ANRV363-EN54-24 ARI 7 November 2008 11:5

Role of Vector Control in theGlobal Program to EliminateLymphatic FilariasisMoses J. Bockarie,1 Erling M. Pedersen,2

Graham B. White,3 and Edwin Michael41Centre for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, PembrokePlace, Liverpool L3 5QA, United Kingdom; email: moses.bockarie@liverpool.ac.uk2DBL-Center for Health Research and Development, Faculty of Life Sciences, Universityof Copenhagen, 1871 Frederiksberg, Denmark; email: emp@life.ku.dk3Department of Entomology and Nematology, University of Florida, Gainesville, Florida32608; email: gbwhite@u.edu4Department of Infectious Disease Epidemiology, Imperial College London, Norfolk Place,London W2 1PG, United Kingdom; email: e.michael@imperial.ac.uk

Annu. Rev. Entomol. 2009. 54:46987

First published online as a Review in Advance onSeptember 17, 2008

The Annual Review of Entomology is online atento.annualreviews.org

This articles doi:10.1146/annurev.ento.54.110807.090626

Copyright c 2009 by Annual Reviews.All rights reserved

0066-4170/09/0107-0469$20.00

Key Words

mosquito ecology, mass drug administration, mathematical modeling,insecticide treated nets, integrated vector management

AbstractLymphatic lariasis (LF) is a major cause of acute and chronic morbid-ity in the tropical and subtropical parts of the world. The availability ofsafe, single-dose, drug treatment regimens capable of suppressing mi-crolaremia to very low levels, along with improvements in techniquesfor diagnosing infection, has resulted in the targeting of this majormosquito-borne disease for global elimination. The Global Program toEliminate Lymphatic Filariasis (GPELF) was launched in 2000 with theprincipal objective of breaking the cycles of transmission of Wuchereriabancrofti and Brugia spp. through the application of annual mass drugadministrations (MDAs) to entire at-risk populations. Although signif-icant progress in initiating MDA programs in endemic countries hasbeen made, emerging challenges to this approach have raised questionsregarding the effectiveness of using MDA alone to eliminate LF withoutthe inclusion of supplementary vector control. Here, we review advancesin knowledge of vector ecology, vector-parasite relationships, and bothempirical and theoretical evidence regarding vector management to as-sess the feasibility and strategic value of including vector control in theGPELF initiative to achieve the global elimination of LF.

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LF: lymphaticlariasis

Mf: microlaremia

Mass drugadministration(MDA):community-widetreatment ofindividuals withantiparasitic drugsregardless of theinfection status of eachindividual

GPELF: GlobalProgram to EliminateLymphatic Filariasis

ALB: albendazole

DEC:diethylcarbamazinecitrate

Limitation: anegative feedbackprocess in which aparasite (at any stage)compromises thesuccess of parasites atthe same or anotherstage

LYMPHATIC FILARIASIS

Lymphatic lariasis (LF) is a major cause ofacute and chronic morbidity affecting humansin tropical and subtropical areas of Asia, Africa,the Western Pacic, and some parts of theAmericas. More than 1.2 billion people are es-timated to live in areas where they are at riskfor the disease (86), and of the 120 millionactual cases of LF currently thought to oc-cur in 83 endemic countries, 91% are causedby Wuchereria bancrofti while Brugia malayi andB. timori infections account for the other 9%(42, 43, 66). These lymphatic-dwelling par-asites can cause severe damage to the lym-phatic system, resulting in the development oflymphedema, genital pathology (especially hy-droceles), and elephantiasis in some 41 mil-lion men, women, and children (85). A fur-ther 76 million have hidden internal damageto their lymphatic and renal systems. The -larial parasites have biphasic life cycles involv-ing the denitive mammalian host and variousgenera of mosquito vectors, including Anophe-les, Aedes, Culex, Mansonia, and Ochlerotatus.W. bancrofti appears to be exclusively a humanparasite, whereas Brugia spp. are zoonotic inlimited situations. Parasite transmission is indi-rect and occurs through the bite of an infectivemosquito containing third-stage infective lar-vae (L3) that have developed through two inter-mediate stages (L1 and L2) from microlaremia(Mf ) ingested with the blood meal taken by fe-male mosquitoes on an infected human.

GLOBAL PROGRAM TOELIMINATE LYMPHATICFILARIASIS: EVOLUTIONAND CURRENT STATUS

The absence of a nonhuman reservoir forW. bancrofti and only minor animal hosts forB. malayi means that transmission can be inter-rupted by reducing the Mf stage through massdrug administration (MDA) alone. This, alongwith the emergence of safe, single-dose, two-drug treatment regimens capable of reducingMf to very low levels for one year or more and

remarkable improvements in techniques for di-agnosing infection, resulted in advocacy for aglobal strategy to eliminate the disease throughMDA (16, 49). This led in 1997 to the land-mark adoption by the World Health Assemblyof Resolution WHA50.29 calling for the elim-ination of LF as a public health problem glob-ally. As a result, in 2000 the World Health Or-ganization, in collaboration with other inter-national agencies from the public health andprivate sectors, formed a global alliance (84)and launched a global campaign to eliminateLF by the year 2020 (87). The main goal of theGlobal Program to Eliminate Lymphatic Filar-iasis (GPELF) is to break the cycle of trans-mission of the parasites between mosquitoesand humans, mainly through MDA with al-bendazole (ALB) in combination with eitherivermectin (IVR) or diethylcarbamazine citrate(DEC) (53, 83, 84). The Ministries of Healthof all 83 countries aficted with LF are nowcommitted to taking action by setting up theirown national elimination programs. By the endof 2006, 44 of the 83 endemic countries hadimplemented MDA (86).

CHALLENGES TOMDA CAMPAIGNS

Despite the progress made in initiating MDAprograms, a number of challenges to these pro-grams have begun to appear. First, many coun-tries initiating MDA have not reached nationalscale even after 56 years and some countriesface major challenges in sustaining MDA, prin-cipally as a result of signicant resource con-straints (86). Resource limitations and avail-ability of rapid diagnostic tests have hamperedprogress in mapping implementation units forMDA. Delivering MDA in urban areas has alsoposed operational challenges. Second, the ex-act level and duration of treatments to achieveLF elimination in different endemic regions re-main unknown (44, 45), such that it is dif-cult to predict or decide when to stop ongo-ing MDA programs. Third, a major challengeto implementing MDA at a level required tomeet elimination targets within a reasonable

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time frame has been the difculty of achievingthe required high drug coverages in endemiccommunities (57). Fourth, there has been a shiftrecently toward linking MDA for LF controlwith programs for controlling other neglectedtropical diseases, such as schistosomiasis, soil-transmitted helminthiasis, and onchocerciasis(31, 48). This integrated approach is provingto be an attractive alternative to an individualprogrammatic approach, because it is perceivedto remove duplication of effort and costs in pro-grams that share common activities. However,with different objectives (e.g., parasite con-trol versus parasite elimination) and the poten-tial increased complexity in drug delivery (e.g.,move from school-based programs to commu-nity treatment in the case of soil-transmittedhelminthiasis and schistosomiasis), it is unclearif this approach will result in enhancing or ham-pering the goal of LF elimination. Finally, con-cerns of the potential for larial parasites un-der mass chemotherapeutic pressure to developdrug resistance raise questions regarding the ef-fectiveness of using MDA alone to achieve suc-cessful LF elimination (46, 68).

GROWING RECOGNITION OFTHE POTENTIAL AND NEED TOINCLUDE VECTOR CONTROL

The challenges to MDA programs have led togrowing concerns regarding the effectivenessof using MDA alone to eliminate LF with-out the inclusion of vector control (12, 13).This is especially pertinent given that vec-tor control was once advocated as the pri-mary tool to control lariasis (66), and theapproach was feasible in some epidemiolog-ical settings, as demonstrated by the elimi-nation of Anopheles-transmitted lariasis fromSolomon Islands (75, 77, 78) and Togo (9,67) by indoor spraying with dichloro-diphenyl-trichloroethane (DDT). Control of mosquito-borne diseases through residual house sprayingand community-wide distribution of long-lasting insecticide-treated netting materials(LLITNs) is also currently occurring in manycountries where malaria and LF are coendemic

Parasite control:reduction of infectionincidence, prevalence,or morbidity to alocally acceptable levelat which the parasiticinfection is no longerconsidered a publichealth problem

Parasite elimination:reduction of theincidence of infectionto zero in a denedgeographic area

Dichloro-diphenyl-trichloroethane(DDT): one of thebest known syntheticpesticides long used tocontrol vectors

LLITNs: long-lastinginsecticide-treatednetting materials

and transmitted by the same mosquitoes (58).Similarly, vector intervention measures to con-trol dengue are in place in many parts of theworld where Aedes mosquitoes transmit LF (13).Thus, an integrated strategy involving vectorcontrol is now thought to have great potentialto become an important supplementary compo-nent of the lariasis elimination strategy. Here,we review advances in knowledge of vector ecol-ogy, vector-parasite relationships, populationdynamics of vector-based interventions, and in-tegrated control involving antimosquito mea-sures such as residual house spraying and dis-tribution of LLITNs to evaluate the feasibilityand strategic value of including vector controlin the GPELF initiative to achieve the globalelimination of LF.

VECTOR SPECIESDISTRIBUTION AND ECOLOGY

W. bancrofti and B. malayi are unique amongthe various mosquito-transmitted parasites inthat larval development can take place in sev-eral genera of mosquitoes. Three main zonesof transmission are recognized: the South Pa-cic islands and some limited areas of South-east Asia, where Aedes vectors predominate;West Africa, Papua New Guinea, Vanuatu, andSolomon Islands, where Anopheles mosquitoesare principal vectors; and China, SoutheastAsia, Egypt, East Africa, the Caribbean, andLatin America, where the infection is transmit-ted mainly by Culex quinquefasciatus and othermembers of the Cx. pipiens complex (81).

Culex Species

Mosquitoes of the Cx. pipiens complex, espe-cially Cx. quinquefasciatus, are urban vectors ofnocturnally periodic W. bancrofti in Asia, Africa,the West Indies, South America, and Microne-sia. Cx. quinquefasciatus breeds in a wide varietyof stagnant water habitats, including waterbarrels, wells, tanks, privies, fresh pools, ponds,and canals near houses, provided that the waterhas been sufciently polluted. It is mainly anight-biting mosquito, although it occasionally

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bites freely in darkened rooms during thedaytime. Feeding is both indoors (endophagic)and outdoors (exophagic). The distribution ofCx. quinquefasciatus is increasing with ur-banization and human activity, and manyrural pockets that were relatively free of thismosquito are now increasingly colonized (20).

Aedes and Ochlerotatus Species(Tribe Aedini)

Aedes mosquitoes are involved in the transmis-sion of W. bancrofti and B. malayi in SouthAsia and the Pacic regions. Chow (21) lists15 species of Aedes as vectors of LF. The di-urnal subperiodic form of W. bancrofti, in whichthe microlariae are present in the blood dur-ing the day as well as in the night, occurs onlyin the South Pacic region and the most im-portant vector is Ae. polynesiensis. Other impor-tant Aedes vectors are Ae. niveus, Ae. poecilus,Ae. samoanus, Ae. scutellaris group, and Ochlero-tatus togoi (formerly called Ae. togoi). Ae. polyne-siensis is the most important vector of the sub-periodic form of W. bancrofti in the Polynesianregion wherever it occurs (12, 14). It breedsin articial and natural containers of rainwa-ter, such as coconut shells, fallen coconut leafbracts, discarded tins, old automobile tires, anddrums, as well as in tree holes, canoes, and crabholes made in sandy beaches. It also breedsin the leaf axils of Pandanus. The females aregenerally exophilic and exophagic day-bitingmosquitoes that feed mainly on humans out-doors, with a minor peak at 08:00 hours and aminor peak at 17:0018:00 hours (12, 14).

Mansonia Species

Six species of Mansonia transmit Brugian laria-sis. The nocturnal subperiodic form is known tooccur only in Brunei, Malaysia, and the Philip-pines, where it is transmitted mainly by M. an-nulata, M. bonneae, M. dives, and M. uniformis.M. uniformis is the most widely distributedspecies of the Mansonia mosquitoes. It is a vec-tor of periodic B. malayi in Sri Lanka, India, andThailand (61). M. annulifera and M. indiana are

minor vectors in Malaysia. M. annulata is alsoa vector of periodic B. malayi in Indonesia andThailand (61). Mansonia mosquitoes generallybreed in swamps and tend to be exophagic andexophilic. Biting occurs mostly during the day,with peak activity soon after sunset. They arepredominantly zoophilic and, although primar-ily exophagic, readily enter houses to feed onhumans.

Anopheles Species

In many rural areas, especially in Africa, LF istransmitted by Anopheles mosquitoes. Nelson(51) lists 26 Anopheles species as vectors ofBancroftian and Brugian lariasis. Eighteenspecies are vectors of W. bancrofti, three ofB. malayi, and ve species transmit both para-sites. An. barbirostris is the only known vector ofB. timori. In Africa, where no Brugia parasitesof humans occur, the most important vectors ofW. bancrofti are the An. funestus group and mem-bers of the An. gambiae complexincluding thefreshwater-breeding An. gambiae s.s. and An.arabiensis, as well as An. melas and An. merus,which breed mainly in saltwater (81). The ecol-ogy and behavior of the An. gambiae complexhave been reviewed by Gillies and Coetzee (28).Anopheles vectors of W. bancrofti in Asia includeAn. jeyporiensis candidiensis and An. minimus inChina; An. avirostris in the Philippines; andAn. balabacensis, An. maculatus, An. letifer, andAn. whartoni in Malaysia (81). The An. punctula-tus group of mosquitoes, including An. punctula-tus, An. koliensis, and An farauti, are the principalvectors of periodic W. bancrofti in Papua NewGuinea, West Papua (Indonesia), Solomon Is-lands, and Vanuatu (5, 6, 10, 12, 14). Charlwoodet al. (18) have written a comprehensive reviewof the ecology and behavior of the An. punc-tulatus group. Most Anopheles mosquitoes areactive at dusk or dawn or are nocturnal. SomeAnopheles mosquitoes feed indoors whereasothers feed outdoors. After blood-feeding,some Anopheles mosquitoes prefer to restindoors whereas others prefer to rest outdoors.Similarly, most Anopheles mosquitoes are alsonot exclusively anthropophilic or zoophilic.

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VECTOR GENERA-PARASITERELATIONSHIPS ANDLYMPHATIC FILARIASISELIMINATIONUnderstanding the quantitative aspects oftransmission of larial parasites by mosquitoesis essential for the rational planning of controlmeasures. An important determinant of trans-mission efciency is the relationship betweenparasite yield, the success rate of ingested mi-crolariae becoming infective L3 larvae in themosquito vector, and the density of micro-laremia in the human host. For lariasis trans-mission to be interrupted, vector density or mi-crolaria intensity needs to be driven belowa threshold that ensures no new infection oc-curs. Two types of vector-parasite relationships,limitation and facilitation, are epidemiologi-cally important. The relevance of these differ-ent relationships to lariasis elimination lies inthe predicted importance of low-density micro-laremia in sustaining transmission in differ-ent epidemiological settings. The impact thatvector genera differences can have on lariasistransmission and control was rst pointed outby Pichon et al. (55, 56), who showed that thisheterogeneous effect may arise primarily fromvariations in the form of density-dependentprocesses acting on parasite uptake and de-velopment in the different laria-transmittingvector genera. The notable ndings from thiswork, subsequently commented upon by otherworkers (26, 70, 72, 74), are that parasite in-fection dynamics in culicines, and to some ex-tent in Aedes mosquitoes (70), may be of thenegative density-dependent or limitation form.In the case of anopheline species, a critical Mfthreshold exists at low-uptake burdens beyondwhich L3 output increases or is facilitated withfurther Mf uptakes but below which develop-ment of this larval stage is hampered (70).

More recent work, which also considers reg-ulatory processes affecting the larial parasitein the human host (25, 44), however, has shownthat this analysis may be somewhat premature.Two key results arise from these fuller analyses.First, they showed that, as in other vector-borneinfections, two types of eradication thresholds

Facilitation: apositive feedbackprocess in which aparasite (at any stage)promotes the successof parasites at the sameor another stage

Density-dependentprocesses: regulatorymechanisms thatgovern parasitetransmission thatdepend in a nonlinearmanner on the parasitedensity

Parasite eradication:permanent reductionto zero of theworldwide incidenceof infection

are also most likely to exist for LF: one relatedto the infection transmission process from thevectors and the other to worm infection levels inthe human host. The theoretical threshold oc-curring in the vector-to-host transmission pro-cess is the vector biting threshold and denesthe critical vector biting density, below whichhost-vector contacts are insufcient to sus-tain infection establishment and transmission(i.e., parasite replacement) in the population.The parasite eradication threshold occurring inthe host-to-vector transmission process, on theother hand, is the breakpoint worm burden anddenes the critical unstable parasite level in thehost population, below which the parasite pop-ulation spontaneously moves to the stable zero-parasite state and above which infection can es-tablish and be sustained at stable steady states.

The second important nding to emergefrom this new work is that, owing to the likelyoccurrence of inverse density-dependent mech-anisms in the host, chief among which is theworm mating probability function, wherein theprobability of nding mates for sexual repro-duction becomes vanishingly small at low bur-dens (25, 41, 44), unstable breakpoint wormburdens may also occur in culicine-transmittedlariasis (44). This result therefore suggestsimproved prospects for the eradicability ofculicine lariasis by MDA, compared with theconclusion of the earlier studies. However, be-cause multiple inverse density-dependent fac-tors may occur in anopheline-transmitted lar-iasis (e.g., the facilitation function regulatinglarval infection in vectors and the inverse wormmating probability function regulating parasitereproduction in the human host), the magni-tudes of the two eradication thresholds are alsolikely to be higher for anopheline lariasis com-pared to the respective values that may occurfor culicine and possibly Aedes-transmitted -lariasis (25, 44). The multiple inverse density-dependent factors would again enhance theeradicability of anopheline lariasis comparedto lariasis transmitted by culicines and Aedesmosquitoes. However, as pointed out byMichael et al. (44), the ultimate values of boththresholds in reality depend crucially on the

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magnitude of the density-dependent processesoperating in vectors and hosts as well as the de-gree of infection aggregation occurring in thehost populations. As these thresholds are likelyto vary among endemic communities, the valueof either threshold is also likely to be variableamong communities. Thus, it is extremely un-likely that single global threshold values existfor LF signifying infection eradication. Thisconclusion has important relevance for the de-sign of LF elimination programs and the roleof vector control in such programs.

EMPIRICAL FIELD EVIDENCEFOR THE IMPACT OF VECTORCONTROL ON LYMPHATICFILARIASIS TRANSMISSION

The incrimination of mosquitoes as vectors ofW. bancrofti by Patrick Manson in India in 1877was the rst time that an insect was associatedwith the active transmission of an agent of anyanimal disease (69). This nding gave rise torenewed hopes about a new, possibly easy wayof eradicating the mosquito-borne diseases byextermination of the vectors. Vector control isparticularly attractive for LF because transmis-sion of the parasite is inefcient. There is nomultiplication of the parasite in the mosquitovector and only continuous exposure to bites ofmany infected mosquitoes maintains the infec-tion in humans. Having evaluated the dynamicsof transmission in Rangoon, Burma, Hairston& Meillon (29) calculated that approximately15,500 infective bites of Cx. quinquefasciatus arerequired to produce a new patent infection.Subsequently, a number of studies involvingCulex, Anopheles, and Aedes vectors in differentparts of the world have provided data that allowestimates of this parameter, ranging from 2700to over 100,000 infective bites per new humancase (71).

For many years, control of Cx. quinquefas-ciatus was based on the use of organophospho-rus insecticides, which gave excellent results insome tropical cities, such as Dar es Salaam,Tanzania, and Rangoon. However, resistanceto chlorpyrifos, fenthion, and temephos were

observed in larval populations from areas ofBrazil, Burma, Kenya, Liberia, Sri Lanka, andTanzania (82). More recently, resistance tomalathion and pyrethroids has been reportedin Cuba (65) and Cameroon (3). The great-est barrier to the effective control of Cx. quin-quefasciatus is the lack of appropriate tools forsustained interruption of breeding in the innu-merable polluted breeding sites such as pit la-trines, soakage pits, septic tanks, and cesspits.A survey of sanitation structures in a sectionof Zanzibar Town, Tanzania, revealed 3075 pitsthat were potential Cx. quinquefasciatus breed-ing sites (39). Finding those 25% of pits thatcontain water and therefore produce the Culexproblem was routinely carried out by a team ofabout 10 people. Even with the best insecticidesor biological agents, persistence is at best threemonths (32), making the required frequent re-treatment of each pit costly and labor intensive.

The treatment of enclosed bodies of waterwith a oating layer of expanded polystyrenebeads can prevent mosquito breeding for ex-tended periods (23, 38, 47, 63). Layers ofpolystyrene beads in pit latrines persist if thepit does not ood. In a survey of Cx. quin-quefasciatus breeding sites conducted in a sec-tion of Dar es Salaam, sanitation structureswere the most prolic breeding places, total-ing 2324 (20). When all the enclosed breed-ing sites were treated with polystyrene beadsand checked seven months later, only one site(from which the polystyrene had been removedduring emptying) contained immature stagesof Cx. quinquefasciatus. Expanded polystyrenebeads are capable of preventing breeding insanitation structures for at least ve years (23),although the periodic emptying of these struc-tures is likely to reduce the effective life of a sin-gle treatment. Nathan et al. (50) used shreddedwaste polystyrene (discarded packaging mate-rial shredded to irregular particles 25 mm indiameter) in the same way to achieve severalmonths of control of Cx. quinquefasciatus breed-ing in pit latrines.

Maxwell et al. (38) applied polystyrene beadsto all the wet, Culex-infested pit latrines inMakunduchia community of 12,000 people

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on Zanzibar, Tanzania. This treatment reducedthe number of bites per person per year from25,000 to 440 (98%). Mass treatment of thecommunity with DEC rapidly reduced the Mfrate from 49% to 10%, which had the effectof reducing the proportion of L3 infectivemosquitoes from 2.4% to 0.4%, so that thenumber of infective bites per person per yearwent down by 99.7%. After this single cam-paign of DEC treatment plus sustained vectorcontrol, follow-up surveys showed continueddecline to a Mf rate of 3% after ve years (39).Evidence that vector control had contributed tothis long-term decline was obtained by compar-ison with another town where DEC was usedwithout vector control. Treatment with DECwithout vector control resulted in a resurgenceof Mf three to six years after the drug campaign.Whereas long-term prevention of resurgenceof infection could probably have been achievedby annual rounds of drug treatment, the 98%reduction in the biting nuisance achieved by thevector control greatly increased public appreci-ation of the benet of this integrated program.

In Zanzibar Town, treatment of 3075 pitlatrines and cracked cesspits with polystyrenebeads reduced the resultant Cx. quinquefascia-tus biting rate by about 65%. Additional treat-ment of the drains and marshes in one sectorof the town with Bacillus sphaericus did not pro-duce a signicant improvement in this reduc-tion of mosquito biting rate compared to an-other sector where only the pit treatment withpolystyrene beads was carried out (39).

In 1981 the Vector Control Research Centerin Pondicherry, India, initiated a ve-year in-tegrated vector control program to reduce thetransmission of W. bancrofti by Cx. quinquefas-ciatus (24, 59). Measures taken to prevent oreliminate the breeding of mosquitoes in theirnatural or human-made habitats included clos-ing of wells and the application of expandedpolystyrene beads in overhead tanks and sanita-tion structures such as cesspits and septic tanks.Biological control methods included the releaseof larvivorous sh such as Gambusia and Tilapiain suitable habitats. In the few areas wherechemical larvicides were required, fenthion was

chosen in addition to synthetic pyrethroids andjuvenile hormone analogues. After ve years ofvector control activities, the indoor resting den-sity of Cx. quinquefasciatus was reduced by 90%and the prevalence of Mf decreased by 60%. Ananalysis of the costs showed that integrated con-trol methods compared favorably with controlmethods using conventional insecticides.

Reuben et al. (64), working in nine villagesin southern India between 1995 and 1999, com-pared the impact of single-dose two-drug treat-ment (DEC plus IVR) alone with its combi-nation with vector control. The nine villageswere randomly allocated to three groups; onegroup of three villages received MDA in 1995and 1996; a second group of three villages re-ceived MDA with vector control in 1995 and1996; and a third group of three villages was nottreated until 1999. Vector control was carriedout using polystyrene beads and larvivorous sh(Tilapia spp.) in the major breeding sites ofCx. quinquefasciatus. Breeding sites where shdid not survive were treated with B. sphaericus.After the rst round of treatment, chemother-apy alone brought about a 60% drop in theAnnual Transmission Potential (ATP), and theintegrated control method reduced ATP by96%. However, when the drug pressure was re-moved two years later, transmission resumed invillages with no vector control but remained in-terrupted for one year in the villages with sup-plemental vector control. In 2001, the threevillages that previously received MDA aloneand the three that received MDA plus vectorcontrol were included in the GPELF programand treated with DEC plus ALB. Vector con-trol continued in the three villages where itwas previously carried out. Analysis in 2006(73) showed that vector density decreased sig-nicantly in villages where vector control wasused as an adjunct to MDA, and no infec-tive mosquitoes were found in the small num-bers caught during 20032005. Filarial anti-genemia was low and continued to decreasesignicantly in 15- to 25-year-olds in villagesreceiving MDA with vector control in con-trast to villages receiving only MDA. The au-thors concluded that the gains of MDA were

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sustained only with the integration of vectorcontrol measures. They advocated the incor-poration of vector control into the GPELF be-cause it can potentially decrease the time re-quired for eliminating LF.

Open breeding sites such as areas of oodedland and blocked drains can be treated withmodern insecticides such as pyriproxyfen, aninsect growth regulator, or the biological agentB. sphaericus. Pyriproxyfen treatment of openbreeding sites in Dar es Salaam (19) inhibitedthe emergence of adult Cx. quinquefasciatus fromthese sites for up to 11 weeks during the dry sea-son. The problem of mosquito breeding sitescaused by bathroom sewage water can be effec-tively addressed through health education in-volving local community leaders. Householdsresponsible for creating such breeding sites canbe encouraged to eliminate them by divertingthe water into an enclosed drainage structure,usually a latrine. Chavasse et al. (19) reporteda 93% compliance from households in Dar esSalaam after ve visits.

In Sarawak, Malaysia, Chang et al. (17)compared the impact of mass treatment alone(DEC) versus its combination with residualhouse spraying of pirimiphos-methyl when acontrol program against subperiodic Brugian -lariasis was implemented in three villages: Kam-pong Ampungan, Kampong Sebangkoi, andKampong Sebamban. In Kampong Ampungan,the mass administration of DEC combined withresidual house spraying of pirimiphos-methylreduced the Mf rate to 8% of the pretreatmentlevel and the Mf density (MfD50) to 44% of thepretreatment level over a period of four years.In Kampong Sebangkoi and Kampong Sebam-ban, where only mass DEC therapy was applied,the Mf rate and MfD50 declined distinctly inthe second blood survey but increased gradu-ally in two subsequent follow-up blood surveys.In Kampong Ampungan, a signicant reductionof infective biting rate (88.3%), infection rate(62.5%), and transmission potential (88.1%) ofMansonia bonneae was observed at the fourthspray round. The corresponding reductionrates in Kampong Sebangkoi and Kampong Se-bamban were 35.3%, 26.7%, and 42.2% and

24%, 30.8%, and 15.4%, respectively. The bit-ing density of the vector was reduced by 79.8%indoors and 31.8% outdoors in the sprayed vil-lage, whereas only a slight decrease in densities(17.9% indoors and 12.4% outdoors) was ob-served in the unsprayed village.

Indoor spraying of residual DDT was widelyused and highly effective in most malaria con-trol programs. House spraying with this insec-ticide led to reduction or interruption of thetransmission of W. bancrofti by the An. punc-tulatus group in Solomon Islands (78), PapuaNew Guinea (5), and Indonesia (33), and bythe An. gambiae complex and An. funestus inTogo (9, 67). Similarly, where malaria controloperations were maintained at adequate levels,W. bancrofti transmission was reduced in partsof Central America where An. darlingi is thevector and in Southeast Asian countries whereB. malayi was transmitted by An. sinensis, An.barbirostris, and other endophilic vectors (82).In the areas where vector control alone in-terrupted lariasis, facilitation was the vector-parasite relationship involved (72, 79).

Vector control dramatically reduced thetransmission rates of Brugian lariasis by Man-sonia species in Sri Lanka, where the preva-lence rate of B. malayi was 6.8% in 1939, be-fore DDT house spraying was implemented tocontrol malaria (66). However, during a surveyconducted between 1959 and 1965, after DDThouse spraying had commenced countrywideto control malaria, microlaremic individualshad completely disappeared from the country(1). The dramatic reduction in Mf rates was at-tributed to vector control by DDT spraying.

Rajagopalan et al. (60) compared infectionand disease rates in Kerala state, India, reportedin earlier studies conducted in 1934, 1955, and1976 with a 1986 survey and concluded thatprevalence of clinical Brugian lariasis can bereduced by integrated vector control alone.Vector control measures were initiated as earlyas 1933 by the state Filariasis Control Works,an organization engaged in physical removalof Pistia plants. In some areas, vector densitywas reduced by replacing Pistia with Salvinia, aweed that is less suitable for Mansonia breeding

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(34). Indoor residual spraying of DDT wasintroduced in 1959 under the malaria con-trol program, and pilot studies conducted inKerala in 1959 showed that indoor applicationof residual insecticides reduced the density ofM. annulifera to practically zero for at least sixmonths (66). The impact of vector control inKerala over the years led the WHO ExpertCommittee on Filariasis to conclude that trans-mission of B. malayi could be greatly reducedby vector control with or without chemother-apy (82). It was also pointed out that B. malayihad disappeared from some Indian villages, inthe states of Madhya Pradesh, Orissa, and TamilNadu, while new foci of W. bancrofti were beingestablished.

Recent studies comparing the effect ofpermethrin-impregnated bednets and DDThouse spraying against malaria transmissionin the Solomon Islands showed the formerto be more effective (30, 36), suggesting thattreated bednets may be as effective against LFas house spraying. Introduction of permethrin-impregnated bednets in a lariasis-endemicarea of Kenya signicantly reduced the indoorresting densities of An. gambiae s.l. by 94.6%and An. funestus by 96.7%, but there was nochange in the number of Cx. quinquefascia-tus collected indoors (8). However, the humanblood index for Cx. quinquefasciatus was reducedfrom 93.1% to 14.4%.

The effect of untreated bednet usage onW. bancrofti Mf and disease was investigated,without undertaking a specic intervention, inthree coastal villages on Bagabag Island, PapuaNew Guinea (7). The majority (60.1%) of the1057 villagers interviewed reported that theyhad used a bednet the previous night. In gen-eral, bednet users had signicantly lower rates(P < 0.003) and intensities (P = 0.010) of Mfthan nonusers. Users were similar to nonusersin prevalence of lymphedema but hydroceleprevalence was 2.8 times higher in nonusersthan users. The impacts of untreated bednetsaccumulate only slowly and cumulative effectsof changes in human-vector contact are morelikely to affect the prevalence of lariasis thanmalaria because the transmission of lariasis is

Integrated vectormanagement (IVM):a vector controlstrategy that involvesusing more than onecontrol method andthat targets eachmethod to the settingsin which it is mostappropriate

less efcient than malaria. Similarly, a modestreduction in the number of mosquitoes bitinghumans, attributable to the use of insecticide-treated nets, strongly suppressed the risk of in-fection of W. bancrofti in the Kwale District ofKenya (54).

Chemical control and the use of impreg-nated materials is not effective when the vec-tor is exophilic and diurnal. This is the case inmost Pacic Island countries where Ae. scutel-laris and Ae. polynesiensis are vectors of the di-urnal subperiodic W. bancrofti. Larval controlof these mosquitoes is also difcult becausethey breed in a wide range of small contain-ers, which are too numerous to locate anddeal with individually. In such situations masschemotherapy offers the best prospect of con-trol. However, the use of the systemic drug IVRin mass chemotherapy may have an effect on thesurvival of Ae. polynesiensis. Cartel et al. (15),working with this species in French Polyne-sia, observed signicant reductions in mosquitosurvival up to three months after feeding onpeople treated with IVR and DEC.

New pyrethroids as well as biological agentssuch as insect growth regulators (pyriprox-yfen) and bacterial toxins (Bacillus sphaericusand Bacillus thuringiensis) are now in opera-tional use. Photostable pyrethroids (e.g., per-methrin, deltamethrin, and lambdacyhalothrin)with residual insecticidal activity on impreg-nated curtains and bednets have proved to beeffective against mosquito populations resistantto organophosphorus compounds (8, 80), al-though resistance to pyrethroids also is becom-ing a problem in many vector species. Note thatthe persistence of polystyrene beads is an orderof magnitude greater than the longest persis-tence ever claimed for any chemical or micro-bial larvicide (Table 1).

Several new and effective antimosquito toolsare now available for integrated vector man-agement (IVM) to become an important com-ponent of the lariasis elimination strategy. Inparticular, the approach is likely to play animportant role in endemic areas where morethan one vector species, with different feed-ing and breeding habits, may be involved in

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Table 1 World Health Organization recommended insecticides for indoor residual spraying for Anopheles mosquito controla

Insecticide compoundsand formulations Class group Dosage (g/m2) Mode of action

Duration of effective action(months)

DDT WP OC 12 Contact >6Malathion WP OP 2 Contact 23Fenitrothion WP OP 2 Contact and airborne 36Pirimiphos-methyl WP and EC OP 12 Contact and airborne 23Bendiocarb WP C 0.10.4 Contact and airborne 26Propoxur WP C 12 Contact and airborne 36Alpha-cypermethrin WP and SC P 0.020.03 Contact 46Cyuthrin WP P 0.020.05 Contact 36Deltamethrin WP P 0.010.025 Contact 23Etofenprox WP P 0.10.3 Contact 36Lambda-cyhalothrin WP P 0.020.03 Contact 36

aReproduced with permission from the World Health Organization (http://www.who.int/malaria/cmc upload/0/000/012/604/IRSInsecticides.htm).Abbreviations: C, carbamates; EC, emulsiable concentrate; OC, organochlorines; OP, organophosphates; P, pyrethroids; WP, wettable powder.

Figure 1(a) Deterministic lariasis transmission model predictions of the number of years of intervention required by various annual MDA andcombined annual MDA plus vector control options to achieve the target elimination threshold of 0.5% Mf prevalence (44) for a rangeof precontrol community endemicity (Mf%) levels. Solid curves give predictions for IVR/ALB and DEC/ALB annual MDA regimens,while dashed curves portray the corresponding results for each of these regimens combined with vector control. Drug efcacy values:DEC/ALB, 55% worm kill, 95% Mf cured, and six months Mf suppression; IVR/ALB, 35% worm kill, 99% Mf cured, and ninemonths Mf suppression. Vector control is assumed to be 90% effective in reducing vector biting. The orange dashed curve with orangesquares denotes the effects of increasing the frequency of mass treatment to the DEC/ALB plus vector control regimen (mass treatmentgiven once every six months). The vertical gray-dotted droplines indicate the maximum endemicity level at which it would be feasibleto achieve the set target threshold of 0.5% Mf prevalence within the prescribed six years of control by each intervention. The shadedregion represents the feasibility domain of the various larial interventions examined and indicates simply that for each intervention-endemicity combination studied and for the given effectiveness and MDA coverage values, it will not be possible to reach the endpointtarget of 0.5% Mf prevalence before the respective estimated years of intervention indicated in the gure (see Reference 44). All resultsat 1 ml blood sampling volume. (b) Model simulations of the number of years of intervention required by the mass annual DEC/ALBregimen either administered alone (solid lines) or with vector control (dashed lines) to achieve the 0.5% Mf prevalence threshold for a mixof precontrol community Mf prevalences (5%, 10%, and 25%) and drug coverage values. Ninety percent vector control efcacyassumed. Vertical gray-dotted droplines show the optimal drug coverage required at each endemicity level by each of these options tomeet the control criterion of achieving the 0.5% Mf prevalence threshold in six years (modied after Reference 44). (c) The existence ofbistable infection states and hysteresis loops in the Mf prevalence/vector biting rate plane for lariasis transmitted by culicineintermediate hosts. Bistable states (the endemic positive infection and the trivial zero-parasite states) (solid purple lines) may occur inlariasis as a result of the operation of inverse density-dependent regulatory processes, such as the mating probability function (44).These states emerge at the threshold vector biting rate and are separated by an unstable worm breakpoint boundary (dashed purplecurve). The system is attracted to the stable zero-parasite state even if infection is introduced until the threshold vector biting rate isreached. Above this biting threshold the introduced infection is attracted either to the endemic stable state or to the zero-parasite statedepending on whether the introduced infection values are above or below the unstable worm breakpoint threshold. The graph showsthe two asymmetrical ways by which a shift between these alternative Mf stable states can occur with varying vector biting rates. If theparasite system is on the lower zero state but at high vector biting rates and thus close to the worm breakpoint bifurcation boundary, aslight incremental change in Mf levels may bring it beyond the bifurcation (e.g., at 0.1% Mf prevalence) and induce a drastic shift of thesystem to its endemic equilibrium (rightmost red arrow). If one attempts to restore the parasite-free equilibrium state by reducing thevector biting rate (leftward black arrow), the system shows hysteresis. A backward shift to the parasite-free equilibrium (leftmost red arrow)will occur only if the vector biting rate is reduced far enough to reach the threshold biting-rate bifurcation point. The hysteresis loop iswider for the anopheline model than for culicine-transmitted lariasis (data not shown), suggesting the vector control will be moreeffective in the case of eliminating culicine-mediated lariasis because it would more rapidly raise the worm breakpoint threshold value,thus enhancing both the prospects of parasite elimination and prevention of re-emergence following control.

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transmitting the same LF parasite. Similarly,concerns about insecticide resistance, safety,and environmental impact, as well as the highcost and sustainability of programs based pre-dominantly on conventional insecticides, havestimulated increased interest in IVM. An IVMapproach combines, in a feasible way, two ormore of the antimosquito measures so that theycan achieve a greater impact. This approachis evidence-based and an essential feature of itis the development of the capacity to generatelocal data on disease epidemiology and vectorecology. IVM activities thus promise to offer

a new potentially highly effective approach forsuccessfully incorporating vector control intoLF elimination programs.

MODELING THE STRATEGICIMPORTANCE OF VECTORCONTROL IN LYMPHATICFILARIASIS ELIMINATION

Recent modeling work has focused on quanti-fying the precise strategic roles that includingvector control can play in LF elimination pro-grams (44, 46). First, as portrayed in Figure 1a,

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Equilibrium: aparasite density (of anystage) that remainssufciently constantover a long period oftime

inclusion of vector control incorporating a 90%reduction in vector biting (7, 22, 39) in MDAprograms with either IVR/ALB or DEC/ALBdrug combinations (given at 80% drug cover-age) not only enables extension of the range ofbaseline community infection endemicities (Mfprevalences) that can be feasibly brought underelimination (i.e., reducing below the 0.5% Mfprevalence elimination target threshold withinthe six-year period recommended by WHO).For a given baseline endemicity level, vectorcontrol also accelerates the effects of MDA inbringing about parasite elimination (i.e., re-ducing the number of years of MDA requiredto meet the elimination target of 0.5% Mfprevalence).

The results in Figure 1a show that addi-tion of vector control to the IVR/ALB MDAregimen allows the achievement of the targetthreshold Mf prevalence in communities withup to 6.65% precontrol Mf prevalence at the1 ml blood sampling volume (from only the3.75% eradicable Mf prevalence possible withMDA alone), whereas in the case of the more ef-fective DEC/ALB regimen, the added benetwould be to increase the controllable precon-trol infection limit from 10% for MDA aloneto 18% Mf prevalence for MDA plus vectorcontrol. Similarly, the number of control yearssaved by the inclusion of vector control to drugtreatment indicates that, on average between6 months to 1 year at low (20%), precontrolcommunity infection levels may be saved byadding vector control to each of the DEC/ALBand IVR/ALB regimens (Figure 1a). Thesendings abundantly underscore the crucialrole that including vector control in MDAprograms will play in areas of high endemicityand in areas, such as Africa, where MDA usingIVR/ALB is to be implemented.

The second important strategic role of in-cluding vector control in MDA programs ishighlighted by the results in Figure 1b. Thekey nding here is that all precontrol infec-tion situations, including vector control, willlower the optimal MDA coverage required tomeet a set control criterion compared with

MDA alone. The gains, however, will be sig-nicantly larger for lower precontrol infectionprevalence communities (e.g., whereas MDAwith the DEC/ALB regimen would require anoptimal drug coverage of 75% to achieve thetarget Mf threshold of

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related to the nding that the unstable wormbreakpoint boundary separating the two par-asite stable states (i.e., the zero and endemicinfection states) is a dynamic function of thevector biting rates above the threshold bit-ing rate. Thus, although the worm breakpointprevalence is highest at the threshold bitingrate, this declines markedly as vector bitingrates above the threshold biting value increase(Figure 1c). This inverse relationship readilyhighlights a strategic role for vector controlin lariasis elimination, as reducing vector bit-ing rates toward the threshold biting rate valuewill shift the values of worm breakpoints up-ward, thus making achievement of eliminationeasier.

Figure 1c further illustrates the signicanceof the occurrence of system hysteresis in -lariasis control. If community vector biting isnot reduced, then following parasite reductionin humans (by chemotherapy), a small uctua-tion or input of parasites into a community cancause the ready re-emergence of the stable lar-ial endemic state. On the other hand, includingvector control would essentially, by reducingthe hysteresis loop, increase the re-emergenceMf prevalence threshold. This result supportsempirical evidence (73) that vector controlwill be crucial to the long-term sustenanceof parasite elimination from treated endemiccommunities.

CONCLUSIONS

The current principal strategy of GPELFfor interrupting the transmission of LF is totreat the entire at-risk population throughcommunity-wide MDA programs. The datasuggest that this strategy may indeed serve asa more effective approach to stop transmissionwhere LF is anopheline-transmitted than whereCulex is responsible, essentially owing to theintrinsically greater efciency of the latter intransmitting LF. Even so, this review shows thatincluding vector control would represent animportant strategic tool to expedite and sustainthe achieved interruption of lariasis transmis-sion by both of these vectors. In addition, the

results show that it could also serve as a majortool to overcome deciencies in obtaining andmaintaining the high drug coverages requiredby MDA programs alone for achieving LF elim-ination. With regard to methods, the emergingevidence that pyrethroid-impregnated screen-ing materials such as bednets and curtainscould be as effective as DDT in reducingtransmission of laria parasites by Anophelesand Mansonia mosquitoes is encouraging.The control of Aedes mosquitoes as vectors ofW. bancrofti, however, remains problematic,and chemotherapy seems the most appropriateway to reduce transmission. This is furthersupported by the results of one study (15),which has shown that Ae. polynesiensis feedingon people treated with IVR or DEC may suffera signicant reduction in survival rate.

Successful vector control requires ade-quate resources and well-trained personnel. Inreviewing decades of lariasis vector control ac-tivities in India and Myanmar, MacDonald (37)recognized that results were good when well-trained staff with substantial resources wereemployed and that results were much poorerwhen less well-equipped general health work-ers took over the programs. Many LF-endemiccountries are resource constrained and there-fore vector control is given low priority. How-ever, strategic planning can make vector controlcost effective. For instance, it may be cheaper toapply polystyrene beads to the limited numberof Cx. quinquefasciatus larval habitat categoriesthat commonly contribute a large proportion ofthe adult population. However, insecticides andbiological control agents should be used as sup-plements, not as alternatives to environmentalmanagement (15). The participation of localcommunities in the implementation of inte-grated control measures is especially importantin resource-poor countries. In many communi-ties where lariasis mosquitoes are a biting nui-sance, the noticeable impact of vector controlmight help to gain community support for inte-grated control programs involving chemother-apy. We suggest that priority now be urgentlygiven to the formulation and evaluation of theimpact that such targeted IVM strategies can

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have on LF elimination in different endemicregions.

LF elimination will also be easier to achieveif MDA and vector control can be integratedinto other public health programs (11, 48).Filariasis and malaria are coendemic in manyparts of Africa (2, 4, 27, 35), Asia (62), andsome Pacic Island countries including PapuaNew Guinea (6) and the Solomon Islands (76),

where disease agents are transmitted by thesame Anopheles mosquitoes. In such settingsGPELF can synergize its activities with malariavector control efforts using LLITNs. Forgingsuch links would also present opportunities forsupport by the Global Fund to ght AIDS, Tu-berculosis and Malaria, which will increase theoverall prospects for the successful control ofboth of these parasites in aficted populations.

SUMMARY POINTS

1. LF, also known as elephantiasis, is a leading cause of permanent and long-term disabilityin many parts of the tropical world.

2. The larial parasites have biphasic life cycles involving the denitive mammalian hostand various genera of mosquito vectors.

3. The parasites responsible for over 90% of global infections, W. bancrofti and B. malayi,have no animal reservoirs, suggesting that transmission can be eliminated by reducingthe parasite load in human populations through mass drug treatments.

4. A global alliance was initiated in 2000 to eliminate LF through mass treatment alone.

5. Owing to emerging problems with mass treatment programs, vector control is increas-ingly recognized as a potential supplemental strategy for tackling the disease.

6. Empirical evidence and the availability of diverse vector management measures that takeaccount of different vector ecologies and biting behaviors show that it may now be feasibleto include integrated vector control activities in LF mass drug campaigns.

7. Mathematical modeling indicates three major strategic roles for including vector controlin LF elimination programs: First, transmission elimination will be accelerated by raisingworm breakpoint thresholds and by reducing the number of years of required drugintervention. Second, the drug coverages required will be lowered. Third, long-termparasite elimination from treated communities will be sustained by raising the infectionthresholds to prevent the re-emergence of stable transmission.

8. The different population ecologies of parasite transmission in Anopheles versus Culex andAedes mosquitoes suggest that it may be theoretically easier to eradicate LF from areaswhere the parasite is transmitted primarily by the rst vector than from areas wherethe parasite is transmitted via the last two vectors. Inclusion of vector control is thusparticularly important in areas with culicine and Aedes transmission.

FUTURE ISSUES

1. Making vector control a part of the global strategy for eliminating LF is predicted toreduce the number of treatment cycles required to interrupt transmission and to preventre-emergence where interruption has been achieved. Field studies are now required toempirically test these predictions.

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2. Comparison of the eld effectiveness of combined MDA and vector control in reduc-ing and even eliminating LF transmission between communities with Anopheles andCulex/Aedes are urgently required. The cost effectiveness and feasibility of using thisapproach versus using MDA alone also needs to be quantied.

3. More detailed evaluation of the effectiveness and sustainability of using available vectorcontrol measures is required, including assessing the formulation and effectiveness ofthe optimal IVM measures for controlling the major vector genera implicated in LFtransmission.

4. More effective mosquito sampling and improved parasite diagnostic methods are requiredto accurately quantify the dynamics of LF control, including determination of when thegoal of elimination has been attained.

5. Better integration of mathematical models with human infection and mosquito surveil-lance data is required to improve predictions and decision making with regard to bothoptimal design and assessment of the impact of interventions.

6. A greater understanding of vector-parasite relationships and spatial and temporal varia-tions in exposure to infection will improve the estimation of elimination thresholds.

DISCLOSURE STATEMENT

The authors are not aware of any biases that might be perceived as affecting the objectivity of thisreview.

ACKNOWLEDGMENTS

We are grateful to Dr. Chris Curtis, who read earlier versions of the manuscript and providedus with helpful comments. M.J.B. is thankful for the nancial support of United States PublicHealth Service NIH ICIDR grant U19 AI33061 during the writing of this review. E.M. grate-fully acknowledges the nancial support of United States Public Health Service NIH grant R01AI69387-01A1 for facilitating this work.

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Annual Review ofEntomology

Volume 54, 2009Contents

FrontispieceEdward S. Ross xiv

Lifelong Safari: The Story of a 93-Year-Old Peripatetic Insect HunterEdward S. Ross 1

Ecology and Geographical Expansion of Japanese Encephalitis VirusAndrew F. van den Hurk, Scott A. Ritchie, and John S. Mackenzie 17

Species Interactions Among Larval Mosquitoes: Context DependenceAcross Habitat GradientsSteven A. Juliano 37

Role of Glucosinolates in Insect-Plant Relationships and MultitrophicInteractionsRichard J. Hopkins, Nicole M. van Dam, and Joop J.A. van Loon 57

Conict, Convergent Evolution, and the Relative Importance ofImmature and Adult Characters in Endopterygote PhylogeneticsRudolf Meier and Gwynne Shimin Lim 85

Gonadal Ecdysteroidogenesis in Arthropoda: Occurrenceand RegulationMark R. Brown, Douglas H. Sieglaff, and Huw H. Rees 105

Roles of Thermal Adaptation and Chemical Ecology in LiriomyzaDistribution and ControlLe Kang, Bing Chen, Jia-Ning Wei, and Tong-Xian Liu 127

Fitness Costs of Insect Resistance to Bacillus thuringiensisAaron J. Gassmann, Yves Carrire, and Bruce E. Tabashnik 147

Insect Herbivore Nutrient RegulationSpencer T. Behmer 165

Manipulation of Host Behavior by Parasitic Insects and Insect ParasitesFrederic Libersat, Antonia Delago, and Ram Gal 189

Bionomics of Bagworms (Lepidoptera: Psychidae)Marc Rhainds, Donald R. Davis, and Peter W. Price 209

vii

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Host-Parasitoid Associations in StrepsipteraJeyaraney Kathirithamby 227

Biology of the Parasitoid Melittobia (Hymenoptera: Eulophidae)Robert W. Matthews, Jorge M. Gonzlez, Janice R. Matthews, and Leif D. Deyrup 251

Insect Pests of Tea and Their ManagementLakshmi K. Hazarika, Mantu Bhuyan, and Budhindra N. Hazarika 267

New Insights into Peritrophic Matrix Synthesis, Architecture,and FunctionDwayne Hegedus, Martin Erlandson, Cedric Gillott, and Umut Toprak 285

Adaptation and Invasiveness of Western Corn Rootworm: IntensifyingResearch on a Worsening PestMichael E. Gray, Thomas W. Sappington, Nicholas J. Miller, Joachim Moeser,and Martin O. Bohn 303

Impacts of Plant Symbiotic Fungi on Insect Herbivores: Mutualismin a Multitrophic ContextSue E. Hartley and Alan C. Gange 323

A Study in Inspiration: Charles Henry Turner (18671923) and theInvestigation of Insect BehaviorCharles I. Abramson 343

Monogamy and the Battle of the SexesD.J. Hosken, P. Stockley, T. Tregenza, and N. Wedell 361

Biology of Subterranean Termites: Insights from Molecular Studiesof Reticulitermes and CoptotermesEdward L. Vargo and Claudia Husseneder 379

Genetic, Individual, and Group Facilitation of Disease Resistancein Insect SocietiesNoah Wilson-Rich, Marla Spivak, Nina H. Fefferman, and Philip T. Starks 405

Floral Isolation, Specialized Pollination, and Pollinator Behaviorin OrchidsFlorian P. Schiestl and Philipp M. Schlter 425

Cellular and Molecular Aspects of Rhabdovirus Interactionswith Insect and Plant HostsEl-Desouky Ammar, Chi-Wei Tsai, Anna E. Whiteld, Margaret G. Redinbaugh,and Saskia A. Hogenhout 447

Role of Vector Control in the Global Program to EliminateLymphatic FilariasisMoses J. Bockarie, Erling M. Pedersen, Graham B. White, and Edwin Michael 469

viii Contents

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Annual Reviews OnlineSearch Annual ReviewsAnnual Review of EntomologyOnlineMost Downloaded Entomology ReviewsMost Cited Entomology ReviewsAnnual Review of Entomology ErrataView Current Editorial Committee

All Articles in the Annual Review of Entomology, Vol. 54Lifelong Safari: The Story of a 93-Year-Old Peripatetic Insect HunterEcology and Geographical Expansion of Japanese Encephalitis VirusSpecies Interactions Among Larval Mosquitoes: Context DependenceAcross Habitat GradientsRole of Glucosinolates in Insect-Plant Relationships and MultitrophicInteractionsConflict, Convergent Evolution, and the Relative Importance ofImmature and Adult Characters in Endopterygote PhylogeneticsGonadal Ecdysteroidogenesis in Arthropoda: Occurrenceand RegulationRoles of Thermal Adaptation and Chemical Ecology in LiriomyzaDistribution and ControlFitness Costs of Insect Resistance to Bacillus thuringiensisInsect Herbivore Nutrient RegulationManipulation of Host Behavior by Parasitic Insects and Insect ParasitesBionomics of Bagworms (Lepidoptera: Psychidae)Host-Parasitoid Associations in StrepsipteraBiology of the Parasitoid Melittobia (Hymenoptera: Eulophidae)Insect Pests of Tea and Their ManagementNew Insights into Peritrophic Matrix Synthesis, Architecture,and FunctionAdaptation and Invasiveness of Western Corn Rootworm: Intensifying Research on a Worsening PestImpacts of Plant Symbiotic Fungi on Insect Herbivores: Mutualismin a Multitrophic ContextA Study in Inspiration: Charles Henry Turner (18671923) and theInvestigation of Insect BehaviorMonogamy and the Battle of the SexesBiology of Subterranean Termites: Insights from Molecular Studiesof Reticulitermes and CoptotermesGenetic, Individual, and Group Facilitation of Disease Resistancein Insect SocietiesFloral Isolation, Specialized Pollination, and Pollinator Behaviorin OrchidsCellular and Molecular Aspects of Rhabdovirus Interactionswith Insect and Plant HostsRole of Vector Control in the Global Program to EliminateLymphatic Filariasis