Abstract
Because exposure to toxicants not only results in mortality but also in multiple sublethal effects, the use of life-table data appears particularly suitable to assess global effects on exposed populations. The present study uses a life table response approach to assess population-level effects of two insecticides used against mosquito larvae, spinosad (8 μg/l) and Bacillus thuringiensis var. israelensis (Bti, 0.5 μl/l), on two non target species, Daphnia pulex and Daphnia magna (Crustacea: Cladocera), under laboratory versus field microcosms conditions. Population growth rates were inferred from life table data and Leslie matrices under a model with resource limitation (ceiling). These were further used to estimate population risks of extinction under each tested condition, using stochastic simulations. In laboratory conditions, analyses performed for each species confirmed the significant negative effect of spinosad on survival, mean time at death, and fecundity as compared to controls and Bti-treated groups; for both species, population growth rate λ was lower under exposure to spinosad. In field microcosms, 2 days after larvicide application, differences in population growth rates were observed between spinosad exposure conditions, and control and Bti exposure conditions. Simulations performed on spinosad-exposed organisms led to population extinction (minimum abundance = 0, extinction risk = 1), and this was extremely rapid (time to quasi-extinction = 4.1 one-week long steps, i.e. one month). Finally, D. magna was shown to be more sensitive than D. pulex to spinosad in the laboratory, and the effects were also detectable through field population demographic simulations.
Similar content being viewed by others
References
ACTA (2009) Index phytosanitaire. Association de Coordination Technique Agricole, Paris
AFNOR (1980) Détermination de l’inhibition de croissance de Scenedesmus subspicatus par une substance. Norme expérimentale T 90–304
Akçakaya HR (2005) RAMAS metapop: viability analysis for stage-structured metapopulations (version 5.0). Applied biomathematics, Setauket, New-York
Akçakaya HR, Stark JD, Bridges TS (2008) Demographic toxicity––methods in ecological risk assessment. Oxford University Press, New York
Ali A (1981) Bacillus thuringiensis serovar israelensis (ABG-6108) against chironomids and some nontarget aquatic invertebrates. J Invert Pathol 38:264–272
Amoros C (1984) Crustacés Cladocères. Bull Mens Soc Linn Lyon 53:72–145
Barata C, Baird DJ, Amat F, Soares AMVM (2000) Comparing population response to contaminants between laboratory and field: an approach using Daphnia magna ephippial egg banks. Funct Ecol 14:513–523
Barnes PB, Chapman MG (1998) Effects of the larvicide (Vectobac) on assemblages of benthic invertebrates in Bicentennial Park. Centre for Research on Ecological Impacts of Coastal Cities, Sydney
Begon M, Townsend CR, Harper JL (2006) Ecology from individuals to ecosystems, 4th edn. Blackwell Publishing Ltd
Beketov MA, Liess M (2005) Acute contamination with esfenvalerate and food limitation: chronic effects on the mayfly, Cloeon dipterum. Environ Toxicol Chem 24:1281–1286
Beketov MA, Liess M (2006) The influence of predation on the chronic response of Artemia sp. populations to a toxicant. J Appl Ecol 43:1069–1074
Blaustein L, Chase JM (2007) Interactions between mosquito larvae and species that share the same trophic level. Annu Rev Entomol 52:489–507
Bøhn T, Primiciero R, Henssen DO, Traavik T (2008) Reduced fitness of Daphnia magna fed a Bt-transgenic maize variety. Arch Environ Contam Toxicol 55:584–592
Bøhn T, Traavik T, Primiciero R (2010) Demographic responses in Daphnia magna fed transgenic Bt-maize. Ecotoxicology 19:419–430
Boisvert M, Boisvert J (2000) Effects of Bacillus thuringiensis var. israelensis on target and non target organisms: a review of laboratory and field experiments. Biocont Sci Tech 10:517–561
Boisvert J, Lacoursière JO (2004) Le Bacillus thuringiensis et le contrôle des insectes piqueurs au Québec. Ministère de l’Environnement Québécois, Québec
Boronat MD, Miracle MR (1997) Size distribution of Daphnia longispina in the vertical profile. Hydrobiologia 360:187–196
Brown RJ, Rundle SD, Hutchinson TH, Williams TD, Jones MB (2003) A copepod life-cycle test and growth model for interpreting the effects of lindane. Aquat Toxicol 63:1–11
Canton JH, Adema DMM (1978) Reproducibility of short-term and reproduction toxicity experiments with Daphnia magna and comparison of the sensitivity of Daphnia magna with Daphnia pulex and Daphnia cucullata in short-term experiments. Hydrobiologia 59:135–140
Caswell H (2001) Matrix population models. Sinauer, Sunderland
Cleveland CB, Bormett GA, Saunders DG, Powers FL, McGibbon AS, Reeves GL, Rutherford L, Balcer JL (2002) Environmental fate of spinosad. 1. Dissipation and degradation in aqueous systems. J Agric Food Chem 50:3244–3256
Consoli FL, Botelho PSM, Parra JRP (2001) Selectivity of insecticides to the egg parasitoid Trichogramma galloi Zucchi, 1988 (Hym. Trichogrammatidae). J Appl Entomol 125:37–43
Coutellec MA, Delous G, Cravedi JP, Lagadic L (2008) Effects of the mixture of diquat and a nonylphenol polyethoxylate adjuvant on fecundity and progeny early performances of the pond snail Lymnaea stagnalis in laboratory bioassays and microcosms. Chemosphere 73:326–336
Crawley MJ (2007) The R book. John Wiley and Sons Ltd
Crouse GD, Sparks TC, Schoonover J, Gifford J, Dripps J, Bruce T, Larson L, Garlich J, Hatton C, Hill RL, Worden TV, Martynow JG (2001) Recent advances in the chemistry of spinosyns. Pest Manag Sci 57:177–185
Duchet C, Larroque M, Caquet Th, Franquet E, Lagneau C, Lagadic L (2008) Effects of spinosad and Bacillus thuringiensis israelensis on a natural population of Daphnia pulex in field microcosms. Chemosphere 74:70–77
Duchet C, Caquet Th, Franquet E, Lagneau C, Lagadic L (2010) Influence of environmental factors on the response of a natural population of Daphnia magna (Crustacea: Cladocera) to spinosad and Bacillus thuringiensis israelensis in Mediterranean coastal wetlands. Environ Pollut 158:1825–1833
Forbes VE (1999) Genetics and ecotoxicology. Taylor and Francis, Philadelphia
Forbes VE, Calow P (1999) Is the per capita rate of increase a good measure of population-level effects in ecotoxicology? Environ Toxicol Chem 18:1544–1556
Forbes VE, Calow P, Sibly RM (2001) Are current species extrapolation models a good basis for ecological risk assessment? Environ Toxicol Chem 20:442–447
Forbes VE, Sibly RM, Linke-Gamenick I (2003) Joint effects of population density and toxicant exposure on population dynamics of Capitella sp. I. Ecol Appl 13:1094–1103
Gill SS, Cowles EA, Pietrantonio PV (1992) The mode of action of Bacillus thuringiensis endotoxins. Annu Rev Entomol 37:615–636
Hajaij M, Carron A, Deleuze J, Gaven B, Setier-Rio M-L, Vigo G, Thiéry I, Nielsen-LeRoux C, Lagneau C (2005) Low persistence of Bacillus thuringiensis serovar israelensis spores in four mosquito biotopes of a salt marsh in southern France. Microb Ecol 50:475–487
Hanazato T, Hirokawa H (2004) Changes in vulnerability of Daphnia to an insecticide application depending on the population phase. Freshwater Biol 49:402–409
Hershey AE, Shannon L, Axler R, Ernst C, Mickelson P (1995) Effects of methoprene and Bti (Bacillus thuringiensis var. israelensis) on non-target insects. Hydrobiologia 308:219–227
Hershey AE, Lima AR, Niemi GJ, Regal RR (1998) Effects of Bacillus thuringiensis israelensis (Bti) and methoprene on non-target macroinvertebrates in Minnesota wetlands. Ecol Appl 8:41–60
Hood GM (2006) PopTools version 2.7.5. http://cse.csiro.au/poptools
Jensen A, Forbes V, Parker ED Jr (2001) Variation in cadmium uptake, feeding rate, and life histories effects in the gastropod Potamopyrgus antipodarum: linking toxicant effects on individuals to the population level. Environ Toxicol Chem 20:2503–2513
Kammenga J, Laskowski R (2000) Demography in ecotoxicology. John Wiley and Sons, Chichester, UK
Kim J, Park J, Kim PG, Lee C, Choi K, Choi K (2010) Implication of global environmental changes on chemical toxicity-effect of water temperature, pH, and ultraviolet B irradiation on acute toxicity of several pharmaceuticals in Daphnia magna. Ecotoxicology 19:662–669
Kondo S, Ohba M, Ishii T (1992) Larvicidal activity of Bacillus thuringiensis serovar israelensis against nuisance chironomid midges (Diptera: Chironomidae) of Japan. Lett Appl Microbiol 15:207–209
Kramarz P, Zwolak M, Laskowski R (2005) Effect of interaction between density dependence and toxicant exposure on population growth rate of the potworm Enchytraeus doerjesi. Environ Toxicol Chem 24:537–540
Liber K, Schmude KL, Rau DM (1998) Toxicity of Bacillus thuringiensis var. israelensis to chironomids in pond mesocosms. Ecotoxicology 7:343–354
Liess M (2002) Population response to toxicants is altered by intraspecific interaction. Environ Toxicol Chem 21:138–142
Lilius H, Hästbacka T, Isomaa B (1995) A comparison of the toxicity of 30 reference chemicals to Daphnia magna and Daphnia pulex. Environ Toxicol Chem 14:2085–2088
Lüning-Krizan J (1997) Selective feeding of third- and fourth-instar larvae of Chaoborus flavicans in the field. Arch Hydrobiol 140:347–365
Mauri M, Barladi E, Simonini R (2003) Effects of zinc exposure on the polychaete Dinophilus gyrociliatus: a life-table response experiment. Aquat Toxicol 65:63–100
Miles M, Dutton R (2000) Spinosad: a naturally derived insect control agent with potential use in glasshouse integrated pest management systems. Meded Fac Landbouwkundige Toegepaste Biol Wet Univ Gent 65:393–400
Miura T, Takahashi RM, Mulligan FS III (1981) Impact of the use of candidate bacterial mosquito larvicides on some selected aquatic organisms. In: CMC Association (ed) Proceeding annual conference of the californian mosquito control association, pp 45–48
Mulla MS, Federici BA, Darwazeh HA (1982) Larvicidal efficacy of Bacillus thuringiensis ser. H-14 against stagnant-water mosquitoes and its effects on nontarget organisms. Environ Entomol 11:788–795
Nasreen A, Ashfaq M, Mustafa G (2000) Intrinsic toxicity of some insecticides to egg parasitoid Trichogramma chilonis (Hym. Trichogrammatidae). Bull Inst Trop Agr Kyushu Univ 23:41–44
Niemi GJ, Hershey AE, Shannon L, Hanowski JM, Lima A, Axler RP, Regal RR (1999) Ecological effects of mosquito control on zooplankton, insects, and birds. Environ Toxicol Chem 18:549–559
Organisation for Economic Cooperation and Development (1998) Daphnia magna reproduction test. OECD guidelines for testing of chemicals
Pieters BJ, Liess M (2006) Population developmental stage determines the recovery potential of Daphnia magna populations after fenvalerate application. Environ Sci Technol 40:6157–6162
Ping L, Wen-Ming Z, Shui-Yun Y, Jin-Song Z, Li-Jun L (2005) Impact of environmental factors on the toxicity of Bacillus thuringiensis var. israelensis IPS82 to Chironomus kiiensis. J Am Mosq Control Assoc 21:59–63
R Development Core Team (2009). R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org
Rey D, Long A, Pautou MP, Meyran JC (1998) Comparative histopathology of some Diptera and Crustacea of aquatic alpine ecosystems, after treatment with Bacillus thuringiensis var. israelensis. Entomol Exp Appl 88:255–263
Rohr JR, Elskus AA, Shepherd BS, Crowley PH, McCarthy TM, Niedzwiecki JH (2004) Multiple stressors and salamanders: effects of an herbicide, food limitation, and hydroperiod. Ecol Appl 14:1028–1040
Roucaute M, Quemeneur A (2007) Echantillonnage de la colonne d’eau dans les écosystèmes aquatiques peu profonds. Les Cahiers Tech de l’INRA 60:5–10
Salgado VL (1998) Studies on the mode of action of spinosad: insect symptoms and physiological correlates. Pestic Biochem Physiol 60:91–102
Sanchez M, Ferrando MD, Sancho E, Andreu E (2000) Physiological perturbations in several generations of Daphnia magna Straus exposed to diazinon. Ecotoxicol Environ Safe 46:87–94
Saunders DG, Bret BL (1997) Fate of spinosad in the environment. Down Earth 52:14–20
Southwood TRE, Henderson PA (2000) Ecological methods. Blackwell Science, Oxford, UK
Sprent P, Ley J trad (1992) Pratique des statistiques non paramétriques. INRA Éditions
Stark JD (2008) Water flea Daphnia pulex: population recovery after pesticide exposure. In: Akçakaya HR, Stark JD, Bridges TS (eds) Demographic toxicity––methods in ecological risk assessment. Oxford University Press, New-York, pp 143–151
Stark JD, Banken JAO (1999) Importance of population structure at the time of toxicant exposure. Ecotoxicol Environ Safe 42:282–287
Stark JD, Banks JE (2003) Population-level effects of pesticides and other toxicants on arthropods. Annu Rev Entomol 48:505–519
Stark JD, Vargas RI (2003) Demographic changes in Daphnia pulex (Leydig) after exposure to the insecticides spinosad and diazinon. Ecotoxicol Environ Safe 56:334–338
Stark JD, Sugayama RL, Kovalesky A (2007) Why demographic and modelling approaches should be adopted for estimating the effects of pesticides on biocontrol agents. Biocontrol 52:365–374
Stearns SC (1992) The evolution of life histories. Oxford University Press, New-York
Stebbing ARD (1982) Hormesis––the stimulation of growth by low-levels of inhibitors. Sci Total Environ 22:213–234
Tillman PG, Mulrooney JE (2000) Effects of selected insecticides on the natural enemies Coleomegilla maculata and Hippodamia convergens (Coleoptera: Coccinellidae), Geocoris punctipes (Hemiptera: Lygaeidae), and Bracon mellitor, Cardiochiles nigriceps, and Cotesia marginiventris (Hymenoptera: Braconidae) in cotton. J Econ Entomol 93:1638–1643
Vinnersten TZP, Lundström JO, Petersson E, Landin J (2009) Diving beetles assemblages of flooded wetlands in relation to time, wetland type and Bti-based mosquito control. Hydrobiologia 635:189–203
Walthall WK, Stark JD (1999) The acute and chronic toxicity of two xanthene dyes, fluorescein sodium salt and phloxine B, to Daphnia pulex. Environ Pollut 104:207–215
Watson GB (2001) Actions of insecticidal spinosyns on gamma-aminobutyric acid responses from small-diameters cockroach neurons. Pestic Biochem Physiol 71:20–28
Whalon ME, Wingerd BA (2003) Bt: mode of action and use. Arch Insect Biochem Physiol 54:200–211
WHO (2007) Spinosad. World Health Organization, Geneva, Switzerland
Widarto TH, Krogh PH, Forbes VE (2007) Nonylphenol stimulates fecundity but not population growth rate(λ) in Folmosia candida. Ecotoxicol Environ Safe 67:369–377
Yousten A, Genthner F, Benfield E (1992) Fate of Bacillus sphaericus and Bacillus thuringiensis serovar israelensis in the aquatic environment. J Am Mosq Control Assoc 8:143–148
Acknowledgements
Financial support for this work was provided by the French Ministry for Ecology, Sustainable Development and Spatial Planning through the National Programme for Ecotoxicology (PNETOX). The authors wish to thank Dow AgroSciences for the generous gift of Conserve® 120SC, Mr. Girand and Mr. Defois for giving access to the study sites, and Thierry Caquet for valuable discussions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Duchet, C., Coutellec, MA., Franquet, E. et al. Population-level effects of spinosad and Bacillus thuringiensis israelensis in Daphnia pulex and Daphnia magna: comparison of laboratory and field microcosm exposure conditions. Ecotoxicology 19, 1224–1237 (2010). https://doi.org/10.1007/s10646-010-0507-y
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-010-0507-y