Skip to main content
Log in

Interactive effects of pesticide exposure and habitat structure on behavior and predation of a marine larval fish

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Coastal development has generated multiple stressors in marine and estuarine ecosystems, including habitat degradation and pollutant exposure, but the effects of these stressors on the ecology of fishes remain poorly understood. We studied the separate and combined effects of an acute 4 h sublethal exposure of the pyrethroid pesticide esfenvalerate and structural habitat complexity on behavior and predation risk of larval topsmelt (Atherinops affinis). Larvae were exposed to four nominal esfenvalerate concentrations (control, 0.12, 0.59, 1.18 μg/L), before placement into 12 L mesocosms with a three-spine stickleback (Gasterosteus aculeatus) predator. Five treatments of artificial eelgrass included a (1) uniform and (2) patchy distribution of eelgrass at a low density (500 shoots per m2), a (3) uniform and (4) patchy distribution of eelgrass at a high density (1,000 shoots per m2), and (5) the absence of eelgrass. The capture success of predators and aggregative behavior of prey were observed in each mesocosm for 10 min of each trial, and mortality of prey was recorded after 60 min. Exposure to esfenvalerate increased the proportion of larvae with swimming abnormalities. Surprisingly, prey mortality did not increase linearly with pesticide exposure but increased with habitat structure (density of eelgrass), which may have been a consequence of compensating predator behavior. The degree of prey aggregation decreased with both habitat structure and pesticide exposure, suggesting that anti-predator behaviors by prey may have been hampered by the interactive effects of both of these factors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allen LG, Horn MH (1975) Abundance, diversity and seasonality of fishes in Colorado Lagoon, Alamitos Bay, California. Estuar Coast Mar Sci 3:371–380

    Article  Google Scholar 

  • Anderson B, Middaugh D, Hunt J, Turpen S (1991) Copper toxicity to sperm, embryos and larvae of topsmelt Atherinops affinis, with notes on induced spawning. Mar Environ Res 31:17–35

    Article  CAS  Google Scholar 

  • Atwood JL, Kelly PR (1984) Fish dropped on breeding colonies as indicators of least tern food habits. Wilson Bull 96:34–47

    Google Scholar 

  • Babbitt KJ, Tanner GW (1998) Effects of cover and predator size on survival and development of Rana utricularia tadpoles. Oecologia 114:258–262

    Article  Google Scholar 

  • Baber MJ, Babbitt KJ (2004) Influence of habitat complexity on predator–prey interactions between the fish (Gambusia holbrooki) and tadpoles of Hyla squirella and Gastrophryne carolinensis. Copeia 2004:173–177

    Article  Google Scholar 

  • Baldwin DH, Spromberg JA, Collier TK, Scholz NL (2009) A fish of many scales: Extrapolating sublethal pesticide exposures to the productivity of wild salmon populations. Ecol Appl 19:2004–2015

    Article  Google Scholar 

  • Beck MW, Heck KL, Able KW et al (2003) The role of nearshore ecosystems as fish and shellfish nurseries. Issues Ecol 11:1–12

    Google Scholar 

  • Beketov MA, Kefford BJ, Schäfer RB, Liess M (2013) Pesticides reduce regional biodiversity of stream invertebrates. Proc Natl Acad Sci 110:11039–11043

    Article  CAS  Google Scholar 

  • Bradbury SP, Coats JR (1989) Toxicokinetics and toxicodynamics of pyrethroid insecticides in fish. Environ Toxicol Chem 8:373–380

    Article  CAS  Google Scholar 

  • Brady J, Wallender W, Werner I et al (2006) Pesticide runoff from orchard floors in Davis, California, USA: a comparative analysis of diazinon and esfenvalerate. Agric Ecosyst Environ 115:56–68

    Article  CAS  Google Scholar 

  • Chamberlain RH, Barnhart RA (1993) Early use by fish of a mitigation salt marsh, Humboldt Bay, California. Estuaries 16:769–783

    Article  Google Scholar 

  • Christensen B, Persson L (1993) Species-specific antipredatory behaviours: effects on prey choice in different habitats. Behav Ecol Sociobiol 32:1–9

    Article  Google Scholar 

  • Courrat A, Lobry J, Nicolas D et al (2009) Anthropogenic disturbance on nursery function of estuarine areas for marine species. Estuar Coast Shelf Sci 81:179–190

    Article  Google Scholar 

  • Dachs J, Méjanelle L (2010) Organic pollutants in coastal waters, sediments, and biota: a relevant driver for ecosystems during the anthropocene? Estuar Coasts 33:1–14

    Article  Google Scholar 

  • Davis MJ, Purrenhage JL, Boone MD (2012) Elucidating predator–prey interactions using aquatic microcosms: complex effects of a crayfish predator, vegetation, and atrazine on tadpole survival and behavior. J Herpetol 46:527–534

    Article  Google Scholar 

  • Department of Pesticide Regulation EMB (2005) Continuing assessment of pyrethroid contamination of surface waters and bed sediments in high pyrethroid-use regions of California

  • Dupuch A, Dill LM, Magnan P (2009) Testing the effects of resource distribution and inherent habitat riskiness on simultaneous habitat selection by predators and prey. Anim Behav 78:705–713

    Article  Google Scholar 

  • Ensminger M, Bergin R, Spurlock F, Goh KS (2011) Pesticide concentrations in water and sediment and associated invertebrate toxicity in Del Puerto and Orestimba Creeks, California, 2007–2008. Environ Monit Assess 175:573–587

    Article  CAS  Google Scholar 

  • Fleeger J, Carman K, Nisbet R (2003) Indirect effects of contaminants in aquatic ecosystems. Sci Total Environ 317:207–233

    Article  CAS  Google Scholar 

  • Floyd EY, Geist JP, Werner I (2008) Acute, sublethal exposure to a pyrethroid insecticide alters behavior, growth, and predation risk in larvae of the fathead minnow (Pimephales promelas). Environ Toxicol Chem 27:1780–1787

    Article  CAS  Google Scholar 

  • Gotceitas V, Colgan P (1989) Predator foraging success and habitat complexity: quantitative test of the threshold hypothesis. Oecologia 80:158–166

    Article  Google Scholar 

  • Heck KL, Thoman TA (1981) Experiments on predator–prey interactions in vegetated aquatic habitats. J Exp Mar Bio Ecol 53:125–134

    Article  Google Scholar 

  • Hovel K, Lipcius R (2001) Habitat fragmentation in a seagrass landscape: patch size and complexity control blue crab survival. Ecology 82:1814–1829

    Article  Google Scholar 

  • Huntingford FA, Ruiz-Gomez ML (2009) Three-spined sticklebacks Gasterosteus aculeatus as a model for exploring behavioural biology. J Fish Biol 75:1943–1976

    Article  CAS  Google Scholar 

  • Johannesen A, Dunn AM, Morrell LJ (2012) Olfactory cue use by three-spined sticklebacks foraging in turbid water: prey detection or prey location? Anim Behav 84:151–158

    Article  Google Scholar 

  • Jones CL, Anderson TW, Edwards MS (2013) Evaluating eelgrass site quality by the settlement, performance, and survival of a marine fish. J Exp Mar Bio Ecol 445:61–68

    Article  Google Scholar 

  • Little EE, Dwyer FJ, Fairchild JF et al (1993) Survival of bluegill and their behavioral responses during continuous and pulsed exposures to esfenvalerate, a pyrethroid insecticide. Environ Toxicol Chem 12:871–878

    Article  CAS  Google Scholar 

  • Lotze HK, Lenihan HS, Bourque BJ et al (2006) Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312:1806–1809

    Article  CAS  Google Scholar 

  • Macneale KH, Kiffney PM, Scholz NL (2010) Pesticides, aquatic food webs, and the conservation of Pacific salmon. Front Ecol Environ 8:475–482

    Article  Google Scholar 

  • Maund SJ, Campbell PJ, Giddings JM et al (2012) Ecotoxicology of synthetic pyrethroids. Top Curr Chem 314:137–166

    Article  CAS  Google Scholar 

  • McGourty CR, Hobbs JA, Bennett WA et al (2009) Likely population-level effects of contaminants on a resident estuarine fish species: comparing Gillichthys mirabilis population static measurements and vital rates in San Francisco and Tomales Bay. Estuaries Coasts 32:1111–1120

    Article  Google Scholar 

  • Middaugh DP, Anderson BS, Hemmer MJ (1992) Laboratory spawning of topsmelt, Atherinops affinis, with notes on culture and growth of larvae. Environ Toxicol Chem 11:393–399

    Article  Google Scholar 

  • Miller N, Gerlai R (2012) From schooling to shoaling: patterns of collective motion in zebrafish (Danio rerio). PLoS ONE 7:e48865

    Article  CAS  Google Scholar 

  • Murphy CA, Rose KA, Alvarez MDC, Fuiman LA (2008) Modeling larval fish behavior: scaling the sublethal effects of methylmercury to population-relevant endpoints. Aquat Toxicol 86:470–484

    Article  CAS  Google Scholar 

  • Orth RJ, Heck KL, van Montfrans J (1984) Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator–prey relationships. Estuaries 7:339–350

    Article  Google Scholar 

  • Relyea RA, Edwards K (2010) What doesn’t kill you makes you sluggish: how sublethal pesticides alter predator–prey interactions. Environ Toxicol 4:558–567

    Google Scholar 

  • Robinson PD (2009) Behavioural toxicity of organic chemical contaminants in fish: application to ecological risk assessments (ERAs). Can J Fish Aquat Sci 66:1179–1188

    Article  CAS  Google Scholar 

  • Rohr JR, Kerby JL, Sih A (2006) Community ecology as a framework for predicting contaminant effects. Trends Ecol Evol 21:606–613

    Article  Google Scholar 

  • Savino JF, Stein RA (1982) Predator–prey interaction between largemouth bass and bluegills as influenced by simulated, submersed vegetation. Trans Am Fish Soc 111:255–266

    Article  Google Scholar 

  • Savino JF, Stein RA (1989) Behavior of fish predators and their prey: habitat choice between open water and dense vegetation. Environ Biol Fishes 24:287–293

    Article  Google Scholar 

  • Scott GR, Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 68:369–392

    Article  CAS  Google Scholar 

  • Sloman KA, McNeil PL (2012) Using physiology and behaviour to understand the responses of fish early life stages to toxicants. J Fish Biol 81:2175–2198

    Article  CAS  Google Scholar 

  • Tait KJ, Hovel KA (2012) Do predation risk and food availability modify prey and mesopredator microhabitat selection in eelgrass (Zostera marina) habitat? J Exp Mar Bio Ecol 426–427:60–67

    Article  Google Scholar 

  • Tanner DK, Knuth ML (1996) Effects of esfenvalerate on the reproductive success of the bluegill sunfish, Lepomis macrochirus in littoral enclosures. Arch Environ Contam Toxicol 31:244–251

    Article  CAS  Google Scholar 

  • Teh SJ, Deng D, Werner I et al (2005) Sublethal toxicity of orchard stormwater runoff in Sacramento splittail (Pogonichthys macrolepidotus) larvae. Mar Environ Res 59:203–216

    Article  CAS  Google Scholar 

  • van den Berg H, Zaim M, Yadav RS et al (2012) Global trends in the use of insecticides to control vector-borne diseases. Environ Health Perspect 120:577–582

    Article  Google Scholar 

  • Vonesh JR, Kraus JM (2009) Pesticide alters habitat selection and aquatic community composition. Oecologia 160:379–385

    Article  Google Scholar 

  • Ward AJW, Duff AJ, Horsfall JS, Currie S (2008) Scents and scents-ability: pollution disrupts chemical social recognition and shoaling in fish. Proc R Soc B 275:101–105

    Article  Google Scholar 

  • Weis JS, Candelmo A (2012) Pollutants and fish predator/prey behavior: a review of laboratory and field approaches. Curr Zool 58:9–20

    Google Scholar 

  • Weis P, Weis JS (1974) Schooling behavior of Menidia menidia in the presence of the insecticide Sevin (Carbaryl). Mar Biol 28:261–263

    Article  Google Scholar 

  • Weis JS, Smith GM, Zhou T (1999) Altered predator/prey behavior in polluted environments: implications for fish conservation. Environ Biol Fishes 55:43–51

    Article  Google Scholar 

  • Weis JS, Smith G, Zhou T et al (2001) Effects of contaminants on behavior: biochemical mechanisms and ecological consequences. Bioscience 51:209–217

    Article  Google Scholar 

  • Werner I, Zalom FG, Oliver MN et al (2004) Toxicity of storm-water runoff after dormant spray application in a french prune orchard, Glenn County, California, USA: temporal patterns and the effect of ground covers. Environ Toxicol Chem 23:2719–2726

    Article  CAS  Google Scholar 

  • Weston DP, Lydy MJ (2010) Urban and agricultural sources of pyrethroid insecticides to the Sacramento-San Joaquin Delta of California. Environ Sci Technol 44:1833–1840

    Article  CAS  Google Scholar 

  • Wootton RJ, Wootton RJ (1984) A functional biology of sticklebacks. University of California Press, Berkeley, CA, p 187

    Book  Google Scholar 

  • Zala SM, Penn DJ (2004) Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges. Anim Behav 68:649–664

    Article  Google Scholar 

Download references

Acknowledgments

We thank S. Wheeler, J. Wolfe, and S. Brander for assistance with predation trials and observations. Staff at the Bodega Marine Laboratory provided invaluable assistance and supplies for the design of this project. M. Edwards and R. Clark provided thoughtful suggestions and input on the analysis of this project. K. Smalling at the U.S. Geological Survey conducted the analytical chemistry for esfenvalerate in water samples. Support was provided by the Department of Biology at SDSU and the Bodega Marine Laboratory at UCD. Funding to V. Renick was provided by the Joint Doctoral Program in Ecology at San Diego State University, the SDSU Graduate Student Travel Fund, and the University of California, Davis.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Violet Compton Renick.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Renick, V.C., Anderson, T.W., Morgan, S.G. et al. Interactive effects of pesticide exposure and habitat structure on behavior and predation of a marine larval fish. Ecotoxicology 24, 391–400 (2015). https://doi.org/10.1007/s10646-014-1388-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-014-1388-2

Keywords

Navigation