Advertisement

Environmental Science and Pollution Research

, Volume 25, Issue 14, pp 13235–13243 | Cite as

Freshwater shrimps as sensitive test species for the risk assessment of pesticides in the tropics

  • Michiel A. DaamEmail author
  • Andreu Rico
Ecotoxicology in Tropical Regions

Abstract

The aquatic risk assessment of pesticides in tropical areas has often been disputed to rely on toxicity data generated from tests performed with temperate species. Given the differences in ecosystem structure between temperate and tropical ecosystems, test species other than those used in temperate regions have been proposed as surrogates for tropical aquatic effect assessments. Freshwater shrimps, for example are important components of tropical freshwater ecosystems, both in terms of their role in ecosystem functioning and their economic value. In the present study, available toxicity data of (tropical and sub-tropical) freshwater shrimps for insecticides and fungicides were compiled and compared with those available for Daphnia magna and other aquatic invertebrates. Freshwater shrimps appeared to be especially sensitive to GABA-gated chloride channel antagonist and sodium channel modulator insecticides. However, shrimp taxa showed a moderate and low sensitivity to acetylcholinesterase inhibiting insecticides and fungicides respectively. Implications for the use of freshwater shrimps in tropical pesticide effect assessments and research needs are discussed.

Keywords

Freshwater shrimps Tropics Insecticides Fungicides Ecological risk assessment Relative tolerance (Trel) Species sensitivity distributions 

Notes

Acknowledgments

The present study was funded by the Brazilian government through the Special Visiting Researcher program (MEC/MCTI/CAPES/CNPq/FAPs reference 402392/2013-2) and the Portuguese government (FCT) through a postdoc grant for the first author (SFRH/BPD/109199/2015).

Supplementary material

11356_2016_7451_MOESM1_ESM.docx (30 kb)
ESM 1 (DOCX 30 kb)

References

  1. Aldenberg T, Jaworska JS (2000) Uncertainty of hazardous concentrations and fraction affected for normal species sensitivity distributions. Ecotoxicol Environ Saf 46:1–18CrossRefGoogle Scholar
  2. Allinson G, Hagen T, Salzman S, Wightwick A, Nugegoda D (2011) Effect of increasing salinity on the acute toxicity of a commercial endosulfan formulation to the bdelloid rotifer Philodina acuticornis odiosa. Toxicol Environ Chem 93:722–728CrossRefGoogle Scholar
  3. Ashauer R, Hintermeister A, Potthoff E, Escher BI (2011) Acute toxicity of organic chemicals to Gammarus pulex correlates with sensitivity of Daphnia magna across most modes of action. Aquat Toxicol 103:38–45CrossRefGoogle Scholar
  4. Barki A, Karplus I, Goren M (1992) Effects of size and morphotype on dominance hierarchies and resource competition in the freshwater prawn Macrobrachium rosenbergii. Anim Behav 44:547–555CrossRefGoogle Scholar
  5. Bragagnolo N, Rodriguez-Amaya DB (2001) Total lipid, cholesterol, and fatty acids of farmed freshwater prawn (Macrobrachium rosenbergii) and wild marine shrimp (Penaeus brasiliensis, Penaeus schimitti, Xiphopenaeus kroyeri). J Food Compos Anal 14:359–369CrossRefGoogle Scholar
  6. Brock T, Bhatta R, Van Wijngaarden R, Rico A (2016) Is the chronic Tier-1 effect assessment approach for insecticides protective for aquatic ecosystems? Integr Environ Assess Manag. doi: 10.1002/ieam.1719 CrossRefGoogle Scholar
  7. Campbell E, Palmer MJ, Shao Q, Warne MSJ, Wilson D (2000) BurrliOZ: a computer program for calculating toxicant trigger values for the ANZECC and ARMCANZ water quality guidelines. Perth, AustraliaGoogle Scholar
  8. Castillo LE, De la Cruz E, Ruepert C (1997) Ecotoxicology and pesticides in tropical aquatic ecosystems of Central America. Environ Toxicol Chem 16:41–51CrossRefGoogle Scholar
  9. Chanmugam P, Donovan J, Wheeler CJ, Hwang DH (2006) Differences in the lipid composition of fresh water prawn (Macrobrachium rosenbergii) and marine shrimp. J Food Sci 48:1440–1462CrossRefGoogle Scholar
  10. Christensen BT, Lauridsen TL, Ravn HW, Bayley M (2005) A comparison of feeding efficiency and swimming ability of Daphnia magna exposed to cypermethrin. Aquat Toxicol 73:210–220CrossRefGoogle Scholar
  11. Cuppen JGM, Van den Brink PJ, Camps E, Uil KF, Brock TCM (2000) Impact of the fungicide carbendazim in freshwater microcosms. I. Water quality, breakdown of particulate organic matter and responses of macroinvertebrates. Aquat Toxicol 48:233–250CrossRefGoogle Scholar
  12. Daam MA, Van den Brink PJ (2010) Implications of differences between temperate and tropical freshwater ecosystems for the ecological risk assessment of pesticides. Ecotoxicology 19:24–37CrossRefGoogle Scholar
  13. Daam MA, Satapornvanit K, Van den Brink PJ, Nogueira AJ (2009) Sensitivity of macroinvertebrates to carbendazim under semi-field conditions in Thailand: implications for the use of temperate toxicity data in a tropical risk assessment of fungicides. Chemosphere 74:1187–1194CrossRefGoogle Scholar
  14. Daam MA, Silva E, Leitão S, Trindade MJ, Cerejeira MJ (2010) Does the actual standard of 0.1 μg/L overestimate or underestimate the risk of plant protection products to groundwater ecosystems? Ecotoxicol Environ Saf 73:750–756CrossRefGoogle Scholar
  15. Davies PE, Cook LSJ, Goenar D (1994) Sublethal responses to pesticides of several species of Australian freshwater fish and crustaceans and rainbow trout. Environ Toxicol Chem 13:1341–1354CrossRefGoogle Scholar
  16. De Grave S, Cai Y, Anker A (2008) Global diversity of shrimps (Crustacea: Decapoda: Caridea) in freshwater. Hydrobiologia 595:287–293CrossRefGoogle Scholar
  17. DeLorenzo ME, Serrano L, Chung KW, Hoguet J, Key PB (2006) Effects of the insecticide permethrin on three life stages of the grass shrimp, Palaemonetes pugio. Ecotoxicol Environ Saf 64:122–127CrossRefGoogle Scholar
  18. Dudgeon D (2000) The ecology of tropical Asian rivers and streams in relation to biodiversity conservation. Annu Rev Ecol Syst 31:239–263CrossRefGoogle Scholar
  19. Dumont HJ (1994) On the diversity of the Cladocera in the tropics. Hydrobiologia 272:27–38CrossRefGoogle Scholar
  20. EFSA (2013) Guidance on tiered risk assessment for plant protection products for aquatic organisms in the edge-of-field surface waters. EFSA J 11:3290CrossRefGoogle Scholar
  21. Fernando CH (2002) Zooplankton and tropical freshwater fisheries. In: CH F (ed) A guide to tropical freshwater zooplankton. Backhuys Publishers, Leiden, pp. 255–280Google Scholar
  22. Ferrando MD, Sancho E, Andreu-Moliner E (1996) Chronic toxicity of fenitrothion to an algae (Nannochloris oculata), a rotifer (Brachionus calyciflorus), and the cladoceran (Daphnia magna). Ecotoxicol Environ Saf 35:112–120CrossRefGoogle Scholar
  23. Freitas EC, Rocha O (2012) Acute and chronic effects of atrazine and sodium dodecyl sulfate on the tropical freshwater cladoceran Pseudosida ramosa. Ecotoxicology 21:1347–1357CrossRefGoogle Scholar
  24. Hoang TC, Klaine SJ (2007) Influence of organism age on metal toxicity to Daphnia magna. Environ Toxicol Chem 26:1198–1204CrossRefGoogle Scholar
  25. Hoi PV, Mol AP, Oosterveer P, van den Brink PJ, Huong PT (2016) Pesticide use in Vietnamese vegetable production: a 10-year study. Int J Agric Sustain 20:1–4Google Scholar
  26. Key PB, Fulton MH, Scott GI, Layman SL, Wirth EF (1998) Lethal and sublethal effects of malathion on three life stages of the grass shrimp, Palaemonetes pugio. Aquat Toxicol 40(4):311–322CrossRefGoogle Scholar
  27. Key PB, Meyer SL, Chung KW (2003) Lethal and sub-lethal effects of the fungicide chlorothalonil on three life stages of the grass shrimp, Palaemonetes pugio. J Environ Sci Health B 38(5):539–549CrossRefGoogle Scholar
  28. Kwok KWH, Leung KMY, Chu VKH, Lam PKS, Morritt D, Maltby L, Brock TCM, Van den Brink PJ, Warne MSJ, Crane M (2007) Comparison of tropical and temperate freshwater species sensitivities to chemicals: implications for deriving safe extrapolation factors. Integr Environ Assess Manag 3:49–67CrossRefGoogle Scholar
  29. Lacher TE Jr, Goldstein MI (1997) Tropical ecotoxicology: status and needs. Environ Toxicol Chem 16:100–111CrossRefGoogle Scholar
  30. Li N, Zhao Y, Yang J (2008) Effects of water-borne copper on digestive and metabolic enzymes of the giant freshwater prawn Macrobrachium rosenbergii. Arch Environ Contam Toxicol 55:86–93CrossRefGoogle Scholar
  31. Lunt GG (1991) GABA and GABA receptors in invertebrates. Semin Neurosci 3:251–258CrossRefGoogle Scholar
  32. Macek K, Lindberg M, Sauter S, Buxton K, Costa P (1976) Toxicity of four pesticides to water fleas and fathead minnows. Acute and chronic toxicology of acrolein, heptachlor, endosulfan and trifluralin to the water flea (Daphnia magna) and the fathead minnow (Pimephales promelas). US Environmental Protection Agency, Washington, DC EPA/600/3-76/099Google Scholar
  33. Maltby L, Blake N, Brock TCM, Van den Brink PJ (2005) Insecticide species sensitivity distributions: importance of test species selection and relevance to aquatic ecosystems. Environ Toxicol Chem 24:379–388CrossRefGoogle Scholar
  34. Maltby L, Brock TCM, Van den Brink PJ (2009) Fungicide risk assessment for aquatic ecosystems: importance of interspecific variation, toxic mode of action, and exposure regime. Environ Sci Technol 43:7556–7563CrossRefGoogle Scholar
  35. Montagna MC, Collins PA (2007) Survival and growth of Palaemonetes argentines (Decapoda; Caridea) exposed to insecticides with chlorpyrifos and endosulfan as active element. Arch Environ Contam Toxicol 53:371–378Google Scholar
  36. Moreira RA, Mansano AS, Silva LCD, Rocha O (2014) A comparative study of the acute toxicity of the herbicide atrazine to cladocerans Daphnia magna, Ceriodaphnia silvestrii and Macrothrix flabelligera. Acta Limnol Bras 26:1–8CrossRefGoogle Scholar
  37. Moreira RA, da Silva MA, Rocha A, Daam MA (2016) The use of rotifers as test species in the aquatic effect assessment of pesticides in the tropics. Hydrobiologia 773:1–9CrossRefGoogle Scholar
  38. Nagai T (2016) Ecological effect assessment by species sensitivity distribution for pesticides used in Japanese paddy fields. J Pestic Sci 41:6–14CrossRefGoogle Scholar
  39. Nyman A-M, Schirmer K, Ashauer R (2014) Importance of toxicokinetics for interspecies variation in sensitivity to chemicals. Environ Sci Technol 48(10):5946–5954CrossRefGoogle Scholar
  40. Palma P, Palma VL, Fernandes RM, Soares AMVM, Barbosa IR (2009) Endosulfan sulphate interferes with reproduction, embryonic development and sex differentiation in Daphnia magna. Ecotoxicol Environ Saf 72:344–350CrossRefGoogle Scholar
  41. Palmquist K, Salatas J, Fairbrother A (2012) Pyrethroid insecticides: Use, environmental fate, and ecotoxicology. In: Perveen F (ed) Insecticides—advances in integrated pest management. InTech, pp 251–278Google Scholar
  42. Rico A, Van den Brink PJ (2015) Evaluating aquatic invertebrate vulnerability to insecticides based on intrinsic sensitivity, biological traits, and toxic mode of action. Environ Toxicol Chem 34:1907–1917CrossRefGoogle Scholar
  43. Rico A, Geber-Corrêa R, Campos PS, Garcia MVB, Waichman AV, Van den Brink PJ (2010) Effect of parathion-methyl on Amazonian fish and invertebrates: a comparison of sensitivity with temperate data. Arch Environ Contam Toxicol 58:765–771CrossRefGoogle Scholar
  44. Rico A, Waichman AV, Geber-Corrêa R, Van den Brink PJ (2011) Effects of malathion and carbendazim on Amazonian freshwater organisms: comparison of tropical and temperate species sensitivity distributions. Ecotoxicology 20:625–634CrossRefGoogle Scholar
  45. Rubach MN, Ashauer R, Maund SJ, Baird DJ, Van den Brink PJ (2010) Toxicokinetic variation in 15 freshwater arthropod species exposed to the insecticide chlorpyrifos. Environ Toxicol Chem 29:2225–2234CrossRefGoogle Scholar
  46. Sánchez-Bayo F (2012) Insecticides mode of action in relation to their toxicity to non-target organisms. J Environ Anal Toxicol S4:002Google Scholar
  47. Satapornvanit K, Baird DJ, Little DC (2009) Laboratory toxicity test and post-exposure feeding inhibition using the giant freshwater prawn Macrobrachium rosenbergii. Chemosphere 74(9):1209–1215CrossRefGoogle Scholar
  48. Savolainen KM, Vähäkangas K (2009) Insecticides. In: Satoh T (ed) Environmental toxicology and human health, Volume I. Eolss Publishers, Oxford, pp. 164–181Google Scholar
  49. Sucahyo D, Van Straalen NM, Kravea A, Van Gestel CAM (2008) Acute toxicity of pesticides to the tropical freshwater shrimp Caridina laevis. Ecotoxicol Environ Saf 69:421–427CrossRefGoogle Scholar
  50. Sumon KA, Rico A, Ter Horst MMS, Van den Brink PJ, Haque MM, Rashid H (2016) Risk assessment of pesticides used in rice-prawn concurrent systems in Bangladesh. Sci Total Environ 568:498–506CrossRefGoogle Scholar
  51. Van den Brink PJ, Blake N, Brock TCM, Maltby L (2006) Predictive value of species sensitivity distributions for effects of herbicides in freshwater ecosystems. Hum Ecol Risk Assess 12:645–674CrossRefGoogle Scholar
  52. Van Vlaardingen P, Traas TP, Wintersen AM, Aldenberg T (2004) ETX 2.0. A program to calculate hazardous concentrations and fraction affected, based on normally distributed toxicity data. RIVM report no. 601501028/2004, Bilthoven, The NetherlandsGoogle Scholar
  53. Van Wijngaarden RPA, Crum SJH, Decraene K, Hattink J, Van Kammen A (1998) Toxicity of derosal (active ingredient carbendazim) to aquatic invertebrates. Chemosphere 37:673–683CrossRefGoogle Scholar
  54. Van Wijngaarden RP, Maltby L, Brock TC (2015) Acute tier-1 and tier-2 effect assessment approaches in the EFSA aquatic guidance document: are they sufficiently protective for insecticides? Pest Manag Sci 71:1059–1067CrossRefGoogle Scholar
  55. Wirth EF, Lund SA, Fulton MH, Scott GI (2002) Reproductive alterations in adult grass shrimp, Palaemonetes pugio, following sublethal, chronic endosulfan exposure. Aquat Toxicol 59:93–99CrossRefGoogle Scholar
  56. Wogram J, Liess M (2001) Rank ordering of macroinvertebrate species sensitivity to toxic compounds by comparison with that of Daphnia magna. Bull. Environ Contam Toxicol 67:360–367Google Scholar
  57. Yaméogo L, Traoré K, Back C, Hougard JM, Calamari D (2001) Risk assessment of etofenprox (Vectron) on non-target aquatic fauna compared with other pesticides used as Simulium larvicide in a tropical environment. Chemosphere 42:965–974CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.DCEA/Faculty of Sciences and TechnologyNew University of LisbonCaparicaPortugal
  2. 2.NEEA/CRHEA São Carlos Engineering SchoolUniversity of São PauloSão CarlosBrazil
  3. 3.IMDEA Water InstituteScience and Technology Campus of the University of AlcaláAlcalá de HenaresSpain

Personalised recommendations