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Effects of Bacillus thuringiensis var. israelensis on nonstandard microcrustacean species isolated from field zooplankton communities

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Abstract

The toxicity of Bacillus thuringiensis var. israelensis on zooplanktonic microcrustaceans was evaluated using individuals collected in coastal wetlands where this larvicide has been used for mosquito control over the last decades. We tested five zooplankton species that coexist with mosquito larvae: two copepods (both nauplii and adults of Tropocyclops prasinus and Acantocyclops americanus), and three cladocerans (Ceriodaphnia reticulata, Chydorus sphaericus, and Daphnia cf. pulex). Our experiments included seven replicates of six concentrations (Bti Vectobac12AS 1200 Bti ITU/mg): 0, 5, 25, 50, 250, and 500 mg L−1. We analyzed acute and sub-chronic effects after a single inoculation. Despite the high variability of responses among our tested organisms, we found a general pattern of increasing mortality with concentration and time. We conclude that negative effects at the community level are not unlikely as some species were affected at doses close to those used in field applications.

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References

  • Aguilar-Alberola JA, Mesquita-Joanes F (2013) Acute toxicity tests with cadmium, lead, sodium dodecyl sulfate, and Bacillus thuringiensis on a temporary pond ostracod. Internat Rev Hydrobiol 97:375–388. doi:10.1002/iroh.201211497

    Article  Google Scholar 

  • Akçakaya HR, Stark JD, Bridges TS (2008) Demographic toxicity methods in ecological risk assessment. Oxford University Press, New York

    Google Scholar 

  • Ali A (1981) Bacillus thuringiensis serovar israelensis (ABG-6108) against chironomids and some nontarget aquatic invertebrates. J Invert Pathol 38:264–272. doi:10.1016/0022-2011(81)90132-4

    Article  Google Scholar 

  • Alonso M (1996) Fauna Ibérica. Crustacea. Branquiopoda. CSIC, Madrid

    Google Scholar 

  • Antón-Pardo M, Armengol X (2010) Zooplankton community from restored peridunal ponds in the Mediterranean region (L’Albufera Natural Park, Valencia, Spain). Limnetica 29:133–143. ISSN: 0213-8409

    Google Scholar 

  • Baldacchino F, Caputo B, Chandre F, Drago A, della Torre A, Montarsi F, Rizzoli A (2015) Control methods against invasive Aedes mosquitoes in Europe: a review. Pest Manag Sci 71:1471–1485. doi:10.1002/ps.4044

    Article  CAS  Google Scholar 

  • 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. doi:10.1046/j.1365-2435.2000.00445.x

    Article  Google Scholar 

  • Barata C, Baird DJ, Soares AMVM, Guilhermino L (2001) Biochemical factors contributing to response variation among resistant and sensitive clones of Daphnia magna Straus exposed to ethyl parathion. Ecotox Environ Saf 49:155–163. doi:10.1006/eesa.2001.2052

    Article  CAS  Google Scholar 

  • Becker N, Margalit J (1993) Use of Bacillus thuringiensis israelensis against mosquitoes. In: Entwistle PF, Cory JS, Bailey MJ, Higgs S (eds) Bacillus thuringiensis, an environmental biopesticide: theory and practice. John Wiley & Sons Ltd., New York. pp 147–170.

  • Becker N, Petrić D, Zgomba M, Boase C, Dahl C, Madon M, Kaiser A (2010) Mosquitoes and their control, 2nd edn. Springer, Heidelberg, doi:10.1007/978-3-540-92874-4

    Book  Google Scholar 

  • Blaustein L, Margalit J (1991) Indirect effects of the fairy shrimp, Branchipus schaefferi and 2 ostracod species on Bacillus thuringiensis var israelensis induced mortality in mosquito larvae. Hydrobiologia 212:67–76. In: Belk, D, Dumont HJ, Munuswamy N (eds) Studies on large branchiopod biology and aquaculture. Springer, Netherlands. pp. 67–76

    Article  Google Scholar 

  • Blaustein L, Margalit J (1994) Differential vulnerability among mosquito species to predation by the cyclopoid copepod, Acanthocyclops viridis. Israel J Zool 40:55–60. doi:10.1080/00212210.1994.10688734

    Google Scholar 

  • Blaustein L, Chase JM (2007) The role of species sharing the same trophic level as mosquitoes on mosquito populations. Annu Rev Entomol 52:489–507. doi:10.1146/annurev.ento.52.110405.091431

    Article  CAS  Google Scholar 

  • 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. doi:10.1080/095831500750016361

    Article  Google Scholar 

  • Boisvert J, Lacoursière JO (2004) Le Bacillus thuringiensis israelensis et le contrôle des insectes piqueurs au Québec, Québec, ministère de l’Environnement, Envirodoq no ENV/2004/0278. document préparé par l’Université du Québec à Trois-Rivières pour le ministère de l’Environnement du Québec, p. 101

  • Caquet Th, Roucaute M, Le Goff P, Lagadic L (2011) Effects of repeated field applications of two formulations of Bacillus thuringiensis var. israelensis on non-target salt marsh invertebrates in Atlantic coastal wetlands. Ecol Environ Saf 74:1122–1130. doi:10.1016/j.ecoenv.2011.04.028

    Article  CAS  Google Scholar 

  • Charbonneau C, Drobney RD, Rabeni CF (1994) Effects of Bacillus thuringiensis var. israelensis on non target benthic organisms in a lotic habitat and factors affecting the efficacy of the larvicide. Environ Toxicol Chem 13:267–279. doi:10.1002/etc.5620130211

    Article  CAS  Google Scholar 

  • Dickman M (2000) Impacts of a mosquito selective pesticide, Bti, on the macroinvertebrates of a subtropical stream in Hong Kong. Chemosphere 41:209–217. doi:10.1016/S0045-6535(99)00413-0

    Article  CAS  Google Scholar 

  • Duchet C, Larroque M, Caquet T, 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. doi:10.1016/j.chemosphere.2008.09.024

    Article  CAS  Google Scholar 

  • Duchet C, Coutellec MA, Franquet E, Lagneau C, Lagadic L (2010a) 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. doi:10.1007/s10646-010-0507-y

    Article  CAS  Google Scholar 

  • Duchet C, Caquet T, Franquet E, Lagneau C, Lagadic L (2010b) 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. doi:10.1016/j.envpol.2009.11.008

    Article  CAS  Google Scholar 

  • Duchet C, Tetreau G, Marie A, Rey D, Besnard G, Perrin Y, Paris M, David JP, Lagneau C, Després L (2014) Persistence and recycling of bioinsecticidal Bacillus thuringiensis subsp. israelensis spores in contrasting environments: evidence from field monitoring and laboratory experiments. Microb Ecol 67:576–586. doi:10.1007/s00248-013-0360-7

    Article  CAS  Google Scholar 

  • Dussart B (1969) Les copépodes des eaux continentales d’Europe Occidentale. Tome II: Cyclopoïdes et Biologie. Centre National de la Recherche Scientifique

  • Freitas EC, Rocha O (2011) Acute and chronic effects of sodium and potassium on the tropical freshwater cladoceran Pseudosida ramosa. Ecotoxicology 20:88–96. doi:10.1007/s10646-010-0559-z

    Article  CAS  Google Scholar 

  • 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. doi:10.1007/s00248-005-0247-3

    Article  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics. Palaeontol Electron 4: 9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm

  • Hershey AE, Lima AR, Niemi GJ, Regal RR (1998) Effects of Bacillus thuringiensis israelensis (BTI) and methoprene on nontarget macroinvertebrates in Minnesota wetlands. Ecol Appl 8:41–60. doi:10510761/10510761(1998)008[0041:EOBTIB]2.0.CO;2

    Article  Google Scholar 

  • Hoffman DJ, Rattner BA, Burton Jr GA, Cairns Jr J (eds) (2002) Handbook of ecotoxicology. CRC Press, Boca Raton.

  • Jeppesen E, Nõges P, Davidson TA, Haberman J, Nõges T, Blank K, Amsinck SL (2011) Zooplankton as indicators in lakes: a scientific-based plea for including zooplankton in the ecological quality assessment of lakes according to the European Water Framework Directive (WFD). Hydrobiologia 676:279–297. doi:10.1007/s10750-011-0831-0

    Article  CAS  Google Scholar 

  • Kallapur VL, Mayes ME, Edens FW, Held GA, Dauterman WC, Kawanishi CY, Roe RM (1992) Toxicity of the crystalline polypeptides of Bacillus thuringiensis subsp. israelensis in Japanese quail. Pest Biochem Physiol 44:208–216. doi:10.1016/0048-3575(92)90091-D

    Article  CAS  Google Scholar 

  • Kroeger I, Duquesne S, Liess M (2013a) Crustacean biodiversity as an important factor for mosquito larval control. J Vector Ecol 38:390–400. doi:10.1111/j.1948-7134.2013.12055.x

    Article  Google Scholar 

  • Kroeger I, Liess M, Dziock F, Duquesne S (2013b) Sustainable control of mosquito larvae in the field by the combined actions of the biological insecticide Bti and natural competitors. J Vector Ecol 38:82–89. doi:10.1111/j.1948-7134.2013.12012.x

    Article  Google Scholar 

  • Lagadic L, Roucaute M, Caquet T (2014) Bti sprays do not adversely affect non-target aquatic invertebrates in French Atlantic coastal wetlands. J Appl Ecol 51:102–113. doi:10.1111/1365-2664.12165

    Article  Google Scholar 

  • Lima JBP, Melo NVD, Valle D (2005) Persistence of Vectobac WDG and Metoprag S-2G against Aedes aegypti larvae using a semi-field bioassay in Rio de Janeiro, Brazil. Rev Inst Med Trop S Paulo 47:7–12. doi:10.1590/S0036-46652005000100002

    Article  Google Scholar 

  • Mano H, Sakamoto M, Tanaka Y (2010) A comparative study of insecticide toxicity among seven cladoceran species. Ecotoxicology 19:1620–1625. doi:10.1007/s10646-010-0547-3

    Article  CAS  Google Scholar 

  • Margalef R (1983) Limnología. Omega, Barcelona, p 1010

    Google Scholar 

  • Marten GG, Reid JW (2007) Cyclopoid copepods. J Am Mosq Control Assoc 23:65–92. doi:10.2987/8756-971X

    Article  Google Scholar 

  • Merritt RW, Walker ED, Wilzbach MA, Cummins KW, Morgan WT (1989) A broad evaluation of B.t.i. for black fly control in a Michigan river: Efficacy, carry and non-target effects on invertebrates and fish. J Mosq Contr Assoc 5:397–415. ISSN: 8756-971X

    CAS  Google Scholar 

  • Mulla MS (1991) Biological control of mosquitoes with entomopathogenic bacteria. Chin J Entomol 6:93–104. doi: 140.112.100.36

    Google Scholar 

  • Narasaiah J, Jamil K (1986) Preliminary studies on biological control of mosquito larvae using B.thuringiensis and B. sphaericus. Entomon. 11:187–192. ISSN 0377-9335

    Google Scholar 

  • 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. doi:10.1002/etc.5620180325

    Article  CAS  Google Scholar 

  • Olmo C, Armengol X, Ortells R (2012) Re-establishment of zooplankton communities in temporary ponds after autumn flooding: does restoration age matter? Limnologica 42:310–319. doi:10.1016/j.limno.2012.08.005

    Article  Google Scholar 

  • Onandia G, Miracle MR, Blasco C, Vicente E (2014) Diel and seasonal variations in bacterioplankton production in a hypertrophic shallow lagoon. Aquat Ecol 48:447–463. doi:10.1007/s10452-014-9497-9

    Article  CAS  Google Scholar 

  • Poulin B (2012) Indirect effects of bioinsecticides on the nontarget fauna: the Camargue experiment calls for future research. Acta Oecol 44:28–32. doi:10.1016/j.actao.2011.11.005

    Article  Google Scholar 

  • Purcell BH (1981) Effects of Bacillus thuringiensis var. israelensis on Aedes taeniorhynchus and some nontarget organisms in the salt marsh. Mosq News 41:476–484

    Google Scholar 

  • Quintana, X, Comín, FA (1993) Modificaciones de las relaciones tróficas en marismas tras la aplicación de insecticidas. Actas VI Congreso Español de Limnología 141–148

  • Rydzanicz K, Sobczyński M, Guz-Regner K (2010) Comparison of activity and persistence of microbial insecticides based on Bacillus thuringiensis israelensis and Bacillus sphaericus in organicly polluted mosquito-breeding sites. Pol J Environ Stud 19:1317–1323

    Google Scholar 

  • Russell TL, Brown MD, Purdie DM, Ryan PA, Kay BH (2003) Efficacy of VectoBac (Bacillus thuringiensis variety israelensis) formulations for mosquito control in Australia. J Econ Entomol 96:1786–1791. doi:10.1093/jee/96.6.1786

    Article  Google Scholar 

  • Russell TL, Kay BH (2008) Biologically based insecticides for the control of immature Australian mosquitoes: a review. Aust J Entomol 47:232–242. doi:10.1111/j.1440-6055.2008.00642.x

    Article  Google Scholar 

  • Siegel JP (2001) The mammalian safety of Bacillus thuringiensis based insecticides. J Invertebr Pathol 77:13–21. doi:10.1006/jipa.2000.5000

    Article  CAS  Google Scholar 

  • Su T, Mulla MS (2005) Toxicity and effects of microbial mosquito larvicides and larvicidal oil on the development and fecundity of the tadpole shrimp Triops newberryi (Packard) (Notostraca: Triopsidae). J Vect Ecol 30:107–114. doi:10.1111/jvec.12109

    Google Scholar 

  • Tietze NS, Hester PG, Shaffer KR, Prescot SJ, Schreiber ET (1994) Integrated management of waste tire mosquitoes utilizing Megacyclops longisetus (Copepoda: Cyclopidae), Bacillus thuringiensis var. israelensis, Bacillus sphaericus and methoprene. J Am Mosq Control Assoc 10:363–373. ISSN 8756-971X

    CAS  Google Scholar 

  • Toumi H, Boumaiza M, Millet M, Radetski CM, Camara BI, Felten V, Ferard JF (2015) Investigation of differences in sensitivity between 3 strains of Daphnia magna (crustacean Cladocera) exposed to malathion (organophosphorous pesticide). J Environ Sci Heal B 50:34–44. doi:10.1080/03601234.2015.965617

    Article  CAS  Google Scholar 

  • USEPA (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. U.S. Environmental Protection Agency. EPA-821-R-02-012.

  • 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. doi:10.1007/s10750-009-9911-9

    Article  Google Scholar 

  • 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. ISSN: 8756-971X

    CAS  Google Scholar 

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Acknowledgments

We are grateful to the Albufera Natural Park and Valencia City Hall technical office for their permission to sample. J. Rueda-Sevilla advised us on Bti application. We also acknowledge Arietellus for English improvement and three anonymous reviewers for helpful comments. This study was supported by the Spanish Ministry of Science and Innovation (Project CGL2008-03760). C. Olmo has an FPI grant from the Spanish Ministry of Science and Innovation (grant: BES-2009-018518).

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Olmo, C., Marco, A., Armengol, X. et al. Effects of Bacillus thuringiensis var. israelensis on nonstandard microcrustacean species isolated from field zooplankton communities. Ecotoxicology 25, 1730–1738 (2016). https://doi.org/10.1007/s10646-016-1708-9

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