Abstract
The purpose of this work was to experimentally analyze the impact of copper, chromium and a commercial pesticide with endosulfan on the escape behavior of two copepods (Notodiaptomus conifer, Argyrodiaptomus falcifer) and three cladocerans (Daphnia magna, Pseudosida variabilis and Ceriodaphnia dubia). The experimental assays were carried out using a novel hydraulic devise designed to mimic three-speed predator capture behavior. Two concentrations, one “high” and one “low”, were employed and the exposure time was 15 (±5) minutes. With two exceptions, the species exposed to heavy metals manifested higher ability to escape than controls. Both concentrations of the pesticide reduced the escape ability of cladocerans but copepods responded, in general, in a similar manner as for heavy metals. The immediate apparent advantage of low and early toxic effects is discussed and the high sensitivity of the escape behavior suggests that it could be a complementary endpoint to be used in future ecotoxicological tests.
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Andersen HR, Wollenberger L, Halling-Sorensen B, Ole Kusk K (2001) Development of copepod nauplii to copepodites—a parameter for chronic toxicity including endocrine disruption. Environ Toxicol Chem 20:2821–2829
Barry MJ (1999) The effects of a pesticide on inducible phenotipic plasticity in Daphnia. Environ Pollut 104:217–224
Barry MJ, Logan DC (1998) The use of temporary pond microcosms for aquatic toxicity testing: direct and indirect effects of endosulfan on community structure. Aquat Toxicol 41:101–124
Baudo R (1987) Ecotoxicology testing with Daphnia. In: Peters RH, De Bernardi R (eds) Daphnia, a special edition of Memorie dell’Istituto Italiano di Idrobiologia. Pallanza, Italy, pp 461–482
Bhavan SP, Geraldine P (2001) Biochemical stress responses in tissues of the prawn Macrobrachium malcolmsonii on exposure to Endosulfan. Pest Biochem Physiol 70:27–41
Biesinger KE, Christensen GM (1972) Effects of various metals on survival, growth, reproduction, and metabolism of Daphnia magna. J Fish Res Board Can 29:1691–1700
Bossuyt BTA, Janssen CR (2005) Copper toxicity to different field-collected cladoceran species: intra- and inter-species sensitivity. Environ Pollut 136:145–154
Brown RJ, Rundle SD, Hutchinson TH, Williams TD, Jones MB (2002) A copepod life-cycle test and growth model for interpreting the effects of lindane. Aquat Toxicol 63:1–11
Buskey EJ (1984) Swimming pattern as an indicator of the roles of copepod sensory systems in the recognition of food. Mar Biol 79:165–175
Calabrese EJ, Baldwin LA, Holland CD (1999) Hormesis: a highly generalizable and reproducible phenomenon with important implications for risk assessment. Risk Anal 19:261–281
Cohen JH, Fordward RB (2005) Diel vertical migration of the marine copepod Calanopia americana. I. Twilight DVM and its relationship to the diel light cycle. Mar Biol 147:387–398
Collumb CJ, Buskey EJ (2004) Effects of the toxic red tide dinoflagellate (Karenia brevis) on survival, fecal pellet production and fecundity of the copepod Acartia tonsa. In: Steidinger KA, Landsberg JH, Tomas CR, Vargo GA (eds) Harmful algae 2002. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO
Dawidowicz P, Loose CJ (1992) Metabolic costs during predator-induced diel vertical migration of Daphnia. Limnol Oceanogr 37:1589–1595
DeLorenzo ME, Taylor LA, Lund SA, Pennington PL, Strozier ED, Fulton MH (2002) Toxicity and bioconcentration potential of the agricultural pesticide endosulfan in phytoplankton and zooplankton. Arch Environ Contam Toxicol 42:173–181
Dodson S, Hanazato T (1995) Commentary on effects of anthropogenic and natural organic chemicals on development, swimming behavior, and reproduction of Daphnia, a key member of aquatic ecosystems. Environ Health Persp 103:7–11
Dodson SI, Ryan S, Tollrian R, Lamper W (1997) Individual swimming behavior of Daphnia: effects of food, light and container size in four clones. J Plankton Res 19:1537–1552
Forbes VE (2000) Is hormesis an evolutionary expectation? Funct Ecol 14:12–24
Gagneten AM, Paggi JC (2009) Effects of heavy metal contamination (Cr, Cu, Pb, Cd) and eutrophication on zooplankton in the lower basin of the Salado river (Argentina). Water Air Soil Poll 198:317–334
Gagneten AM, Vila I (2001) Effects of Cu+2 and pH on the fitness of Ceriodaphnia dubia (Richard 1894) (Crustacea, Cladocera) in microcosm experiments. Environ Toxicol 16:428–438
Gagneten AM, Gervasio S, Paggi JC (2007) Heavy metal pollution and eutrophication in the lower Salado river basin (Argentina). Water Air Soil Poll 178:335–349
Gill CW, Crisp DJ (1985) Sensitivity of intact and antennule amputated copepods to water disturbance. Mar Ecol Prog Ser 21:221–227
Gliwicz ZM (1990) Why do cladocerans fail to control algal blooms? Hydrobiologia 200–201:83–97
Guerritsen J, Strickler JR (1997) Encounter probabilities and community structure in zooplankton: a mathematical model. Can J Fish Res Board 34:73–82
Hanazato T (1995) Combined effect of the insecticide carbaryl and the Chaoborus kairomone on helmet development in Daphnia ambigua. Hydrobiologia 310:95–100
Hanazato T (2001) Pesticide effects on freshwater zooplankton: an ecological perspective. Environ Poll 112:1–10
Hanazato T, Dodson SI (1993) Morphological responses of four species of cyclomorphic Daphnia to a short-term exposure to the insecticide carbaryl. J Plankton Res 14:1743–1755
Jergentz S, Pessacq P, Mugni H, Bonetto C, Schulz R (2004) Linking in situ bioassays and dinamics of macroinvertebrates to assess agricultural contamination in streams of the Argentine pampa. Ecotox Environ Safe 59:133–141
Kenaga E (1982) Predictability of chronic toxicity from acute toxicity of chemicals in fish and aquatic invertebrates. Environ Toxicol Chem 1:347–358
Koivisto S, Ketola M (1995) Effects of copper on life-history traits of Daphnia pulex and Bosmina longirostris. Aquat Toxicol 32:255–269
Kühn R, Pattard M, Pernak K, Winter A (1989) Results of the harmful effects of water pollutants to Daphnia magna in the 21 day reproduction test. Water Res 23:501–510
Lass S, Spaak P (2003) Chemically induced anti- predator defences in plankton: a review. Hydrobiologia 491:221–239
Lauder GV (1980) Hydrodinamic of prey capture by teleost fishes. Proceeding of the 2nd conference on biofluid mechanics, vol 2. Plenum Press, New York, pp 161–181
Liu XJ, Ni IH, Wang WX (2002) Trophic transfer of heavy metals from freshwater zooplankton Daphnia magna to zebrafish Danio reiro. Water Res 36:4563–4569
Lonsdale DJ, Frey MA, Snell TW (1998) The role of chemical signals in copepod reproduction. J Marine Syst 15:1–12
Lopes I, Donald JB, Riveiro R (2004) Avoidance of copper contamination by field population of Daphnia longispina. Environ Toxicol Chem 7:1702–1708
Maier G (1995) Mating frequency and interspecific matings in some freshwater cyclopoid copepods. Oecologia 101:245–250
Mc Kee MJ, Knowles CO (1986) Effects of fenvalerate on biochemical parameters, survival, and reproduction of Daphnia magna. Ecotox Environ Safe 12:70–84
McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. New York
National Hidric Resources Secretary (2003) Desarrollo de niveles guía nacionales de calidad de agua ambiente correspondiente a cromo. Argentina
National Hidric Resources Secretary (2005) Desarrollo de niveles guía nacionales de calidad de agua ambiente correspondiente a cobre. Argentina
Ohman MD (1988) Behavioral responses of zooplankton to predation. B Mar Sci 43:530–550
Pijanowska J, Dawidowicz P, Weider LJ (2006) Predator-induced escape response in Daphnia. Arch Hydrobiol 167:77–87
Preston BJ, Cecchine G, Snell TW (1999) Effects of pentachlorophenol on predator avoidance behavior of the rotifer Brachionus calyciflorus. Aquat Toxicol 44:201–212
Rinderhagen M, Ritterhoff J, Zauke GP (2000) Biomonitoring of polluted water—reviews on actual topics, vol. 9. Environmental research forum. Trans Tech Publications, Uetikon-Zuerich, pp 161–194
Rodgher S, Lombardi AT, Gama Mela MG, Tonietto AE (2008) Change in life cycle parameters and feeding rate of Ceriodaphnia silvestrii Daday (Crustacea, Cladocera) exposure to dietary copper. Ecotoxicology 17:826–833
Sharp AA, Stearns DE (1997) Sublethal effects of cupric ion activity on the grazing behaviour of three calanoid copepods. Mar Poll Bull 34:1041–1048
Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. WH Freeman and Co., New York
Standard Methods (2000) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association/American Water Works Association/Water Environment Federation, Washington, DC
Stearns SC (1992) The evolution of life histories. Oxford Univerisity Press, Oxford
Strickler RI, Bal A (1973) Setae of the first antennae of the copepod Cyclops scutifer (Sars): Their structure and importance. Proc Natl Acad Sci USA 70:2656–2659
Suedel BC, Deaver E, Rodgers JH (1996) Experimental factors that may affect toxicity of aqueous and sediment-bound copper to freshwater organisms. Arch Environ Contam Toxicol 30:40–46
Sullivan BK, Buskey E, Miller DC, Ritacco PJ (1983) Effects of copper and cadmium on growth, swimming and predator avoidance in Eurytemora affinis (Copepoda). Mar Biol 77:299–306
Szlauer L (1964) Reaction of Daphnia pulex de Geer to the approach of different objects. Polskie Arch Hydrobiologii 12:5–16
United States Environmental Protection Agency (1980) Ambient water quality criteria for endosulfan. EPA 440/5-80-046. Office of Water Regulations and Standards, Washington, DC
Vitasalo M, Kioerboe T, Flinkman J, Pedersen LW, Visser AW (1998) Predation vulnerability of planktonic copepods: consequences of predator foraging strategies and prey sensory abilities. Mar Ecol Prog Ser 175:129–142
Watras CJ, Back RC, Halvorsen S, Hudson RJM, Morrison KA, Wente SP (1998) Bioaccumulation of mercury in pelagic freshwater food webs. Sci Total Environ 219:183–208
Webb PW, Skadsen JM (1980) Strike tactics of Esox. Can J Zool 58:1462–1469
Winner RW, Farrell MP (1976) Acute and chronic toxicity of copper to four species of Daphnia. J Fish Res Board Can 33:1685–1691
Zauke GP, Schmalenbach I (2006) Heavy metals in zooplankton and decapod crustaceans from the Barents Sea. Sci Total Environ 359:283–294
Acknowledgments
We thank the anonymous reviewers for their constructive comments and important contributions. We are also grateful to Leonardo Paggi and Oscar Mendoza for their technical assistance. This research was supported with grants from the Universidad Nacional del Litoral, Santa Fe, Argentina (Project CAI+D 2009 No. PI 69-351).
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Gutierrez, M.F., Paggi, J.C. & Gagneten, A.M. Microcrustaceans escape behavior as an early bioindicator of copper, chromium and endosulfan toxicity. Ecotoxicology 21, 428–438 (2012). https://doi.org/10.1007/s10646-011-0803-1
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DOI: https://doi.org/10.1007/s10646-011-0803-1