Red flag for green spray: adverse trophic effects of Bti on breeding birds

Summary 1. The expanding use of selective pest-control agents provides a unique opportunity to study food web interactions in the field while addressing major environmental issues. Bacillus thuringiensis israelensis (Bti) is the most commonly used microbial agent to control mosquitoes worldwide. 2. Using breeding house martins Delichon urbicum as a model species, we assessed the effect of Bti spraying on foraging rates and chick diet prior to and during 3 years of Bti spraying in the Camargue, France. Some 9051 feeding flights and 14 857 prey items were recorded in the early, mid and late nesting season at up to three control and three treated sites. Breeding parameters were assessed during 1 year at two control and two treated sites. 3. Intake of Nematocera (Diptera sub-order including midges and mosquitoes) and their predators (spiders and dragonflies) decreased significantly at treated sites, concurrently with increase of flying ant intake. Small prey ( 7·5 mm) at control sites, with lower foraging rates at treated sites. 4. Clutch size and fledgling survival were significantly lower at treated sites relative to control with respectively 2·3 vs. 3·2 chicks produced per nest. Breeding success was positively correlated with intake of Nematocera and their predators at the nest level. 5. No previous study has provided compelling evidence of Bti affecting vertebrate populations following the suppression of prey species. Indirect effects caused by repeated application of Bti through food web interactions warrant more attention. 6. Synthesis and applications. Bti is considered the most selective and least toxic agent currently available to control mosquitoes. Mosquito-control programmes should integrate non-biased awareness campaigns and mitigation measures balancing the social demands for mosquito reduction with the factors involved in mosquito proliferation and dispersion. Such measures could consist in improved wetland management; reduction in areas and periods of Bti spraying; consideration of alternatives to Bti spraying, such as mosquito traps; specific measures to reinforce animal populations affected by Bti; and suspension of mosquito control in environmentally sensitive areas where nature preservation is a priority.

[1]  A. Turner,et al.  Central place foraging by swallows (Hirundinidae): The question of load size , 1982, Animal Behaviour.

[2]  A. Turner.  Time and energy constraints on the brood size of swallows, Hirundo rustica, and sand martins, Riparia riparia , 1983, Oecologia.

[3]  P. Armitage,et al.  The Chironomidae: the biology and ecology of non-biting midges. , 1995 .

[4]  Tomas Jonsson,et al.  Biodiversity lessens the risk of cascading extinction in model food webs , 2000 .

[5]  D. Bryant.  BREEDING BIOLOGY OF HOUSE MARTINS DELICHON URBICA IN RELATION TO AERIAL INSECT ABUNDANCE , 2008 .

[6]  Klaas R. Westerterp,et al.  Time and energy limits to brood size in house martins (Delichon urbica) , 1983 .

[7]  R. Regal,et al.  Do mosquito control treatments of wetlands affect red‐winged blackbird (Agelaius phoeniceus) growth, reproduction, or behavior? , 1997 .

[8]  A. Margaritis,et al.  Specific Oxygen Uptake Rate Variations during Batch Fermentation of Bacillus thuringiensis Subspecies kurstaki HD‐1 , 2003, Biotechnology progress.

[9]  Kent H. Redford,et al.  The nutritional value of invertebrates with emphasis on ants and termites as food for mammals , 2009 .

[10]  A. Turner.  Food selection and the timing of breeding of the Blue‐and‐White Swallow Notiochelidon cyanoleuca in Venezuela , 2008 .

[11]  R. Relyea,et al.  Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. , 2006, Ecology letters.

[12]  D. Bryant,et al.  Energetics of growth in House martins (Delichon urbica) , 2009 .

[13]  J. Boisvert,et al.  Effects of Bacillus thuringiensis var. israelensis on Target and Nontarget Organisms: A Review of Laboratory and Field Experiments , 2000 .

[14]  L. Sopuck,et al.  Responses of songbirds to aerial spraying of the microbial insecticide Bacillus thuringiensis var. kurstaki (Foray 48B®) on Vancouver Island, British Columbia, Canada , 2002, Environmental toxicology and chemistry.

[15]  D. Bryant.  ENVIRONMENTAL INFLUENCES ON GROWTH AND SURVIVAL OF NESTLING HOUSE MARTINS DELICHON URBICA , 2008 .

[16]  S. Holm.  A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[17]  R. Mittermeier,et al.  Biodiversity hotspots for conservation priorities , 2000, Nature.

[18]  D. Bryant.  Reproductive Costs in the House Martin (Delichon urbica) , 1979 .

[19]  P. Robertson,et al.  The relationship between yellowhammer breeding performance, arthropod abundance and insecticide applications on arable farmland , 2006 .

[20]  S. Holmes.  Reproduction and nest behaviour of Tennessee warblers Vermivora peregrina in forests treated with Lepidoptera‐specific insecticides , 1998 .

[21]  L. Després,et al.  Long Lasting Persistence of Bacillus thuringiensis Subsp. israelensis (Bti) in Mosquito Natural Habitats , 2008, PloS one.

[22]  D. Bryant.  The Factors Influencing the Selection of Food by the House Martin (Delichon urbica (L.)) , 1973 .

[23]  V. Maris,et al.  From Adaptive Management to Adjustive Management: A Pragmatic Account of Biodiversity Values , 2010, Conservation biology : the journal of the Society for Conservation Biology.

[24]  Jonathan M. Chase,et al.  Trophic cascades across ecosystems , 2005, Nature.

[25]  P. Corbet.  Dragonflies: Behavior and Ecology of Odonata , 1999 .

[26]  C. Henny,et al.  FIELD STUDIES ON PESTICIDES AND BIRDS: UNEXPECTED AND UNIQUE RELATIONS , 1997 .

[27]  J. P. Mccarty,et al.  Foraging ecology and diet selectivity of tree swallows feeding nestlings , 1999 .

[28]  S. Jenni-Eiermann,et al.  Recognizability of different food types in faeces and in alimentary flushes of Sylvia warblers , 2008 .

[29]  D. Batzer,et al.  Ecology of insect communities in nontidal wetlands. , 1996, Annual review of entomology.

[30]  A. Turner.  Optimal foraging by the swallow (Hirundo rustica, L): Prey size selection , 1982, Animal Behaviour.

[31]  J. Margalit,et al.  A bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex univitattus, Aedes aegypti and Culex pipiens [Insect pests] , 1977 .

[32]  D. Bryant,et al.  Barn swallows Hirundo rustica form eggs mainly from current food intake , 2006 .

[33]  C. D. Ankney,et al.  Prey Size Selection by Tree Swallows , 1985 .