Review Paper Aquatic insect predators and mosquito control_Canyon_… · 223 Tropical Biomedicine...
Transcript of Review Paper Aquatic insect predators and mosquito control_Canyon_… · 223 Tropical Biomedicine...
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Tropical Biomedicine 26(3): 223–261 (2009)
Review Paper
Aquatic insect predators and mosquito control
Essam Abdel-Salam Shaalan1 and Deon V Canyon2
1 Zoology Department, Aswan Faculty of Science, South Valley University, Aswan 81528, Egypt2 School of Public Health and Tropical Medicine, James Cook University, Townsville Qld 4811, AustraliaEmail address corresponding author: [email protected] 2 May 2009; received in revised form 28 July 2009; accepted 30 July 2009
Abstract. Mosquitoes are serious biting pests and obligate vectors of many vertebrate pathogens.Their immature larval and pupal life stages are a common feature in most tropical and manytemperate water bodies and often form a significant proportion of the biomass. Control strategiesrely primarily on the use of larvicides and environmental modification to reduce recruitment andadulticides during periods of disease transmission. Larvicides are usually chemical but can involvebiological toxins, agents or organisms. The use of insect predators in mosquito control has beenexploited in a limited fashion and there is much room for further investigation and implementation.Insects that are recognized as having predatorial capacity with regard to mosquito prey havebeen identified in the Orders Odonata, Coleoptera, Diptera (primarily aquatic predators), andHemiptera (primarily surface predators). Although their cpacity is affected by certain biologicaland physical factors, they could play a major role in mosquito control. Furthermore, betterunderstanding for the mosquitoes-predators relationship(s) could probably lead to satisfactoryreduction of mosquito-borne diseases by utilizing either these predators in control programs, forinstance biological and/or integrated control, or their kairomones as mosquitoes’ovipoistingrepellents. This review covers the predation of different insect species on mosquito larvae, predator-prey-habitat relationships, co-habitation developmental issues, survival and abundance, ovipositionavoidance, predatorial capacity and integrated vector control.
INTRODUCTION
Mosquitoes are important insects not onlyas nuisance biters but also as vectors ofimportant diseases such as malaria, filariaand dengue particularly in the tropics. TheWorld Health Organization adoptedmosquito control as the only method toprevent or control such diseases. Althoughinterest in mosquitos’ biological controlagents was large at the beginning of the 20th
century, it is stopped since the discovery ofinsecticidal properties of the DDT in 1939.Since that time insecticides were extensivelyused for mosaquito control. Due to theirdeleterious health and environmentalimpacts, search for environmentaly friendlyinsecticide alternatives has become
incressingly necessary. For this aspect,renewed interest in biological control agentsparticularly aquatic predaceous insects thatinhibit mosquitoes’ breeding sites couldprovide acceptable reductions in mosquitopopulation and it could be included inintegrated vector management (IVM)program.
Mosquito’s life cycle includes for stages:egg, larva, pupa and adult. The first threestages are aquatic giving high opportunity forthe success of predaceous insects formosquito control. Although informationabout contribution of aquatic predaceousinsects in mosquito eggs predation is veryrare, a few refrences exist on aquatic insectspreying upon adult mosquitoes. Thepredaceous bug Emesopsi streiti
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(Reduviidae) preying upon adult mosquitoesin bamboo internodes (Kovac & Yang, 1996).Yanovisk (2001) also mentioned thatMicrovelia cavicola and Paravelia myersi
(Vellidae) fed on adult mosquitoes emergingin tree holes. Fly larvae of Xenoplatyura
beaveri preying upon emerging adultmosquitoes in Nepenthes pitcher plants(Mogi & Chan, 1996). The DragonfliesPantala hymenaea and Erythemis collocate
attack swarming of Anopheles freeborni
after sunset (Yuval & Bouskila, 1993).Because of predation of aquatic insects onmosquito larvae and pupae is more observedand significantly affecting mosquitoesemerging, therefore the present reviewincludes only predation against larval stage.
Such predaceous insects are not onlypreying on nuisance mosquitoes but alsopreying on mosquito vectors of diseases suchas Anopheles gambiae (malaria vector),Aedes aegypti (dengue vector) and Culex
annulirostris (encephalitis vector). WhileYasuoka & Levins (2007) suggest thatconserving aquatic insects associated withmosquito larvae could be effective incontrolling mosquito vectors in the studysite. Walker & Lynch (2007) stated thattargeting malaria vector larvae, particularlyin human-made habitats, can significantlyreduce malaria transmission.
Although predaceous aquatic insectsinhabit a wide variety of aquatic habitats,which would seem to support theirusefulness, the selection of biological controlagents relies on more important factors.Selection should be generally based on thecapacity of a predator to maintain veryclose interaction with its prey population,capacity to self-replicate/reproduce, climaticcompatibility, and potential for unintendedand possibly adverse impacts (Waage &Greathead, 1988). Research has confirmedthat natural enemies are frequentlyresponsible for significant reductions inmosquito populations and should beindispensable to integrated control whichseeks to maintain mosquito vectorpopulations below annoyance and/ordisease transmission level (Legner, 1994).Furthermore, introducing and/or augmentingsuch natural enemies has in some cases
provided satisfactory control (Sebastian et
al., 1990; Chandra et al., 2008; Mandal et al.,2008) and sustained release of them overseveral years may reduce the relative highcost of massive releases.
Since there are some other biologicalcontrol agents such as bacterium, one of theadvantages of the predaceous insects overthe other biological control agents is, theseinsects could reach mosquitoes in somehabitats such as tree holes and phytotelmata,water bodies held by plants, in tropics andsubtropics that are very difficult to becontrolled with other biological controlmeasures.
Some articles have discussed andsummarized both aquatic insects and otherinvertebrates that prey upon mosquitoes.Biology, colonization and potential ofToxorhynchites mosquitoes as a biologicalcontrol agent of vector mosquitoes are fullycovered by Collins & Blackwell (2000) whileGarcia (1982) discussed the difficultiesassociated with such methodologies whichprevent more widespread utilization ofarthropod predators. In addition toToxorhynchites mosquitoes, the predaceouscharacters of Culex (Subgenus Lutzia)mosquitoes were reviewed by Pal &Ramalingam (1981). Moreover, Bay (1974)reviewed many aquatic insects that preyupon mosquito larvae and categorized themaccording to their taxonomic orders. Lacey& Orr (1994) limited their discussion toinsect predators that are used as biologicalcontrol agents in integrated vector controlto Notonecta and Toxorhynchites specieswhilst Kumar & Hwang (2006) reviewedlarvicidal efficiency of amphibian tadpoles,larvivorous fish, cyclopoid copepods inaddition to aquatic insects for mosquitobiocontrol. Mogi (2007) reviewed insects andinvertebrate predators based on adult, egg,larval and pupal mosquito predation besidepossibilities of using such predators formosquito control. Quiroz-Martinez et al.(2007) disscused the arthropods (insects,mites and spiders) that prey on mosquitolarvae and considerations for the success ofthese predators in mosquitoes’ biologicalcontrol programs.
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The present article not only reviews thepredation of different insect groups onmosquito, particularly larvae, but alsoincludes predator-prey associations indifferent aquatic habitats, the degree towhich predators affect mosquitodevelopment, survival, abundance andfitness, oviposition avoidance of mosquitoesin response to the presence of aquatic insectpredators, factors influencing predatorialcapacity, predaceous insects used inintegrated vector control and finallydifficulities for utilizing predaceous insectsfor mosquito control. Although the predationof different insects on mosquito larvae andthe predators-mosquitoes association indifferent habitats may be little bit similar tothe previously mentioned reviews, the otherparts are completely different and presentingnew information for utilizing predaceousinsects in mosquito biocontrol.
Predaceous insects
Many aquatic insects in the ordersColeoptera, Diptera, Hemiptera and Odonataare known to prey upon mosquito larvae(principal genera and species of interest areshown in Table 1). Predators may bepolyphagous, feeding on a broad range ofprey species (generalist predator),oligophagous, with a restricted range of prey;or monophagous, with a very limited rangeof prey (specialist predators). Mostpredators of mosquitoes tend to be from thegeneralist type (Collins & Washino, 1985).Some predators (especially those withchewing mouthparts) eat their prey(Odonata) but others suck the body fluid(hemolymph) of the prey (many beetle larvaeand Hemiptera). Although predation mayoccur during any life stage, most researchfocused on mosquito larval and pupal stagesbecause egg predation appears to be a minorcomponent of mosquito mortality andpredation on the adult stage seems unlikelyto provide reliable levels of control in mostcases (Collins & Washino, 1985). Also surplusor ‘wasteful’ killing of uneaten prey ischaracteristic to the fourth larval instar ofvarious species of the predatory mosquitogenus Toxorhynchites, it is recentlydocumented in the fourth larval instar of the
predatory midge genus Corethrella
(Lounibos et al., 2008). Furthermore, surplusor killing activity of Toxorhynchites larvaeto mosquito pupae is fortunate in the contextof control, because pupal production is mosthighly correlated with subsequent adultdensities (Padget & Focks, 1981) andprobability of disease transmission.
According to hunting strategies,predators are classified into neuston thatfloat on the top of the water (Vellidae:Hemiptera), free swimming (somemicrocrustaceans), climbing stalkers(Zygoptera: Odonata), sprawling ambushers(Anisoptera: Odonata), and cursorialsearchers (Dytiscidae and Hydrophyilidae:Coleoptera). Predaceous insects are alsocategorized into surface predators andaquatic predators. The first group comprisedinsects that forage near or below the watersurface to catch their prey and all belong toOrder Hemiptera. Predators in the lattergroup are good swimmers and are able toforage beneath water or/and on subsurfaceterrain beneath vegetation such as OrdersOdonata and Coleoptera and somehemipterans. The following sections presentinformation on the major predator groupsand their capacity for mosquito control.
Coleopteran predators
Although aquatic coleopterans arecommonly associated with mosquito larvaein different habitats, they have been lessexplored compared to other insect predators(Chandra et al., 2008). Among coleopterans,families Dytiscidae and Hydrophilidae havereceived attention as mosquito larvaepredators. Adults and larvae of Dytiscidaeand Hyydrophilidae are common predatorsin ground pools, permanent and temporaryponds, and artificial mosquito breeding sitesand were reported from phytotelmata aswell. Although they can reduce mosquitoesdensities in some pools (Nilsson &Soderstrom, 1988; Nilsson & Svensson, 1994;Lundkvist et al., 2003), their mosquito controlefficacy perhaps is limited by incompletehabitat overlap, alternative prey preference,emigration and cannibalism (Juliano &Lawton, 1990; Lundkvist et al., 2003). Likely,species of the genera Laccophilus, Agabus
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Table 1. Most common and principal genera and species of predaceous insects
References
Chandra et al., 2008Nilsson & Soderstrom, 1988
Lundkvist et al., 2003
Lee, 1967Lee, 1967Sulaiman & Jeffery, 1986Aditya et al., 2006
Peterson et al., 1969Koenraadt & Takken, 2003Hribar & Mullen, 1991Bay, 1974Borkent, 1980Kesavaraju & Juliano, 2004 &Griswold & Lounibos, 2006McLaughlin, 1990Yanovisk, 2001Bai et al., 1982 & Kuldip et
al., 1984Ikeshoji, 1966Prakash & Ponniah, 1978Thangam & Kathiresan, 1996Clark & Fukuda, 1967Bay, 1974Kirkpatrick, 1925 & Al-Saadi& Mohsen, 1988Laing & Welch, 1963Bay, 1974Fellipe-Bauer et al., 2000Minakawa et al., 2007Focks et al., 1985Gerberg & Visser, 1978Sempala, 1983Sempala, 1983Padgett & Focks, 1981Focks et al., 1982
Griswold & Lounibos, 2006
Aditya et al., 2006Amalraj & Das, 1998,Wattal et al., 1996 &Wongsiri & Andre, 1984Yasuda & Hagimori, 1997
Washino, 1969Shaalan, 2005 &Shaalan et al., 2007Washino, 1969Rodriguez-Castro et al., 2006Washino, 1969Venkatesan & Sivaraman, 1984Shaalan, 2005 &Shaalan et al., 2007Wattal et al., 1996
Mosquito prey
Cx. quinquefasciatus
Ae. communis
Culex mosquitoes
Culiseta incidens
Culiseta incidens
Ae. albopictus
Cx. quinquefasciatus
Tree-hole mosquito larvaeLarvae of same speciesMosquito larvaeMosquito larvaeMosquito larvaeAe. albopictus &Ochlerotatus triseriatus
An. quadrimaculatus
Tree-hole mosquito larvaeAe. aegypti, An. stephensi &Cx. quinquefasciatus
Cx. quinquefasciatus
Cx. fatigans
Cx. quinquefasciatus
Ae. sierrensis
Ae. aegypti
Cx. quinquefasciatus
Mosquito larvaeAe. communis
Mosquito larvaeAn. Gambiae s.s.Ae. aegypti
Ae. aegypti
Ae. africanus
Ae. africanus
Ae. aegypti
Ae. aegypti &Cx. quinquefasciatus
Ae. albopictus &Ochlerotatus triseriatus
Cx. quinquefasciatus
Ae. aegypti
mosquito larvae
mosquito larvaeCx. annulirostris
Mosquito larvaeCx. quinquefasciatus
Mosquito larvaeAe. aegypti & Cx. fatigans
Cx. annulirostris
An. stephensi, An. stephensi
& Cx. quinquefasciatus
Genera and species
Acilius sulcatus
Agabus erichsoni
Agabus opacus
Colymbetes paykulli,Ilybius ater
Ilybius fuliginosus
Dytiscus marginicolis
Lestes congener
Lacconectus punctipennis
Rhantus sikkimensis
Anopheles barberi
Anopheles gambiae
Bezzia expolita
Chaoborus crystallinus
Chaoborus cooki
Corethrella appendiculata
Corethrella brakeleyi
Cx. allostigma
Cx. fuscanus
Cx. raptor
Culicoides cavaticus
Culicoides guttipennis
Culiseta longiareolata
Dolichopus gratus
Mochlonyx culiciformis
Monohelea maya
Ochthera chalybesceens
Tx. amboinesis
Tx. brevipalpis
Tx. brevipalpis conradti
Tx. kaimosi
Tx. rutilus rutilus
Tx. splendens
Tx. towadensis
Abedus indentatus
Anisops sp.
Belostoma flumineum
Buenoa scimitar
Corisella sp.Diplonychus indicus
Diplonychus sp.
Enithares indica
Order
Coleoptera
Diptera
Hemiptera
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Service, 1965Beketov & Liess, 2007Scott & Murdoch, 1983 &Murdoch et al., 1984Lee, 1967Ellis & Borden, 1970Bay, 1967Alahmed et al., 2009Aditya et al., 2005
Mandal et al., 2008
Chatterjee et al., 2007Sebastian et al., 1990Miura & Takahashi, 1988Bay, 1974 &Sebastian et al., 1980Cordoba & Lee, 1995Lee, 1967
EL Rayah, 1975
Ae. vittatus
Cx. pipiens
mosquito larvae
Culiseta incidens
Mosquito larvaeCulex larvaeCx. quinquefasciatus
Armigeres subalbatus
Cx. quinquefasciatus
An. subpictus
Ae. aegypti
Cx. tarsalis
Ae. aegypti
(larvae and pupae)Mosquito larvaeCuliseta incidens
An. pharoensis
Laccotrephes sp.Notonecta glauca
Notonecta hoffmani
Notonecta shootrii
Notonecta undulate
Notonecta unifasciata
Siagra hoggarica
Sphaerodema annulatum
Sphaerodema rusticum
Aeshna flavifrons,Coenagrion kashmirum,Ischnura forcipata,Rhinocypha ignipennis andSympetrum durum
Brachytron pratense
Crocothemis servilia
Enallagma civile
Labellula sp.
Orthemis ferruginea
Tramea lacerate &Tramea torosa
Trithemis annulata scortecii
Odonata
and Rhantus have been also reported aspotential agents of biological control ofmosquitoes (Lee, 1967; Nilsson &Soderstrom 1988; Aditya et al., 2006). Arecent field study (Chandra et al., 2008)showed that Acilius sulcatus (Family:Dytiscidae) larvae have significant impact onmosquito larvae (Culex quinquefasciatus,Culex bitaeniorhynchus, Culex
tritaeniorhynchus, Culex vishnui, Culex
gelidus, Anopheles subpictus, Anopheles
vagus, Anopheles aconitus, Anopheles
barbirostris, Anopheles annularis andArmigeres subalbatus) that prevail incement tanks in Sainthia in the district ofBirbhum, West Bengal, India. A significantdecrease in larval density of differentmosquito species after 30 days from theintroduction of A. sulcatus larvae was noted,while with the withdrawal, a significantincrease in larval density was notedindicating the efficacy of A. sulcatus inregulating mosquito immatures. In thecontrol tanks, mean larval density did notdiffer throughout the study period.
Dipteran predators
The most common and famous dipteranmosquito predator is Toxorhynchites
mosquito that has been introduced as a
biological control agent of container-breeding mosquitoes in many differentecological habitats. A preliminary field trialon the Caribbean island of St. Maartendemonstrated the feasibility of using thepredaceous mosquito larva, Toxorhynchites
brevipalpis to control Ae. aegypti larvae(Gerberg & Visser, 1978). Sixteen daysafter the introduction of Tx. brevipalpis
eggs into Ae. aegypti breeding containers,the 21 houses sampled were negative forAe. aegypti and Cx. quinquefasciatus
and the house index (the percentage ofexamined houses that are positive forAe. aegypti larvae) dropped to zero. Fockset al. (1982) used Toxorhynchites rutilus
rutilus to control Ae. aegypti and Cx.quinquefasciatus mosquitoes in residentialblocks within a substandard urban area ofNew Orleans, Lousiana. Mosquitoesemergence from automobile tires, bucketsand paint cans, treated with 1 or 2 first instarlarvae of Tx. r. rutilus decreased by 65 and72% respectively, while overall control forboth treatment levels was 74%. Weeklyreleases of another Toxorhynchites larvalpredator, Toxorhynchites amboinensis, intoa 16-block neighborhood with substandardhousing in New Orleans, Louisiana, during1982 reduced Ae. aegypti densities by 45%
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when compared with similar but untreatedareas (Focks et al., 1985). Increasing thenumber of adults released per week from 100to 300 females per block did not improve thedegree of control achieved, indicated thatlower release numbers may be adequate toachieve this level of control, whilst releasing100 female predators per block resulted in a40% reduction in Cx. quinquefasciatus.Collins & Blackwell (2000) reported thatother attempts to control vector mosquitoesusing Toxorhynchites spp. mosquitoes havebeen made in many regions of the worldincluding the Caribbeans, Asia and Africa.In one example, the larval density of Ae.aegypti were reduced by more than 90%after the release of Toxorhynchites
splendens in water tanks in suburbanBangkok, Thailand (Wongsiri & Andre, 1984).These results suggest that it may be possibleto develop a practical method to controlAe. aegypti mosquitoes in urban areas usingTx. amboinensis.
The application of Toxorhynchites
mosquitoes to control Ae. aegypti larvae indeveloping countries has two additionalbenefits. Firstly, they have an unusual lifecycle in that they are not capable of bloodfeeding and therefore are not pests orvectors. Secondly, these mosquitoes couldbe reared locally instead of importinginsecticides. Although the aforementioneddata are examples of successful mosquitosuppression with Toxorhynchites
mosquitoes, Annis et al. (1989 & 1990)reported that this predator is unsuccessfulin field application in Indonesia. Repeatedrelease of Toxorhynchites first instar larvaein waterlogged places had no effect onmosquito population in Indonesia due totheir inability to withstand periods ofstarvation and to their accidental removalfrom containers during the act of waterconsumption. The same maybe true for otheraedines since a study conducted in Zikaforest, Uganda, on the breeding interactionsbetween Aedes africanus and two mosquitopredators, Toxorhynchites brevipapis
conradti and Toxorhynchites kaimosi,revealed a significant reduction in thenumbers of Ae. africanus larvae and pupae
in the tree holes that were also inhabited bypredator larvae (Sempala, 1983).
Likewise, other mosquito larvae,particularly Culex (Ikeshoji, 1966; Panickeret al., 1982; Thangam & Kathiresan, 1996;Mariappan et al., 1997; Yanovisk, 2001),Culiseta (Kirkpatrick, 1925; Al-Saadi &Mohsen, 1988), certain Anopheles larvae(Peterson et al., 1969), Aedes (Ramalingam& Ramakrishnan, 1971; Mogi & Chan, 1996),the Ochlerotatus subgenus Mucidus
(Mattingly, 1961), the Psorophora subgenusPsorophora (Carpenter & LaCasse, 1955;Campos et al., 2004) and Topomyia
(Ramalingam, 1983; Miyagi & Toma, 1989)are known to prey upon mosquito larvae.Ikeshoji (1966) used larvae of Cx. fuscanus
to control Cx. quinquefasciatus larvae insmall ditches in simulated field conditions.When daily 63 egg rafts of Cx.quinquefasciatus were released into theditches for a period of 3 weeks and 25 firstinstar larvae of Cx. fuscanus wereintroduced daily starting from the fifth day,an average of 156 larvae of Cx.quinquefasciatus per day survived to pupate(indicating about 99.98 reduction inpupation). Furthermore, when 2000 larvaeof Cx. quinquefasciatus were introduced atone end of a ditch 20 cm wide and 100 larvaeof Cx. fuscanus were introduced at the otherend, most of the predaceous larvae hadswum about 6 m to reach the prey populationwithin 3½ h of their release indicating howmuch this predator could find its prey. Underlaboratory conditions, An. barberi larvaewere shown to prey upon early instars ofvarious tree hole mosquito larvae. Moreinterestingly, recent study has shown thatpredation occur within and between larvaeof members of the malaria vector An.gambiae complex and may affect their adultpopulation densities (Koenraadt & Takken,2003).
Other Dipteran insects particularlyceratopogonid (Hribar & Mullen, 1991;Fellipe-Bauer et al., 2000), chaoborid(McLaughlin, 1990), chironomid (Naeem,1988), corethrellid (Kesavaraju & Juliano,2004; Griswold & Lounibos, 2006), culicoid(Clark & Fukuda, 1967; Bay, 1974),
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dolichopodid (Laing & Welch, 1963), tipulid(Yanoviak, 2001) and other brachyceran(Kitching, 1990) larvae were recorded asmosquito larvae predators (Table 1).
Hemipteran predators
Belostomatidae, Nepidae and Notonectidaeare the most important families ofpredaceous Hemipteran bugs. Thebackswimmers (Family: Notonectidae) arethe most common bugs preying uponmosquito larvae, important factor inreducing immature mosquito population andconsidered promising in mosquito control.
The role of hemipteran predators incontrolling mosquito larvae has beenrecognized since 1939 in New Zealand, whenstock troughs with Anisops assimilis werefound to be free of mosquitoes whereaspuddles in depressions surrounding thetroughs contained mosquitoes (Kumar &Hwang, 2006). Bay (1967) found that almost100 % of mosquito emergence was preventedin field-situated, screened, 100 gallonfibreglass tubs with one square meter ofwater surface and Notonecta unifasciata
compared to more than 12000 adultmosquitoes emerged from the control tubs.In another field experiments, in stock tanks(troughs holding drinking water for cattleand horses) in Santa Barbara County,California, Notonecta hoffmani were alsoshown to strongly influence mosquito larvaepopulations (Murdoch et al., 1984).
The striking effects of those predaceousbugs, Notonecta and Anisops, are probablydue to the physical simplicity of thesetroughs, tanks and tubes, and particularly tothe lack of prey refuges. For instance,emergent vegetation in ponds and otherwater bodies provide partial protection formosquito immatures. This effect wasexperimentally investigated and confirmedby Shaalan (2005) and Shaalan et al. (2007)whereas predation potential of Anisops andDiplonychus bugs was significantly reducedby the presence of vegetation.
Although the costs of colonization andmass production, coupled with the logisticsof distribution, handling and timing ofrelease at the appropriate breeding site,impede the use of notonectids in mosquito
control (Legner, 1994), results of a recentstudy for mass rearing and egg release of thepredatory backswimmer Buenoa scimitar
for the biological control of Cx.quinquefasciatus were impressive(Rodriguez-Castro et al., 2006). Productionof backsimmer eggs were observed for 263days and eggs that were released in artificialcontainers continued to produce newindividuals until adult stage. Thesebackswimmers produced a significantreduction in mosquito larval density in 5sampling dates out of 7.
Odonatan predators
Odonata larvae are voracious and importantpredators of mosquito larvae in freshwaterecosystems. They detect their preys bycompound eyes and mechanicalreceptorsand capture them with their labium.
The dragonfly larvae of Trithemis
annulata scortecii were intense and activepredators when used to control mosquitolarvae, especially Anopheles pharoensis, inirrigation channels in Gezira Province, Sudan(EL Rayah, 1975). Bay (1974) reported thatdragonfly larvae are known to prey heavilyon bottom feeder mosquitoes like Aedes
larvae. Sebastian et al. (1980) found thatcomplete elimination of all Ae. aegypti larvaeand pupae were achieved between day 4 and9 depending on the density of aquatic stagesof mosquitoes present per container whendragonfly larva, Labellula sp., was used. Thelarval stages were found to last 2-3 monthsin the containers. This long life coupled withhigh predation rate is likely to makedragonfly larvae highly successful predatorsand could be used in biological control ofAedes mosquitoes. Again, Sebastian et al.(1990) conducted a pilot field study,involving periodic augmentative release ofpredaceous larvae of a dragonfly,Crocothemis servilia, to suppress Ae.aegypti during the rainy season in Yangon,Myanmar. Four laboratory-reared, three-week-old C. servilia larvae were placed ineach major source of Ae. aegypti larvaeimmediately after the 3rd collection and thenmonthly for 3 successive months. The larvalpopulation of Ae. aegypti reduced to verylow levels in 2 to 3 weeks and suppressed it
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progressively until the trial ended. The adultmosquito population was greatly reducedafter about 6 weeks and progressivelydiminished thereafter until the trial ended.Chatterjee et al. (2007) found that significantdecrease in An. subpictus larval density indipper samples was observed 15 days afterthe introduction of Brachytron pratense
dragonfly larvae in concrete tanks underfield conditions in India. Similarly, the larvaeof 5 odonate species Aeshna flavifrons,Coenagrion kashmirum, Ischnura
forcipata, Rhinocypha ignipennis andSympetrum durum in semifield conditionsin West Bengal, India, significantly loweredthe mosquito larval density in dipper samplesafter 15 days from the introduction, followedby a significant increase of larval mosquitodensity after 15 days from the withdrawal ofthe larvae (Mandal et al., 2008). These results(Sebastian et al., 1980, 1990; Chatterjee et
al., 2007; Mandal et al., 2008) are suggestiveof the use of odonate larvae as potentialbiological agent in regulating the larvalpopulation of mosquito vectors.
Unlike the strong mosquito predationcapacity of dragonfly larvae, damselflylarvae may feed less on mosquito larvae.Breene et al. (1990) found no mosquito larvaein the gut of the larvae of the damselflyEnallagma civile. Larvae gut contentsanalysis revealed that they preyed uponchironomid larvae and other aquaticinvertebrates rather than mosquito larvaealthough they were observed in the pondwhere the larvae were collected.
Although odonate larvae have beeninvestigated less compared to otherpredaceous aquatic insects, their long lifecycle, predation capacity and sharing ofhabitats with mosquito immatures areadvantagious for their being a potentialbiological control agents.
Predator - Mosquito association by
habitat type
Several ecological studies of predator-preyassociations involving mosquito larvae indifferent aquatic habitats have beendocumented. The following sections arereviewing this association beside factorsinfluencing it in different habitats.
Temporary water bodies (Habitats)
associations:
Many predaceous insects were foundassociated with both nuisance and mosquitovectors in temporary habitats such as man-made ponds, snow melt pools, rain pools,flood water pools and other different pools.McDonald & Buchanan (1981) found thatmosquitoes colonized the man-made pondswithin one day of formation followed bypredaceous Coleoptera, Hemiptera and thenOdonata. A significant inverse relationshipwas noted between mosquitoes andpredators densities in 3 out of 4 trials.
Predators distributed in melted poolshave been investigated by few scientists.Larson & House (1991) studied the arthropodfauna of small, acidic pools in a domed,ombrotrophic bog over an ice-free season.Taxa varied in abundance between pools ofvarious classes and two principlecommunities were identified. Oligochaetes(segmented worms with few setae), beetlesand mosquitoes dominated small, astaticpools and odonates, chironomids and severalother taxa predominated in large, stable,vegetated pools. Within the large pools,odonate larvae were the dominant predators.In a similar study, Nilsson & Svensson (1994)compared assemblages of dytiscid waterbeetles and immature mosquitoes in twoboreal snowmelt pools that differed chieflyin temperature owing to difference inshading and duration. The total abundanceof dytiscids (including larvae) was similar inthe two pools, whereas species richness wasmore than twice as high in the warmer, lessephemeral pools. The mosquito fauna of bothpools were strongly dominated by Aedes
communis, whose initial numbers weresimilar in the two pools, however, first-instarlarvae suffered much higher mortality in thewarmer pools.
A large number of different predatorfauna have been associated with Anopheles
larvae in different aquatic bodies. Lozano et
al. (1997), found that the most abundant anddiverse predators associated with Anopheles
albimanus larvae in various hydrologicaltypes in southern Mexico, were aquaticColeoptera (20 genera) followed byHemiptera and Odonata (each with 16
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genera). All the predators were significantlymore abundant in temporary lagoons.Coleopterans and Hemipterans variedsignificantly among all locations however nosignificant difference was found in theabundance of odonates. Insect predatorswere correlated with occurrence ofAnopheles immature stages in water bodiesin south Punjab, Pakistan (Herrel et al.,2001). Six Anopheles species and 9 insectpredators were collected. Out of the 6Anopheles species 4 (An. subpictus,Anopheles culicifacies, Anopheles stephensi
and Anopheles pulcherrimus) were highlycorrelated with presence of predators. Mogiet al. (1995, 1999) studied the mosquitolarvae and larvivorous predator communitieson lands deforested for rice fielddevelopment in dry and wet area in centralSulawesi, Indonesia. Collected predatorswere from 3 insect orders (Odonata,Hemiptera and Coleoptera). In the dry area,Anisoptera larvae, notonectids and dytiscidswere the dominant predators while in thewet area; dytiscids, zygopterans andanisopterans were the dominant predators.Surface predators all belonged to orderHemiptera and they were less abundantthan aquatic predators. Munga et al. (2007)identified seven families (Hydrophilidae,Dytiscidae, Corixidae, Nepidae, Notonectidae,Belostomatidae, and Corduliidae) of larvalmosquito predators from the larval habitats(drainage ditches, cow hoofprints anddisused goldmines) of the malaria vector An.gambiae s.l. in natural habitats in WesternKenya Highlands. Predator density in disusedgoldmines was significantly higher than thatof other habitat types. Invertebrate predatorswere found to associate larvae of the malariavector An. albimanus in 78.6% of the bodytypes harbouring immature mosquitoes in alow-lying area of Haiti (Caillouët et al., 2008).Larval An. albimanus and associatedpredators were found in permanent andsemi-permanent groundwater habitatsincluding (in order of greatest abundance)hoof/footprints, ditches, rice fields, andground pools. Predators were dominated byorder Coleoptera (Hydrophilidae andDytiscidae) followed by orders Hemiptera(Belostomatidae, Corixidae, Notonectidae
and Gerridae), Odonata (Libellulidae,Aeshnidae and Coenagrionidae),Ephemeroptera (Baetidae) and Diptera(Syrphidae), respectively.
Fischer et al. (2000) described theseasonal variations of insect community ofthe rain pools during a 1-year period. A totalof 45 insect taxa were identified: 18Coleoptera, 15 Diptera, 9 Heteroptera,1Ephemeroptera and 2 Odonata. Culicidmosquitoes represented 76 % of the pooledabundance of insects. The maximumrichness of entomofauna was at the end ofthe summer (32), in coincidence withmaximum rainfall and temperature whilstthe minimum faunal richness (2) wasrecorded during the spring drought.Similarly, Fischer & Schweigmann (2008)found six mosquito species and 23 predatoryinsect taxa in temporary rain pools duringthe summer and fall season in Buenos Airescity. Both mosquito immatures and predatorswere disproportionally more abundant inpools with high flooded surface, depth, andduration. In another study, Campos et al.(2004) found that 41 predaceous insect taxaassociated with the floodwater mosquitoOchlerotatus albifasciatus from spring tofall. Coleoptera and Diptera were dominantand diverse while Ephemeroptera andOdonata were scarce in numbers andspecies. Six lentic aquatic habitats: (1)cemented temporary pools (cementedwalls); (2) cemented open water storagetanks (mainly for rain water storage); (3)house hold water storage tanks (large plasticcontainers to buckets); (4) stagnant streamside pools; (5) temporary roadside ditches;and (6) clogged sewage drains were foundto be hosting mosquito immatures andpredators in Darjeeling Himalaya, India(Aditya et al., 2006). Toxorhynchites
splendens, dytiscids (Coleoptera) andodonates were associated with mosquitoimmatures in both temporary pools andcement tanks whilst gerrids (Hemiptera)were associated with mosquito immaturesin temporary pools, stream pools and sewagedrains. The population of Tx. splendens
immatures was positively correlated withthe population mosquito immatures (r =0.071).
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Tree-hole associations:
A variety of invertebrates utilize tree holesas breeding sites. Because they are primarybreeding sites for many disease vectors,particularly mosquitoes and biting midges,tree holes are an economically importanthabitat (Yanovisk, 2001). AlthoughToxorhynchites mosquitoes are well knownas tree-hole mosquito predators, severalother predaceous insects are important tree-hole occupants. This article primarilyfocuses on predators other thanToxorhynchites mosquitoes since they wererecently reviewed by Collins & Blackwell(2000), however, they will be brieflymentioned.
Commonly recorded predaceous insectsin tree holes are dragonflies, damseflies anda new genus of water bug in the familyVellidae. Tree holes are not the primaryhabitat for odonates. Out of approximately6000 species, only 47 have been reportedfrom this habitat, at least 64% beingZygoptera (Corbet, 1983). Anisopteran andzygopteran larvae inhabiting tree holes wererecorded in forests of different geographicalregions. Orr (1994) reported that Pericnemis
triangularis (Coenagrionidae), Indaeschna
grubaueri (Aeshnidae) and Lyriothemis
cleis (Libellulidae) were breeding inphytotelmata in the understorey of lowlandmixed dipterocarp rainforest in Borneo.Corbet & McCrae (1981) collected 2 largenymphs of Hadrothemis scabrifrons froma water containing cavity in a tree root inlowland rainforest near the Kenya cost.Larvae of the anisopteran odonateHadrothemis camarensis (Kirby) werefound in water-containing tree holes, inKakamega forest, western Kenya (Copelandet al., 1996). Larvae were collected during 4consecutive years of sampling in 46% of treeholes, and in 26% of tree-hole samples.Larvae were more likely to be found in treeholes during wetter months. Distribution oflarvae among tree holes was clumped. Larveoccurred more often in tree holes of largersurface area and gape size. These attributescorrelated positively with median watervolume (0.15 - 42 L) and height above theforest floor (up to 22.45 m). Larvae of
chironomidae and culicidae predominatednumerically among prey of odonate larvae,with smaller larvae preying more on theformer and larger ones on the latter. Twoother insect predators were encountered intree holes: Toxorhynchites sp. and a newgenus of the water bugs of family Veliidae(order: Hemiptera). Veliids were found in11.2% and Toxorhynchites sp. in 41% oftreehole samples for which their presenceor absence was noted. Neither taxon wasassociated negatively or positively withthe occurrence of odonates. Louton et al.(1996) surveyed the aquatic macrofaunaof water-filled internodes of Guadua
bamboo in a lowland tropical forest inPeru. They found a community of 29species dominated by Diptera and Odonata.The predaceous insects comprised4 damseflies (Mecistogaster jocaste,Mecistogaster linearis, unknownMecistogaster species and Microstigma
rotundatum) and Dipterous larvae includingfamily Ceratopogonidae (subfamily:Ceratopogoninae) and family Culicidae(Toxorhynchites sp. and the facultativepredators Sabethes spp. A and B, andTrichoprosopon pallidiventer andTrichoprosopon sp.). Besides thepredaceous mosquito, Toxorhynchites
theobaldi, larvae of 5 common species ofOdonata (Gynacantha membranalis,Triacanthagyna dentata, M. linearis,Mecistogaster ornata and Megaloprepus
coerulatus) were collected from water-filledtree holes in a lowland forest in Panama(Fincke, 1999). Another study for themacrofauna of water-filled tree holes onBarro Colorado Island, Panama revealed thepresence of 54 macroinvertebrate taxa(Yanovisk, 2001). Most of the species werein the insect order Diptera and out of the totalfauna, 36% (20 species) were mosquitopredators in the insect orders Hemiptera(2 species), Coleoptera (2 species), Odonata(6 species) and Diptera (10 species).Interestingly, Yanovisk (2001) reported thatCx. allostigma and Sigmatomera
amazonica prey on mosquitoes in water-filled tree holes on Barro Colorado Island,Panama.
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Rice field associations:
The following studies showing that predatorcomplex is a major source of mortality forimmature stages of mosquitoes in rice fieldsand strongly supports the hypothesis thatnatural enemies should be an importantcomponent in rice field mosquito controlprogram.
Except for damselfly larvae, predaceousinsects were significantly more abundant inrain-fed fields than in irrigated fields ofnorthern Sulawesi, Indonesia (Mogi et al.,1995). Various factors could be involved suchas the scarcity of submerged plants thatprovide oviposition substrates, perchingsites and refuges for some aquatic predators,and emergent and floating vegetation whichobstruct oviposition by some predators.Larvivorous fish may reduce the abundanceof insect predators and significantdetesimental interaction also may existamong insect predators. Furthermore,insecticides and other chemicals for riceproduction probably are used morefrequently in irrigated fields than in rain-fedfields. According to plant age and maturity,damselfly larvae were more abundant inmature and harvested fields, whereasdragonfly larvae, Notonectidae, Vellidae,Hydrophyllidae and Dytiscidae were oftenabundant in ploughed and young fields.Another study investigating the colonizationof rice fields by mosquitoes and larvivorouspredators in asynchronous rice cultivationareas in the Philippines was conducted byMogi & Miyagi (1990). The samples weretaken from rice fields at 6 different phasesof maturity (fallow, ploughed, nursery, newlytransplanted, after tillering, mature).Dytiscidae, Anisoptera and Zygoptera werethe primary aquatic predators in fallow ormature fields while Hydrophilidae andNotonectidae had no clear successionpatterns. Nepidae were collected only frommature fields. Among surface predators,Vellidae was most abundant in fallow fields(in one study site) and in planted fields (inthe other study site) and other predatorswere rare. These results indicated that theabundance of aquatic predators decreasedat the onset of ploughing and then recoveredslowly as rice plants grew. In case of surface
predators, the pattern is similar but lessconspicuous.
Notonectids, dytiscids and larvae ofAnisoptera and Zygoptera were among bioticfactors influencing the abundance ofJapanese encephalitis vectors in rice fieldsin India (Sunish & Reuben, 2002). Notonectidpopulations decreased with rice plantgrowth and were the most abundant insectpredators. Dytiscids dominated the earlyweeks of the cultivation cycle but Anisopteraand Zygopteran larvae were also abundantearly in the cycle. Multiple regressionanalysis showed that notonectids (bothnymphs and adults) were negativelyassociated with larval abundance. While theimpact of Zygoptera was observed onlyduring short and long-term crop seasons,dytiscids showed a significant mortalityfactor for mosquito larvae once during thesummer season. In a latter study, Sunish et
al. (2006) mentioned that predatorynotonectids, anisopterans and dytiscidssignificantly influenced the survival ofimmatures of Cx. vishnui complex, aJapanese encephalitis vector, in rice fieldsin Southern India.
Andis & Meek (1985) studied mortalityand survival patterns for immature ofPsorophora columbiae in the laboratorysetting and in rice fields in Louisiana, USA.Predators consumed at least 24% (youngerage classes) of the larvae in each field, amaximum of 56% (older age classes) andwere the most significant mortality factor forimmature Ps. columbiae in rice fields. Totalmortality of the mosquito larvae was highwith only 2.6% surviving to the pupal stage.It can be inferred that predation may berestricted to older age classes and reducelarval survival, which finally lead to areduction in the adult Ps. columbiae
population density. Likewise, insectpredation was the most important mortalityfactor for mosquito larvae and pupae inPhilippine rice fields (Mogi et al., 1984).Survival from hatching to emergence was 50- 88.8% in predator – free cages set in the ricefields, whereas survival of naturalpopulations exposed to predators was 0.0-1.8% for Culex and 1.1-4.7% for Anopheles inthe same rice fields. In Thai rice fields,
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mortality of immature anophelinemosquitoes attributed to aquatic predatorswas variable (19-54%) and correlatedpositively with the predators abundance.Surface predators were a non-significantminor mortality factor (0-10%) (Mogi et al.,1986). Diabaté et al. (2008) found thatemergence success of An. gambiae in Ricefields and puddles experiments in BurkinaFaso was significantly affected bypredaceous insects. The backswimmersAnisops sp. and Anithares sp. (Hemiptera:Notonectidae), the water boatmanMicronecta sp. (Hemiptera: Corixidae), thedragonfly Tramea sp. (Odonata:Libellulidae) and the beetles Berosus sp. andLaccophilus sp. (Coleoptera: Hydrophilidaeand Dytiscidae) were associated to An.gambiae larvae. The number of predatorswas higher in rice fields than in puddles andthe backswimmers were the most abundantpredators in both rice field and puddles witha mean collection of 45.7 and 21.8 predators/m2 , respectively.
Recent techniques for detecting
predator – mosquito associations:
In addition to classical surveys, recenttechniques could be used to detect naturalpredators associated with mosquito larvae.By using Precipitin tests performed on thegut contents of possible predators collectedfrom different areas and habitats in Kenya,Service (1973) identified Coleoptera andDiptera as insect predators. In a later study,Service (1977) used the same technique tocompare mosquito predator fauna in ricefields, pools and ponds in Kenya. Forty twopredator species were identified, the mostimportant of which were Coleoptera larvae,Hemiptera and predaceous adult Diptera.Rice fields harbored more predator faunathan temporary pools and small ponds. ADNA-assay was utilized to confirm predationamong larvae of the An. gambiae complex(Koenraadt & Takken, 2003). Furthermore,a range of molecular techniques andapplications that allow prey to be identified,often to the species and even stage level,were reviewed by Symondson (2002). Thesetechniques include enzyme electrophoresis,
a range of immunological approachesutilizing monoclonal and polyclonalantibodies to detect protein epitopes, and thepolymerase chain reaction (PCR)-basedmethods for detecting prey DNA. The PCR-based techniques are displacing all othermethods since they have been shown to behighly effective and more reliable.
Predators’ influence on mosquito
oviposition, development, survival,
abundance and fitness
Research findings indicating that thedevelopment, survival and abundance oflarval mosquito populations in the field arelimited by predaceous insects which areprimarily responsible for mortality inimmature stages of mosquitoes. This effecthas been reported in many different aquatichabitats and is responsible for restraining thedensity of such prey populations below thecritical threshold where transmission ofdiseases could not occur (Das et al., 2006).
Predators’ influence on mosquito
oviposition:
Animals take risk of predation into accountwhen making decisions about how to behavein particular situations. Chemosensory cuesare important and are used to detect thepresence of predators or even their presencein the immediate past, and may also provideinformation on predator activity level anddiet (Kats & Dill, 1998). In their review articlefor chemical detection of natural enemies byarthropods, Dicke & Grostal (2001) reportedthat of all chemical information gathered byanimals, cues about predation risk usuallyhas important and immediate consequencesfor the future fitness of animals and theyresult in various responses strategiestowards such predators including avoidance.For all mosquito species, location andselection of an oviposition site is essentiallife-cycle behavior and involves visual,olfactory and tactile responses (Bentley &Day, 1989). Oviposition is an importantcomponent of most mosquito borne diseasesbecause pathogen acquisition by mosquitovectors usually requires taking of at least oneblood meal and disease transmission usually
235
requires the completion of at least oneoviposition cycle before pathogen transfercan occur with subsequent blood meal.
It was believed for a long period thatpredator-prey interaction was largelyattributed to predation mechanisms untilChesson (1984) showed that the effect ofnotonectid bugs on mosquito larvae is mainlydue to selective oviposition by gravidmosquitoes. He manipulated the density ofaquatic predaceous bugs (N. hoffmani andN. kirbyi) in stock troughs to assess thepredator’s effect on mosquito larvae. Over athree-month sampling period very few largemosquito larvae or pupae were collectedfrom the side of the trough wherenotonectids were located, whereas largedensities were collected from the side freefrom notonectids. To ensure that this was notan artifact of the side of the trough chosenfor notonectid addition or removal, thepredators were moved from one side to theother and same results were obtained. It wasthought that these experimental resultscould be explained by selective mosquitooviposition. This hypothesis was supportedby laboratory experiments in which femalemosquitoes laid the fewest egg rafts in tubescontaining the predaceous notonectids.Moreover, laboratory and field experimentsalso demonstrated that notonectids maydisrupt mosquito egg rafts, but no evidenceof a reduction in subsequent hatchingsuccess was obtained. This means that thepredator does not feed on the mosquito eggrafts and confirms the selective ovipositionhypothesis. Other predators such asdragonfly larvae, however, consume eggrafts. Likely, later studies have investigatedovipositional responses of the mosquitoCuliseta longiareolata to some insectpredators.
Stav et al. (1999) reported that thepredaceous dragonfly larvae of Anax
imperator produced 52% reduction in Cs.longiareolata oviposition in outdoorartificial pools. The reduced number of Cs.longiareolata egg rafts found in the presenceof A. imperator was largely due tooviposition habitat selection by Cs.longiareolata females. Larvae of Cs.longiareolata were highly vulnerable to
predation compared to Cx. laticinctus andwere also the only dipteran species thatavoided Anisops pools when ovipositing(Eitam et al., 2002). Stav et al. (2000) foundthat the egg rafts of the mosquito Cs.longiareolata deposited in the free Anax
treatment were fewer than deposited incaged Anax and control treatments. Therewas no statistically significant difference inthe number of egg rafts between control andcaged Anax pools which means that, whileCuliseta females oviposit fewer egg rafts inthe presence of Anax, they did not respondto predation risk from the caged Anax. Ingeneral, this individual response could havepopulation-level consequences. Forinstance, it may increase the equilibrium sizeof the Cs. longiareolata population relativeto the population in which oviposition isdiscriminative with respect to Notonecta
maculata (Spencer et al., 2002).Furthermore, females of the malariamosquito vector An. gambiae laidsignificantly fewer eggs in rainwaterconditioned with the predatorybackswimmer Notoecta sp. than inunconditioned rainwater, indicating thatpredators influence selection of ovipositionsite by this malaria mosquito vector (Mungaet al., 2006). More interestingly, females ofthe malaria mosquito vector An. gambiae s.l. tend to avoid oviposition sites containingolder instar larvae of the An. gambiae
(McCrae, 1984). The reason was discoveredlater on to be avoidance of offspringpredation by older instar larvae (Koenraadt& Takken, 2003).
These previously mentioned studiesshowed that notonectid bugs and dragonflylarva A. imperator affect oviposition habitatselection in some mosquito species at astable density of these predators. However,the relationship between predator densityand mosquito oviposition response was notstudied until Eitam & Blaustein (2004) testedthe oviposition response of 2 mosquitospecies, Cs. longiareolata and Cx.laticinctus, to a range of the predator N.maculata in artificial pools. Both mosquitospecies oviposited less in predator pools butthe response was not related to the predatordensity, whereas vulnerability of Culiseta
236
immatures to predation was densitydependent. So, although mosquitoes candetect the predator at any density, they maybe unable to discriminate predator density.The vulnerability of Culiseta to predationcould thus be due to mitigating effects of thebiotic community inside the pools. Similarly,effects of pool depth combined with risk ofpredation on oviposition habitat selection byCs. longiareolata were studied recently(Arav & Blaustein 2006). Results indicatedthat although N. maculate affectedoviposition pattern of this mosquito, pooldepth did not affect oviposition habitatselection for this mosquito.
All these studies have not assessed themode of detection of predators untilBlaustein et al. (2004) demonstrated andconfirmed that the cue for ovipositionavoidance of Cs. longiareolata to N.maculata was a predator-released chemical(kairomone): Notonecta water (withoutNotonecta replenishment) repelledoviposition for 8 days. Consequently, thismode of detection is an advantage forpredators and it is very important from themosquito control point of view whereas suchkairomones could be producedcommercially for mosquito control.Furthermore, oviposition habitat selection inCs. longiareolata is an adaptive response tothe trade-off between the risk of predationand negative density-dependent effects(Spencer et al., 2002) whilst findings ofKiflawi et al. (2003) suggest that it is drivenby a mixed strategy, played by all females,whereas all females follow a single, simplebehavioral ‘decision rule’ that is responsiblefor the lack of complete predator avoidance.Mosquitoes may detect predators cues eitherfrom the air, when the cues possessessufficient volatility, or by a gustatorymechanism involving direct contact with thewater, when the cues possess low volatility(Clements, 1992). Silberbush & Blaustein(2008) tested whether Cs. longiareolata candetect the chemical cues from N. maculata,
without touching the water. Cs.longiareolata oviposited significantly morein the central pools surrounded by channelscontaining control water than in poolssurrounded by Notonecta conditioned water
channel (56 of 81 egg rafts (69%) wereoviposited in the control pools) indicatingthat gravid Cs. longiareolata femalesdetected predators cues from the air whichmeans that predator-released cues(kairomones) are air-borne cues.
The predators cues not only affectingmosquitos’ oviposition but also alter their lifecycle traits (Beketov & Liess, 2007). Resultsof their experiments showed that chemicalcues from the predator N. glauca feed withprey’s (Cx. pipiens) conspecifics caused adecrease survival, delayed immaturesdevelopment and reduction in body size ofemerged mosquitoes while chemical cuesfrom predators fed with Daphnia magna (acrustacean invertebrate animal) producedonly delayed development. The effect of thecues on larval development and body size ofimagoes were significantly stronger forfemales than for males which is veryimportant for mosquitoes suppressingparticularly diseases vectors.
In summary, selection of oviposition siteby female mosquitoes depends more on thepresence of predators and less on predatordensity. Furthermore, predator density, asindicated by the concentration of theirkairomones, could affect the ovipositiondeterrent potential and would be animportant consideration in utilizing eitherpredators or their kairomones for biologicalcontrol of mosquitoes.
Predators’ influence on mosquitoes
development, survival, abundance:
Influences of predaceous aquatic insects onthe development, survival and abundance ofimportant Aedes, Anopheles and Culex
mosquito vectors are briefly summarized inTable 2. Unlike Culex, information about roleof predators on development, survival andabundance of Aedes and Anopheles
mosquitoes is limited.In some cases, variations in predation
effects are due to difference in predatorspecies breeding with the mosquito species.For instance, role of predators on thedevelopment and survival of immaturestages of Cx. annulirostris in differentregions in Australia was variable. In Victoria,McDonald & Buchanan (1981) mentioned
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Table 2. Influences of predators on mosquito development, survival and abundance
Reference
Marten et al., 1996
Robert et al., 1998
Service, 1973 &1977
Diabaté et al., 2008
Christie, 1958
Grill & Juliano,1996
Garcia et al., 1996
Casanova & DoPrado, 2002
McDonald &Buchanan, 1981
Mottram & Kettle,1997
Rae, 1990
Stav et al., 2005
Garcia et al., 1996
Aditya et al., 2004
Predation influence
Mosquito production was negatively associated with predators
Populations of predators (notably odonates) were one of theconditions associated with the abundance of An. arabiensis larvaein market-garden wells.
Predators, parasites and pathogens have been identified as majorcauses of larval mortality up to 98%.
Field experiment indicated that emergence success was over 3 foldhigher in predator free cages than in cages with predators (164.8adults/cage and 49.6 adults/cage respectively).
Survival increased when first stage larvae introduced into semipermanent pools, before and after removing the natural fauna from3% (presence of fauna), to 58% when the fauna had been removed.When a number of first stage larvae was introduced daily, survivalto pupation increased from nil to 7-20% when the other fauna hadbeen effected.
When exposed to Tx. rutilus (hatch to adult) Ae. aegypti usuallyfailed to produce adults whilst Ae. triseriatus always producedadults.
Immature stages were found in water reservoirs where aquaticinsects are not observed but no mosquito larvae were found whenpredators were found.
Mortality ranged from 68 to 96 % and was the most important causeof death and was the key-factor best accounting for the populationfluctuations of this mosquito species.
Survival rate from egg hatching to eclosion was 11%.
Predators killed 69.1%, 68.7% and 43.2% of immatures in the floodedgrassland, semi-permanent pool and temporary pool respectively.
Predators dominated by dytiscids and dragonfly naiads, reducedlarval survival by 58%.
Anax imperator caused statistically significant reduction (32.4%)in the number of Cx. pipiens larvae surviving to the pupal stage.
Immature stages were found in water reservoirs where aquaticinsects are not observed but no mosquito larvae were found whenpredators were found.
Sphaerodema annulatum significantly reduced the rate of pupation(6 – 35) and adult emergence (0.4 – 28.8 per day) under laboratoryconditions.
Mosquitoes
Anopheles
albimanus
An. arabiensis
An. gambiae s. l.
An. gambiae
Aedes aegypti &Ae. triseriatus
Ae. scapulari
Culex
annulirostris
Cx. pipiens
Cx.quinquefasciatus
that the survival rate of Cx. annulirostris
from egg hatch to eclosion was 11% andpredation by associated Coleoptera,Hemiptera and Odonata was estimated to belargely responsible for the low survival. In
the Brisbane area of southeast Queensland,Mottram & Kettle (1997) found that predatordensities in three surveyed sites weresignificantly different, being lowest in thetemporary pools (0.32 %) and highest in the
238
Miura et al., 1978
Reisen et al., 1989
Walton et al., 1990
Apiwathnasorn et
al., 1990
Mogi et al., 1980
Reisen & Siddiqui,1979
Stav et al., 2005
In insecticide treated pond, larval population densities fluctuatedbetween 0 and 15/dip, while in the untreated pond, where differentpredaceous insects are found, population densities remained lowand never approached a 1/dip level.
Predation mortality ranged from 3.7 to 84.5% and was the mostimportant cause of death at 5 of 6 study sites.
Predation by coleopteran larvae significantly affected larvalpopulation.
Mortality from egg hatching to adult emergence was 95.2, 95.7 and93.9% in rice fields, borrow-pits and groud-pools respectively.
Predators complex were very important factor for the larvalpopulation in fallow rice fields while adult emergence rate wasvery low in the presence of the predators, the average being 0.02and the higher the predator density the lower the emergence rate.
Effect of predation on the survivorship ranged from 0.017% duringthe monsoon to 0.725% during the postmonsoon season.
Anax imperator reduced Cs. longiareolata larvae survival to thepupation (78%).
Cx. tarsalis
Cx.tritaeniorhynchus
Culiseta longiareolata
flooded grassland (1.76 %). The mortalitycalculations suggested that predators killed69.1%, 68.7% and 43.2% of immature Cx.annulirostris in the flooded grassland, semi-permanent pool and temporary pool,respectively. For the same mosquito speciesat the Ross River dam in Townsville, NorthQueensland, Australia, the invertebratepredators, dominated by dytiscids anddragonfly larvae, reduced larval survival by58% (Rae, 1990).
In other cases this variation is attributedto both mosquito species and differentpredators. The most obvious example is thefield experiment that has been conducted byLundkvist et al. (2003) in artificial ponds overtwo successive years to determine howpopulation levels of mosquito larvae areaffected by predaceous diving beetles(Dytiscidae). Mosquitoes that colonized theponds were predominantly species of thegenus Culex. In 2000, most of the dytiscidsthat had colonized the ponds were small(Hydroporus spp.) and had no impact on thesize of larval mosquito populations.Conversely, in 2001, larger beetles (Ilybius,Rhantus and Agabus spp.) were morecommon and mosquito larvae weresignificantly fewer in ponds with highsnumbers of dytiscids.
A recent study conducted by Das et al.(2006) mentioned that breakdown ofpredator populations was responsible for thesudden increases in vector populationsabove the threshold for disease transmissionduring heavy rainy periods. In rice fields,notonectid predators exhibited a significantpositive correlation with Cx. vishnui larvae.Important predators recorded in shallowpools were notonectids, damsefly larvae,Diplonychus indicus and hydrophilids.Dragonfly larvae and gerrids were recordedin cement tanks. The conclusion was thatrice fields are stable ecosystems whereregular interaction occurs between mosquitolarvae and their natural enemies and asudden increase in the mosquito populationis uncommon. Contrarily, in transienthabitats (shallow water pools and cementtanks) no such stability is present and theybecome more important as breeding habitatsin terms of seasonality and number.
Predators inhabiting water-filled treeholes are known to decrease the prevalenceof mosquito larvae. Predation by predaceousmidge larvae, Pentaneura sp., produced lowdensities of mosquito larvae found in thewater field bracts of Heliconia imbricate
(Naeem, 1988). This predation affected 2mosquito species, Wyeomyia pseudopecten,
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a resident species, and Trichoprosopon
digitatum, a non-resident species. Predationkept resident mosquito densities low whilecompletely excluded the non-residentmosquito from the bracts. Larvae of 4common species of odonata, a mosquito anda tadpole were the major predators collectedfrom tree holes in the lowland moist forestof Barro Colorado Island, Panama, andmosquito larvae were their common prey(Fincke et al., 1997). Tree holes colonizednaturally by predators and prey had lowerdensities of mosquitoes if odonates werepresent than if they were absent. Whilecontrolling for the quantity and species ofpredator, hole volume and nutrient inputwere tested by using artificial tree holesplaced in the field. In large and small holeswith low nutrient input (number of mosquitolarvae), odonates suppressed both thenumber of mosquitoes present and thenumber that survived to pupation. Increasingnutrient input (and consequently, mosquitoabundance) to abnormally high levelsdamped the effect of predation whenodonates were relatively small. However, thepredators grew faster with higher nutrients,and large larvae in all three genera reducedthe number of mosquitoes surviving topupation, even though the abundance ofmosquito larvae remained high. Thepresence of a 4th instar Tx. rutilus
significantly reduced the abundance of latestage Ae. triseriatus mosquitoes (Louniboset al., 1997). The pupal stage of this prey wasmore negatively affected by Tx. rutilus
(Bradshow & Holzapfel, 1983) than othertree-hole mosquitoes in Southern NorthAmerica. Extinctions of aquatic stages of Ae.triseriatus within tree holes were common,but in most holes were not significantlyassociated with the presence of Tx. rutilus,indicating that predation does not routinelydrive mosquito prey locally extinct in thisecosystem.
Predators’ influence on mosquitoes
fitness:
The influence of predators on mosquitofitness was first reported by Lounibos et al.(1993) when they investigated the influencesof food type and predation on fitness of the
treehole mosquito Ae. triseriatus. Resultsindicated that the presence of Tx. rutilus
significantly affected the fitness of Ae.triseriatus to a greater degree than foodtype. Survivorship of immature stages incohorts with predator access was very lowwhile the mean of P50 (time to 50% pupation)was significantly greater than cohorts withdetritus. The female size in cohorts with thepredaceous mosquito, particularly wing size,was unexpectedly smaller than other cohortswith or without food access. It was suggestedto be due to the fact that the presence of Tx.rutilus may reduce movement of larval Ae.triseriatus, thereby decreasing food intakeand size at metamorphosis. Additionally,Dicke & Grostal (2001), in their review forchemical detection of natural enemies byarthropods, reported that predation riskusually has important and immediateconsequences on prey fitness. Lundkvist et
al. (2003) found a negative correlationbetween the number of diving beetles inartificial ponds and the mean body length ofmosquito larvae that has seriousconsequences on the fitness of emergingfemales.
More interestingly, recent study (Diabatéet al., 2008) indicated that predaceousinsects influencing the divergent selectionamongst the molecular forms of the malariavector An. gambiae. Predtion increased thedevelopmental success of larvae of M formover the S form in both puddeles and ricefields. Higher density of predators belongingto Notonectidae (Anisops sp. and Anithares
sp.) and Dytiscidae (Laccophilus sp.)families increased the relative success of theM form whilst higher density of Libellulidae(Tramea sp. ) and Hydrophilidae (Berosus
sp.) specimens appeared to decrease therelative success of the M form, but theireffects were not significant.
Factors’ influencing capacity of
predaceous insects
Factors influencing predation potential ofpredaceous insects are shown in Table 3.These factors are classified into biologicaland physical. Unfortunately, the literatureshave shown that investigations for factorsinfluencing predation capacity of aquatic
240
beetles are limited compared to the otherpredaceous insects (Diptera, Hemiptera andOdonata).
Increased predation of one mosquitoprey species over another by a predaceousinsect does not always mean a realpreference since it could be due todifferences in their means of evaluatingpredation risk (Sih, 1986). Sih (1986)reported that the behavior of Ae. aegypti
larvae towards the predator N. undulata wasa response to disturbance per se, whilst theCx. pipiens response was mediated bychemical cues that may have involved acombination of notonectid digestiveenzymes and partially digested mosquitomaterials, associated with the actualpredation act. So, because Cx. pipiens hasan evolutionary history of contact withnotonectids, it suffered a lower predationrate from Notonecta than did the Ae. aegypti
that lacking this evolutionary behavior.Consequently, the reduced predation ratecould be explained as Cx. pipiens showedboth stronger and more precise antipredatorresponses than Ae. aegypti. Further to this,the findings of Husbands (1978) imply thatprey behavior could influence its persistencein the mosquito larvae-notonectid system. Hefound that notoectid predators quicklydestroyed Aedes nigromaculis compared toCulex tarsalis due to the former showinglittle reduction in their movement or shift intheir habitat use but, in contrast, the lattershifting to feed quickly among emergentvegetation. Grill & Juliano (1996) alsosuggested that in some systems, preybehavior patterns are more related tovulnerability to predation. In furtherconfirmation of this hypothesis, Ae.albopictus did not respond to cues producedby Tx. rutilus and was more vulnerable topredation than O. triseriatus (Kesavaraju &Juliano 2004).
Collins & Resh (1985) stated otherfactors influencing the capacity ofdamselflies at Coyote Hills Marsh, Fremont,CA. The damselfly microdistribution, age-specific feeding habits, phenology, and thearchitecture of the habitat that supports thelarvae were anticipated to reduce thepredaceous capacity of Enallagma civile, E.
carunculatum and Ischnura cervula
against An. occidentalis.Lee (1967) found that mosquito larvae
are consumed more than pupae by predatorsand assumed that this was due to theinclination of pupae to exhibit rapid tumblingaction when startled. Contrarily, both bugsof family belostomatidae (Order: Hemiptera)and Toxorhynchites mosquito larvae have anadvantage over the other aquatic predaceousinsects that restrict their prey selection tothe larval instar only. This is worthy of note,inparticular for mosquito vectors of diseases,since pupal reduction directly reducesmosquito emergence and subsequent diseasetransmission.
Predaceous insects and integrated
mosquitoes control
The concept of integrated control is a fairlyspecific one, which historically has meantthe use of a combination of chemical andbiological agents in as compatible a manneras possible (Axtell, 1979). Sometimescultural and/or physical control methodshave been included. The role of biologicalcontrol agents, especially arthropodpredators, in integrated vector control (IVC)was reviewed by Lacey & Orr (1994). Theymentioned that selection of candidatebiological control agents for integratedvector control would depend on a varietyof factors including efficacy, costconsideration, environmental impact andcompatibility with other interventions.
The microbial insecticides Bacillus
thuringiensis and Bacillus sphaericus werecombined with predaceous insects moreoften than other contro measures inintegrated mosquito control. The toxin of B.t. serotype H.14 was applied to control Cx.tarsalis mosquitoes in pesticide-sensitivehabitats (Mulligan & Schaefer, 1981).Complete control of Cx. tarsails at a wildlifearea was obtained with B.t. H14 at 0.8 kg/haand predation by naturally-occurring aquaticbeetle larvae extended the control of Cx.tarsalis through 22 days after treatment. B.t.H14 was innocuous to the selected non-target fauna. Similarly, application of B.t. H14at 1.1 kg/ha reduced Cx. tarsalis numbersby 93% at a duck club without affecting
241
Tabl
e 3.
F
acto
rs i
nflu
enci
ng p
reda
tion
pot
enti
al o
f aq
uati
c pr
edac
eous
ins
ects
Refe
ren
ce
Elli
s &
Bor
den,
197
0
Bai
et
al.,
198
2
Kul
dip
et
al.,
198
4
Wat
tal
et
al.,
199
6
Seba
stia
n et
al.,
1980
Ala
hmed
et
al.,
200
9
Pad
gett
& F
ocks
,19
81
Min
akaw
a et
al.,
2007
Reb
olla
r- T
elle
z et al.,
1994
Al-S
aadi
& M
ohse
n,19
88
Kes
avar
aju
&Ju
liano
, 20
04
In
flu
en
ce
Mos
quit
o la
rvae
pre
ferr
ed o
ver
the
othe
r pr
eys
No
appa
rent
pre
fere
nce
by C
x.
fuscan
us
Pre
dati
on w
as g
ener
ally
hig
hest
aga
inst
An
. ste
phen
si f
ollo
wed
by C
x. q
uin
qu
efa
scia
tus a
nd A
e. a
egypti
.
Fee
ding
rat
es w
ere
high
er fo
r fi
rst i
nsta
r la
rvae
than
for
pupa
e
Co
nsu
med
bo
th s
tage
s w
ith
pre
fere
nce
to
war
ds
larv
ae,
part
icul
arly
sm
alle
st o
nes,
ove
r pu
pae
The
pre
dato
ry e
ffic
acy
was
hig
hest
aga
inst
fir
st l
arva
l in
star
and
it d
ecre
ased
as
the
larv
ae g
rew
old
er u
nder
lab
orat
ory
and
fiel
d co
ndit
ions
Mor
e 4th
ins
tar
prey
was
con
sum
ed s
igni
fica
ntly
tha
n pu
pae
or 1
st in
star
s, b
ut th
ey k
illed
wit
hout
eat
ing,
sig
nifi
cant
ly m
ore
pupa
e th
an 4
th i
nsta
rs a
nd n
o 1st
ins
tar
killi
ng w
as o
bser
ved.
Sign
ific
antl
y m
ore
2nd in
star
larv
ae w
ere
cons
umed
than
pup
aew
hen
they
wer
e bo
th a
vaila
ble.
Pre
dati
on r
ate
exhi
bite
d by
Bu
en
oa
sp
. w
as t
he s
ame,
and
was
ind
epen
dent
of
prey
bod
y si
ze.
4th
inst
ar l
arva
e of
Cs.
lon
giar
eola
ta f
ed o
n 1s
t, 2
nd a
nd 3
rdin
star
lar
vae
of
Cx
. qu
inqu
efas
ciat
us.
Th
e ra
te o
f p
rey
cons
umpt
ion
was
1.6
5 la
rvae
/day
/pre
dato
r.
Sec
on
d
inst
ars
of
spec
ies
wer
e m
ore
vu
lner
able
to
pred
atio
n th
an w
ere
3rd i
nsta
rs a
nd t
he 3
rd i
nsta
r A
ed
es w
asm
ore
vuln
erab
le t
han
Och
lerota
tus o
f th
e sa
me
stag
e.
Mo
sq
uit
o p
rey
mos
quit
o la
rvae
& o
ther
inse
ct p
reys
Aedes, A
nophele
s &
Cu
lex
Ae. a
egypti
, An
. ste
phen
si
& C
x.
qu
inqu
efa
scia
tus
An
. ste
phen
si
& C
x.
qu
inqu
efa
scia
tus
Ae.
aegypti
(la
rvae
and
pupa
e)
Cx
. qu
inqu
efa
scia
tus
(lar
vae
and
pupa
e)
Ae.
aegypti
An
. gam
bia
e s
.s.
Cx
. pip
ien
s
qu
inqu
efa
scia
tus
Cx
. qu
inqu
efa
scia
tus
Ae.
alb
opic
tus &
Ochle
rota
tus t
ris
eria
tus
Pred
ato
r
Noto
necta
un
du
late
(Hem
ipte
ra)
Cx
. (L
utz
ia)
fuscan
us
(Dip
tera
)
En
ithares i
ndic
a (
Hem
ipte
ra)
Labellu
la s
p.
(Nai
ad)
(Odo
nata
)
Sia
gra h
oggaric
a (
Hem
ipte
ra)
Tx
. ru
tilu
s r
uti
lus (
Dip
tera
)
Ochth
era c
haly
besceen
s
(Dip
tera
)
Bu
en
oa s
p.
(Hem
ipte
ra)
Cu
liseta
lon
gia
reola
ta
(Dip
tera
)
Coreth
rella a
ppen
dic
ula
ta
(Dip
tera
)
Facto
r
Pre
y sp
ecie
s
Bio
logi
cal
Pre
y st
age
Pre
y si
ze
242
Scot
t &
Mur
doch
,19
83
Yasu
da &
Hag
imor
i,19
97
Pra
kash
& P
onni
ah,
1978
Tha
ngam
&K
athi
resa
n, 1
996
Sula
iman
& J
effe
ry,
1986
Min
akaw
a et
al.,
2007
Wat
tal
et
al.,
199
6
Pra
kash
& P
onni
ah,
1978
Nils
son
&So
ders
trom
, 19
88
Was
hino
, 19
69
pre
fere
nce
fi
rst
incr
ease
d
and
th
en
dec
reas
ed
wit
hin
crea
sing
pre
y si
ze
Con
sum
ptio
n of
2nd
ins
tar
prey
inc
reas
ed c
onve
xly
tow
ard
an u
pp
er a
sym
pto
te,
ho
wev
er s
igm
oid
ass
oci
atio
n w
asob
serv
ed w
ith
4th i
nsta
r pr
ey.
Alt
houg
h yo
unge
r pr
edac
eous
larv
ae c
onsu
med
mor
e 2nd
ins
tar
prey
tha
n 4th
ins
tar,
old
erpr
edac
eous
lar
vae
pref
erre
d 4th
ins
tar
prey
Wit
h i
ncr
easi
ng
pre
y si
ze,
Cx
. ra
pto
r r
equ
ire
1,6
and
62
min
utes
to
hand
le s
ingl
e 2nd
, 3rd
and
4th
inst
ar l
arva
wei
ghin
g0.
2, 1
.2 a
nd 4
.3 m
g re
spec
tive
ly
1st,
2nd i
nsta
rs p
reda
tors
pre
ferr
ed t
he 1
st i
nsta
r of
the
pre
yw
hile
ins
tars
3 a
nd 4
pre
ferr
ed p
rey
inst
ars
2 an
d 3
Lar
vae
cou
ld e
ach
co
nsu
me
up
to
10
1st i
nst
ar a
nd
10
4th
inst
ar p
rey
larv
ae p
er d
ay.
Pre
y si
ze d
oes
not
affe
ct p
reda
tion
cap
acit
y
An
. ste
ph
en
si
was
p
refe
rred
fo
llo
wed
b
y C
x.
qu
inqu
efa
scia
tus a
nd
Ae.
aegy
pti
Th
e p
erce
nta
ge
of
pre
y k
ille
d
and
le
ft
un
con
sum
edin
crea
sed
wit
h an
inc
reas
e in
pre
y de
nsit
y
At
a hi
gh d
ensi
ty o
f pr
ey l
arva
e, l
arva
e of
all
ins
tars
of
the
larg
er
spec
ies
A.
erich
so
ni
had
si
gnif
ican
tly
hig
her
con
sum
pti
on
rat
es t
han
th
e sm
alle
r sp
ecie
s A
. op
acu
s.
At
a lo
w p
rey
den
sity
th
e d
iffe
ren
ces
wer
e sm
alle
r an
d o
nly
3rd i
nsta
r pr
edat
ors
larv
ae d
iffe
red
sign
ific
antl
y.
Co
rix
ids
fed
les
s u
po
n m
osq
uit
o l
arva
e th
an t
he
oth
erp
red
ato
rs
mos
quit
o la
rvae
mos
quit
o la
rvae
Cx
. fa
tigan
s
Cx
. qu
inqu
efa
scia
tus
Ae.
alb
opic
tus
An
. gam
bia
e s
.s.
Ae. a
egypti
, An
. ste
phen
si
& C
x.
qu
inqu
efa
scia
tus
Cx
. fa
tigan
s
Ae.
com
mu
nis
mos
quit
o la
rvae
Noto
necta
hoff
man
i
(Hem
ipte
ra)
Tx
. to
waden
sis
(D
ipte
ra)
Cx
. rapto
r (
Dip
tera
)
Laccon
ectu
s p
un
cti
pen
nis
(Col
eopt
era)
Ochth
era c
haly
besceen
s
(Dip
tera
)
En
ithares i
ndic
a
(Hem
ipte
ra)
Cx
. r
apto
r (
Dip
tera
)
Agabu
s e
ric
hson
i &
A. o
pacu
s
(Col
eopt
era)
Abedu
s i
nden
tatu
s,
Belo
sto
ma f
lum
ineu
m,
Coris
ella s
p.
& c
orix
ids
(Hem
ipte
ra)
Pre
y st
age
abun
danc
e
Pre
y de
nsit
y
243
Man
dal
et
al.,
200
8
Saha
et
al.,
200
7
Lund
kvis
t et
al.,
2003
Shaa
lan
et
al.,
200
7
Nel
son,
197
7
Stew
art
& M
iura
,19
78
Adi
tya
et
al.,
2005
Th
e d
aily
fee
din
g ra
te v
arie
d a
mo
ng
the
od
on
ate
spec
ies.
The
mea
n nu
mbe
r of
IV
inst
ars
Cx
. qu
inqu
efa
scia
tus l
arva
ek
ille
d p
er d
ay,
ran
ged
bet
wee
n 1
4 an
d 6
4 (6
4 m
osq
uit
ola
rvae
fo
r I.
forcip
ata
, 57
fo
r A
. fl
av
ifr
on
s,
45 f
or
R.
ign
ipen
nis
, 25
for
S.
du
ru
m a
nd 1
4 fo
r C
. ka
sh
mir
um
).
A s
ingl
e ad
ult
of A
. bou
vie
ri,
D.
ru
sti
cu
s a
nd D
. a
nn
ula
tus
con
sum
ed 2
-34,
11-
87 a
nd
33-
122
fou
rth
-in
star
mo
squ
ito
larv
ae p
er d
ay r
espe
ctiv
ely.
The
pre
dato
ry im
pact
(P
I) v
alue
sw
ere
14.7
7–17
.31,
46.
9–55
.73,
and
61.
74–7
2.72
lar
vae/
day
for
A.
bou
vie
ri,
D.
ru
sti
cu
s,
and
D.
an
nu
latu
s,
resp
ecti
vely
wh
ile
the
clea
ran
ce r
ate
(CR
) va
lue
ran
ge w
as 9
.06–
13.2
5fo
r A
. bou
vie
ri,
13.
64–1
5.99
for
D.
ru
sti
cu
s, a
nd 1
3.50
–16.
52la
rvae
l/da
y/pr
edat
or f
or D
. a
nn
ula
tus. T
he v
alue
s of
mut
ual
inte
rfer
ence
co
nst
ant,
“m
,” r
emai
ned
0.0
6–0.
78 f
or
A.
bou
vie
ri,
0.0
03–0
.25
for
D.
ru
sti
cu
s,
and
0.0
9–0.
27 f
or
D.
an
nu
latu
s, a
nd d
id n
ot v
ary
betw
een
the
days
. The
dif
fere
nce
in p
reda
tory
eff
icie
ncy,
CR
, and
PI v
alue
s va
ried
sig
nifi
cant
lyam
ong
the
thre
e pr
edat
ors,
indi
cati
ng th
e po
ssib
le d
iffe
renc
ein
the
fun
ctio
n as
pre
dato
rs o
ccup
ying
the
sam
e gu
ild.
Coly
mbete
s p
ay
ku
lli
cho
sed
mo
squ
ito
lar
vae
mo
re o
ften
but,
bot
h o
ther
pre
dato
rs p
refe
rred
Da
ph
nia
sp
p.
Dip
lon
ych
us s
p. p
reye
d up
on l
arva
l an
d pu
pal
stag
es o
f C
x.
an
nu
lirostr
is a
nd m
ore
effi
cien
t th
an A
nis
op
s s
p.
that
fed
on l
arva
l st
age
only
.
Dy
tiscu
s m
argin
ali
s w
as c
onsi
sten
tly
mor
e ef
fect
ive
than
Hy
drop
hil
us t
ria
ngu
laris
.
N.
un
ifa
scia
ta a
dult
s ha
ve a
n ov
eral
l hi
gher
dai
ly k
illi
ng o
fth
an B
. scim
itra
Bot
h bu
g sp
ecie
s co
nsum
ed b
oth
4th in
star
larv
ae a
nd p
upae
of A
r.
su
ba
lba
tus i
n qu
ite
good
num
bers
dep
endi
ng o
n th
eir
rela
tive
ab
un
dan
ce
Cx
. qu
inqu
efa
scia
tus
Cx
. qu
inqu
efa
scia
tus
Cu
lex m
osqu
itoe
s &
Daphn
ia
Cx
. an
nu
lirostr
is
2nd, 3
rd a
nd 4
th s
tage
larv
ae C
x.
qu
inqu
efa
scia
tus
4th i
nsta
r C
x.
pip
ien
s
qu
inqu
efa
scia
tus l
arva
e
Arm
igeres s
ubalb
atu
s
(dif
fere
nt r
atio
s &
dens
itie
s of
lar
vae
and
pupa
e)
Aeshn
a f
lavif
ron
s,
Coen
agrio
n k
ashm
iru
m,
Ischn
ura f
orcip
ata
,R
hin
ocypha i
gn
ipen
nis
and
Sym
petr
um
du
ru
m (O
dona
ta)
An
isops b
ou
vie
ri,
Dip
lon
ych
us
(=
Sphaerodem
a) r
usti
cu
s
and
Dip
lon
ychu
s a
nn
ula
tus
(Hem
ipte
ra)
Coly
mbete
s p
ayku
lli,
Ily
biu
s
ate
r &
I. f
uli
gin
osu
s
(Col
eopt
era)
Dip
lon
ychu
s s
p. &
An
isops
sp
. (H
emip
tera
)
Dyti
scu
s m
argin
ali
s a
ndH
ydrophil
us t
ria
ngu
laris
(Col
eopt
era)
.
Noto
necta
un
ifascia
ta a
ndB
uen
oa s
cim
itar (
Hem
ipte
ra)
Sphaerodem
a a
nn
ula
tum
and
S.
ru
sti
cu
m (
Hem
ipte
ra)
Pre
dato
r sp
ecie
s
244
Pre
dato
r st
age
Ony
eka,
198
3
Gri
swol
d &
Loun
ibos
, 20
06
Adi
tya
et
al.,
200
6
Wat
tal
et
al.,
199
6
Cor
doba
& L
ee,
1995
Wat
tal
et
al.,
199
6
Th
e an
iso
pte
ran
S
ym
petr
um
str
io
latu
m
was
m
ore
vora
ciou
s th
an t
he z
ygop
tera
n C
oen
agrio
n p
uell
a.
Ove
rall
sur
vivo
rshi
p of
bot
h pr
eys
decr
ease
d gr
eatl
y in
the
pre
sen
ce o
f th
e to
p p
red
ato
r T
ox
orh
yn
ch
ites w
hil
st t
he
inte
rmed
iate
p
red
ato
r C
oreth
rell
a
incr
ease
d
the
surv
ivo
rsh
ip o
f th
e n
ativ
e p
rey
spec
ies
Och
lerota
tus an
dde
crea
sed
surv
ivor
ship
of
the
inva
sive
pre
y sp
ecie
s A
ede
sco
mp
ared
to
tre
atm
ents
wit
ho
ut
pre
dat
ors
in
art
ific
ial
anal
ogue
s of
wat
er-f
ille
d tr
ee h
oles
Pre
dat
ion
rat
e o
f R
ha
ntu
s r
ange
d b
etw
een
21.
56 &
86.
89la
rvae
/ d
ay d
epen
din
g o
n p
rey-
pre
dat
or
den
siti
es.
Th
ep
red
ato
r im
pac
t (P
I) r
emai
ned
bet
wee
n 1
8.67
& 3
5.33
larv
ae/d
ay d
epen
ding
on
prey
den
siti
es, w
hile
the
cle
aran
cera
te (
CR
) ra
nge
s b
etw
een
2.2
1 &
2.2
3 la
rvae
lit
res/
day
/p
red
ato
r. C
om
par
ativ
ely,
th
e T
ox
orh
yn
ch
ite
s co
nsu
med
pre
y la
rvae
at
the
rate
of
0.67
to
34.
22 l
arva
e/ d
ay,
depe
ndin
g pr
ey-p
reda
tor
dens
itie
s. T
hepr
edat
or i
mpa
ct (
PI)
rang
es b
etw
een
7.67
& 1
1.33
lar
vae/
day,
and
the
cle
aran
cera
te (
CR
) ra
nge
d b
etw
een
1.4
1 &
1.7
6 la
rvae
lit
res/
day
/p
red
ato
r.
No
mar
ked
dif
fere
nce
in
pre
dat
ion
by
1st t
o 4
th n
ymp
hal
inst
ars
of t
he p
reda
tor
whi
le p
reda
tion
of
5th n
ymph
al i
nsta
ran
d ad
ult
bugs
was
not
icea
bly
low
for
An
ophe
les
larv
ae b
utqu
ite
high
for
Cu
lex
lar
vae
Lar
ger
nai
ads
ate
mo
re l
arva
e w
ith
ou
t sh
ow
ing
any
pre
fere
nce
fo
r 1st
or
4th i
nst
ar w
hil
e sm
alle
r n
aiad
spr
efer
enti
ally
ate
4th
ins
tar.
Seco
nd i
nsta
r la
rvae
of
the
pred
ator
con
sum
ed A
e.
aegy
pti
larv
ae s
igni
fica
ntly
at
a hi
gher
rat
e th
an t
he o
ther
ins
tars
.E
xce
pt
for
2nd i
nst
ar p
red
ato
rs,
oth
er i
nst
ars
sho
wed
asi
gnif
ican
t re
du
ctio
n i
n a
ttac
k r
ate
and
an
in
crea
se i
nha
ndli
ng t
ime
3rd i
nsta
r la
rvae
of
Cu
lex
pip
ien
s
Ae.
Alb
opic
tus &
Ochle
rota
tus t
ris
eria
tus
Cx
. qu
inqu
efa
scia
tus
An
. ste
phen
si
& C
x.
qu
inqu
efa
scia
tus
Mos
quit
o la
rvae
Ae.
aegypti
lar
vae
Sym
petr
um
str
iola
tum
an
d
Coen
agrio
n p
uella
(Odo
nata
)
Tx
. R
uti
lus &
Coreth
rella
appedic
ula
ta (
Dip
tera
)
Tx
. Sple
nden
s &
R
han
tus
sik
kim
en
sis
(D
ipte
ra &
Col
eopt
era)
En
ithares i
ndic
a
(Hem
ipte
ra)
Orth
em
is f
erru
gin
ea
(Odo
nata
)
Tx
. sple
nden
s (
Dip
tera
)
245
Pre
dato
r pr
eyde
nsit
y
Aqu
atic
veg
etat
ion
Tem
pera
ture
Pra
man
ik &
Rau
t,20
03
Cha
ndra
et
al.,
200
8
Venk
ates
an &
Siva
ram
an,
1984
Miu
ra &
Tak
ahas
hi,
1988
Shaa
lan
et
al.,
200
7
Mur
doch
et
al.,
198
4
Nils
son
&So
ders
trom
, 19
88
Man
dal
et
al.,
200
8
The
1st
and
3rd
ins
tars
of
Tx.
spl
ende
ns s
how
ed l
owes
t an
dhi
ghes
t pr
edat
ion
rate
, re
spec
tive
ly.
Pre
dati
on r
ate
by a
nyst
age
of
the
pre
dat
or
was
hig
hes
t in
1st
in
star
lar
vae
and
low
est
in 4
th in
star
larv
ae o
f al
l pre
y sp
ecie
s. T
he v
aria
tion
sin
con
sum
ptio
n ra
te s
eem
ed t
o be
rel
ated
wit
h th
e si
ze o
fth
e pr
ey la
rvae
off
ered
rat
her
than
to
the
pref
eren
ce f
or a
nysp
ecie
s.
The
pre
y co
nsum
ptio
n of
the
lar
vae
of A
. su
lca
tus d
iffe
red
sign
ific
antl
y w
ith
dif
fere
nt
pre
y, p
red
ato
r an
d v
olu
me
com
bin
atio
ns
Att
ack
rat
e in
crea
sed
wh
ilst
han
dli
ng
tim
e d
ecre
ased
.La
rges
t pr
edat
or i
nsta
r ki
lled
max
imum
num
ber
of s
mal
lest
prey
and
sm
alle
st p
reda
tor
inst
ar k
ille
d m
inim
um
nu
mb
ero
f la
rges
t p
rey
of
bo
th m
osq
uit
o s
pec
ies.
Lar
ger
pre
dat
or
inst
ars
exh
ibit
ed m
ore
su
cces
sfu
l at
tack
an
d s
ho
rter
hand
ling
tim
e th
an s
mal
ler
pred
ator
ins
tars
.
Whe
n de
nsit
y of
pre
y an
d pr
edat
ors
wer
e va
ried
mor
e pr
eyw
as c
on
sum
ed a
s p
rey
den
sity
in
crea
sed
ho
wev
er f
ewer
prey
wer
e co
nsum
ed a
t hi
gher
pre
dato
r de
nsit
ies
Sig
nif
ican
tly
affe
cted
th
e p
red
atio
n p
ote
nti
al o
f b
oth
pre
dat
ors
.
Han
dli
ng
tim
e d
ecli
ned
wh
ile
atta
ck r
ate
incr
ease
d w
ith
tem
per
atu
res
At
low
tem
per
atu
re (
2Cº)
, la
rvae
of
A.
op
acu
s h
ad a
sign
ific
antl
y h
igh
er c
on
sum
pti
on
rat
e th
an t
ho
se o
f A
.co
ng
en
er
bu
t at
15
Cº,
no
sig
nif
ican
t d
iffe
ren
ce w
aso
bse
rved
.
The
pre
y co
nsum
ptio
n w
as i
nver
sely
rel
ated
wit
h sp
ace
Ae. a
egypti
, An
. ste
phen
si,
Arm
igeres s
ubalb
atu
s
and
Cx
. qu
inqu
efa
scia
tus
Cx
. qu
inqu
efa
scia
tus
Ae. a
egypti
and
Cx
.fa
tigan
s (
4 la
rval
ins
tars
of t
he p
reys
at
vary
ing
dens
itie
s)
Cx
. ta
rsali
s
Cx
. an
nu
lirostr
is
Mos
quit
o la
rvae
Ae.
com
mu
nis
Cx
. qu
inqu
efa
scia
tus
Acil
ius s
ulc
atu
s
(Col
eopt
era)
Dip
lon
ychu
s i
ndic
us
(Hem
ipte
ra)
En
allagm
a c
ivil
e (
Odo
nata
)
Dip
lon
ychu
s s
p. &
An
isops
sp
. (H
emip
tera
)
Noto
necta
hoff
man
i
(Hem
ipte
ra)
Agabu
s e
ric
hson
i &
A.
opacu
s (
Col
eopt
era)
Aeshn
a f
lavif
ron
s,
Coen
agrio
n k
ashm
iru
m,
Ischn
ura f
orcip
ata
,R
hin
ocypha i
gn
ipen
nis
and
Sym
petr
um
du
ru
m
(Odo
nata
)
246
Phy
sica
l
For
agin
g ar
ea
Wat
er t
empe
ratu
re
Wat
er D
epth
Illu
min
atio
n
Cha
ndra
et
al.,
200
8
Pra
kash
& P
onni
ah,
1978
Shaa
lan
et
al.,
200
7
Am
alra
j &
Das
, 19
98
Am
alra
j &
Das
, 19
98
Min
akaw
a et
al.,
2007
Man
dal
et
al.,
200
8
Cha
ndra
et
al.,
200
8
Cha
tter
jee
et
al.,
2007
Lee,
196
7
Fee
ding
rat
e de
crea
sed
wit
h th
e vo
lum
e of
wat
er.
Th
e p
red
atio
n c
apac
ity
was
no
t in
flu
ence
d b
y ch
ange
s in
wat
er v
olum
e
Sign
ific
ant
effe
cted
An
isop
s c
apac
ity
but
effe
ct o
f fo
ragi
ngar
ea w
as p
rono
unce
d in
Dip
lon
ych
us n
ymph
s on
ly.
For
agin
g su
rfac
e di
d no
t in
flue
nce
the
pred
atio
n ra
te
Pre
dati
on w
as h
igh
at h
igh
wat
er t
empe
ratu
re h
owev
er;
itdi
d no
t in
flue
nce
prey
han
dlin
g ti
me.
Th
e p
red
atio
n c
apac
ity
was
no
t in
flu
ence
d b
y ch
ange
s in
wat
er d
epth
Th
e fe
edin
g ra
tes
vari
ed s
ign
ific
antl
y b
etw
een
dar
k a
nd
ligh
t co
nd
itio
ns,
in
all
th
e o
do
nat
e sp
ecie
s. D
ark
nes
s h
adn
egat
ive
infl
uen
ce.
Fee
ding
rat
e of
did
not
dif
fer
betw
een
the
ligh
t-on
and
dar
k.
Th
e co
nsu
mp
tio
n r
ate
was
sig
nif
ican
tly
hig
her
du
rin
g th
eli
ghts
-on
phas
e th
an d
urin
g th
e li
ghts
-off
pha
se
Dar
knes
s di
d no
t si
gnif
ican
tly
affe
ct t
he p
reda
tion
act
ivit
yb
ut
the
od
on
ate
nai
ads,
Tra
mea
, h
ave
co
nsu
med
mo
rela
rvae
in
dark
ness
tha
n in
nor
mal
ill
umin
atio
n
Cx
. qu
inqu
efa
scia
tus
Cx
. fa
tigan
s
Cx
. an
nu
lirostr
is
Ae.
aegypti
lar
vae
Ae.
aegypti
lar
vae
An
. G
am
bia
e s
.s.
Cx
. qu
inqu
efa
scia
tus
Cx
. qu
inqu
efa
scia
tus
An
. su
bpic
tus
Cs.
incid
en
s
Acil
ius s
ulc
atu
s (
Col
eopt
era)
Cx
. rapto
r (
Dip
tera
)
Dip
lon
ychu
s s
p. &
An
isops
sp
. (H
emip
tera
)
Tx
. Sple
nden
s (
Dip
tera
)
Tx
. sple
nden
s (
Dip
tera
)
Ochth
era c
haly
besceen
s
(Dip
tera
)
Aeshn
a f
lavif
ron
s,
Coen
agrio
n k
ashm
iru
m,
Ischn
ura f
orcip
ata
,R
hin
ocypha i
gn
ipen
nis
and
Sym
petr
um
du
ru
m
(Odo
nata
)
Acil
ius s
ulc
atu
s
(Col
eopt
era)
Brachytr
on
prate
nse
Dyti
scu
s m
argin
icoli
s,
Leste
s c
on
gen
er,
Noto
necta
shootr
ii, T
ram
ea l
acerate
, T.
torosa
(C
oleo
pter
a, O
dona
ta&
Hei
pter
a)
247
predacious beetle larvae. Contrarily,treatment with parathion 7 days after the B.t.H14 application severely reduced thenumbers of the beetle larvae. Cx. pipiens
quinquefasciatus larvae predation wasgreater when a combination of thehemipteran predator Buenoa sp. and thebacteria B. t. var. israelensis were presentthan when each was used separately(Rebollar-Tellez et al., 1994). The predaceousbackswimmer N. irrorata and the bacteriumB. t. var. israelensis were assessedseparately and in combination with eachother to suppress mosquitoes on larvalpopulation of mosquitoes maintained underexperimental field conditions (Barbosa et al.,1997). The combination treatment of bothbacterium and predator gave the best resultwith no harmful effect on the predators. Zerodensities of Ae. aegypti larvae per dipoccurred more frequently in plasticcontainers treated with both agents thanwith individual agents. Painter et al. (1996)mentioned that repeated applications of B.t. i. to the mosquito predator Erythemis
simplicicollis (Odonata: Libellulidae) fromhatching to final instar did not affectdevelopment to the adult stage, morphologyor maiden flight capability. A 3-year study,2000-2002, field study for mosquito controlwith B. s. in southeastern Wisconsin revealedthat no detrimental effects to nontargetorganisms, in particular predaceous insects,could be attributed to this microbialinsecticide (Merritt et al., 2005).
Although both Bti and Bs are safe toother non-target organisms (Mittal, 2003) andrecommended as ideal control agents inintegrated mosquito control (Lacey, 2007),Collins & Blackwell (2000) reported that,problems have arisen in combining themwith some Toxorhynchites mosquitoes.Lacey & Dame (1982) showed that fourthinstar Tx. r. rutilus larvae exposed to 1, 5and 10 ppm of Bti in the presence of excessprey (20 Ae. aegypti larvae) responded with23, 62 and 95% mortality respectively after10 days. In the presence of excess larvae 98%mortality was observed 10 days afterexposure to 0.5 ppm. A positive correlationbetween concentration of Bt (H-14; IPS-78)and mortality was observed in fourth instars
of Tx. amboinensis and Tx. brevipalpis inthe presence of Ae. aegypti larvae but Bs
toxins were lethal only to Tx. r. rutilus
(Lacey, 1983).Combinations of insecticides and
predators to control mosquito vectorsshowed a wide range of risk to predators. Insome studies there was no or little risk tothe predators. Djam & Focks (1983) foundthat, except for resmethrin, the ED90 forfenithion, chlorypyrifos, naled and malathionfor Tx. amboinensis were 1.6 times greaterthan Ae. aegypti and females of theToxorhynchites mosquito were somewhatless susceptible than the males to all of thecompounds tested. These results suggestthat there is little possibility of applyingthose insecticides (except resmethrin) at alevel sufficient to control Ae. aegypti adultswithout affecting the Tx. amboinensis adultpopulation. The relatively short lifespan ofTx. amboinensis suggests that the optimaltime for insecticide application would be justprior to the release of the predators. Inanother similar investigation, theconcentrations of resmethrin, malathion andnaled caused 50% mortality to first instar Tx.splendens larvae were 2.87, 69.1 and 623 ppbrespectively (Tietze et al., 1993). Theintegrated treatment using a groundapplication of ULV-applied malathion andweekly release of the predaceous mosquitoTx. amboinensis reduced the Ae. aegypti
population by 96% compared to 29% formalathion alone during the 14-week study inresidential neighbourhoods in New Orleans,Louisiana, USA (Focks et al., 1986). Rawlins& Ragoonansingh (1990) found thatpredaceous larvae, Toxorhynchites
moctezuma, from Trindad were lesssusceptible to temephos insecticide than Ae.aegypti larvae, indicating its possibleusefulness in an integrated managementprogram. In a laboratory study Focks (1984)investigated the impact of sublethalexposure on subsequent longevity, fecundityand egg hatch on Tx. r. rutilus if thepyrethroid insecticide resmethrin was usedwithout regard to the date of predatorrelease. The exposure of Tx. r. rutilus toresmethrin at the LD90 dose for Ae. aegypti
reduced neither the adult survival nor egg
248
hatch. Contrarily, average fecundity wasreduced from 5.6 to 2.3 eggs/female/dayduring the first three or four days ofoviposition. Accordingly, the authorconcluded that; minimizing the reduction infecundity of Tx. r. rutilus in integrating usewith resmethrin requires certain adjustmentsparticularly limiting insecticide applicationprior to predator release. If this practicewere followed, only those predators whichhad already been in the field for several dayswould be exposed and consequently theeffect on fecundity would be minimized.Although previous studies showed no or littlerisk of insecticides to the predators, otherstudies showed highest levels of risk. In fieldstudy using insecticide to control rice fieldmosquitoes in California, Schaefer et al.(1981) reported that a single application ofnon-selective toxic agent to rice fields couldsufficiently disrupt the predator complex sothat resurgence of mosquito larvaepopulations can continue for a long period.The spraying of the Kenyan rice fields killedboth An. gambiae and predators (Service,1977). Moreover, the mosquitoes re-established themselves very quickly but re-colonization by the predators was slower.Jebanesan & Vadani (1995) found that anincrease in the concentration of thepyrethroid insecticide, K-Othrine, resulted ina decrease in the predation of Cx.quinquefasciatus larvae by Diplonychus
indicus. A reduction in predation wasnoticed at the highest concentration and wasproportional to the interference of theinsecticide in the nervous co-ordination ofthe bug. The application of fipronil andlambda-cyhalothrin insecticides for controlof the rice water weevil, Lissorhoptrus
oryzophilus, in Arkansas rice fieldsproduced deleterious effects on nontargetpredaceous insects (Dennett et al., 2003). Amarked difference in susceptibility wasfound between selected nontarget insects.Lambda-cyhalothrin adversely affectedpopulations of nontarget beneficial insects,such as the scavenger beetle Tropisternus
lateralis and the backswimmer N. indica,whereas nontarget pestilent species, such asAnopheles quadrimaculatus, proliferated.Contrarily, Fipronil achieved higher
percentages of control against An.quadrimaculatus and was less harmful toboth nontarget predators.
Unlike the use of combined insecticidesand Bacillus bacteria, the reported use ofcombining IGRs with predators in integratedmosquitoes management is rare. Applicationof Methoprene, Stauffer-20458 andThompson-Hayward-6o40 at 0.025 Ib AI/acrefor controlling Psorophora columbiae in ricefields caused significant reductions in certainpredaceous aquatic insect populations(Tropisternus spp. adults and libellulidimmatures) while no significant reductionsin other predaceous aquatic insects “Votonecta spp. adults and immatures, corixidadults and immatures and Thermotieclus
spp. Adults” occurred at 0.25 Ib AI/acre(Steelman et al., 1975). In another field studyevaluating safety and integration ofmethoprene and predaceous insects, Miuraet al. (1978a) stated that combined effect ofmethoprene briquet treatments and thenotonectid bugs, N. unifasciata and B.scimitar, suppressed Cx. tarsalis
populations in the breeding sites and thetreatments did not affect the reproductive,developmental or predatory activities of bothpredators. Impact of the insect growthregulator hexaflumuron was studied againstAnisops bouvieri and Diplonychus rusticus,which are potential predators of mosquitoimmatures (Vasuki, 1996). These predatorswere not susceptible to hexaflumuron at adose range from 0.0001- 1.0 mg/l and theirefficacy did not significantly alter atsublethal concentrations. Other predators(Ranatra sp., dragon fly larvae and acyclopoid copepod, Mesocyclops leukarti)also survived at 1.0 mg/l which indicated thesafety and utility of hexaflumuron inintegrated mosquito management.
It could be concluded that contributionsof predators in integrated mosquito controlwill reduce the percentage of nuisancemosquitoes emergence and in terms ofmosquito vectors transmitted disease willalso reduce the probability of diseasestransmission. The lack of interactionbetween larvae of mosquito vectors and theirnatural enemies and/or lower predatorsurvivorship in certain habitats, particularly
249
shallow water pools and cement tanks (Daset al., 2006) and urban environments suchas temporal habitats (Carlson et al., 2004),may cause a sudden increase in mosquitovectors densities and subsequent diseasetransmission. Furthermore, utilizingpredaceous aquatic insects with Bacillus
bacteria was more successful thancombinations of predaceous insects andinsecticides in particular against containerbreeding mosquitoes such as the denguevector mosquito Ae. aegypti. Contrarily,combinations of predaceous insects andinsecticides for controlling both rice fieldand container breeding mosquito vectors arenot risk free because some insecticidesproduce predators’ mortalities andpredators’ re-colonizing is slower thanmosquitoes re-establishing. Preliminaryresults of the IGRs, in particularhexaflumuron, suggest their safety andadaptability in integrated mosquito control.
Difficulities for utilizing predaceous
insects for mosquito control
Although these are successful examples ofpredators, there are difficulties associatedwith rearing; colonization and handlingwhich are obstacles to a more widespreadutilization of predaceous aquatic insects(Garcia, 1982). The second difficulty ispolyphagy that has advantages anddisadvantges (Murdoch et al., 1984). Anadvantage is that these predators can survivewhen mosquito larvae are rare or absent,while a disadvantage is that they may notreduce mosquito larvae due to availabilityof alternative preys. The third difficulity isthe presence of other invertebrates andvertebrates predators that may reduce theabundance of the predaceous insects(Larson, 1990). The fourth difficulty ispredators may interfere through chemical orother cues; for instances the hydrophilidTropisternus lateralis (Resetarits, 2001) andthe phantom midge Chaoborus albatus
(Petranka & Fakhoury, 1991) avoid layingeggs in pools with fish. The fifth difficulty isthe avoidance by mosquitoes of watercontaining invertebrate predators such asbackswimmers and dragonflies and makespredator’s impact more complicated.
Additionally, Washburn (1995) pointedout that control of ground pool mosquitoesusing biological control agents is morefeasible than container breeding mosquitoesdue to the following physical and biologicalfeatures: (1) Natural enemies limit mosquitolarvae in ground pools whereas those incontainers are limited by resourceavailability, ( 2) Containers are smaller thanground pools and lack internal primaryproductivity, (3) Container habitats supportsmaller populations of fewer speciescompared with ground pools, implying thatit may be more difficult to establish naturalenemies in small container habitats, (4) Thelake of primary productivity withincontainers may limit the number of trophiclevels and reduce the likelihood ofestablishing and maintaining predatorpopulation, and (5) Larval mosquitopopulations in containers are regulated bycompetitive interactions and mortality fromnatural enemies is likely to be compensatory.
These habitat and populationcharacteristics, combined with difficulties inlocating and treating containers have limitedthe implementation of biological controlagents to suppress mosquitoes developing inwater filled containers. Contrarily, Kumar &Hwang (2006) pointed out in their reviewthat only biological control agents such asaquatic predaceous insects carry thepotential for overcoming such obstacles andhave the ability to adapt to various aquaticbodies including containers. The successfulcontrol strategy for container breedingmosquitoes that they pointed in their reviewwas eliminating Ae. aegypti populations byintroducing dragonfly larvae into domesticcontainers accommodating Ae. aegypti
larvae in Myanmar (the experiment wasconducted by Sebastian et al., 1990). Theyhave also pointed out that the selection of abiological control agent, mainly predator, inany vector suppression program should bebased on: (1) Its self-replicating capacity, (2)Preference for the target mosquito vectorpopulation in the presence of alternatenatural prey, (3) Adaptability to theintroduced environment, and (4) Overallinteractions with the indigenous organisms.
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CONCLUSION
In conclusion, predaceous insects are closelyassociated with mosquito immatures as theycohabit in a wide variety of aquatic habitatssuch as rice fields, tree holes, man-madeponds, snowmelt pools, temporary lagoons,floodwaters and rain pools. Those predatorssignificantly affect the survival, developmentand recruitment levels of mosquitoes whichmost likely has an influence on vector-bornedisease transmission rates. Biological andphysical conditions were found to influencecapacity of such predators. Biologicalconditions divided into predator and preyfactors. Species, competence and predator-prey density were the most commonpredator factors while species, stage andprey density were more likely prey factors.Illumination, temperature, container size andforaging area were the physical conditionsthat have been searched. Also field studiesand implementation of predaceous aquaticinsects in integrated vector control weredocumented in some circumstances. As canbe expected, further studies are needed toensure successful and satisfactory mosquitocontrol with predaceous insects.
Another important advantage ofpredators is their released kairomones thathave the potency to repel ovipositing femalemosquitoes for over a week. If thesekairomones were commercially produced,they may provide eco-friendly and effectivemosquito control, but more research isnecessary to determine total impact. Thus,understanding the interaction betweenmosquito vectors and their aquaticpredaceous insects is imperative fordeveloping and implementing successfulbiological or integrated control measuresthat include the use of predators and/or theirkairomones.
Utilizing biological organisms to controlmosquito larvae is not only eco-friendly, butconstitutes a means by which more effectiveand sustainable control can be achieved.This would be preferable to relying solelyupon synthetic insecticides which are notbeing developed fast enough to combatresistance. As is always the case, the
elimination of aquatic larval stages is aproactive measure whereas control ofpotentially infective adult mosquitoes is areactive response necessitated byinadequate management. In this context,predators should be seriously considered forthey have the advantage that they can adaptto various water bodies that are enormouslyscattered around and within humansettlements. Once established andeffectively auto-reproducing, predators canachieve sustainable mosquito control to adegree that no chemical can hope to aspire.
Finally and likewise Quiroz-Martine &Rodriguez-Castro (2007), we alsorecommend certain factors to must be takeninto account when considering predaceousinsects for mosquito control. These factorsinclude: preference or selectivity of the preyby the predator, species diversity in mosquitobreeding site, stability of the aquatic system,larval density, position of the predator in thewater column, appropriate number ofpredators to be released, recovery of thelarval population, predator-prey co-evolution, predator-prey synchronization,refuge and community participation.
Acknowledgment. We thank the anonymousreviewers whose comments led to a greatlyimproved manuscript.
REFERENCES
Aditya, G., Ash, A. & Saha, G.K. (2006).Predatory activity of Rhanyus
sikkimensis and larvae of Toxo-
rhynchites splendens on mosquitolarvae in Darjeeling, India. Journal of
Vector borne Diseases 43(1): 66-72.Aditya, G., Bhattacharyya, S., Kundu, N.,
Saha, G.K. & Raut, S.K. (2004). Predatoryefficiency of the water bug Sphaerodema
annulatum on mosquito larvae (Culex
quinquefasciatus) and its effect onthe adult emergence. Bioresource
Technology 95: 169–172.Aditya, G., Bhattacharyya, S., Kundu, N.,
Saha, G.K. & Raut, S.K. (2005).Frecuency-dependent prey-selection of
251
predaceous water bugs on Armigeres
subalbatus immatures. Journal of Vector
Borne Diseases 42(1): 9-14.Aditya, G., Pramanik, M.K. & Saha, G.K.
(2006). Larval habitats and speciescomposition of mosquitoes in DarjeelingHimalayas, India. Journal of Vector
Borne Diseases 43(1): 7-15.Alahmed, A.M., Alamr, S.A. & Kheir, S.M.
(2009). Seasonal activity and predatoryefficacy of the water bug Siagra
hoggarica Poisson (Hemiptera:Corixidae) against the mosquito larvaeCulex quinquefasciatus (Diptera:Culicidae) in Riyadh city, Saudi Arabia.Journal of Entomology 6(2): 90-95.
Al-Saadi, M. & Mohsen, Z.H. (1988).Predatory and cannibalistic behavior ofCuliseta longiareolata (Macquart)(Diptera: Culicidae) In Iraq. Journal of
Biological Science and Research 19(2):339-351.
Amalraj, D.D. & Das, P.K. (1998). Estimationof predation by the larvae of Toxo-
rhynchites splendens on the aquaticstages of Aedes aegypti. Southeast Asian
Journal of Tropical Medicine and
Public Health 29: 177-183.Andis, M.D. & Meek, C.L. (1985). Mortality
and survival patterns for the immaturestages of Psorophora columbiae.Journal of the American Mosquito
Control Association 1(3): 357-362.Anis, B., Krisnowardojo, S., Atmosoedjono,
S. & Boewono, D.T. (1990). Toxo-
rhynchites amboinensis larvae releasedin domestic containers fail to controldengue vectors in domestic containersin a rural village in central Java. Journal
of the American Mosquito Control
Association 6(1): 75-78.Anis, B., Krisnowardojo, S., Atmosoedjono,
S. & Supardi, S. (1989). Suppression oflarval Aedes aegypti populations inhouse hold water storage containers inJakarta, Indonesia, through release offirst instar Toxorhynchites splendens
larvae. Journal of the American
Mosquito Control Association 5(2):
235-238.Apiwathnasorn, C., Sucharit, S., Rongsriyam,
Y., Thongrungkiat, S., Deesin, T. &
Punavuthi, N. (1990). Survival ofimmature Culex titaeniorhynchus inpaddy fields. Mosquito Borne Diseases
Bulletin 7(1): 11-16.Arav, D. & Blaustein, L. (2006). Effects of
pool depth and risk of predation onoviposition habitat selection bytemporary pool dipterans. Journal of
Medical Entomology 43(3): 393-397.Axtell, R.C. (1979). Principles of integrated
pest management (IPM) in relation tomosquito control. Mosquito News
39(4): 709-718.Bai, M.G, Viswam, K. & Panicker, K.N. (1982).
Culex (Lutzia) fuscanus (Diptera :Culicidae) – a predator mosquito. Indian
Journal of Medical Research 76(12):
837-839.Barbosa, J.F.N., Martinez, H.Q., Tovar, M.L.R.,
Tejada, L.O. & Badii, M.H. (1997). Use ofbactimos® briquets (B. t. i. Formulation)combined with the back swimmerNotonecta irrorata (Hemiptera:Notonectidae) for control of mosquitolarvae. Journal of the American
Mosquito Control Association 13(1):
87-89.Bay, E.C. (1967). Potential for naturalistic
control of mosquitoes. ProceedingPaper. 35th Annual Conference of
California Mosquito Control
Association 35: 34-37. (Cited in: Bay,E.C. (1974). Predatory-prey relationshipsamong aquatic insects. Annual Review
of Entomology 19: 441-453).Bay, E.C. (1974). Predatory-prey relation-
ships among aquatic insects. Annual
Review of Entomology 19: 441-453.Beketov, M.A. & Liess, M. (2007). Predation
risk perception and food scarcity inducealterations of life-cycle traits of themosquito Culex pipiens. Ecological
Entomology 32: 405-410.Bentley, M.D. & Day, J.F. (1989). Chemical
ecology and behavioral aspects ofmosquito oviposition. Annual Review of
Entomology 34: 401-421.Blaustein, L., Kiflawi, M., Eitam, A., Mangel,
M. & Cohen, J.E. (2004). Ovipositionhabitat selection in response to risk ofpredation in temporary pools: mode ofdetection and consistency across
252
experimental venue. Oecologia 138: 300-305.
Borkent, A. (1980). The potential use oflarvae of Chaoborus cooki Sakther(Diptera: Chaoboridae) as a biologicalcontrol of mosquito larvae. Mosquito
News 40(4): 634-635.Bradshow, W.E. & Holzapfel, C.M. (1983).
Predator-mediated, non-equilibriumcoexistence of tree-hole mosquitoes inSouthern North America. Oecologia 57:
239-256.Breene, R.G., Sweet, M.H. & Olson, J.K.
(1990). Analysis of the gut contents ofnaiads of Enallagma civile (Odonata:Coenagrionidae) from a Texas pond.Journal of the American Mosquito
Control Association 6(3): 547-548.Caillouët, K.A., Joseph, K.J. & Eisele, T.P.
(2008). Characterization of aquaticmosquito habitat, natural enemies, andimmature mosquitoes in the ArtiboniteValley, Haiti. Journal of Vector Ecology
33:191-197.Campos, R.E., Fernandez, L.A. & Sy, V.E.
(2004). Study of insects associated withthe floodwater mosquito Ochlerotatus
albifasciatus (Diptera: Culicidae) andtheir possible predators in Buenos AiresProvince, Argentina. Hydrobiologia
524(1): 91-102.Carlson, J., Keating, J., Mbogo, C.M., Kahindi,
S. & Beier, C. (2004). Ecologicallimitations of aquatic predatorcolonization in the urban environment.Journal of Vector Ecology 29(2): 331-339.
Carpenter, S.J. & LaCasse, W.J. (1955).Mosquitoes of North America (North
Mexico). Univiversity of CaliforniaPress, Berkeley.
Casanova, C. & Do Prado, A.P. (2002). Key-factor analysis of immature stages ofAedes scapularis (Diptera: Culicidae)populations in southern Brazil. Bulletin
of Entomological Research 92(4): 271-277.
Chandra, G., Mandal, S.K., Ghosh, A.K., Das,D., Banerjee, S.S. & Chakraborty, S.(2008). Biocontrol of larval mosquitoesby Acilius sulcatus (Coleoptera:
Dytiscidae). BMC Infectious Diseases 8:
138.Chatterjee, S.N., Ghosh, A. & Chandra, G.
(2007). Eco-friendly control of mosquitolarvae by Brachytron pratense nymph.Journal of Environmental Health
69(8): 44–49.Chesson, J. (1984). Effect of notonectids
(Hemiptera: Notonectidae) onmosquitoes (Diptera: Culicidae):predation or selective oviposition?Environmental Entomology 13(2): 351-358.
Christie, M. (1958). Predation on larvae ofAnopheles gambiae Giles. The Journal
of Tropical Medicine and Hygiene 61:
168-176.Clark, T.B. & Fukuda, T. (1967). Predation of
Culicoides cavaticus Wirth and Joneslarvae on Aedes sierrensis (Ludlow).Mosquito News 27: 424. (Cited in: Bay,E.C. (1974). Predatory-prey relationshipsamong aquatic insects. Annual Review
of Entomology 19: 441-453).Clements, A.N. (1992). The Biology of
Mosquitoes. Vol. 1. Chapman and Hall.London. (Cited in: Silberbush, A. &Blaustein, L. (2008). Oviposition habitatselection by a mosquito in response to apredator: Are predator-releasedkairomones air-borne cues? Journal of
Vector Ecology 33(1): 208-211).Collins, L.E. & Blackwell, A. (2000). The
biology of Toxorhynchites mosquitoesand their potential as biocontrol agents.Biocontrol News and Information 21:
105-116.Collins, J.N. & Resh, V.H. (1985). Factors that
limit the role of immature damselflies asnatural mosquito control agents atCoyote Hills Marsh. 53rd Annual
Conference of California Mosquito
Vector Control Association: 87-92.Collins, F.H. & Washino, R.K. (1985). Insect
predators. Chapman, H.C., ed. Biologicalcontrol of mosquitoes. Bulletin of the
American Mosquito Control Associa-
tion 6: 25-42. (Cited in: Lacey, L.A. & Orr,B.K. (1994). The role of biological controlof mosquitoes in integrated vectorcontrol. American Journal of Tropical
Medicine and Hygiene 50: 97-115).
253
Collins, J.N. & Resh, V.H. (1985). Factors thatlimit the role of immature damselflies asnatural mosquito control agents atCoyote Hills Marsh. 53rd Annual
Conference of California Mosquito
Vector Control Association: 87-92.Copeland, R.S., Okeka, W. & Corbet, P.S.
(1996). Treeholes as larval habitat of thedragonfly Hadrothemis camarensis
(Odonata: Libellulidae) in Kakamegaforest, Kenya. Aquatic Insects 18:129-147.
Corbet, P.S. (1983). Odonata in phytotelmata.In: Phytotelmata : terrestrial plants ashosts for aquatic insect communities,Frank, J.H. & Lounibos, L.P. (eds.)Plexus, Marlton, New Jersey. pp. 29-54.(Cited in: Copeland, R.S., Okeka, W. &Corbet, P.S. (1996). Treeholes as larvalhabitat of the dragonfly Hadrothemis
camarensis (Odonata: Libellulidae) inKakamega forest, Kenya. Aquatic
Insects 18:129-147).Corbet, P.S. & MacCrae, A.W.R. (1981).
Larvae of Hadrothemis scabrifrons
(Ris) in a tree cavity in East Africa(Anisoptera: Libellulidae). Odonato-
logica 10: 311-317.Cordoba, A.A. & Lee, M. (1995): Prey size
selection by Orthemis ferruginea
(Fabricius) larvae (Odonata:Libellulidae) over mosquito instar. Folia
Entomologica Mexicana 91: 23-30.Das, P.K., Sivagnaname, N. & Amalraj, D.D.
(2006). Populations interactionsbetween Culex vishnui mosquitoes andtheir natural enemies in Pondicherry,India. Journal of Vector Ecology 31(1):
84-88.Dennett, J.A., Bernhardt, J.L. & Meisch, M.V.
(2003). Operational note effects offipronil and lambda-cyhalothrin againstlarval Anopheles quadrimaculatus andnontarget aquatic mosquito predators inArkansas small rice plots. Journal of the
American Mosquito Control Asociation
19(2): 172-174.Diabaté, A., Dabiré, R.K., Heidenberger, K.,
Crawford, J., Lamp, W.O., Culler, L.E. &Lehmann, T. (2008). Evidence fordivergent selection between themolecular forms of Anopheles gambiae:
role of predation. BMC Evolutionary
Biology 8: 5.Dicke, M. & Grostal, P. (2001). Chemical
detection of natural enemies byarthropods: An ecological perspective.Annual Review of Ecology and
Systematics 32: 1-23.Djam, J.C. & Focks, D.A. (1983).
Susceptibility of Toxorhynchites
amboinensis and Aedes aegypti toseveral adulticides currently used formosquito control. Mosquito News 43:471-473.
Eitam, A. & Blaustein, L. (2004). Ovipositionhabitat selection by mosquitoes inresponse to predator (Notonecta
maculata) density. Physiological
Entomology 29: 188-191.Eitam, A., Blaustein, L. & Mangel, M. (2002).
Effects of Anisops sardea (Hemiptera :Notonectidae) on oviposition habitatselection by mosquitoes and otherdipterans and on community structurein artificial pools. Hydrobiologia
485:183-189.EL Rayah, E. (1975). Dragonfly nymphs as
active predators of mosquito larvae.Mosquito News 35: 229-230.
Ellis, R.A. & Borden, J.H. (1970). Predationby Notonecta undulata on larvae of theyellow fever mosquito. Annals of the
Entomological Scociety of America 63:
963-973 (Cited in: Bay, E.C. (1974).Predatory-prey relationships amongaquatic insects. Annual Review of
Entomology 19: 441-453).Fellipe-Bauer, M.L, Huerta, H. & Bernal, S.I.
(2000). A new species of predaceousmidge of the genus Monohelea Kiefferfrom Mexico (Diptera: Ceratopogonidae).Memorias do Instituto Oswaldo Cruz
95: 815-818.Fincke, O.M. (1999). Organization of
predator assemblages in neotropical treeholes: effects of abiotic factors andpriority. Ecological Entomology 24: 13-23.
Fincke, O.M., Yanoviak, S.P. & Hanschu, R.D.(1997). Predation by odonates depressesmosquito abundance in water-filled treeholes in Panama. Oecologia 112: 244-253.
254
Fischer, S. & Schweigmann, N. (2008).Association of immature mosquitoes andpredatory insects in urban rain pools.Journal of Vector Ecology 33(1): 46-55.
Fischer, S., Marinone, M.C., Fontanarrosa,M.S., Nieves, M. & Schweigmann, N.(2000). Urban rain pools: Seasonaldynamics and entomofauna in a park ofBuenos Aires. Hydrobilogia 441: 45-53.
Focks, D.A. (1984). Effects of a sublethaldose of resmethrin on reproduction ofToxorhynchites rutilus rutilus.Mosquito News 44: 534-536.
Focks, D.A., Sackett, S.R. & Bailey, D.L.(1982). Field experiments on thecontrol of Aedes aegypti and Culex
quinquefasciatus by Toxorhynchites
rutilus rutilus (Diptera: Culicidae).Journal of Medical Entomology 19: 336-339.
Focks, D.A., Sackett, S.R., Dame, D.A. &Bailey, D.L. (1985). Effect of weeklyrelease of Toxorhynchites amboinensis
(Doleschall) on Aedes aegypti (L.)(Diptera: Culicidae) in New Orleans,Louisiana. Journal of Economic
Entomology 78: 622-626.Focks, D.A., Sackett, S.R., Kloter, K.O.,
Dame, D.A. & Carmichael, G.T. (1986).The integrated use of Toxorhynchites
amboinensis and ground-level ULVinsecticide application to suppress Aedes
aegypti (Diptera: Culicidae). Journal of
Medical Entomology 23: 513-519.Garcia, A.I., Vivar, G.R., Quezada, M.J. &
Huaman, M.P. (1996). Aquatic insectsthat are bioregulators of mosquito larvaepresent in Pantanos de Villa, Lima, Peru.Revista Cubana de Medicina Tropica
48: 227-228.Garcia, R. (1982). Arthropod predators of
mosquitoes. Bulletin of the Society of
Vector Ecology 7: 45-47.Gerberg, E.J. & Visser, W.M. (1978).
Preliminary field trial for the biologicalcontrol of Aedes aegypti by means ofToxorhynchites brevipalpis, a predatorymosquito larva. Mosquito News 38:197-200.
Grill, C.P. & Juliano, S.A. (1996). Predictingspecies interactions based on behaviour:Predation and competition in container-
dwelling mosquitoes. Journal of Animal
Ecology 65: 63-67.Griswold, M.W. & Lounibos, L.P. (2006).
Predator identity and additive effects ina treehole community. Ecology 87(4):
987-995.Herrel, N., Amerasinghe, F.P., Ensink, J.,
Mukhtar, M., Hoek, W.V.D. & Konradsen,F. (2001). Breeding of Anopheles
mosquitoes in irrigated areas of SouthPunjab, Pakistan. Medical and
Veterinary Entomology 15: 236-248.Hribar, L.J. & Mullen, G.R. (1991). Predation
by Bezzia larvae (Diptera: Cerato-pogonidae) on mosquito larvae (Diptera:Culicidae). Entomological News 102:
183-186.Husbands, R.C. (1978). The influence of
mosquito larvae behaviour on predatorefficacy in a natural habitat. California
Mosquito Vector Control Association
Bio Briefs 4: 2 (Cited in: Sih, A. (1986).Antipredator responses and theperception of danger by mosquito larvae.Ecology 67(2): 434-441).
Ikeshoji, T. (1966). Bionomics of Culex
(Lutzia) fuscanus. Japanese Journal of
Experimental Medicine 36: 321-334(Cited in: Pal, R. & Ramalingam, S.(1981). Invertebrate predators ofmosquitoes. World Health Organization
WHO/VBC/81.799).James, H.J. (1969). Insect predators of
univoltine mosquitoes in woodland poolsof the Pre-Cambrian shield in Ontario.Canadian Entomology 98: 550-555(Cited in: Kumar, R. & Hwang, J.S. (1983).Larvicidal efficacy of aquatic predators:A perspective for mosquito control.Zoological Studies 45(4): 447-466).
James, H.J. (1961). Some predators of Aedes
stimulans (Walk) and Aedes trichurus
(Dyar) (Diptera: Culicidae) in woodlandpools. Canadian Journal Of Zoology 29:533-540. (Cited in: Kumar, R. & Hwang,J.S. (1983). Larvicidal efficacy of aquaticpredators: A perspective for mosquitocontrol. Zoological Studies 45(4): 447-466).
Jebanesan, A. & Vadani, B.P. (1995).Advantage of insecticide (K-Othrine) -bio-agent (Diplonychus indicus) Venk
255
and Rao, system in the control ofmosquito larvae Culex quinquefasciatus
(Say). Environmint and Ecology 13(2):
336-339.Juliano, S.A. & Lawton, J.H. (1990). The
relationship between competition andmorphology: II Experiments oncooccurring dytiscid beetles. Journal of
Animal Ecology 59: 831-848.Kats, L.B. & Dill, L.M. (1998). The scent of
death: Chemosensory assessment ofpredation risk by prey animals.Ecoscience 5(3): 361-394.
Kesavaraju, B., Alto, B.W., Lounibos, L.P. &Juliano, S.A. (2007). Behaviouralresponses of larval container mosquitoesto a size-selective predator. Ecological
Entomology 32: 262-272.Kesavaraju, B. & Juliano, S.A. (2004).
Differential behavioural responses towater-borne cues to predation in twocontainer-dwelling mosquitoes. Annals
of the Entomological Society of America
97(1): 194-201.Kiflawi, M., Blaustein, L. & Mangel, M. (2003).
Predation-dependent oviposition habitatselection by the mosquito Culiseta
longiareolata: a test of competinghypotheses. Ecology Letters 6: 35-40.
Kirkpatrick, T.W. (1925). The Mosquitoes of
Egypt. Government Press, Cairo, pp 224.Kitching, R.L. (1990). Foodwebs from
phytotelmata in Madang, Papua NewGuinea. Entomologist 109:153-164.
Koenraadt, C.J.M. & Takken, W. (2003).Cannibalism and predation among larvaeof the Anopheles gambiae complex.Medical and Veterinary Entomology 17:
61-66.Kovac, D. & Yang, C.M. (1996). A new species
of Emesopsis Uhler, 1893 (Insecta:Hemiptera: Reduviidae) from PeninsularMalaysia, with notes on its biology.Raffles Bulletin of Zoology 43: 453-462.
Kuldip, S, Kumar, K. & Biswas, S. (1984).Laboratory studies on the predaciousefficacy Culex (Lutzia) fuscanus larvaeagainst other mosquito larvae. Journal
of Communicable Diseases 16(4): 320-322.
Kumar, R. & Hwang, J.S. (2006). Larvicidalefficacy of aquatic predators: Aperspective for mosquito control.Zoological Studies 45(4): 447-466.
Lacey, L.A. (1983). Larvicidal activity ofBacillus pathogens againstToxorhynchites mosquitoes (Diptera:Culicidae). Journal of Medical
Entomology 20(6): 620-624.Lacey, L.A. (2007). Bacillus thuringiensis
serovariety israelensis and Bacillus
sphaericus for mosquito control.Journal of the American Mosquito
Control Association 23(2 Suppl):133-63.Lacey, L.A. & Dame, D.A. (1982). The effect
of Bacillus thuringiensis var.israelensis on Toxorhynchites rutilus
rutilus (Diptera: Culicidae) in thepresence and absence of prey. Journal
of Medical Entomology 19(5): 593-596.Lacey, L.A. & Orr, B.K. (1994). The role of
biological control of mosquitoes inintegrated vector control. American
Journal of Tropical Medicine and
Hygiene 50(6): 97-115.Laing, J. & Welch, H.E. (1963). A
dolichopodid predacious on larvae ofCulex restuans Theo. Procceeding of
Entomological Society of Ontario 93: 89-90. (Cited in: Bay, E.C. (1974). Predatory-prey relationships among aquaticinsects. Annual Review of Entomology
19: 441-453).Larson, D.J. (1990). Odonate predation as a
factor influencing dytiscid beetledistribution and community structure.Questiones Entomology 26: 151-162.
Larson, D.J. & House, N.L. (1991). Insectcommunities of Newfoundland bogpools with emphasis on the odonata.Canadian Entomologist 122(5-6): 469-502.
Lee, F.C. (1967). Laboratory observations oncertain mosquito larval predators.Mosquito News 27(3): 332-338.
Legner, E.F. (1994). Biological control ofdiptera of medical and veterinaryimportance. Journal of Vector Ecology
20(1): 59-120.
256
Lounibos, L.P., Escher, R.L., Nishimura, N. &Juliano, S.A. (1997). Long-term dynamicsof a predator used for biological controland decoupling from mosquito prey in asubtropical treehole ecosystem.Oecologia 111: 189-200.
Lounibos, L.P., Makhni, S., Alto, B.W. &Kesavaraju, B. (2008). Surplus Killing bypredatory larvae of Corethrella
appendiculata: Prepupal timing andsite-specific attack on mosquito Prey.Journal of Insect Behaviour 21: 47–54.
Lounibos, L.P., Nishimura, N. & Escher, R.L.(1993). Fitness of a treehole mosquito:Influences of food type and predation.Oikos 66:114-118.
Louton, J., Gelhaus, J. & Bouchard, R. (1996).The aquatic macrofauna of water-filledbamboo (Poaceae: Bambusoideae:Guadua) internodes in a Peruvianlowland tropical forest. Biotropica
28(2): 228-242.Lozano, R.D., Rodriguez, M.H., Jimenez,
J.I.A., Avila, M.H. & Mallorca, C. (1997).Aquatic insects associated withAnopheles albimanus (Diptera:Culicidae) breeding sites in SouthernMexico. Environmental Entomology
26(4): 828-838.Lundkvist, E., Landin, J., Jackson, M. &
Svensson, C. (2003). Diving beetles(Dytiscidae) as predators of mosquitolarvae (Culicidae) in field experimentsand in laboratory tests of preypreference. Bulletin of Entomological
Research 93(3): 219-226.Mandal, S.K., Ghosh, A., Bhattacharjee, I. &
Chandra, G. (2008). Biocontrol efficiencyof odonate nymphs against larvae of themosquito, Culex quinquefasciatus Say,1823. Acta Tropica 106: 109-114.
Mariappan, P., Narayanan, M. &Balasundaram, C. (1997). Occurrence ofmosquito larvae and its predators in andaround Palayankottai, Tamil Nadu.Environment and Ecology 15(3): 678-682.
Marten, G.G., Suarez, M.F. & Astaeza, R.(1996). An ecological survey ofAnopheles albimanus larval habitat inColombia. Journal of Vector Ecology
21(2): 122-131.
Mattingly, P.F. (1961). The culicinemosquitoes of the Indomalayan area,Part V: Genus Aedes Meigen, subgeneraMucidus Theobald, Ochlerotatus LynchArribalzaga and Neomelaniconion
Newstead. London, United Kingdom:British Museum (Natural History) (Citedin: Mogi, M. (2007). Insects and otherinvertebrate predators. Journal of the
Amercan Mosquito Control Association
23 (3 suppl): 93-109).McCrae, A.W. (1984). Oviposition by African
malaria vector mosquitoes. II. Effects ofsite tone, water type and conspecificimmatures on target selection byfreshwater Anopheles gambiae Giles,sensu lato. Annals of Tropical Medicine
and Parasitology 78: 307-318. (Cited in:Koenraadt, C.J.M. & Takken, W. (2003).Cannibalism and predation among larvaeof the Anopheles gambiae complex.Medical and Veterinary Entomology 17:
61-66).McDonald, G. & Buchanan, G.A. (1981). The
mosquito and predatory insect faunainhabiting fresh-water ponds, withparticular reference to Culex annuli-
rostris Skuse (Diptera: Culicidae).Australian Journal of Ecology 6: 21-27.
McLaughlin, R.E. (1990). Predation rate oflarval Corethrella brakeleyi (Diptera:Chaoboridae) on mosquito larvae.Florida Entomologist 73(1): 143-146.
Merritt, R.W., Lessard, J.L., Wessell, K.J.,Hernandez, O., Berg, M.B., Wallace, J. R.,Novak, J.A., Ryan, J. & Merritt, B.W.(2005). Lack of effects of Bacillus
sphaericus (Vectolex) on nontargetorganisms in a mosquito-controlprogram in southeastern Wisconsin: a 3-year study. Journal of the American
Mosquito Control Association 21(2):
201-212.Minakawa, N., Futami1, K., Sonye, G.,
Akweywa, P. & Kaneko, S. (2007).Predatory capacity of a shorefly,Ochthera chalybesceens, on malariavectors. Malaria Journal 6(1): 104-108.
Mittal, P.K. (2003). Biolarvicides in vectorcontrol: challenges and prospects.Journal of Vector Borne Diseases 40(1-
2): 20-32.
257
Miura, T. & Takahashi, R. (1988). A laboratorystudy of predation by damselfly nymphs,Enallagma civile, upon mosquito larvae,Culex tarsalis. Journal of the American
Mosquito Control Association 4(2):
129-131.Miura, T., Schaefer, C.H. & Mulligan, F.S.
(1978a). Integration of chemical andbiological control agents against naturalpopulations of Culex tarsalis. Mosquito
News 38(4): 542-545.Miura, T., Takahashi, R.M. & Mulligan, F.S.
(1978). Field evaluation of theeffectiveness of predaceous insects as amosquito control agent. 46th Annual
Conference of California Mosquito
Control Association: 80-81.Miyagi, I. & Toma, T. (1989). A new species
of Topomyia (Suaymyia) suchariti fromThailand. Mosquito Systematics 21:16-24.
Mogi, M. (2007). Insects and otherinvertebrate predators. Journal of the
American Mosquito Control
Association 23 (suppl 3): 93-109.Mogi, M. & Chan, K.L. (1996). Predatory
habits of dipteran larvae inhabitingNepenthes pitchers. Raffles Bulletin of
Zoology 44: 233-245.Mogi, M. & Miyagi, I. (1990). Colonization of
rice fields by mosquitoes (Diptera :Culicidae) and larvivorous predators ina synchronous rice cultivation areas inthe Philippines. Journal of Medical
Entomology 27(4): 530-536.Mogi, M., Memah, V., Miyagi, I., Toma, T. &
Sembel, D.T. (1995). Mosquito (Diptera:Culicidae) and predator abundance inirrigated and rain-fed rice fields in northSulawesi, Indonesia. Journal of Medical
Entomology 32(3): 361-367.Mogi, M., Miyagi, I. & Cabrera, B.D. (1984).
Development and survival of immaturemosquitoes (Diptera: Culicidae) inPhilippine rice fields. Journal of Medical
Entomology 21(3): 283-291.Mogi, M., Mori, A. & Wada, Y. (1980). Survival
rates of Culex tritaeniorhynchus
(Diptera: Culicidae) larvae in fallow ricefields before summer cultivation.Tropical Medicine 22(1): 47-59.
Mogi, M., Okazawa, T., Miyagi, I., Sucharit,S., Tumrasvin, W., Deesin, T. &Khamboonruang, C. (1986). Develop-ment and survival of anophelineimmatures (Diptera: Culicidae) in ricefields in northern Thailand. Journal of
Medical Entomology 23(3): 244-250.Mogi, M., Sunahara, T. & Selomo, M. (1999).
Mosquito and aquatic predatorcommunities in ground pools on landsdeforested for rice field development incentral Sulawesi, Indonesia. Journal of
the American Mosquito Control
Association 15(2): 92-97.Mottram, P. & Kettle, D.S. (1997).
Development and survival of immatureCulex annulirostris mosquitoes insoutheast Queensland. Medical and
Veterinary Entomology 11: 181-186.Mulligan, F.S. & Schaefer, C.H. (1981).
Integration of a selective mosquitocontrol agent Bacillus thuringiensis
serotype H. 14, with natural predatorpopulations in pesticide sensitivehabitats. 49th Annual Conference of
California Mosquito Vector Control
Association: 19-22.Munga, S., Minakawa, N., Zhou, G., Barrack,
O.J., Githeko, A.K. & Yan, G. (2006).Effects of larval competitors andpredators on oviposition site selectionof Anopheles gambiae Sensu Stricto.Journal of Medical Entomology 43(2):
221-224.Munga, S., Minakawa, N., Zhou, G., Githeko,
A.K. & Yan, G. (2007). Survivorship ofimmature stages of Anopheles gambiae
s.l. (Diptera: Culicidae) in naturalhabitats in Western Kenya highlands.Journal of Medical Entomology 44(5):
758-764.Murdoch, W.W., Scott, M.A. & Ebsworth, P.
(1984). Effects of the general predator,Notonecta (Hemiptera) upon a freshwater community. Journal of Animal
Ecology 53: 791-808.Naeem, S. (1988). Predator-prey interactions
and community structure: Chironomids,mosquitoes and copepods in Heliconia
imbricate (Musaceae). Oecologia 77:
202-209.
258
Nelson, F.R.S. (1977). Predation on mosquitolarvae by beetle larvae, Hydrophilus
triangularis and Dytiscus marginalis.Mosquito News 37(4): 628-630.
Nilsson, A.N. & Savensson, B.W. (1994).Dytiscid predators and culicid prey intwo boreal snowmelt pools differing intemperature and duration. Annales
Zoologici Fennici 31(4): 365-376.Nilsson, A.N. & Soderstrom, O. (1988). Larval
consumption rates, interspecificpredation, and local guild compositionof egg-overwintering Agabus
(Coleoptera: Dytiscidae) species invernal ponds. Oecologia 76: 131-137.
Onyeka, J.O.A. (1983). Studies on the naturalpredators of Culex pipiens L. and C.torrentium Martini (Diptera: Culicidae)in England. Bulletin of Entomological
Research 73: 185-194.Orr, A.G. (1994). Life histories and ecology
of odonata breeding in phytotelmata inBornean rainforest. Odonatologica
23(4): 365-377.Padgett, P.D. & Focks, D.A. (1981). Prey stage
preference of the predator, Toxo-
rhynchites rutilus rutilus on Aedes
aegypti. Mosquito News 41(1): 67-70.Painter, M.K., Tennessen, K.J. & Richardson,
T.D. (1996). Effects of repeatedapplications of Bacillus thuringiensis
israelensis on the mosquito predatorErythemis simplicicollis (Odonata:Libellulidae) from hatching to finalinstar. Environmental Entomology
25(1): 184-191.Pal, R. & Ramalingam, S. (1981). Invertebrate
predators of mosquitoes. World Health
Organization WHO/VBC/81.799.Panicker, K.N, Bai, M.G. & Sabesan, S. (1982).
A note on laboratory colonization ofCulex (Lutzia) fuscanus Wiedemann,1820 (Diptera: Culicidae). Indian
Journal of Medical Research 75(1): 45-46.
Peterson, J.J., Chapman, H.C. & Willis, O.R.(1969). Predation of Anopheles barberi
Coquillett on first instar mosquito larvae.Mosquito News 29: 134-135. (Cited in:Bay, E.C. (1974). Predatory-preyrelationships among aquatic insects.
Annual Review of Entomology 19: 441-453).
Petranka, J.W. & Fakhoury, K. (1991).Evidence of a chemically-mediatedavoidance response of ovipositinginsects to bluegills and green frogtadpoles. Copeia 1: 234-239.
Prakash, R.N. & Ponniah, A.G. (1978).Predatory behaviour of Lutzia on Culex
fatigans. Hydrobiologia 57(2): 159-162.Pramanik, M.K. & Raut, S.K. (2003).
Occurrence of the giant mosquitoToxorhynchites splendens in drains andits predation potential on some vectormosquitoes of Kolkata (Calcutta), India.Medical Entomolology and Zoology
54(4): 315-323.Quiroz-Martine, H. & Rodriguez-Castro, A.
(2007). Aquatic insects as predators ofmosquito larvae. Journal of the
American Mosquito Control
Association 23 (2 Suppl): 110-117.Rae, D.J. (1990). Survival and development
of the immature stages of Culex
annulirostris (Diptera: Culicidae) at theRoss river dam in tropical easternAustralia. Journal of Medical
Entomology 27(5): 756-762.Ramalingam, S. (1983). Topomyia houghtoni
Feng, a new record in Malaysia and aredescription of the adult and immaturestages. Mosquito Systematics 15: 33-49.
Ramalingam, S. & Ramakrishnan, K. (1971).Redescription of Aedes (Alanstonea)brevitibia (Edwards) from Brunei,Borneo. Proceedings of the Entomo-
logical Society of Washington 73: 231-238.
Rawlins, S.C. & Ragoonansingh, R. (1990).Comparative organophosphorusinsecticide susceptibility in Caribbeanpopulations of Aedes aegypti andToxorhynchitis moctezuma. Journal of
the American Mosquito Control
Association 6(2): 315-317.Rebollar- Tellez, E.A., Gorrochotegui-
Escalante, N., Reyna- Nava, M. & Solis-Santamaria, A. (1994). Effect of Bacillus
thuringiensis var. israelensis upon thepredatory capacity of Buenoa sp.(Hemiptera: Notonectidae) against
259
Culex pipiens quinquefasciatus
(Diptera: Culicidae) larvae. Ento-
mological news 105(5): 295-298.Reisen, W.K. & Siddiqui, T.F. (1979).
Horizontal and vertical estimates ofimmature survivorship for Culex
tritaeniorhynchus (Diptera: Culicidae)in Pakistan. Journal of Medical
Entomology 16(3): 207-218.Reisen, W.K., Meyer, R.P., Shields, J. &
Arbolante, C. (1989). Population ecologyof preimaginal Culex tarsalis (Diptera:Culicidae) in Kern County, California.Journal of Medical Entomology 26(1):
10-22.Resetarits, Jr. W.J. (2001). Colonization under
threat of predation: avoidance of fish byan aquatic beetle, Tropisternis lateralis
(Coleoptera: Hydrophilidae). Oecologia
129: 155-160.Robert, V., Ambene, H.P.A. & Thioulouse, J.
(1998). Ecology of larval mosquitoeswith special reference to Anopheles
arabiensis (Diptera: Culicidae) inmarket-garden wells in urban Dakar,Senegal. Journal of Medical Entomology
35(6): 948-955.Rodriguez-Castro, V.A., Quiroz-Martinez, H.,
Solis-Rojas, H. & Tejada, L.O. (2006).Mass rearing and egg release of Buenoa
scimitra Bare as biocontrol of larvalCulex quinquefasciatus. Journal of the
American Mosquito Control Asso-
ciation 22(1): 123-125.Saha; N., Aditya, G., Bal, A. & Saha, G.K.
(2007). A comparative study of predationof three aquatic heteropteran bugs onCulex quinquefasciatus larvae.Limnology 8: 73–80.
Schaefer, C.H., Miura, T. & Wilder, W.H.(1981). Mosquito production on aCalifornia rice field treated with a non-selective insecticide. Mosquito News
41(4): 791-793.Sebastian, A., Sein, M.M. Thu, M.M. & Corbet,
P.S. (1990). Suppression of Aedes aegypti
(Diptera: Culicidae) using augmentativerelease of dragonfly larvae (Odonata:Libellulidae) with communityparticipation in Yangon, Myanmar.Bulletin of Entomological Research 80:
223-232.
Sebastian, A., Thu, M.M., Kyaw, M. & Sein,M.M. (1980). The use of dragonflynymphs in the control of Aedes aegypti.Southeast Asian Journal of Tropical
Medicine and Public Health 11(1): 104-107.
Sempala, S.D.K. (1983). Interactionsbetween immatureAedes africanus
(Theobald) and larvae of two predatoryToxorhynchites (Diptera: Culicidae) inZika forest, Uganda. Bulletin of
Entomological Research 73:19-24.Service, M.W. (1973). Mortalities of the larvae
of the Anopheles gambiae Giles complexand detection of predators by theprecipitin test. Bulletin of Entomo-
logical Research 62: 359-369.Service, M.W. (1965). Predators of the
immature stages of Aedes (Stegomyia)vittatus (Bigot) in water-filled rock-pools in Northern Nigeria. WHO/EBL/33
65: 1-19 (Cited in: Bay, E.C. (1974).Predatory-prey relationships amongaquatic insects. Annual Review of
Entomology 19: 441-453).Service, M.W. (1977). Mortalities of the
immature stages of species B of theAnopheles gambiae complex in Kenya:Comparison between rice fields andtemporary pools, identification ofpredators, and effects of insecticidalspraying. Journal of Medical Ento-
mology 13(4-5): 535-545.Shaalan, E.A. (2005). Integrated control of
two mosquito species Aedes aegypti andCulex annulirostris. Ph. D. Thesis.South Valley University, Egypt.
Shaalan, E.A., Canyon, D.V., Reinhold, M.,Yones, W.F.M., Abdel-Wahab, H. &Mansour, A. (2007). A mosquito predatorsurvey in Townsville, Australia and anassessment of Diplonychus sp. andAnisops sp. predatorial capacity againstCulex annulirostris mosquitoimmatures. Journal of Vector Ecology
32(1): 16-21.Sih, A. (1986). Antipredator responcses and
the perception of danger by mosquitolarvae. Ecology 67(2): 434-441.
Silberbush, A. & Blaustein, L. (2008).Oviposition habitat selection by amosquito in response to a predator: Are
260
predator-released kairomones air-bornecues? Journal of Vector Ecology 33(1):
208-211.Spencer, M., Blaustein, L. & Cohen, J.E.
(2002). Oviposition habitat selection bymosquitoes (Culiseta longiareolata) andconsequences for population size.Ecology 83: 669-679.
Stav, G., Blaustein, L. & Margalith, J. (1999).Experimental evidence for predationrisk sensitive oviposition by a mosquito,Culiseta longiareolata. Ecological
Entomology 24: 202-207.Stav, G., Blaustein, L. & Margalith, Y. (2000).
Influence of nymphal Anax imperator
(Odonata: Aeshnidae) on oviposition bythe mosquito Culiseta longiareolata
(Diptera: Culicidae) and communitystructure in temporary pools. Journal of
Vector Ecology 25(2): 190-202.Stav, G., Blaustein, L. & Margalith, Y. (2005).
Individual and interactive effects ofpredator and controphic species onmosquito population. Ecological
applications 15(2): 587-598.Steelman, C.D., Farlow, E., Breaud, T.P. &
Schilling, P.E. (1975). Effects of growthregulators on Psorophora columbiae
(Dyar and Knab) and non-target aquaticinsect species in rice fields. Mosquito
News 35(1): 67-76.Stewart, R.J. & Miura, T. (1978). Laboratory
studies on Notonecta unifasciata Guerinand Buenoa scimitar Bare as predatorsof mosquito larvae. 46th Annual
Conference of California Mosquito
Control Association: 84-86.Sulaiman, S. & Jeffery, J. (1986). The ecology
of Aedes aegypti (Skuse) (Diptera:Culicidae) in a rubber estate in Malaysia.Bulletin of Entomological Research 76:
553-557.Sunahara, T., Ishizaka, K. & Mogi, M. (2002).
Habitat size: a factor determining theopportunity for encounters betweenmosquito larvae and aquatic predators.Journal of Vector Ecology 27(1): 8-20.
Sunish, I.P., Reuben, R. & Rajendran, R.(2006). Natural survivalship of immaturestages of Culex vishnui (Diptera:Culicidae) complex, vector of Japaneseencephalitis virus, in rice fields in
Southern India. Journal of Medical
Entomol 43(2): 185-191.Sunish, I.P. & Reuben, R. (2002). Factors
influencing the abundance of Japaneseencephalitis vectors in rice fields inIndia-II. Biotic. Medical and Veterinary
Entomology 16: 1-9.Symondson, W.O.C. (2002). Molecular
identification of prey in predator diets.Molecular Ecology 11: 627-641.
Thangam, T.S. & Kathiresan, K. (1996). Theprey consumption and prey preferenceof the larvae of the mosquito Culex
(Lutzia) raptor on the larvae of Culex
quinquefasciatus. Experientia 52(4):
380-382.Tietze, N.S., Schreiber, E.T., Hester, P.G.,
Hallmon, C.F., Olson, M.A. & Shaffer, K.R.(1993). Susceptibility of first instarToxorhynchites splendens to malathion,naled and resmethrin. Journal of the
American Mosquito Control Association
9(1): 97-99.Toma, T. & Miyagi, I. (1992). Laboratory
evaluation of Toxorhynchites splendens
(Diptera: Culicidae) for predation ofAedes albopictus mosquito larvae.Medical and Veterinary Entomology
6(3): 281-289.Vasuki, V. (1996). Insect growth regulator: Its
impact on some predatory arthropods ofmosquito immatures. Entomon 21(3-4):
217-220.Venkatesan, P. & Sivaraman, S. (1984).
Changes in the functional response ofinstars of Diplonychus indicus Venk. &Rao (Hemiptera: Belostomatidae) in itspredation of two species of mosquitolarvae of varied size. Entomon 9(3):
191-196.Waage, J.K. & Greathead, D.J. (1988).
Biological control: Challenges andopportunities. Philosophical Transac-
tions of the Royal Society of London
318: 111-128.Walker, K. & Lynch, M. (2007). Contributions
of Anopheles larval control to malariasuppression in tropical Africa: review ofachievements and potential. Medical
and Veterinary Entomology 21(1): 2-21.
261
Walton, W.E., Tietze, N.S. & Mulla, M.S.(1990). Ecology of Culex tarsalis
(Diptera: Culicidae): Factors influencinglarval abundance in mesocosms insouthern California USA. Journal of
Medical Entomology 27(1): 57-67.Washburn, J.O. (1995). Regulatory factors
affecting larval mosquito populations incontainer and pool habitats: Implicationsfor biological control. Journal of the
American Mosquito Control Associa-
tion 11(2): 279-283.Washino, R.K. (1969). Progress in biological
control of mosquitoes-invertebrate andvertebrate predators. Proceeding Paper.The 37th Annual Conference of
California Mosquito Control Associa-
tion 37: 16-19 (Cited in: Bay, E.C. (1974).Predatory-prey relationships amongaquatic insects. Annual Review of
Entomology 19: 441-453).Wattal, S., Adak, T., Dhiman, R.C. & Sharma,
V.P. (1996). The biology and predatorypotential of notonectid bug, Enithares
indica (Fabr) against mosquito larvae.Southeast Asian Journal of Tropical
Medicine and Public Health 27(3): 633-636.
Wongsiri, S. & Andre, R.G. (1984). Biologicalcontrol of mosquitoes in Thailand.Journal of the Science Society of
Thailand 10: 73-88.Yanovisk, S.P. (2001). The macrofauna of
water-filled tree holes on Barro ColoradoIsland, Panama. Biotropica 33(1): 110-120.
Yasuda, H. & Hagimori, K. (1997). Preyconsumption patterns of the predatorymosquito Toxorhynchites towadensis inrelation to prey abundance, prey agestructure and patch size. Japanese
Journal of Entomology 65(2): 295-302.Yasuoka, J. & Levins, R. (2007). Ecology of
vector mosquitoes in Sri Lanka –suggestions for future mosquito controlin rice ecosystems. Southeast Asian
Journal of Tropical Medicine and
Public Health 38(4): 646-57.Yuval, B. & Bouskila, A. (1993). Temporal
dynamics of mating and predation inmosquito swarms. Oecologia 95: 65-69.