Castro ÍB (2017) Butyltin contamination in Northern Chilean coast: is there a potential risk for consumers? Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2017.03.264
McClanahan TR (1992) Epibenthic gastropods of the Middle Florida Keys: the role of habitat and environmental stress on assemblage composition. J Exp Mar Biol Ecol. https://doi.org/10.1016/0022-0981(92)90236-4
Miloslavich P, Penchaszadeh PE, Bigatti G (2007) Imposex en gastrópodos de Venezuela. Cienc Mar 33:319–324
Morabito R, Sonak S, Bhosle N, Chaudhury R, Gipperth L, Veld G, Mukherjee A (2009) TBT IMPACTS: towards improved management of organotin compounds. T. T. E. a. R. Institute, European Commission, Brussels
Otegui MB, Zamprogno GC, França MA, Daros BN, Albino J, Costa MB (2019) Imposex response in shell sizes of intertidal snails in multiple environments. J Sea Res. https://doi.org/10.1016/j.seares.2019.02.003
Paz-Villarraga CA, Castro ÍB, Miloslavich P, Fillmann G (2015) Venezuelan Caribbean Sea under the threat of TBT. Chemosphere. https://doi.org/10.1016/j.chemosphere.2014.07.068
Peralta AC, Miloslavich P, Bigatti G (2014) Imposex in Voluta musica (Caenogastropoda: Volutidae) from Northeastern Península de Araya. Venezuela Rev Biol Trop 62:523–532
Radke B, Staniszewska M, Wasik A, Namieśnik J, Bolałek J (2008) Organotin compounds in marine sediments. Pol J Environ Stud 17:643–654
Ramón M, Amor MJ (2002) Reproductive cycle of Bolinus brandaris and penis and genital duct size variations in a population affected by imposex. J Mar Biol Assoc UK. https://doi.org/10.1017/s0025315402005696
Rico JP (2017) Variación en la forma y estructura de la concha de neogastrópodos del Caribe colombiano, asociada al fenómeno de imposex (Tesis para optar por el grado de Maestría). Universidad Nacional de Colombia-Sede Caribe, Santa Marta
Rodríguez-Grimón RO, Arroyo MF, de Freitas DM, Castro ÍB (2016) Tributyltin impacts in Galapagos Islands and Ecuadorian shore: marine protected areas under threat. Mar Policy. https://doi.org/10.1016/j.marpol.2016.03.017
Rossato M, Costa MB, Castro ÍB, Pinho GLL (2019) Size, season and origin of gastropods matter in imposex assessments. Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2018.05.013
Ruiz JM, Carro B, Albaina N, Barreiro R, Rial D, Bellas J (2018) Extended imposex monitoring in N Atlantic Spain confirms punctual attainment of European environmental objectives for TBT. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2017.11.048
Schøyen M, Green NW, Hjermann DØ, Tveiten L, Beylich B, Øxnevad S, Beyer J (2019) Levels and trends of tributyltin (TBT) and imposex in dogwhelk (Nucella lapillus) along the Norwegian coastline from 1991 to 2017. Mar Environ Res. https://doi.org/10.1016/j.marenvres.2018.11.011
Sierra-Marquez L, Sierra-Marquez J, De la Rosa J, Olivero-Verbel J (2018) Imposex in Stramonita haemastoma from coastal sites of Cartagena, Colombia. Braz J Biol. https://doi.org/10.1590/1519-6984.173301
Strand J, Jørgensen A, Tairova Z (2009) TBT pollution and effects in molluscs at US Virgin Islands Caribbean Sea. Environ Int. https://doi.org/10.1016/j.envint.2009.01.007
Susan P (2004) Análisis de datos biométricos del molusco Purpura patula (Lineo, 1758) de la playa rocosa de Boca Andrea, Ver. (Especialización). Universidad Veracruzana, Xalapa
Titley-O’Neal CP, Munkittrick KR, MacDonald BA (2011) The effects of organotin on female gastropods. J Environ Monit. https://doi.org/10.1039/c1em10011d
Vasconcelos P, Moura P, Barroso CM, Gaspar MB (2011) Size matters: importance of penis length variation on reproduction studies and imposex monitoring in Bolinus brandaris (Gastropoda: Muricidae). Hydrobiologia. https://doi.org/10.1007/s10750-010-0544-9
Wang X, Kong L, Cheng J, Zhao D, Chen H, Sun R, Yang W, Han J (2019) Distribution of butyltins at dredged material dumping sites around the coast of China and the potential ecological risk. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2018.11.043
Acknowledgements
This research was finantially supported by Universidad Nacional de Colombia-Sede Caribe (Cód. HERMES 2747) and (Cód. HERMES 32267), and was developed with the permission of Universidad Nacional de Colombia and Parques Nacionales Naturales de Colombia, for the collection of biological samples. The authors express their sincere gratitude to the anonymous reviewers for fruitful and constructive comments to enhance this work´s quality.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Rodríguez-Grimon, R., Campos, N.H. & Castro, Í.B. Imposex Incidence in Gastropod Species from Santa Marta Coastal Zone, Colombian Caribbean Sea. Bull Environ Contam Toxicol 105, 728–735 (2020). https://doi.org/10.1007/s00128-020-03020-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00128-020-03020-7