Abstract
This study tested the hypothesis that the snail Hydrobia ulvae will recognise differences in the contamination levels of sediment and avoid the more contaminated zones. Instead of testing avoidance behaviour in a two-compartment system, a linear contamination gradient has been devised in which several zones containing sediment with different contamination levels could be “chosen”. A sediment of known severe contamination was collected and mixed with a non-toxic sediment to comprise a linear gradient with four concentrations of 0, 30, 60 and 100% contamination. Thus, the individuals were free to move between fields of different concentration (unforced conditions). During 24 h of exposure, the distribution of the organisms on fields was recorded and organisms’ percentage that avoided each field was calculated for each concentration. At 30 and 60% of contamination, avoidance was around 50% for all periods of exposure. Avoidance at 100% contamination ranged between 11 and 56% (rates lower than expected). Organisms that did not avoid the 100% contamination revealed that they were inactive, indicating either that non-mobility and retraction within their shell may be alternative defence strategies, or else the high contamination may have impaired their ability to escape. The percentage of preference shown to the uncontaminated sediment ranged between 64 and 74%. The initial hypothesis was supported: H. ulvae avoids the more contaminated sediment. The assay proposed has been shown to be simple, rapid and effective; in addition, it is considered ecologically useful since the effects resulting from the avoidance are similar to the extinction of the population.
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Aldaya MM, Lors C, Salmon S, Ponge J-F (2006) Avoidance bio-assays may help to test the ecological significance of soil pollution. Environ Pollut 140:173–180
Alonso A, De Lange HJ, Peeters ETHM (2009) Development of a feeding behavioural bioassay using the freshwater amphipod Gammarus pulex and the multispecies freshwater biomonitor. Chemosphere 75:341–346
Araújo CVM, Diz FR, Laíz I, Lubián LM, Blasco J, Moreno-Garrido I (2009) Sediment integrative assessment of the bay of Cádiz (Spain): an ecotoxicological and chemical approach. Environ Int 35:831–841
Araújo CVM, Diz FR, Tornero V, Lubián LM, Blasco J, Moreno-Garrido I (2010) Ranking sediment samples from three Spanish estuaries in relation to its toxicity for two benthic species: the microalga Cylindrotheca closterium and the copepod Tisbe battagliai. Environ Toxicol Chem 29:393–400
ASTM-American Standard for Testing and Materials (1975) Standard specification for substitute ocean water. Designation D 1141-75
Barnes RSK (1990) Reproductive strategies in contrasting populations of the coastal gastropod Hydrobia ulvae. II. Longevity and life-time egg production. J Exp Mar Biol Ecol 138:183–200
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
Boldina-Cosqueric I, Amiard J-C, Amiard-Triquet C, Dedourge-Geffard O, Métais I, Mouneyrac C, Moutel B, Berthet B (2010) Biochemical, physiological and behavioural markers in the endobenthic bivalve Scrobicularia plana as tools for the assessment of estuarine sediment quality. Ecotoxicol Environ Saf 73:1733–1741
Cairns J Jr (1992) The threshold problem in ecotoxicology. Ecotoxicology 1:3–16
Campana O (2006) Evaluación de la contaminación de metales en los sedimentos del estuario del Río Guadalete. PhD Thesis, University of Cádiz
Cardoso PG, Raffaelli D, Pardal MA (2008a) The impact of extreme weather events on the seagrass Zostera noltii and related Hydrobia ulvae population. Mar Pollut Bull 56:483–492
Cardoso PG, Raffaelli D, Lillebø AI, Verdelhos T, Pardal MA (2008b) The impact of extreme flooding events and anthropogenic stressors on the macrobenthic communities’ dynamics. Estuar Coast Shelf Sci 76:553–565
Chandrasekara WU, Frid CLJ (1998) A laboratory assessment of the survival and vertical movement of two epibenthic gastropod species, Hydrobia ulvae (Pennant) and Littorina littorea (Linaeus), after burial in sediment. J Exp Mar Biol Ecol 221:191–207
Chapman PM, Wang F (2001) Assessing sediment contamination in estuaries. Environ Toxicol Chem 20:3–22
De Silva PMCS, van Gestel CAM (2009) Comparative sensitivity of Eisenia andrei and Perionyx excavatus in earthworm avoidance tests using two soil types in the tropics. Chemosphere 77:1609–1613
Diz FR, Araújo CVM, Moreno-Garrido I, Hampel M, Blasco J (2009) Short-term toxicity tests on the harpacticoid copepod Tisbe battagliai: lethal and reproductive endpoints. Ecotoxicol Environ Saf 72:1881–1886
Drake P, Arias A (1995) Distribution and production of three Hydrobia species (Gastropoda: Hydrobiidae) in a shallow coastal lagoon in the Bay of Cádiz, Spain. J Moll Stud 61:185–196
El-Rayis OA (1985) Re-assessment of the titration method for determination of organic carbon in recent sediments. Rapport Commission Int Mer Méditerraneé 29:45–47
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
Forbes VE, Lopez GR (1989) The role of sediment particle size in the nutritional energetics of a surface deposit-feeder. I. Ingestion and absorption of sedimentary microalgae by Hydrobia truncata (Vanatta). Mar Ecol Prog Ser 126:181–192
Gaudette HE, Flight WR, Toner L, Folger D (1974) An inexpensive titration method for the determination of organic carbon in recent sediments. J Sediment Petrol 44:249–253
Grudemo J, Bohlin T (2000) Effects of sediment type and intra- and interspecific competition on growth rate of the marine snails Hydrobia ulvae and Hydrobia ventrosa. J Exp Mar Biol Ecol 253:115–127
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 mechanisms for explaining abundance and distribution of trout species in a metal impacted river. Environ Toxicol Chem 18:313–317
Haubois A-G, Guarini J-M, Richard P, Fichet D, Radenac G, Blanchard GF (2005) Ingestion rate of the deposit-feeder Hydrobia ulvae (Gastropoda) on epipelic diatoms: affect of cell size and algal biomass. J Exp Mar Biol Ecol 317:1–12
Hellou J (2011) Behavioural ecotoxicology, an “early warning” signal to assess environmental quality. Environ Sci Pollut Res 18:1–11
Hellou J, Cook A, Lalonde B, Walker P, Dunphy K, MacLeod S (2009) Escape and survival of Corophium volutator and Ilyanassa obsoleta exposed to freshwater and chlorotalonyl. J Environ Sci Health 44:778–790
Kobetičová K, Hofman J, Holoubek I (2010) Ecotoxicity of wastes in avoidance tests with Enchytraeus albidus, Enchytraeus crypticus and Eisenia fetida (Oligochaeta). Waste Manage 30:558–564
Kravitz MJ, Lamberson JO, Ferraro SP, Swartz RC, Boese BL, Specht DT (1999) Avoidance response of the estuarine amphipod Eohaustorius estuarius polycyclic aromatic hydrocarbon-contaminated, field collected sediments. Environ Toxicol Chem 18:1232–1235
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 Oecologica 20:289–304
Lopes I, Baird DJ, Ribeiro R (2004) Avoidance of copper contamination by Field population of Daphnia longispina. Environ Toxicol Chem 23:1702–1708
Lopez GR, Cheng I-J (1983) Synoptic measurements of ingestion rate, ingestion selectivity, and absorption efficiency of natural foods in the deposit-feeding molluscs Nucula annulata (Bivalvia) and Hydrobia totteni (Gastropoda). Mar Ecol Prog Ser 11:55–62
Loring DH, Rantala RTT (1992) Manual for the geochemical analyses of marine sediments and suspended particulate matter. Earth Sci Rev 32:235–283
Loureiro S, Amorim MJB, Campos B, Rodrigues SMG, Soares AMVM (2009) Assessing joint toxicity of chemicals in Enchytraeus albidus (Enchytraeidae) and Porcellionides pruinosus (Isopoda) using avoidance behaviour as an endpoint. Environ Pollut 157:625–636
Marklevitz SAC, Almeida E, Flemming J, Hellou J (2008a) 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 Sediments 8:86–91
Marklevitz SAC, Almeida E, Flemming J, Hellou J (2008b) Determining the bioavailability of contaminants and assessing the quality of sediments. Part 2: behavioural response of snails, Ilyanassa obsoleta, towards contaminated harbour sediments. J Soils Sediments 8:92–97
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
Moreira-Santos M, Donato C, Lopes I, Ribeiro R (2008) Avoidance tests with small fish: determination of the median avoidance concentration and of the lowest-observed-effect gradient. Environ Toxicol Chem 27:1576–1582
Novais SC, Soares AMVM, Amorim MJB (2010) Can avoidance of Enchytraeus albidis be used as screening parameter for pesticide testing? Chemosphere 79:233–237
Orvain F, Sauriau P-G (2002) Environmental and behavioural factors affecting activity in the intertidal gastropod Hydrobia ulvae. J Exp Mar Biol Ecol 272:191–216
Owojori OJ, Reinecke AJ (2009) Avoidance behaviour of two eco-physiologically different earthworms (Eisenia fetida and Aporrectodea caliginosa) in natural and artificial saline soils. Chemosphere 75:279–283
Pascual E, Drake P (2008) Physiological and behavioural responses of the mud snails Hydrobia glyca and Hydrobia ulvae to extreme water temperature and salinities: implications for their spatial distribution within a system of temperate lagoons. Physiol Biochem Zool 81:594–604
Sanz-Lázaro C, Martín A (2009) A manipulative field experiment to evaluate an integrative methodology for assessing sediment pollution in estuarine ecosystems. Sci Total Environ 407:3510–3517
Shipp E, Grant A (2006) Hydrobia ulvae feeding rates: a novel way to assess sediment toxicity. Environ Toxicol Chem 25:3246–3252
Sola JC (1996) Population dynamics, reproduction, growth, and secondary production of the mud-snail Hydrobia ulvae (Pennant). J Exp Mar Biol Ecol 205:49–62
Svecevičius G (2001) Avoidance response of rainbow trout Oncorhynchus mykiss to heavy metal model mixtures: a comparison with acute toxicity tests. Bull Environ Contam Toxicol 67:680–687
Wiklund AKE, Börjesson T, Wiklund SJ (2006) Avoidance response of sediment living amphipods to zinc pyrithione as a measure of sediment toxicity. Mar Pollut Bull 52:96–99
Acknowledgments
This work was partially funded by the Spanish Ministry of Science and Innovation (projects PHYTOBIOMARK: CTM2009-10563/MAR, RNM306 of the Plan Andaluz de Investigación) and 0042_RISE_5_E funded by POCTEP 2007-2013. C.V.M. Araújo is grateful to FCT (Fundação para a Ciência e a Tecnologia—Portugal) for a postdoctoral grant (SFRH/BPD/74044/2010). The authors also thank Araceli Rodríguez, José María Espigares, María del Carmen Agulló Cornejo, Pilar Drake, and especially Lourdes Bordonado, for their contributions and support.
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Araújo, C.V.M., Blasco, J. & Moreno-Garrido, I. Measuring the avoidance behaviour shown by the snail Hydrobia ulvae exposed to sediment with a known contamination gradient. Ecotoxicology 21, 750–758 (2012). https://doi.org/10.1007/s10646-011-0835-6
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DOI: https://doi.org/10.1007/s10646-011-0835-6