Abstract
Since mudsnails are able to avoid contaminated sediment and that the contaminants in sediment are not uniformly distributed, the mudsnail Peringia ulvae was exposed to cadmium (Cd) spiked sediment and assessed for avoidance response in a heterogeneous contamination scenario. Four Cd concentrations were prepared and disposed in patches on dishes, which were divided in 25 fields (six fields for each sediment concentration); 24 organisms were deployed in the central field, with no sediment. Observations were made at 2, 4 and 6 h (corresponding to immediate response), 8, 10 and 12 h (very short term), and 24 h (short term). A trend to avoid contaminated patches was observed in the immediate and very short term. After 24 h exposure, the organisms exposed to the highest level of contamination seemed to have lost the ability to move and avoid contaminated patches. In a contamination scenario in which non- and contaminated sediment patches are heterogeneously distributed, local mudsnail populations can simply rearrange their locality without needing to move to a different habitat. Such less contaminated patches can become donor areas in a future recolonization scenario.
Similar content being viewed by others
References
Araújo CVM, Blasco J, Moreno-Garrido I (2012) Measuring the avoidance behaviour shown by the snail Hydrobia ulvae exposed to sediment with a known contamination gradient. Ecotoxicology 21:750–758
Araújo CVM, Blasco J, Moreno-Garrido I (2013) Motionless of snail Hydrobia ulvae (Pennant) as response to sediment toxicity and its consequences for the post-exposure feeding. Ecotoxicol Environ Contam 8:69–75
Araújo CVM, Moreira-Santos M, Sousa JP, Ochoa-Herrera V, Encalada AC, Ribeiro R (2014a) Active avoidance from crude oil soluble fraction by an Andean páramo copepod. Ecotoxicology 23:1254–1259
Araújo CVM, Shinn C, Moreira-Santos M, Lopes I, Espíndola ELG, Ribeiro R (2014b) Copper-driven avoidance and mortality in temperate and tropical tadpoles. Aquat Toxicol 146:70–75
Araújo CVM, Shinn C, Vasconcelos AM, Ribeiro R, Espíndola ELG (2014c) Preference and avoidance responses by tadpoles: the fungicide pyrimethanil as a habitat disturber. Ecotoxicology 23:851–860
Araújo CVM, Moreira-Santos M, Sousa JP, Ochoa-Herrera V, Encalada AC, Ribeiro R (2014d) Contaminants as habitat disturbers: PAH-driven drift by Andean paramo stream insects. Ecotoxicol Environ Saf 108:89–94
Araújo CVM, Moreira-Santos M, Patrício J, Martins I, Moreno-Garrido I, Blasco J, Marques JC, Ribeiro R (2015) Feeding niche preference of the snail Peringia ulvae. Mar Freshw Res 66:573–581
Balachandran KK, Lalu Raj CM, Nair M, Joseph T, Sheeba P, Venugopal P (2005) Heavy metal accumulation in a flow restrict, tropical estuary. Estuar Coast Shelf Sci 65:361–370
Barnes RSK, Greenwood JG (1978) The response of the intertidal gastropod Hydrobia ulvae (Pennant) to sediments of differing particle size. J Exp Mar Biol Ecol 31:43–54
Campana O, Rodríguez A, Blasco J (2013) Evaluating the suitability of Hydrobia ulvae as a test species for sediment metal toxicity testing applying a tissue residue approach to metal mixtures in laboratory and field exposures. Chemosphere 91:1136–1145
Cardoso PG, Lillebø AI, Pardal MA, Ferreira SM, Marques JC (2002) The effect of different primary producers on Hydrobia ulvae population dynamics: a case study in a temperature intertidal estuary. J Exp Mar Biol Ecol 277:173–195
Cardoso PG, Sousa E, Matos P, Henriques B, Pereira E, Duarte AC, Pardal MA (2013) Impact of mercury contamination on the population dynamics of Peringia ulvae (Gastropoda): implications on metal transfer through the trophic web. Estuar Coast Shelf Sci 129:189–197
Chakraborty P, Raghunadh Babu PV, Sarma VV (2012) A study of lead and cdmium speciation in some estuarine and coastal sediments. Chem Geol 294–295:217–225
Chakraborty S, Bhattacharya T, Singh G, Maity JP (2014) Benthic macroalgae as biological indicators of heavy metal pollution in the marine environments: a biomonitoring approach for pollution assessment. Ecotoxicol Environ Saf 100:61–68
Chapman PM, Wang F (2001) Assessing sediment contamination in estuaries. Environ Toxicol Chem 20:3–22
Costa FO, Correia AD, Costa MH (1998) Acute marine sediment toxicity: a potential new test with the amphipod Gammarus locusta. Ecotoxicol Environ Saf 40:81–87
Dallinger R, Höckner M (2013) Evolutionary concepts in ecotoxicology: tracing the genetic background of differential cadmium sensitivities in invertebrate lineages. Ecotoxicology 22:767–778
De Lange HJ, Sperber V, Peeters ETHM (2006) Avoidance of polycyclic aromatic hydrocarbon–contaminated sediments by the freshwater invertebrates Gammarus pulex and Asellus aquaticus. Environ Toxicol Chem 25:452–457
Dolbeth M, Cardoso PG, Ferreira SM, Verdelhos T, Raffaelli D, Pardal MA (2007) Anthropogenic and natural disturbance effects on a macrobenthic estuarine community over a 10-year period. Mar Pollut Bull 54:576–585
Elliott M, Quintino V (2007) The estuarine quality paradox, environmental homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Mar Pollut Bull 54:640–645
Forbes VE, Lopez GR (1986) Changes in feeding and crawling rates of Hydrobia truncata (Prosobranchia: Hydrobiidae) in response to sedimentary chlorophyll-a and recently egested sediment. Mar Ecol Prog Ser 33:287–294
García-Alonso J, Greenway GM, Munshi A, Gómez JC, Mazik K, Knight AW, Hardege JD, Elliott M (2011) Biological responses to contaminants in the Humber Estuary: disentangling complex relationships. Mar Environ Res 71:295e303
Gomes IDL, Lemos MFL, Soares AMVM, Díez S, Barata C, Faria M (2014) Effects of Barcelona harbor sediments in biological responses of the polychaete Capitella teleta. Sci Total Environ 485–486:545–553
Granberg ME, Forbes TL (2006) Role of sediment organic matter quality and feeding history in dietary absorption and accumulation of pyrene in the mud snail (Hydrobia ulvae). Environ Toxicol Chem 25:995–1006
Gutierrez MF, Paggi JC, Gagneten AM (2012) Microcrustaceans escape behavior as an early bioindicator of copper, chromium and endosulfan toxicity. Ecotoxicology 21:428–438
Hack LA, Tremblay LA, Wratten SD, Forrester G, Keesing V (2008) Toxicity of estuarine sediments using a full life-cycle bioassay with the marine copepod Robertsonia propinqua. Ecotoxicol Environ Saf 70:469–474
Hampel M, Moreno-Garrido I, González-Mazo E, Blasco J (2009) Suitability of the marine prosobranch snail Hydrobia ulvae for sediment toxicity assessment: a case study with the anionic surfactant linear alkylbenzene sulphonate (LAS). Ecotoxicol Environ Saf 72:1303–1308
Hansen JA, Woodward DF, Little EE, DeLonay AJ, Bergman HL (1999) Behavioral avoidance: possible mechanism for explaining abundance and distribution of trout species in a metal-impacted river. Environ Toxicol Chem 18:313–317
Holmes CW, Slade EA, McLerran CJ (1974) Migration and redistribution of zinc and cadmium in marine estuarine systems. Environ Sci Technol 8:255–259
Hutchins CM, Teasdale PR, Lee SY, Simpson SL (2009) The effect of sediment type and pH-adjustment on the porewater chemistry of copper- and zinc-spiked sediments. Soil Sedim Contam 18:55–73
Keilty TJ, White DS, Landrum PF (1988) Short-term lethality and sediment avoidance assays with endrin-contaminated sediment and two oligochaetes from Lake Michigan. Arch Environ Contam Toxicol 17:95–101
Kravitz MJ, Lamberson JO, Ferraro SP, Swartz RC, Boese BL, Specht DT (1999) Avoidance response of the estuarine amphipod Eohaustorius estuarius to polycyclic aromatic hydrocarbon-contaminated, field-collected sediments. Environ Toxicol Chem 18:1232–1235
Krell B, Mreira-Santos M, Ribeiro R (2011) An estuarine mudsnail in situ toxicity assay based on postexposure feeding. Environ Toxicol Chem 30:1935–1942
Lefcort H, Abbott DP, Cleary DA, Howell D, Keller NC, Smith MM (2004) Aquatic snails from mining sites have evolved to detect and avoid heavy metals. Arch Environ Contam Toxicol 46:478–484
Leung KMY, Morley NJ, Grist EPM, Morritt D, Crane M (2004) Chronic toxicity of tributyltin on development and reproduction of the hermaphroditic snail Physa fontinalis: influence of population density. Mar Environ Res 58:157–162
Lillebø AI, Pardal MA, Marques JC (1999) Population structure, dynamics and production of Hydrobia ulvae (Pennant) (Mollusca: Prosobranchia) along an eutrophication gradient in the Mondego estuary (Portugal). Acta Oecol 20:289–304
Lopes I, Baird DJ, Ribeiro R (2004) Avoidance of copper contamination by field populations of Daphnia longispina. Environ Toxicol Chem 23:1702–1708
Luoma SN (1996) The developing framework of marine ecotoxicology: pollutants as a variable in marine ecosystems? J Exp Mar Biol Ecol 200:29–55
Macken A, Giltrap M, Foley B, McGovern E, McHugh B, Davoren M (2008) A model compound study: the ecotoxicological evaluation of five organic contaminants employing a battery of marine bioassays. Environ Pollut 153:627–637
Marklevitz SAC, Almeida E, Flemming J, Hellou J (2008) Determining the bioavailability of contaminants and assessing the quality of sediments. Part 1: variables affecting the behavioural response of Ilyanassa obsoleta towards contaminated sediments. J Soils Sedim 8:86–91
Martinez-Haro M, Taggart MA, Mateo R (2010) Pb-Al relationships in waterfowl feces discriminate between sources of Pb exposure. Environ Pollut 158:2485–2489
Martinez-Haro M, Moreira-Santos M, Marques JC, Ribeiro R (2014) A short-term laboratory and in situ sediment assay based on the postexposure feeding of the estuarine isopod Cyathura carinata. Environ Res 134:242–250
Maufrett A, Rico-Rico A, Temara A, Blasco J (2010) Exposure of the marine deposit feeder Hydrobia ulvae to sediment-associated LAS. Environ Pollut 158:529–535
Maurer BA, Holt ED (1996) Effects of chronic pesticide stress on wildlife populations in complex landscape: processes al multiple scales. Environ Toxicol Chem 15:420–426
Mil-Homens M, Vale C, Raimundo J, Pereira P, Brito P, Caetano M (2014) Major factors influencing the elemental composition of surface estuarine sediments: the case of 15 estuaries in Portugal. Mar Pollut Bull 84:135–146
Moe SJ, De Schamphelaere K, Clements WH, Sorensen MT, Van den Brink PJ, Liess M (2013) Combined and interactive effects of global climate change and toxicants on populations and communities. Environ Toxicol Chem 32:49–61
Moreira-Santos M, Donato C, Lopes I, Ribeiro R (2008) Avoidance tests with small fish: determination of themedian avoidance concentration and of the lowest-observed-effect gradient. Environ Toxicol Chem 27:1575–1582
Pereira P, Vale C, Ferreira AM, Pereira E, Pardal MA, Marques JC (2005) Seasonal variation of surface sediments composition in Mondego River estuary. J Environ Sci Health A Tox Hazard Subst Environ Eng 40:317–329
Rosa R, Materatski P, Moreira-Santos M, Sousa JP, Ribeiro R (2012) A scaled-up system to evaluate zooplankton spatial avoidance and population immediate decline concentration. Environ Toxicol Chem 31:1301–1305
Sakuma M (1998) Probit analysis of preference data. Appl Entomol Zool 33:339–347
Serafim A, Company R, Lopes B, Pereira C, Cravo A, Fonseca VF, França F, Bebianno MJ, Cabral HN (2013) Evaluation of sediment toxicity in different Portuguese estuaries: ecological impact of metals and polycyclic aromatic hydrocarbons. Estuar Coast Shelf Sci 130:30–41
Shipp EY, Grant A (2006) Hydrobia ulvae feeding rates: a novel way to assess sediment toxicity. Environ Toxicol Chem 25:3246–3252
Spromberg JA, John BM, Landis WG (1998) Metapopulation dynamics: indirect effects and multiple distinct outcomes in ecological risk assessment. Environ Toxicol Chem 17:1640–1649
Stringer TJ, Glover CN, Keesing V, Northcott GL, Gaw S, Tremblay LA (2014) Development of acute and chronic sediment bioassays with the harpacticoid copepod Quinquelaophonte sp. Ecotoxicolo Environ Saf 99:82–91
USEPA (1994) Assessment and Remediation of Contaminated Sediments (ARCS) Program. Assessment Guidance Document. US Environmental Protection Agency. ARCS Assessment Guidance Document, EPA 905-B94-002, Chicago, Great Lakes National Program Office
Ward DJ, Simpson SL, Jolley DF (2013) Avoidance of contaminated sediments by an amphipod (Melita plumulosa), a harpacticoid copepod (Nitocra spinipes), and a snail (Phallomedusa solida). Environ Toxicol Chem 32:647–652
West CW, Ankley GT (1998) A laboratory assay to assess avoidance of contaminated sediments by the freshwater oligochaete Lumbriculus variegatus. Arch Environ Contam Toxicol 35:20–24
White DS, Kielty TJ (1988) Burrowing avoidance assays of contaminated Detroit River sediments, using the freshwater oligochaete Stylodrilus heringianus (Lumbriculidae). Arch Environ Contam Toxicol 17:673–681
Acknowledgments
CVM Araújo is grateful to FCT (Fundação para a Ciência e a Tecnologia, Portugal) for postdoctoral fellowships and SENESCYT (Secretaría Nacional de Educación Superior, Ciencia, Tecnología e Innovación, Ecuador) (reference SFRH/BPD/74044/2010 and PROMETEO program, respectively). This research was partially funded by the 7th Framework Programme (FP7 2007-2013) of the European Commission, through a Marie Curie Intra-European Fellowship for Career Development (PIEF-GA-2011-299747) awarded to M. Martinez-Haro. Currently, M. Martinez-Haro benefits from a postdoctoral contract with the Junta de Comunidades de Castilla-La Mancha and the European Social Fund (Operational Programme FSE 2007/2013; POST 2014/7780). AJ Pais-Costa is grateful to FCT for PhD fellowship. The authors are grateful to Jon Nesbit for his revision of the English text.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Araújo, C.V.M., Martinez-Haro, M., Pais-Costa, A.J. et al. Patchy sediment contamination scenario and the habitat selection by an estuarine mudsnail. Ecotoxicology 25, 412–418 (2016). https://doi.org/10.1007/s10646-015-1599-1
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-015-1599-1