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Efficacy of Clostridium Bifermentans Serovar Malaysia on Target and Nontarget Organisms

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Efficacy of Clostridium Bifermentans Serovar Malaysia on Target and Nontarget Organisms Journal of the American Mosquito Control Association, lO(I):51-55,1994 Copyright @ 1994 by the American Mosquito Control Association, Inc. EFFICACY OF CLOSTRIDIUM BIFERMENTANS SEROVAR MALAYSIA ON TARGET AND NONTARGET ORGANISMS M. YIALLOUROS,T V. STORCH,: I. THIERYT erp N. BECKERI ABSTRACT. Clostridium bifermentansserovar malaysia (C.b.m.) is highly toxic to mosquito larvae. In this study, the following aquatic nontarget invertebrateswere treated with high C.b.,,?.concentrations (up to 1,600-fold the toxic concentration for Anophelesstephensi) to study their susceptibility towards the bacterial toxrn: Planorbis planorbis (Pulmonata); Asellus aquaticzs (Isopoda); Daphnia pulex (Cla- docera);Cloeon dipterun (Ephemeroptera);Plea leachi (Heteroptera);and Eristalis sp., Chaoboruscrys' tallinus, Chironomus thummi, and Psychodaalternata (Diptera). In addition, bioassayswere performed with mosquito Larvae(Aedes aegypti, Anopheles stephensi, and Culex pipiens). Psychodaalternatalamae were very susc€ptible,with LCro/LCro values comparable to those of mosquito larvae (about 103-105 spores/ml). The tests with Chaoboruscrystallinus larvae showed significant mortality rates at high con- centrations,but generallynot before 4 or 5 days after treatment. The remaining nontargetorganisms did not show any susceptibility.The investigation confirms the specificityof C.b.m.lo nematocerousDiptera. INTRODUCTION strains of Aedesaegypti (Linn ) larvae, which are about I 0 times lesssensitiv e than A nophe I e s. The For several years, 2larvicidal bacteia, Bacil- LCr' (48 h) rangesfrom 5 x 103to 2 x lOscells/ lus thuringiensls Berliner var. israelensis (B.t.i.) ml (Thiery et al. 1992b).Larvae of Simulium and Bacillus sphaericus Neide, have been used speciesseem to be less susceptible(de Barjac et successfully for mosquito and blackfly control all al. 1990).Toxicity was not found for lepidop- over the world. Nevertheless, in consideration of teran, coleopteran, and dipteran (Brachycera) the increasing resistance to chemical insecticides larvae or for Biomphalaria glabrata Say snails and the need for alternative control agents (Gastropoda) (Thiery et al. 1992b). The safety (Anonymous 1987), there has been an ongoing for vertebrateswas demonstratedby a classical search for new mosquitocidal pathogens (Thiery seriesoftests recommendedby the World Health et al. 1992b). Organization (Thiery et al. 1992a). About 3 years ago, a Clostridium bifermentans Our objective was to extend the investigations Weinberg and Seguin strain toxic to mosquito concerning specificity and thus environmental and blackfly larvae was isolated from soil sam- compatibility of the bacterial toxin(s) by study- ples of a Malaysian mangrove swamp. Further ing possiblee ffects of C.b. m. on severalnontarget characterization and the existence of a specific organismsthat inhabit the larval habitatsofmos- H-antigen allowed it to be individualized as a quitoes and would, therefore, be directly con- serovar-malaysia(C.b.m.). It is the first strictly cernedby mosquito control operations.The se- pathogen anaerobic mosquitocidal that has been lection of the nontarget organismswas made in (de characterized Barjac et al. 1990). respectto their significanceand frequencyin the The larvicidal activity of C.b.m. is closely habitat. Another aspectof selection was the re- partly linked to the sporulation stage and is due presentationof different systematicgroups of or- to the existence of parasporal inclusion bodies ganisms and different feeding strategies. (Charles et al. 1990, de Barjac et al. 1990). The toxic proteins have not yet been clearly charac- terized, but they are very different from B.l.i. and MATERIAL AND METHODS B. sphaericus crystal toxins (Nicolas et al. I 993). Bacterial culture: The C.b.m. was grown un- The determination of the host range shows a der anaerobic.conditionsas describedin Nicolas specificity for larvae of the Culicidae and the et al. (1990)and wasstopped at t, ofsporulation Simuliidae. Susceptibility varies according to the (16 h culture).A lyophilizedpreparation ofthis mosquito species, wit}:, Anopheles species being whole culture (700/ocells contained spores,spore the most susceptible, followed by Culex and all density: 1.6 x 108spores/ml) was used for all assays.The sample was suspendedin deionized water prior The I to the start ofthe tests. suspen- German Mosquito Control Association(K.A.B.S.), sion was either used immediately or frozen in LudwigstraBe99, D-67 165 Waldsee,Germany. aliquots at -2O"C to prevent a loss of toxicity. 2 University of Heidelberg (ZoologielMorphologie gained l), Im Neuenheimer Feld 230, D-6912O Heidelberg, Appropriate concentrationswere by fur- Germany. ther dilution of the whole culture. 3 Unit6 des Bact6ries Entomopathog6nes,Institut Bioassaysof mosquitolarvae: a) Culicini lar- Pasteur,25 Rue du Docteur Roux, 75724 Paris Cedex vae: Laboratory-reared larvae of Ae. aegypti 15, France. (strain Bora-Bora) and Culex pipiens Linn. were 5l 52 Jounxer or nrE AunruceN Moseurro Cor.rrnol Assocr,q,rroN Table l. Larvicidal activity of Clostridium bifermentans ser. malaysia on Culicidae larvae and on other Nematocera (Diptera). Species LC5o(24 h)l LCeo (24 h) LCso (48 h) LC,o (48 h) Aedesaegypti 600 20.2 + 1r.32 143+ 8l 10.9+ 7.9 42.7 + 20.8 (Bora-Bora) 3.2+ 1.83 22.9+ t3 1.7+ 1.2 6.9+ 3.4 Anophelesstephensi 420 1.63.4 7.8 0.5 1.8 An. stephensi 525 0.7 + 0.2t.s 1.6+ 0.3 0.4+0 l.l + 0.1 Culex pipiens 600 92.3 + 19.92 263.3+ 89.6 65 -r 26 195+ 55 14.7+ 3.13 42.0 + t4.5 10.6+ 4.4 3l+9 Psychodaalternata 350 8.0+ 3.1' 52.O+ 27 2.O+ 1.9 7.3+ 6.2 1.3+ 0.53 8.3 + 4.2 0.3 + 0.3 1.2+ 1.0 Chaoborus crystal linus 300 3,577+ 359 22,355 + 9562'6 572+ 58 3,577+ 1533 ' Mean of 3 experiments + SE (P < 0.05). 'lJthal concentrationexpressed in l0 5 x dilution ofC.b.z. whole culture. 3 lrthal concentrationexpressed in lOa x spores/ml. 4 Result of one experiment. 5 Resultsobtained by Thiery et al. (1992b) (P < 0.05). 6 Mean of2 experiments + SE (P < 0.05), LC values on 7th day. testedagainst the above-mentionedpreparation lated for Anophelesstephensi (1.1 x l0 4 dilu- at dilutionsof 0.5,l, 2,4,8,16,and 33 x l0-o tion : 1.76 x 104spores/ml) served as a basis (spores/mlranging from 8 x 103to 5.3 x 105). for the choiceofthe bacterialconcentrations used Twenty-five early 4th-instar larvae were placed for nontargetorganisms: for Planorbisplanorbis, in plasticcups containing 150 ml of the appro- Cloeon dipterum, Plea leachi, Asellus aquaticus, priate bacterial suspension.Three cupswere pre- Dapnia pulex, and,E ristalis sp.: 3.5 x I 06spores/ pared per dilution and testswere run in triplicate ml (: 200-fold concentration); for the larvae of at24 + 2oC.Three cups served as controls. Mor- Chironomusthummi s.l.: 4.4 x 106spores/ml (: tality was determined 24 and 48 h after appli- 250-fold concentration); for Chaoboruscrystal- cation of the C.b.m. preparation. The LCr,, and linus: up to 2.8 x 107spores/ml (: 1,600-fold LCro values (P < 0.05) were calculatedby log concentration), and finally, for Psychodaalter- probit analysis by use of a computer program nata, concentrations varying between 103 and (Raymond1985). 105 spores/ml. To exclude nonspecific effects b) Anophelini larvae: Three cups containing basedon the activity of exotoxinsor metabolite 20 early 4th-instar lawae of Anophelesstephensi toxins, autoclaved C.b.m. mateial was used in Liston were prepared per dilution (series of 6 sometests. dilutions;rangeT x 10-6to 2.2 x l0 a, corre- Twenty to 25 individuals were placed in each spondingto l.l x 103to 3.5 x 104spores/ml), of the test dishescontaining 100-150 ml water 3 cupsserved as controls. The testwas run once. (mixture of original and spring water) and the Nontarget organisms: The following species appropriateC.b.m. concentration. Two to 3 rep- served as test organisms: Planorbis planorbis licates were prepared for each concentration; a Linn. (Pulmonata); nymphs of Cloeon dipterum respective number served as a control. Small Linn. (Ephemeroptera);Plea leachi MacGregor amounts of food were added meeting the special (Heteroptera);Asellus aquaticus Linn. (Isopoda); requirementsof the organisms(Tetra Min, plant Daphnia pulex De Geer (Cladocera);larvae of material,or preyorganisms, i.e., Daphnia pulex). Eristalis sp. (Brachycera,Diptera); and 2nd-4th- Experiments were conducted at 20'C. The du- instar larvae of Chaoboruscrystallinus De Geer, ration of the experiment was up to 2 wk, obser- Chironomusthummi s.1.,and Psychodaalternata vations were made every I or 2 days. Tests were Say (Nematocera, Diptera). The animals were run in duplicate or triplicate. Test results were collectedfrom their natural habitats, transferred interpreted by calculation of the percent mor- to the laboratory, and allowed to adapt to lab- talities observed.Deviations betweencontrol and oratory conditions (20'C; day-night rhythm: 14: treated batches were checked for their signifi- l0 h) for I or 2 days.Psychoda alternatalawae canceby meansof multiple rangetests according remained in their substrate until the beginning ro Duncan(1955). ofthe test, then they werewashed out with small- Psychodaalternata: LC5o/LCeotests were car- meshedsieves. ried out with this speciesdue to its susceptibility Toxicity tests.' The LCnn value (48 h) calcu- towards C.b.m. Dead and living animals were M,c,RcH1994 Ctosranotutt anexuanrt rs Senoven MAr/ffsIA Table 2. Larvicidal activity of Clostridium bifermentans ser. malaysia on nontarget organisms. o/o Dose Test Species Order n (spores/ml) (days) Test Control Planorbis planorbis Pulmonata 60 3.5 x lOe 12 0 0 Cloeon dipterum Ephemeroptera 60 3.5 x 106 8 0 2.5+ 0.8 Plea leachi Heteroptera 60 3.5 x 106 7 0 6.7+ 0 Asellus aquaticus Isopoda 60 3.5 x 106 8 J.U+ t.7 4.3+ 1.0 Daphnia pulex Cladocera 75 3.5 x 106 6 4.3 I 2.3 J + I Eristalis sp.
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