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Interactive Effects of Mosquito Control Insecticide Toxicity, Hypoxia, and Increased Carbon Dioxide on Larval and Juvenile Eastern Oysters and Hard Clams

  • R. N. Garcia
  • K. W. Chung
  • P. B. Key
  • L. E. Burnett
  • L. D. Coen
  • M. E. DeLorenzoEmail author
Article

Abstract

Mosquito control insecticide use in the coastal zone coincides with the habitat and mariculture operations of commercially and ecologically important shellfish species. Few data are available regarding insecticide toxicity to shellfish early life stages, and potential interactions with abiotic stressors, such as low oxygen and increased CO2 (low pH), are less understood. Toxicity was assessed at 4 and 21 days for larval and juvenile stages of the Eastern oyster, Crassostrea virginica, and the hard clam, Mercenaria mercenaria, using two pyrethroids (resmethrin and permethrin), an organophosphate (naled), and a juvenile growth hormone mimic (methoprene). Acute toxicity (4-day LC50) values ranged from 1.59 to >10 mg/L. Overall, clams were more susceptible to mosquito control insecticides than oysters. Naled was the most toxic compound in oyster larvae, whereas resmethrin was the most toxic compound in clam larvae. Mortality for both species generally increased with chronic insecticide exposure (21-day LC50 values ranged from 0.60 to 9.49 mg/L). Insecticide exposure also caused sublethal effects, including decreased swimming activity after 4 days in larval oysters (4-day EC50 values of 0.60 to 2.33 mg/L) and decreased growth (shell area and weight) in juvenile clams and oysters after 21 days (detected at concentrations ranging from 0.625 to 10 mg/L). Hypoxia, hypercapnia, and a combination of hypoxia and hypercapnia caused mortality in larval clams and increased resmethrin toxicity. These data will benefit both shellfish mariculture operations and environmental resource agencies as they manage the use of mosquito control insecticides near coastal ecosystems.

Keywords

Mosquito Control Naled Grass Shrimp Methoprene Hard Clam 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This research was funded by a Grant from the Southern Regional Aquaculture Center, in cooperation with the United States Department of Agriculture, Cooperative State Research, Education and Extension Service, to M. E. DeLorenzo and L. D. Coen and the College of Charleston Graduate Program in Marine Biology, Biology Department, and Graduate Student Association. We acknowledge the kind experimental assistance of Paul Pennington, Shannon Whitehead, and John Venturella (NOAA/NOS/CCEHBR) as well as Karen Burnett, Anna Tommerdahl, Rebecca Derex, and Sarah Song (College of Charleston). We thank Mike Fulton, Tina Mikulski, Cheryl Woodley, and Pat Fair for helpful review of the manuscript. The NOAA, National Ocean Service does not approve, recommend, or endorse any proprietary product or material mentioned in this publication. This is Contribution No. 418 of the Grice Marine Laboratory, College of Charleston, Charleston, SC.

Supplementary material

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Supplementary material 1 (PDF 106 kb)

References

  1. Atlantic States Marine Fisheries Commission (2007) The importance of habitat created by shellfish and shell beds along the Atlantic Coast of the US Prepared by Coen LD and Grizzle R with contributions by Lowery J and Paynter KT Jr. ASMFS, MoreheadGoogle Scholar
  2. Baker SM, Mann R (1992) Effects of hypoxia and anoxia on larval settlement, juvenile growth, and juvenile survival of the oyster Crassostrea virginica. Biol Bull 182:265–269Google Scholar
  3. Beck MW, Brumbaugh RD, Airoldi L, Carranza A, Coen LD, Crawford C et al (2011) Oyster reefs at risk and recommendations for conservation, restoration, and management. Bioscience 61:107–116CrossRefGoogle Scholar
  4. Bolton-Warberg M, Coen LD, Weinstein JE (2007) Acute toxicity and acetylcholinesterase inhibition in grass shrimp (Palaemonetes pugio) and oysters (Crassostrea virginica) exposed to the organophosphate Dichlorvos: Laboratory and field experiments. Arch Environ Contam Toxicol 52:207–216CrossRefGoogle Scholar
  5. Bondarenko S, Putt A, Kavanaugh S, Poletika N, Gan J (2006) Time dependence of phase distribution of pyrethroids insecticides in sediment. Environ Toxicol Chem 25:3148–3154CrossRefGoogle Scholar
  6. Cai WJ, Wang Y (1998) The chemistry, fluxes, and sources of carbon dioxide in the estuarine waters of the Satilla and Altamaha rivers, Georgia. Limnol Oceanogr 43:657–668CrossRefGoogle Scholar
  7. Carriker MR (2001) Embryogenesis and organogenesis of veligers and early juveniles. In: Kraeuter JN, Castagna M (eds) The biology of the hard clam. Elsevier Science BV, Amsterdam, pp 77–112CrossRefGoogle Scholar
  8. Chandler GT, Cary TL, Volz DC, Walse SS, Ferry JL, Klosterhaus SL (2004) Fipronil effects on estuarine copepod (Amphiascus tenuiremis) development, fertility, and reproduction: A rapid life-cycle assay in 96-well microplate format. Environ Toxicol Chem 23:117–124CrossRefGoogle Scholar
  9. Cochran RE, Burnett LE (1996) Respiratory responses of the salt marsh animals Fundulus heteroclitus, Leiostomus xanthurus, and Palaemonetes pugio to environmental hypoxia and hypercapnia and to the organophosphate insecticide, azinphosmethyl. J Exp Mar Biol Ecol 195:125–144CrossRefGoogle Scholar
  10. Coen LD, Heck KL Jr (1991) The interacting effects of siphon nipping and habitat on bivalve (Mercenaria mercenaria (L)) growth in a subtropical seagrass (Halodule wrightii Aschers) meadow. J Exp Mar Biol Ecol 145:1–13CrossRefGoogle Scholar
  11. Coen LD, Lukenbach MW (2000) Developing success criteria and goals for evaluating oyster reef restoration: Ecological function or resource exploitation? Ecol Eng 15:323–343CrossRefGoogle Scholar
  12. Coen LD, Dumbauld BR, Judge ML (2011) Expanding shellfish aquaculture: A review of the ecological services provided by and impacts of native and cultured bivalves in shellfish-dominated ecosystems. In: Shumway SE (ed) Shellfish aquaculture and the environment. Wiley-Blackwell, New York, pp 239–295CrossRefGoogle Scholar
  13. Dame R (1996) Ecology of marine bivalves: an ecosystem approach. CRC Marine Science Series, Boca RatonCrossRefGoogle Scholar
  14. DeLorenzo ME, Fulton MH (2012) Comparative risk assessment of permethrin, chlorothalonil, and diuron to coastal aquatic species. Mar Pollut Bull 64:1291–1299CrossRefGoogle Scholar
  15. DeLorenzo ME, Plante C, Coen LD (2012) Effects of mosquito abatement pesticides on various life stages of commercially important shellfish aquaculture species in the South. Final project report. Southern Regional Aquaculture Center, StonevilleGoogle Scholar
  16. Dickinson GH, Ivanina AV, Matoo OB, Pörtner HO, Lannig G, Bock C et al (2012) Interactive effects of salinity and increased CO2 levels on juvenile eastern oysters, Crassostrea virginica. J Exp Biol 215:29–43CrossRefGoogle Scholar
  17. Dickinson GH, Matoo OB, Tourek RT, Sokolova IM, Beniash E (2013) Environmental salinity modulates the effects of increased CO2 levels on juvenile hard-shell clams, Mercenaria mercenaria. J Exp Biol 216:2607–2618CrossRefGoogle Scholar
  18. Dove MC, Sammut J (2007) Impacts of estuarine acidification on survival and growth of Sydney rock oysters Saccostrea glomerata (Gould 1850). J Shellfish Res 26:519–527CrossRefGoogle Scholar
  19. Dumbauld BR, Ruesink JL, Rumrill SS (2009) The ecological role of bivalve shellfish aquaculture in the estuarine environment: a review with application to oyster and clam culture in West Coast (USA) estuaries. Aquaculture 290:196–223CrossRefGoogle Scholar
  20. Forrest BM, Keeley NB, Hopkins GA, Webb SC, Clement DM (2009) Bivalve aquaculture in estuaries: review and synthesis of oyster cultivation effects. Aquaculture 298:1–15CrossRefGoogle Scholar
  21. Grabowski JH, Brumbaugh RD, Conrad RF, Keeler AG, Opaluch JJ, Peterson CH et al (2012) Economic valuation of ecosystem services provided by oyster reefs. Bioscience 62:900–909CrossRefGoogle Scholar
  22. Habig C, DiGiulio R (1991) Biochemical characteristics of cholinesterases in aquatic organisms. In: Mineau P (ed) Cholinesterase-inhibiting insecticides: Their impact on wildlife and the environment. Elsevier Science, New York, pp 19–33Google Scholar
  23. Hales S, de Wet N, Maindonald J, Woodward A (2002) Potential effect of population and climate changes on global distribution of dengue fever: an empirical model. Lancet 360:830–834CrossRefGoogle Scholar
  24. Hennessey MK, Nigg HN, Habeck DH (1992) Mosquito (Diptera: Culicidae) adulticide drift into wildlife refuges of the Florida Keys. Entomol Soc Am 14:714–720Google Scholar
  25. Henrick CA (2007) Methoprene: biorational control of mosquitoes. J Am Mosq Control Assoc 23:225–239CrossRefGoogle Scholar
  26. Hill IR (1985) Effects on non-target organisms in terrestrial and aquatic environments. In: Leahey J (ed) The pyrethroid insecticides. Taylor and Francis, Philadelphia, pp 189–238Google Scholar
  27. Hoguet J, Key PB (2007) Activities of biomarkers in multiple life stages of the model crustacean, Palaemonetes pugio. J Exp Mar Biol Ecol 353:235–244CrossRefGoogle Scholar
  28. Holland AF, Sanger DM, Gawle CP, Lerberg SB, Santiago MS, Riekerk GHM et al (2004) Linkages between tidal creek ecosystems and the landscape and demographic attributes of their watersheds. J Exp Mar Biol Ecol 298:151–178CrossRefGoogle Scholar
  29. Hubálek Z, Halouzka J (1999) West Nile fever—a reemerging mosquito-borne viral disease in Europe. Emerg Infect Dis 5:643–650CrossRefGoogle Scholar
  30. Jaffe R (1991) Fate of hydrophobic organic pollutants in the aquatic environment: a review. Environ Pollut 69:237–257CrossRefGoogle Scholar
  31. Kellogg ML, Cornwell JC, Owens MS, Paynter KT (2013) Denitrification and nutrient assimilation on a restored oyster reef. Mar Ecol Prog Ser 480:1–19CrossRefGoogle Scholar
  32. Kemp WM (1989) Estuarine chemistry. In: Day JW, Hall CA, Kemp WM, Yanez-Arancibia A (eds) Estuarine ecology. Wiley, New York, pp 79–145Google Scholar
  33. Kennedy VS, Krantz LB (1982) Comparative gametogenic and spawning patterns of the oyster Crassostrea virginica in central Chesapeake Bay, USA. J Shellfish Res 2:133–140Google Scholar
  34. Key P, DeLorenzo M, Gross K, Chung K, Clum A (2005) Toxicity of the mosquito control pesticide Scourge® to adult and larval grass shrimp (Palaemonetes pugio). J Environ Sci Health B 40:585–594CrossRefGoogle Scholar
  35. Kraeuter JN, Castagna M (2000) Predators and predation. In: Kraeuter JN, Castagna M (eds) The biology of the hard clam. Elsevier Science BV, Amsterdam, pp 441–590Google Scholar
  36. Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117CrossRefGoogle Scholar
  37. Kurihara H, Kato S, Ishimatsu A (2007) Effects of increased seawater pCO2 on early development of the oyster Crassostrea gigas. Aquat Biol 1:91–98CrossRefGoogle Scholar
  38. Lehotay SJ, Harman-Fetcho JA, McConnell LL (1998) Agricultural pesticide residues in oysters and water from two Chesapeake Bay tributaries. Mar Pollut Bull 37:32–44CrossRefGoogle Scholar
  39. Lerberg SB, Holland AF, Sanger DM (2000) Responses of tidal creek macrobenthic communities to the effects of watershed development. Estuaries 23:838–853CrossRefGoogle Scholar
  40. Luckenbach MW, Coen LD, Ross PG, Stephen JA (2005) Oyster reef habitat restoration: relationships between oyster abundance and community development based on two studies in Virginia and South Carolina. J Coast Res 40:64–78Google Scholar
  41. Martens P, Hall L (2000) Malaria on the move: human population movement and malaria transmission. Emerg Infect Dis 6:103–109CrossRefGoogle Scholar
  42. Milam CD, Farris JL, Wilhide JD (2000) Evaluating mosquito control pesticides for effect on target and nontarget organisms. Arch Environ Contam Toxicol 39:324–328CrossRefGoogle Scholar
  43. Miller TA, Salgado VL (1985) The mode of action of pyrethroids on insects. In: Leahy JP (ed) The pyrethroid insecticides. Taylor and Francis, London, pp 43–97Google Scholar
  44. Miller AW, Reynolds AC, Sobrino C, Riedel GF (2009) Shellfish face uncertain future in a high CO2 world: Influence of acidification on oyster larvae calcification and growth in estuaries. PLoS One 4:e5661CrossRefGoogle Scholar
  45. National Marine Fisheries Service (2011) Fisheries of the United States 2010. Office of Science and Technology, Silver SpringGoogle Scholar
  46. Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge MCM, Clay J et al (2000) Effect of aquaculture on world fish supplies. Nature 405:1017–1024CrossRefGoogle Scholar
  47. Newell RIE (2004) Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve mollusks: a review. J Shellfish Res 23:51–61Google Scholar
  48. Norberg-King TJ (1993) A linear interpolation method for sublethal toxicity: the inhibition concentration (ICP) approach. Technical report 03-93. United States Environmental Protection Agency, DuluthGoogle Scholar
  49. North EW, Schlag Z, Hood RR, Li M, Zhong L, Gross T et al (2008) Vertical swimming behavior influences the dispersal of simulated oyster larvae in a coupled particle-tracking and hydrodynamic model of Chesapeake Bay. Mar Ecol Prog Ser 359:99–115CrossRefGoogle Scholar
  50. Peterson CH, Grabowski JH, Powers SP (2003) Estimated enhancement of fish production resulting from restoring oyster reef habitat: quantitative valuation. Mar Ecol Prog Ser 264:249–264CrossRefGoogle Scholar
  51. Pierce RH, Henry MS, Blum TC, Mueller EM (2005) Aerial and tidal transport of mosquito control pesticides into the Florida Keys National Marine Sanctuary. Rev Biol Trop 53:117–125Google Scholar
  52. Rand GM (2002) Hazard assessment of resmethrin: effects and fate in aquatic systems. Ecotoxicology 11:101–111CrossRefGoogle Scholar
  53. Reichenberger S, Bach M, Stikschak A, Frede HG (2007) Mitigation strategies to decrease pesticide inputs into ground- and surface water and their effectiveness: a review. Sci Total Environ 384:1–35CrossRefGoogle Scholar
  54. Roop T, Greenberg MJ (1967) Acetylcholinesterase activity in Crassostrea virginica and Mercenaria mercenaria. Am Zool 7:737–738Google Scholar
  55. Scott GI, Fulton MH, Wirth EF, Chandler GT, Key PB, Daugomah JW et al (2002) Toxicological studies in tropical ecosystems: an ecotoxicological risk assessment of pesticide runoff in south Florida estuarine ecosystems. J Agric Food Chem 50:4400–4408CrossRefGoogle Scholar
  56. Shumway SE (1996) Natural environmental factors. In: Kennedy VS, Newell RIE, Eble AF (eds) The eastern oyster Crassostrea virginica. Maryland Sea Grant, College Park, pp 467–513Google Scholar
  57. Soderlund DM, Bloomquist JR (1989) Neurotoxic actions of pyrethroid insecticides. Annu Rev Entomol 34:77–96CrossRefGoogle Scholar
  58. Solomon KR, Giddings JM, Maund SJ (2001) Probabilistic risk assessment of cotton pyrethroids: I. Distributional analyses of laboratory aquatic toxicity data. Environ Toxicol Chem 20:652–659CrossRefGoogle Scholar
  59. Spurlock F, Lee M (2008) Synthetic pyrethroid use patterns, properties, and environmental effects. In: ACS symposium series. American Chemical Society, Washington. pp 3–25Google Scholar
  60. Stunz GW, Minello TJ, Rozas LP (2010) Relative value of oyster reef as habitat for estuarine nekton in Galveston Bay, Texas. Mar Ecol Prog Ser 406:147–159CrossRefGoogle Scholar
  61. Suter GW II (1995) Introduction to ecological risk assessment for aquatic toxic effects. In: Rand GM (ed) Fundamentals of aquatic toxicology, 2nd edn. Taylor and Francis, Washington, pp 803–816Google Scholar
  62. Talmage SC, Gobler CJ (2011) Effects of increased temperature and carbon dioxide on the growth and survival of larvae and juveniles of three species of Northwest Atlantic bivalves. PLoS One 6:e26941CrossRefGoogle Scholar
  63. Tamburri MN, Zimmer-Faust RK, Tamplin ML (1992) Natural sources and properties of chemical inducers mediating settlement of oyster larvae: a re-examination. Biol Bull 183:327–338CrossRefGoogle Scholar
  64. Thompson B, Anderson B, Hunt J, Taberski K, Phillips B (1999) Relationships between sediment contamination and toxicity in San Francisco Bay. Mar Environ Res 48:285–309CrossRefGoogle Scholar
  65. Tomanek L, Zuzow MJ, Ivanina AV, Beniash E, Sokolova IM (2011) Proteomic response to increased PCO2 level in eastern oysters, Crassostrea virginica: Evidence for oxidative stress. J Exp Biol 214:1836–1844CrossRefGoogle Scholar
  66. Waldbusser GG, Steenson RA, Green MA (2011) Oyster shell dissolution rates in estuarine waters: effects of pH and shell legacy. J Shellfish Res 30:659–669CrossRefGoogle Scholar
  67. Watson S, Southgate PC, Tyler PA, Peck LS (2009) Early larval development of the Sydney rock oyster Saccostrea glomerata under near-future predictions of C02-driven ocean acidification. J Shellfish Res 28:431–437CrossRefGoogle Scholar
  68. Weston DP, Amweg EL, Mekebri A, Ogle RS, Lydy MJ (2006) Aquatic effects of aerial spraying for mosquito control over an urban area. Environ Sci Technol 40:5817–5822CrossRefGoogle Scholar
  69. Wheeler MW, Park RM, Bailer AJ (2006) Comparing median lethal concentration values using confidence interval overlap or ratio tests. Environ Toxicol Chem 25:1441–1444CrossRefGoogle Scholar
  70. Wilson JD (2002) Productivity, fisheries, and aquaculture in temperate estuaries. Est Coast Shelf Sci 55:953–967CrossRefGoogle Scholar
  71. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle RiverGoogle Scholar
  72. Zulkosky AM, Ruggieri JP, Terracciano SA, Brownawell BJ, McElory AE (2005) Acute toxicity of resmethrin, malathion, and methoprene to larval and juvenile American lobsters (Homarus americanus) and analysis of pesticide levels in surface waters after Scourge®, Anvil®, and Altosid® application. J Shellfish Res 24:795–804Google Scholar

Copyright information

© Springer Science+Business Media New York (outside the USA) 2014

Authors and Affiliations

  • R. N. Garcia
    • 1
  • K. W. Chung
    • 2
  • P. B. Key
    • 2
  • L. E. Burnett
    • 1
  • L. D. Coen
    • 3
  • M. E. DeLorenzo
    • 2
    Email author
  1. 1.Grice Marine LaboratoryCollege of CharlestonCharlestonUSA
  2. 2.National Ocean ServiceNational Oceanic and Atmospheric AdministrationCharlestonUSA
  3. 3.Department of Biological Sciences and HBOIFlorida Atlantic UniversityFort PierceUSA

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