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Can nutrients mask community responses to insecticide mixtures?

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Abstract

The ecological effect of simultaneous exposure to two nutrient gradients, three insecticides and different predator intensities was investigated over a 3-week period in 80 outdoor, artificial streams using field-collected benthic invertebrates. The experimental design consisted of a 2 × 5 factorial structure with two nutrient levels (oligotrophic or mesotrophic) and five concentrations of the ternary insecticide mixture consisting of the insecticides (chlorpyrifos, dimethoate and imidacloprid). Equivalent toxic unit doses were summed to create a ternary insecticide dose (e.g., 0.1 + 0.1 + 0.1 = 0.3 TU) resulting in a range of ternary insecticide mixture toxicity (i.e., control groundwater, 0.3, 0.6, 0.9 and 1.2 TU). Two genera of insect predators, Gomphus spp. (Odonata) and Agnetina spp. (Plecoptera) were also added into each replicate stream, at densities and sizes comparable to those found at our collection site, to evaluate how the contribution of predators may change in nutrient limited (oligotrophic) versus amended (mesotrophic) systems. We describe a causal mechanism whereby the combined action of nutrients and insecticides reshaped aquatic community structure by interacting through multiple pathways. Specifically, mesotrophic conditions reduced the toxic effects of ternary insecticide mixtures for aquatic insects which, in some cases, appeared to increase abundance of aquatic insects. However, higher levels of insecticides in mesotrophic streams negated this effect and were even more toxic; for example, to aquatic insect grazers than the same insecticide doses in oligotrophic treatment levels. Effects of predators were only significant in oligotrophic streams. Evidence is provided as to how nutrient and contaminant interactions can greatly complicate the assessment of community level responses to insecticide mixtures due to direct and indirect effects of the resulting changes in the density of different genera and functional feeding groups within a community.

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References

  • Alexander AC, Culp JM (2013) Predicting the effects of insecticide mixtures on non-target aquatic communities. In: Trdan S (ed) Insecticides development of safer and more effective technologies. Intech Open Publishers, Rijeka. http://www.intechopen.com/books/insecticides-development-of-safer-and-more-effective-technologies/predicting-the-effects-of-insecticide-mixtures-on-non-target-aquatic-communities

  • Alexander AC, Culp JM, Liber K, Cessna AJ (2007) Effects of insecticide exposure on feeding inhibition in mayflies and oligochaetes. Environ Toxicol Chem 26:1726–1732

    Article  CAS  Google Scholar 

  • Alexander AC, Heard KS, Culp JM (2008) Emergent body size of mayfly survivors. Fresh Biol 53:171–180

    Google Scholar 

  • Allan JD (1982) Feeding habits and prey consumption of three Setipalpian stoneflies (Plecoptera) in a mountain stream. Ecology 63(1):26–34

    Article  Google Scholar 

  • Allan JD (2004) Landscapes and riverscapes: the influence of land use on stream ecosystems. Ann Rev Ecol Evol Syst 35:257–284

    Article  Google Scholar 

  • Baekken T, Aanes KJ (1991) Pesticides in Norwegian agriculture. Their effects on benthic fauna in lotic environments (preliminary results). Int Ver Theor Angew Limnol Verh 24:2277–2281

    CAS  Google Scholar 

  • Biggs BJF (2000) Eutrophication of streams and rivers: dissolved nutrient–chlorophyll relationships for benthic algae. J N Am Benthol Soc 19:17–31

    Article  Google Scholar 

  • Campero M, Slos S, Ollevier F, Stoks R (2007) Sublethal pesticide concentrations and predation jointly shape life history: behavioral and physiological mechanisms. Ecol Appl 17:2111–2122

    Article  Google Scholar 

  • Cardinale BJ, Bennett DM, Nelson CE, Gross K (2009) Does productivity drive diversity or vice versa? A test of the multivariate productivity-diversity hypothesis in streams. Ecology 90:1227–1241

    Article  Google Scholar 

  • Carter JL, Resh VH, Hannaford MJ, Myers MJ (2006) Macroinvertebrates as biotic indicators of environmental quality. In: Hauer FR, Lamberti GA (eds) Methods in stream ecology, 2nd edn. Elsevier, Boston, pp 805–854

    Google Scholar 

  • Chambers JE, Meek EC, Chambers HW (2010) The metabolism of organophosphorus insecticides. In: Krieger R (ed) Hayes’ handbook of pesticide toxicology, 3rd edn. Academic Press, New York, pp 1399–1407

    Chapter  Google Scholar 

  • Cooper SD, Smith DW, Bence JR (1985) Prey selection by freshwater predators with different foraging strategies. Can J Fish Aquat Sci 42:1720–1732

    Article  Google Scholar 

  • Coors A, Decaestecker E, Jansen M, De Meester L (2008) Pesticide exposure strongly enhances parasite virulence in an invertebrate host model. Oikos 117:1840–1846

    Article  Google Scholar 

  • Culp JM, Baird DJ (2006) Establishing cause-effect relationships in multi-stressor environments. In: Hauer FR, Lamberti GA (eds) Methods in Stream Ecology, 2nd edn. Elsevier, Boston, pp 835–854

    Google Scholar 

  • Culp JM, Podemski CL, Cash KJ (2000) Interactive effects of nutrients and contaminants from pulp mill effluents on riverine benthos. J Aquat Ecosyst Stress Recovery 8:67–75

    Article  CAS  Google Scholar 

  • Culp JM, Cash KJ, Glozier NE, Brua RB (2003) Effects of pulp mill effluent on benthic assemblages in mesocosms along the Saint John River, Canada. Environ Toxicol Chem 22:2916–2925

    Article  CAS  Google Scholar 

  • Davis JM, Rosemond AD, Eggert SL, Cross WF, Wallace JB (2010) Long-term nutrient enrichment decouples predator and prey production. Proc Natl Acad Sci USA 107:121–126

    Article  CAS  Google Scholar 

  • Dodds WK, Jones JR, Welch EB (1998) Suggested classification of stream trophic state: distributions of temperate stream types by chlorophyll, total nitrogen, and phosphorus. Water Res 32:1455–1462

    Article  CAS  Google Scholar 

  • Dunn A (2004) A relative risk ranking of pesticides used in Prince Edward Island. Report EPS-5-AR-04-03. Environment Canada, Dartmouth, p 41

  • EPA (2009) ECOTOX (ECOTOXicology) database, Version 4. U.S. Environmental Protection Agency, Office of Research and Development (ORD), and the National Health and Environmental Effects Research Laboratory’s (NHEERL’s) Mid-Continent Ecology Division (MED). http://cfpub.epa.gov/ecotox/. Accessed 1 June 2009

  • European Commission (2003) Technical guidance document on risk assessment in support of commission directive 93/67/EEC on risk assessment for new notified substances and commission regulation (EC) No. 1488/94 on risk assessment for existing substances

  • Forbes VE, Calow P (2002) Extrapolation in ecological risk assessment: balancing pragmatism and precaution in chemical controls legislation. Bioscience 52:249–257

    Article  Google Scholar 

  • Gilliom RJ (2007) Pesticides in U.S. streams and groundwater. Environ Sci Technol 41:3408–3414

    Article  CAS  Google Scholar 

  • Goedkoop W, Spann N, Akerblom N (2010) Sublethal and sex-specific cypermethrin effects in toxicity tests with the midge Chironomus riparius Meigen. Ecotoxicology 19:1201–1208

    Article  CAS  Google Scholar 

  • Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Grimaldi S, Petroselli A, Serinaldi F (2012) Design hydrograph estimation in small and ungauged watersheds: continuous simulation method versus event-based approach. Hydrol Processes 26:3124–3134

    Article  Google Scholar 

  • Hall SR, Shurin JB, Diehl S, Nisbet RM (2007) Food quality, nutrient limitation of secondary production, and the strength of trophic cascades. Oikos 116:1128–1143

    Google Scholar 

  • Hoffman ER, Fisher S (1994) Comparison of a field and laboratory-derived population of Chironomus riparius (Diptera, Chironomidae) - biochemical and fitness evidence for population divergence. J Econ Entomol 87:320–325

    Google Scholar 

  • LeBlanc HMK, Culp JM, Baird DJ, Alexander AC, Cessna AJ (2012) Single versus combined lethal effects of three agricultural insecticides on larvae of the freshwater insect Chironomus dilutus. Arch Environ Contam Toxicol 63:378–390

    Article  CAS  Google Scholar 

  • Luis AT, Alexander AC, de Almeida SFP, da Silva EAF, Culp JM (2013) Benthic diatom communities in streams from zinc mining areas in continental (Canada) and mediterranean climates (Portugal). Water Quality Res J Can 48:180–191

    Google Scholar 

  • Matsuda K, Shimomura M, Ihara M, Akamatsu M, Sattelle DB (2005) Neonicotinoids show selective and diverse actions on their nicotinic receptor targets: electrophysiology, molecular biology, and receptor modeling studies. Biosci Biotechnol Biochem 69:1442–1452

    Article  CAS  Google Scholar 

  • McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395:794–797

    Article  CAS  Google Scholar 

  • McGrady-Steed J, Morin PJ (2000) Biodiversity, density compensation, and the dynamics of populations and functional groups. Ecology 81:361–373

    Article  Google Scholar 

  • Merritt RW, Cummins KW (1996) An introduction to the aquatic insects of North America. Kendall Hunt Pub, Dubuque

    Google Scholar 

  • Mishra SK, Pandey RP, Jain MK, Singh VP (2008) A rain duration and modified AMC-dependent SCS-CN procedure for long duration rainfall-runoff events. Water Resour Manag 22:861–876

    Article  Google Scholar 

  • Murphy C, Mutch JP, Reeves D, Clark T, Lavoie S, Rees H, Chow L, Nunn L, Hebb D (2006) Multi-media pesticide monitoring program in Prince Edward Island, New Brunswick and Nova Scotia. An Environment Canada Pesticide Science fund project final project report: 3 year monitoring report program—2003/04 to 2005/06. Environment Canada

  • Peckarsky BL (1982) Aquatic insect predator-prey relations. Bioscience 32:261–266

    Article  Google Scholar 

  • Peckarsky BL, Dodson SI (1980) Do stonefly predators influence benthic distributions in streams? Ecology 61:1275–1282

    Article  Google Scholar 

  • Peckarsky BL, Cowan CA, Penton MA, Anderson C (1993) Sublethal consequences of stream-dwelling predatory stoneflies on mayfly growth and fecundity. Ecology 74:1836–1846

    Article  Google Scholar 

  • Petersen DG, Sundback K, Larson F, Dahllof I (2009) Pyrene toxicity is affected by the nutrient status of a marine sediment community: implications for risk assessment. Aquat Toxicol 95:37–43

    Article  CAS  Google Scholar 

  • Pintor LM, Sih A (2011) Scale dependent effects of native prey diversity, prey biomass and natural disturbance on the invasion success of an exotic predator. Biol Invasions 13:1357–1366

    Article  Google Scholar 

  • Poff NL, Olden JD, Vieira NKM, Finn DS, Simmons MP, Kondratieff BC (2006) Functional trait niches of North American lotic insects: traits-based ecological applications in light of phylogenetic relationships. J N Am Benthol Soc 25:730–755

    Article  Google Scholar 

  • Relyea RA, Mills N (2001) Predator-induced stress makes the pesticide carbaryl more deadly to gray tree frog tadpoles (Hyla versicolor). Proc Natl Acad Sci USA 98:2491–2496

    Article  CAS  Google Scholar 

  • Schulz R (2004) Field studies on exposure, effects, and risk mitigation of aquatic nonpoint-source insecticide pollution: a review. J Environ Qual 33:419–448

    CAS  Google Scholar 

  • Schulz R, Dabrowski JM (2001) Combined effects of predatory fish and sublethal pesticide contamination on the behavior and mortality of mayfly nymphs. Environ Toxicol Chem 20:2537–2543

    Article  CAS  Google Scholar 

  • Shears NT, Ross PM (2010) Toxic cascades: multiple anthropogenic stressors have complex and unanticipated interactive effects on temperate reefs. Ecol Lett 13:1149–1159

    Article  Google Scholar 

  • Shipley B (2000) Cause and correlation in biology: a user’s guide to path analysis, structural equations and causal inference. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Suhling F (1996) Interspecific competition and habitat selection by the riverine dragonfly Onychogomphus uncatus. Fresh Biol 35:209–217

    Article  Google Scholar 

  • Tilman D (1996) Biodiversity: population versus ecosystem stability. Ecology 77:350–363

    Article  Google Scholar 

  • Townsend CR, Uhlmann SS, Matthaei CD (2008) Individual and combined responses of stream ecosystems to multiple stressors. J Appl Ecol 45:1810–1819

    Article  Google Scholar 

  • Traas TP, van de Meent D, Posthuma L, Hamers T, Kater BJ, de Zwart D, Aldenberg T (2002) The potentially affected fraction as a measure of ecological risk (Chapter 16). In: Posthuma L, Suter GW, Traas TP (eds) Species sensitivity distributions in ecotoxicology. CRC Press, Boca Raton, pp 315–344

    Google Scholar 

  • Traas TP, Janse JH, Van den Brink PJ, Brock TCM, Aldenberg T (2004) A freshwater food web model for the combined effects of nutrients and insecticide stress and subsequent recovery. Environ Toxicol Chem 23:521–529

    Article  CAS  Google Scholar 

  • Underwood AJ (2002) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, New York

    Google Scholar 

  • Usseglio-Polatera P, Bournaud M, Richoux P, Tachet H (2000) Biological and ecological traits of benthic freshwater macroinvertebrates: relationships and definition of groups with similar traits. Fresh Biol 43:175–205

    Article  Google Scholar 

  • van Wijngaarden R, Leeuwangh P, Lucassen WGH, Romijn K, Ronday R, van der Velde R, Willigenburg W (1993) Acute toxicity of chlorpyrifos to fish, a newt, and aquatic invertebrates. Bull Environ Contam Toxicol 51:716–723

    Article  Google Scholar 

  • Vinebrooke RD, Cottingham KL, Norberg MSJ, Dodson SI, Maberly SC, Sommer U (2004) Impacts of multiple stressors on biodiversity and ecosystem functioning: the role of species co-tolerance. Oikos 104:451–457

    Article  Google Scholar 

  • Walde SJ, Davies RW (1984) Invertebrate predation and lotic prey communities: evaluation of in situ enclosure/exclosure experiments. Ecology 65:1206–1213

    Article  Google Scholar 

  • Wesner JS (2012) Predator diversity effects cascade across an ecosystem boundary. Oikos 121:53–60

    Article  Google Scholar 

  • Westfall MJ, Tennessen KJ (1996) Chapter 12, Odonata. In: Merrit RW, Cummins KW (eds) An introduction to the aquatic insects of North America, 2nd edn. Kendall Hunt, Dubuque, pp 164–211

    Google Scholar 

  • Wooster D (1994) Predator impacts on stream benthic prey. Oecologia 99:7–15

    Article  Google Scholar 

  • Wooster D, Sih A (1995) A review of the drift and activity responses of stream prey to predator presence. Oikos 73:3–8

    Article  Google Scholar 

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Acknowledgments

We thank Bob Brua for his thoughtful review of an early draft of the manuscript. Jon Bailey at NHRC (Saskatoon) who conducted the chemical analyses. Also, Dave Hryn provided invaluable technical expertise and assistance in conducting the experiment. The authors declare that they have no conflict of interest. This work was supported in part by the Pesticide Science Fund awarded to Culp, Baird, Cessna and Alexander and an NSERC (PGS-D3 #362641) to ACA.

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Correspondence to Alexa C. Alexander.

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Alexander, A.C., Luis, A.T., Culp, J.M. et al. Can nutrients mask community responses to insecticide mixtures?. Ecotoxicology 22, 1085–1100 (2013). https://doi.org/10.1007/s10646-013-1096-3

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