Fear and loathing in the benthos: Responses of aquatic insect larvae to the pesticide imidacloprid in the presence of chemical signals of predation risk

Aquatic Toxicology

Volumn 93, Issue 2-3, 2009, Pages 138-149

  Pestana, João L T ^a,b   Loureiro, Susana ^a   Baird, Donald J ^b   Soares, Amadeu M V M ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b UNIVERSITY OF NEW BRUNSWICK   (Canada)

Author keywords

Chironomus riparius; Insecticide; Multiple stressors; Predator prey interactions; Salmo trutta; Sericostoma vittatum

Indexed keywords

IMIDACLOPRID;

BEHAVIORAL RESPONSE; BENTHOS; BURROWING ORGANISM; CONCENTRATION (COMPOSITION); DOSE-RESPONSE RELATIONSHIP; EXPERIMENTAL STUDY; FEEDING; LARVA; NUMERICAL MODEL; PESTICIDE; PREDATION RISK; PREDATOR-PREY INTERACTION; RESPIRATION; SUBLETHAL EFFECT; VARIANCE ANALYSIS;

ARTICLE; BENTHOS; CHIRONOMUS RIPARIUS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; INSECT; LARVA; MICROBIAL GROWTH; MICROBIAL RESPIRATION; NONHUMAN; PREDATION; PRIORITY JOURNAL; RISK ASSESSMENT; SERICOSTOMA VITTATUM; WATER POLLUTANT;

ANIMALS; BEHAVIOR, ANIMAL; CHIRONOMIDAE; FOOD CHAIN; FRESH WATER; IMIDAZOLES; INSECTICIDES; INSECTS; LARVA; MODELS, BIOLOGICAL; NITRO COMPOUNDS; PREDATORY BEHAVIOR; RISK FACTORS; STRESS, PHYSIOLOGICAL; TROUT; WATER POLLUTANTS, CHEMICAL;

CHIRONOMIDAE; CHIRONOMUS RIPARIUS; HEXAPODA; SALMO TRUTTA; SALMONIDAE; SERICOSTOMA VITTATUM; TRICHOPTERA;

EID: 67349276676     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2009.04.008     Document Type: Article

References (72)

1. Abrams P.A., and Rowe L. The effects of predation on the age and size of maturity of prey. Evolution 50 (1996) 1052-1061
2. Alexander A.C., Culp J.M., Liber K., and Cessna A.J. Effects of insecticide exposure on feeding inhibition in mayflies and oligochaetes. Environmental Toxicology and Chemistry 26 (2007) 1726-1732
3. Alexander A.C., Heard K.S., and Culp J.M. Emergent body size of mayfly survivors. Freshwater Biology 53 (2008) 171-180
4. Backhaus T., Arrhenius A., and Blanck H. Toxicity of a mixture of dissimilarly acting substances to natural algal communities: Predictive power and limitations of independent action and concentration addition. Environmental Science & Technology 38 (2004) 6363-6370
5. Ball S.L., and Baker R.L. Predator-induced life history changes: Antipredator behavior costs or facultative life history shifts?. Ecology 77 (1996) 1116-1124
6. Barata C., and Baird D.J. Determining the ecotoxicological mode of action of chemicals from measurements made on individuals: results from instar-based tests with Daphnia magna Straus. Aquatic Toxicology 48 (2000) 195-209
7. Barata C., Baird D.J., Nogueira A.J.A., Agra A.R., and Soares A. Life-history responses of Daphnia magna Straus to binary mixtures of toxic substances: pharmacological versus ecotoxicological modes of action. Aquatic Toxicology 84 (2007) 439-449
8. Beckerman A.P., Wieski K., and Baird D.J. Behavioural versus physiological mediation of life history under predation risk. Oecologia 152 (2007) 335-343
9. Beketov M.A., and Liess M. Predation risk perception and food scarcity induce alterations of life-cycle traits of the mosquito culex pipens. Ecological Entomology 32 (2007) 405-410
10. Benard M.F. Predator-induced phenotypic plasticity in organisms with complex life histories. Annual Review of Ecology Evolution and Systematics 35 (2004) 651-673
11. Bengtsson G. Energetic costs of amino-acids exudation in the interaction between the predator gammarus-pulex l and the prey asellus-aquaticus L. Journal of Chemical Ecology 8 (1982) 1271-1281
12. Boyero L., Rincon P.A., and Bosch J. Case selection by a limnephilid caddisfly [potamophylax latipennis (curtis)] in response to different predators. Behavioral Ecology and Sociobiology 59 (2006) 364-372
13. Campero M., Slos S., Ollevier F., and Stoks R. Sublethal pesticide concentrations and predation jointly shape life history: behavioral and physiological mechanisms. Ecological Applications 17 (2007) 2111-2122
14. CCME 2007. Canadian Water Quality Guidelines: Imidacloprid. Scientific Supporting Document.Canadian Council of Ministers of the Environment, Winnipeg.
15. Dahl J., and Peckarsky B.L. Induced morphological defenses in the wild: Predator effects on a mayfly. Drunella Coloradensis Ecology 83 (2002) 1620-1634
16. Dahl J., and Peckarsky B.L. Developmental responses to predation risk in morphologically defended mayflies. Oecologia 137 (2003) 188-194
17. Dahl J., and Peckarsky B.L. Does living in streams with fish involve a cost of induced morphological defences?. Canadian Journal of Zoology-Revue Canadienne De Zoologie 81 (2003) 1825-1828
18. De Coen W.M., and Janssen C.R. The missing biomarker link: relationships between effects on the cellular energy allocation biomarker of toxicant-stressed daphnia magna and corresponding population characteristics. Environmental Toxicology and Chemistry 22 (2003) 1632-1641
19. DeWitt T.J., Sih A., and Wilson D.S. Costs and limits of phenotypic plasticity. Trends in Ecology and Evolution 13 (1998) 77-81
20. Dicke M., and Grostal P. Chemical detection of natural enemies by arthropods: an ecological perspective. Annual Review of Ecology and Systematics 32 (2001) 1-23
21. Elliott J.M. Quantitative Ecology and the Brown Trout (1994), Oxford University Press, Oxford
22. Faria M.S., Re A., Malcato J., Silva P., Pestana J., Agra A.R., Nogueira A.J.A., and Soares A. Biological and functional responses of in situ bioassays with Chironomus riparius larvae to assess river water quality and contamination. Science of the Total Environment 371 (2006) 125-137
23. Feio M.J., and Graca M.A.S. Food consumption by the larvae of Sericostoma vittatum (Trichoptera), an endemic species from the Iberian Peninsula. Hydrobiologia 439 (2000) 7-11
24. Ferreira A.L.G., Loureiro S., and Soares A. Toxicity prediction of binary combinations of cadmium, carbendazim and low dissolved oxygen on Daphnia magna. Aquatic Toxicology 89 (2008) 28-39
25. Gupta S., Gajbhiye V.T., Kalpana, and Agnihotri N.P. Leaching behavior of imidacloprid formulations in soil. Bulletin of Environmental Contamination and Toxicology 68 (2002) 502-508
26. Hanazato T. Pesticide effects on freshwater zooplankton: an ecological perspective. Environmental Pollution 112 (2001) 1-10
27. Heugens E.H.W., Hendriks A.J., Dekker T., van Straalen N.M., and Admiraal W. A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Critical Reviews in Toxicology 31 (2001) 247-284
28. Holker F., and Stief P. Adaptive behaviour of chironomid larvae (Chironomus riparius) in response to chemical stimuli from predators and resource density. Behavioral Ecology and Sociobiology 58 (2005) 256-263
29. Huryn A.D., and Chivers D.P. Contrasting behavioral responses by detritivorous and predatory mayflies to chemicals released by injured conspecifics and their predators. Journal of Chemical Ecology 25 (1999) 2729-2740
30. Jemec A., Tisler T., Drobne D., Sepcic K., Fournier D., and Trebse P. Comparative toxicity of imidacloprid, of its commercial liquid formulation and of diazinon to a non-target arthropod, the microcrustacean Daphnia magna. Chemosphere 68 (2007) 1408-1418
31. Jonker M.J., Svendsen C., Bedaux J.J.M., Bongers M., and Kammenga J.E. Significance testing of synergistic/antagonistic, dose level-dependent, or dose ratio-dependent effects in mixture dose-response analysis. Environmental Toxicology and Chemistry 24 (2005) 2701-2713
32. Kats L.B., and Dill L.M. The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5 (1998) 361-394
33. Kohler S.L., and McPeek M.A. Predation risk and the foraging behavior of competing stream insects. Ecology 70 (1989) 1811-1825
34. Kuhara N., Nakano S., and Miyasaka H. Interspecific competition between two stream insect grazers mediated by non-feeding predatory fish. Oikos 87 (1999) 27-35
35. Kuhara N., Nakano S., and Miyasaka H. Alterations in the grazing activities of cased caddisfly larvae in response to variations in predation risk and resource level. Ecological Research 16 (2001) 705-714
36. Laforsch C., Beccara L., and Tollrian R. Inducible defenses: the relevance of chemical alarm cues in Daphnia. Limnology and Oceanography 51 (2006) 1466-1472
37. Lass S., and Spaak P. Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491 (2003) 221-239
38. Lefcort H., Ammann E., and Eiger S.M. Antipredatory behavior as an index of heavy-metal pollution? A test using snails and caddisflies. Archives of Environmental Contamination and Toxicology 38 (2000) 311-316
39. Lima S.L., and Dill L.M. Behavioral decisions made under the risk of predation-a review and prospectus. Canadian Journal of Zoology-Revue Canadienne De Zoologie 68 (1990) 619-640
40. Maltby L. Studying stress: the importance of organism-level responses. Ecological Applications 9 (1999) 431-440
41. Matsuda K., Buckingham S.D., Kleier D., Rauh J.J., Grauso M., and Sattelle D.B. Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends in Pharmacological Sciences 22 (2001) 573-580
42. McIntosh A.R., and Peckarsky B.L. Are mayfly anti-predator responses to fish odour proportional to risk?. Archiv Fur Hydrobiologie 160 (2004) 145-151
43. McPeek M.A., and Peckarsky B.L. Life histories and the strengths of species interactions: combining mortality, growth, and fecundity effects. Ecology 79 (1998) 867-879
44. Merrit R.W., and Cummins K.W. Aquatic Insects of North America. third ed. (1996), Kendall/Hunt Publishing Company, Dubuque, Iowa
45. Minitab, I. 2000. Minitab Statistical Software 13.0. in.
46. Naylor C., Maltby L., and Calow P. Scope for growth in gammarus-pulex, a fresh-water benthic detritivore. Hydrobiologia 188 (1989) 517-523
47. Noonburg E.G., and Nisbet R.M. Behavioural and physiological responses to food availability and predation risk. Evolutionary Ecology Research 7 (2005) 89-104
48. Nowak C., Czeikowitz A., Vogt C., Oetken M., Streit B., and Schwenk K. Variation in sensitivity to cadmium among genetically characterized laboratory strains of the midge Chironomus riparius. Chemosphere 71 (2008) 1950-1956
49. OECD 2001. Guideline 219-Sediment-water chironomid toxicity test using spiked water.21.
50. Peckarsky B.L., McIntosh A.R., Taylor B.W., and Dahl J. Predator chemicals induce changes in mayfly life history traits: a whole-stream manipulation. Ecology 83 (2002) 612-618
51. Peckarsky B.L., Taylor B.W., McIntosh A.R., McPeek M.A., and Lytle D.A. Variation in mayfly size at metamorphosis as a developmental response to risk of predation. Ecology 82 (2001) 740-757
52. Penczak T., and Formigo N. Fish stocks in the Ancora River, north Portugal food consumption estimated with a bioenergetics model. Fisheries Research 49 (2000) 117-128
53. Preston B.L., Snell T.W., and Dusenbery D.B. The effects of sublethal pentachlorophenol exposure on predation risk in freshwater rotifer species. Aquatic Toxicology 47 (1999) 93-105
54. Relyea R., and Hoverman J. Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecology Letters 9 (2006) 1157-1171
55. Relyea R.A. Predator cues and pesticides: a double dose of danger for amphibians. Ecological Applications 13 (2003) 1515-1521
56. Relyea R.A. The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecological Applications 15 (2005) 618-627
57. Relyea R.A., Schoeppner N.M., and Hoverman J.T. Pesticides and amphibians: the importance of community context. Ecological Applications 15 (2005) 1125-1134
58. Schoeppner N.M., and Relyea R.A. Damage, digestion, and defence: the roles of alarm cues and kairomones for inducing prey defences. Ecology Letters 8 (2005) 505-512
59. Schulz R., and Dabrowski J.M. Combined effects of predatory fish and sublethal pesticide contamination on the behavior and mortality of mayfly nymphs. Environmental Toxicology and Chemistry 20 (2001) 2537-2543
60. Schulz R., and Liess M. Toxicity of fenvalerate to caddisfly larvae: chronic effects of 1-vs 10-h pulse-exposure with constant doses. Chemosphere 41 (2000) 1511-1517
61. Song M.Y., Stark J.D., and Brown J.J. Comparative toxicity of four insecticides, including imidacloprid and tebufenozide, to four aquatic arthropods. Environmental Toxicology and Chemistry 16 (1997) 2494-2500
62. Soucek D.J. Effects of freshly neutralized aluminum on oxygen consumption by freshwater invertebrates. Archives of Environmental Contamination and Toxicology 50 (2006) 353-360
63. Stoks R. Food stress and predator-induced stress shape developmental performance in a damselfly. Oecologia 127 (2001) 222-229
64. Stoks R., De Block M., Van de Meutter F., and Johansson F. Predation cost of rapid growth: behavioural coupling and physiological decoupling. Journal of Animal Ecology 74 (2005) 708-715
65. Stoughton S.J., Liber K., Culp J., and Cessna A. Acute and chronic toxicity of imidacloprid to the aquatic invertebrates Chironomus tentans and Hyalella azteca under Constant-and Pulse-Exposure Condition. Archives of Environmental Contamination and Toxicology (2008) 10.1007/s00244-007-9073-6
66. Tilman D., Fargione J., Wolff B., D'Antonio C., Dobson A., Howarth R., Schindler D., Schlesinger W.H., Simberloff D., and Swackhamer D. Forecasting agriculturally driven global environmental change. Science 292 (2001) 281-284
67. Tomizawa M., and Casida J.E. Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annual Review of Entomology 48 (2003) 339-364
68. Van Straalen N. Ecotoxicology becomes stress ecology. Environmental Science and Technology 37 (2003) 324A-330A
69. Walker C.H., Hopkin S.P., Sibly R.M., and Peakall D.B. Principles of Ecotoxicology. second ed. (2001), Taylor & Francis, London
70. Widdows J. Physiological-responses to pollution. Marine Pollution Bulletin 16 (1985) 129-134
71. Wissinger S.A., Whissel J.C., Eldermire C., and Brown W.S. Predator defense along a permanence gradient: roles of case structure, behavior, and developmental phenology in caddisflies. Oecologia 147 (2006) 667-678
72. Zar J.H. Biostatistical Analysis (1996), Prentice-Hall International Inc., New Jersey