260 JouRul oF THEArrlpnrclN Mosquno CoNrRor,AssocrarroN Vor..7, No.2

PERSPECTIVESON MANAGEMENT OF PESTIFEROUS CHIRONOMIDAE (DIPTERA), AN EMERGING GLOBAL PROBLEM ARSHADALI

Uniuersity of Florida, IFAS, Central Florida Researchand Education Center,2700 East CeleryAuenue. Sanford,FL 32771-9608

ABSTRACT. In recent years, adult Chironomidae emerging from some urban natural or man-made habllats have increasingly posed a variety of nuisance and economic problems, and in some situations medical problems to humans in different parts of the world. Although there are an estimated 4,000 or more speciesof chironomid midgesworldwide, lessthan 100species have been reported to be pesti'ferous. Among midge control methods, numerous laboratory and field studies have been conducted on the use of o^rqanochlorines,organophosphates (OPs), pyrethroids and insect growth regulators (IGRs). Field use of OP insecticides such as chlorpyrifos, temephos and others in the USA ind Japan hai generally resulted in larval control for 2-5 wk or longeiwith application rates below 0.56 kg AI/ha (U=S.q)ani 51-5 ppln (Japan).Frequent use of some OP insecticidesin the USA and Japan has caused.their increasedtolerance in severalmidge species.The IGRs, diflubenzuron and methoprene,provide alternate means for midge control. These IGRs in some situations suppressedadult midge eme.ge.tceby >g\Vo at rates (0.3 tBacillus thuringiensis serovar. israelensisis effective igainst some mid-gespecies, but at rates at least 10x or higher established for mosquito larvicidal aciiuity. The flatriorm, Dugesia doro.tocephala,and some fish speciesoffer a goodpotential for midge control in somesituations. In l"arge habitatscovering hundreds or thousands of ha, information on t[e basic ecology of larval midges arid adult behavior is essential for formulating midge control criteria. More reseirch is neededln the biological and physical and cultural control of these pestiferousinsects.

INTRODUCTION 1978), in the lagoon surrounding the city of Venice, Italy (AIi et al. 1985b),in man-made Nonbiting midge flies of the dipteran family urban and suburban aquatic environments, such Chironomidae commonly occur in most inland as shallow and open wastewater channels (Ali natural or man-made aquatic ecosystemsof di- and Mulla 1976a),water spreadingbasins (Ali verse natures. They inhabit shallow and fast and Mulla 1978a),sewage oxidation and settling flowing headwaters of streamsand rivers as well ponds and overflow gutters (Edwardset al. 1964, as deep and slow moving waters in lagoons. Spiller 1965,Tabaru1985b), and residential-rec- Midges occur in stagnant waters in small and reational lakes (Ali and Mulla 1977b,Ali et al. shallow temporary or permanent ditches and 1978). ponds and in large shallow or deep lakes. Chi- Generally, water bodies in urban and subur- ronomid larvae exhibit a very wide range of ban areasexposed to intensivehuman use (res- toleranceto environmentalconditions as indi- "clean" idential,recreational, agricultural, etc.) and also cated by their presencein waters satu- "pol- receiving discharges from point and nonpoint rated with dissolved oxygen, as well as in sourcesare becomingincreasingly eutrophic. As luted" waters very low in oxygen. The occur- a consequence,macrofaunal speciesdiversity in rence of certain speciesof midges in polluted these habitats is gradually decreasing and re- waters is indicative of the type of pollution in sults in the survival and profuse breeding of their habitat. Due to their adaptive nature, some morepollution-tolerant organisms, such as some midgespecies survive evenin brackish, estuarine speciesof Chironomidae that constitute a major or marine environments. Although most chiron- component of the macroinvertebrates.It should omids are aquatic, a few speciesoccur in decay- be understood that generally chironomid larvae ing organic matter, under bark, or in moist soil. play a beneficial role as an important source of In recent years, large populations of midge food for the predatory fish and some other in- larvae have been reported in different countries vertebrates in the food web of aquatic ecosys- (e.g., USA, Japan, Italy, Sudan and others). tems. The larvae also keep the aquatic environ- Somecentral Florida lakes support midge larval ment clean by consuming and recycling organic densities of 10,000-40,000/m'or higher, result- debris; hence, they are consideredhighly desir- ing in heavy emergenceof adult midges from able organisms in the ecosystem.However, the these lakes (AIi and Baggs 1982, Callahan and adult midges from some denselypopulated hab- Morris 1987, Patterson 1964). Similar larval itats frequently emergein large numbers, caus- densities of midges are encountered in some ing a variety of nuisance,economic and in some rivers and lakes of Japan (Moriya 1977,Ohno situations medicalproblems for humans residing and Shimizu 1982, Tabaru 1975. Tabaru et al. or working near their breeding sources.The ever JUNE1991 MeNecnupNt or PosrlrnRous CnrRoNolrroen increasing importance of chironomids as a pest (Cranston et al. 1981, Gad-El-Rab and Kay and the somewhat scattered literature on their 1980),Europe (Giacomin and Tassi 1988) and chemical, biological, physical and cultural con- Asia (Ito et al. 1986). It is believed that midges trol necessitatedcompilation of this review. are a potential cause of allergies worldwide (Cranstonet al. 1983).Adult midgesmay even cause anaphylactic shock in some individuals NUISANCE, ECONOMIC AND (M. Sasa,personal communication). MEDICAL PROBLEMS Chironomid larvae, too, can produce certain storage Dense swarms of midges often limit outdoor undesirable effects. When inhabiting potable lar- human activity since the adults can be inhaled and distribution systemsfor water, concern to or fly into the mouth, eyesand ears of an indi- vae may pass through taps causing reports of vidual. They are liable to cause asphyxia in householders. There are numerous parts cattle. During summer, midges seek cool and midges infesting water systemsin various (e.9., 1945a, shady places in the daytime leaving behind of the world Hafrz 1939, Flentje stained stucco,paint and other wall finishes on Wilhelmi 1925,Williams 1974).Larvae of sev- which they rest. They also soil automobiles,and eral midge speciesalso have been implicated as cover the headlights and windshields, causing agricultural pests.For example,there are several plants traffic accidents. At night, the adults are at- reports of damage to rice seedsand by tracted to light, swarming around indoor and chironomid larvae (Darby 1962,Ishihara 1972, outdoor fixtures. Adults of somesmall-sized spe- Risbec1951); members of the subfamilyOrtho- ciespass through standardscreens on doorsand cladiinae injure roots of Japanesehorseradish windows and thus create nuisanceand economic (Yokogi and Ueno 1971);and Stenochironomus (Nel- problems indoors, such as staining laundry, nelumbusfeeds on floating leavesof lotus walls, ceilings, draperies and other furnishings umbo wcifera) (Tokunaga and Kuroda 1936). as well as causing discomfort for the residents. Adult midgescause a considerableeconomic loss PREDOMINANT NUISANCE SPECIES to the hotel and tourism industry (Ali 1980b). Accumulations of deadmidges and the unsightly There are probably more than 2,500 species spider websin which midgesare trapped require of Chironomidae in North America (Coffman frequent washing and maintenance of proper- and Ferrington 1984).It is estimated that there ties. They clog automobile radiators and air- are 4,000 or more speciesof midges worldwide conditioning wall units and are a problem for (A. Soponis,personal communication). A sum- somepaint, pharmaceuticaland food processing mary of ecological and distributional data on industries where hordes of adults fly into the Chironomidae was given by Coffman and Fer- final products. The dead midges produce an rington (1984). Of the 7 subfamilies of Chiron- unpleasant odor similar to rotting fish. This omidae, speciesmost commonly encounteredin odor persists in damp weather for several days, heavy midge producing urban and suburban even afber the adults have been removed. At habitats are in the genera Chirornmus, Crypto- times, the dead adults accumulate on roads in chironnrnus, Goeldichironomw, Glyptotendipes, such quantities that they make the roads slip- D icrotendipe s, P aralnuterborniella, P olypedilum, pery, causingtraffrc hazards.At the Marco Polo Tanytarsus, Cla.dotanytarsus,Rheotanytarsus, Airport near Venice, Italy, there is a great con- Tokunagayusurika,Cricotopus, Proclad,ius, Coe- cern for the potential of airplanes skidding over latanypus, Tanypus and Pentaneura. SpeciesoI massive accumulations of dead midges on the a few other quantitatively less important genera runways, and also, of economic loss due to the may also occur in some locations. adults flying into delicate equipment (gauges) In general, Chironomus deconts,C. frommeri, mounted on the planes (E. Tsuroplis, personal Dicrotendipes californicus, Cricotopusbicinctus, communication).Midge swarmspose severe nui- C. syluestris,Procladius freemani and a few spe- sanceproblems to passengersand crewsofcargo cies of Tanytarsus are most widely distributed vesselsand other boats moving through the la- in California and are potentially pestiferous (Ali goon of Venice, thus adverselyaffecting human and Mulla 1979b). Specifically, in 1-2 m deep activity in that historically touristic area. man-made lakes, water spreading basins and Adult midges are not vectors of any disease flood control channels in southern California, organism although they are considered to be Tanytarstn, Chironornus and, Procladius are mechanical carriers of some microorganisms most common (Ali and Mulla 1975,1976b; AIi when emerging from polluted waters (Lysenko et al. 1978), while Cricotopuspredominates in 1957,Steinhaus and Brinley 1957).They are, storm drains (Ali and Mulla 1979c,Ali et al. however, associatedwith human allergic reac- 1977).In 2-4 m deeprecreational lakes in Cali- tions such as asthma and rhinitis in Africa fornia, Chironomtts and Procla.dius are most JouRNer,oF rHEAupRrceN Mosqurro CowrRor, AssocrnrroN Vor..7, No. 2 abundantand emergeat nuisancelevels (Ali and sirable and should produce better results. In Mulla 1977b,Mulla et al. 1925,1926). The spe- Iakesand lagoonscovering several thousand ha, cies composition of adult midgesin some south- such as in central Florida or around Venice, ern problem California situations was compiled Italy, midge control by the use of insecticidesas (1968) by Grodhaus and AIi and Mulla (19?9b). Iarvicides is not economically feasible because In Florida, Glyptotendipesparipes, Chirono- of the large volumes of water to be treated. mus crassicaudatusand. C. decorusare the maior Chemical displacement, adverse effects on pest speciesof midges (Ali and Baggs 1982,ili aquatic nontarget organismsand other environ- and Fowler 1985).Beck and Beck (1969) also mental concernsalso severelyrestrict or prevent provided a list of nuisance speciesof chironom- the use of insecticides as larvicides. In such ids in Florida. In Illinois, ihirono*us riparius habitats, an understanding of the ecology and causesannoyance (Polls et al. 19Zb).C. decorus manipulation of the larval environment and was a problem in New York (Jamnback 19b6) the adult behavior,combined with the useof nat- andC.plumosus (Hilsenhoff in Wisconsin 1g5g). ural enemies,may provide somesolution to the There may be severalmore unreportedpestifer- problem. ousspecies of chironomidsin the United States. Physical and cultural: Midge control methods Outside of the United States in recent years, through environmental managementare poorly Cladotanytarsus (Cranston lewisi in Sudan et al. developed,primarily becausea precise under- l98l), Chironomussalinarlus in Italy (Ali et al. standing of the ecologicalbases for midge pro- 1985b),and Tokunagayusurikaakamusi, Chiron- duction in various problem habitats is lacking. omus yoshimatsui and C. plumosus in Japan Among the methods used to reduce larval den- (Tabaru et al. 1987) have been reported to be sities, the mechanical removal of sludgeand egg pestiferous and/or a causeof allergies. massesof chironomidsfrom the sidesof rivers, Identification of larval and adult chironomids and disturbing the riverbeds by dredging and to the specieslevel is somewhat difficult due to mixing the substratematerials (Shimizu 1978) the proper lack of taxonomic keys; however, were ineffective in producing control. In semi- generic identification is feasibleunder most cir- permanent habitats, such as water spreading cumstances.In combination, the keys provided basins, some reductions in midge populations (1969), by Beck and Beck Coffmanand Ferring- may be achieved by rotational flooding and (1984), (1962), ton Darby Mason (1973),Oliver drying of partial areas of breeding sources(An- (1978), et al. Roback (1971), Sublette (1960, derson et al. 1964). However, more frequent (1971) 1964),Sublette and Sublette and Wirth drying, dredging and reflooding of such habitats (1956) and Stone are useful.For taxonomicpur- may be conducive to higher midge productivity poses and other laboratory investigations, some and midge nuisance problems (Ali and Mulla midge speciescan be reared and/or colonizedby 1978a).Increase in depth of sometemporary or usingthe techniquesofBiever (1965,1971). permanent habitats also reduced some midge populations(Ali and Mulla 1976c).In concrete- CONTROL METIIODS lined storm drains, removal of substrate mate- rials by mechanical means,or by natural factors A variety of control methods have been inves- such as rainfall, reduced populations of midge tigatedin the past severaldecades. Most ofthese larvae(Ali et al. 1976b,1977). Proper designing studies were focusedon chemical control. Some of reservoirsand lakes in some situations would work has been conducted on biological control be helpful in keepingmidge populations at lower of this pest through the use of predators. A Ievels (Magy 1968). Information related to nu- number of parasites and pathogens have been trient cycles and availability, and the influence reported from midges, but very few of these of nutrients on primary and secondaryproduc- microbial organisms have been subjected to tivity, which in turn have an impact on the massculturing and inoculation of natural breed- abundance of nuisance chironomids in some ing sources,or studied in a quantitative manner. man-made habitats, is desirable (Johnson and Physical and cultural control methodologiesof Mulla 1984).Understanding the role of macro- chironomids also remain the least explored. phytes as physical barriers or as sourcesof re- In somesituations, satisfactorybut temporary leaseof biologically active chemicalsthat inter- control of chironomidsmay be achievedby em- fere with midge survival and development in ploying physical and cultural, biological or somehabitats is useful for the ecologicalmanip- chemical means, depending upon the nature of ulation of midgeproduction (Johnsonand Mulla the breeding source. Usually, in small habitats 1982b.1983). (<200 ha) one or more control techniques are Exploration of midge control by physical and effective.However, an integrated approachcom- cultural control techniquesis highly desirablein bining the various control methodologiesis de- huge breeding sources,such as the lakes in cen- JUNE MANAGEMENT OF PESTIFEROUS CHIRONOMIDAE 263 tral Florida and the lagoonof Venice,Italy. In Another possibility of cultural control of such situations, knowledgeof the physicochem- midgesis through the understandingand manip- ical environment of the nuisancespecies, i.e., ulation of their adult behavior. For example, the physical and chemical composition of the studies in the laboratory (Ali et al. 1984) and substrate materials and chemistry of the over- field (AIi et al. 1986)in central Florida on the Iying water in relation to the spatial and sea- attraction of G. paripes, C. crassicaudatus,G. sonal abundance and distribution of larvae of holoprasinus,P. halterale and other speciesre- the pest species,may provide a clue to their vealed that among a combination of white (in- ecologicalbasis of production. Their prolifera- candescentand fluorescent), yellow, orange, tion could then be discouragedby manipulating blue, greenand red lamps of the samewattage, the nutrients (pollutants) and/or other factors these specieswere generally attracted the most conducive to their breeding and rapid propaga- to white light (highest intensity) and the least tion. Recently, chemistry of sediments, water to blue, green or red light (lowest intensity). chemistry and midge populations in a central This behavior of adult midges is in contrast to Florida lake, Lake Monroe, were monitored by adult mosquito behavior; a majority of mosqui- AIi (1989).These studies revealedthat larval toes respondto a specific color or wavelength in densities of G. paripes and C. crassicaud,atus the electromagneticspectrum (Ali et al. 1989b), were inversely related with water depth, and while midge speciesrespond more to the quan- that populationsof the former specieswere in- tity (poweror intensity) of light (AIi et al. 1984). verselyassociated with total phosphorus(TP), Such information is of practical significance in Kjeldahl nitrogen (kj-N), organic carbon and controlling midges.Fifty or so speciesof chiron- somemicronutrients while the latter specieswas omids and 3 of Chaoboruswere collectively re- "lakefly distributed irrespective of the concentrations of sponsiblefor the nuisance" at Entebbe, thesechemical parameters. Uganda;this nuisancewas being amelioratedin Thus, environmental requirements of midge 1962 by the use of UV mercury-vapor lamps speciesmay differ from speciesto species.Both faced away from occupied buildings, combined G. paripes and C. crassicaud,atus,however, with window-screening,the elimination of showedsignificant (0.01level) positive correla- hedges in the lakeward side of dwellings, and tions with electrical conductivity, concentra- the planting of hedgeson the Iandward side to tions of chlorophyll o, and the standing crop of direct the flies beyond housesand their gardens Cyanobacteria(:"blue-green algae") and total (M. Laird, personalcommunication). Many hab- phytoplankton. Since larvae of C. crassicaudatus itats producing midges at nuisance Ievels in (Ali 1990)and G. paripes (Provost and Branch Florida, Italy (Venicelagoon) and perhapselse- 1959) feed on phytoplankton, particularly Cy- where are surroundedby a high density of homes anobacteria,and the abundanceofthese species and businessesinterspersed with less densely is directly related to the phytoplankton abun- inhabited areas.If dimmer lights could be used dance, it was concluded that the occurrenceof in the denselyinhabited areasand high intensity high densitiesof C. crassicaudatusand, G. paripes (brighter) lights installed in and around the less was a function of phytoplankton abundancein densely inhabited areas,adult midges would be water. However, many other interrelated biolog- drawn to the latter areaswhere suitable control ical and chemical parameters may also play measurescould be implemented.Along the Iines somerole in the population fluctuations of these of midge adult behavioral studies for control midges.Since Lake Monroe is a part of the St. purpose,information on adult dispersal(AIi and Johns River system, it may be possible to arti- Fowler 1983),patterns of abundance(Ali et al. ficially increasethe water flow through the lake 1983, 1985a)and diel eclosionperiodicity (AIi at times of midge larval abundanceto displace 1980a,Ali and Mulla 1979a,Ferrarese and Cer- phytoplankton populations and, in turn, reduce etti 1989) should be useful in reducing the cost midge densities. Thus, it appears that in some of adulticiding. Applications of insecticides Iarge habitats, physical and cultural control of could be synchronized with the emergenceof midges may be practical through knowledge of adults, thereby reducing the area to be treated the basic ecologyof the nuisancespecies. The and the amount of material needed. ecologyshould be investigated in habitats such In somesituations, relief from adult midgesis as the lagoon of Venice and in other locations achievedby using electrocutor traps. However, becauseeach habitat possessesits own charac- the attraction of huge numbers of adults in most teristics in terms of midge and other inverte- situations cause the traps to malfunction as brate fauna. Information gatheredin one habitat their body fragments stick and completely cover may not be applicable to another with similar the grid in the trap. Intensive researchis pres- problems. ently being conductedto improve the efficiency JouRrulr,oF THEAMERTCAN Mosqurro CourRor. Assocrlrtox VoL. 7, No. 2

of electrocutortraps for midgecontrol (W. Ad- incidenceof diseaseranged from 0.g to g.1Voin kins, personalcommunication). flreldpopulations with no viable adults maturing Binlngical: parasites and pathogens.. Many from the infected larvae. This a$eed-Microsporidia with an biotic control agentsregulate populations of chi - earlier report of Weiser (1963). ronomidsin nature. Viruses,rickettsiae, proto- can play an important role in the regulation of zoans,nematodes and fungi have been reported aquatic insect populations. A good example of in the literature. the potential value of microsporidian infection Among aquatic insects, only chironomid is the annihilation of midgesin B semiperma- midges are reported to be hosts of entomopox- nent ponds 3 wk after initial detection of the viruses (Anthony 1975).Weiser (1969),Hlger diseasedlarvae (Hunter 1968). et al. (1970),Stoltz and Summers(1921), Fed- Most reports of ciliates parasitizing insects erici et al. (1974), Harkrider and Hall (1975) concern the genus Tetrahymena. The system- and Majori et al. (1986)have reportedentomo- atics and parasitism of this genuswas reviewed poxviruses in Camptochironomu,stentans, Chi- by Corliss(1960), who reporteda fatal attack of ronomus luridus, C. attenuatus (a junior syn- T. chironomi and ?. pyriforrnis on C. pluntosus. onym of C. decorus) and C. plumosus, Goel.di- Theseciliates were found in up to lL8% of C. chironomus holoprasinus, C. decorus and C. plumosus larvae in 8 samplesand the incidence salinar ius, respectively. was greaterin larger larvae; 43.2Voofthird instar Entomopoxviruseshave been shown to play a larvae in one sample were parasitized. Bar- significant role in the natural regulation of nui- thelmes (1960)found another species,T. para- sance midge populations (Harkrider and Hall sitica,in C.plumosus. However, no epizooticsof 1978).In laboratorystudies, Harkrider and Hall ciliatescontrolling midge populations have been (1979) demonstratedthe important role of high reportect. midge population density in the precipitation-of A number of nematode parasites of midge an epizootic of entomopoxvirus. However, the larvae have been reported in the literature (e.g., reported larval mortalities of field populations Gotz 1964,Karanukaran 1966,McCaulev 19Zd). of chironomid speciesinfected by poxviruses in Johnson (1963, 1965) reported Octornyornermis different habitats range from <1 to 100% (An- itascensisin C. plum.osusand, Hydromerrnis itos- thony 1975,Huger et al. 1g70,Majori et al. 1986, censisin Glyptotendipeslobiferus in the central Weiser 1948).In addition to the poxviruses,a United States. Parenti (1966) found paramer- cytoplasmicpolyhedrosis virus (CPV) in chiron- mis contorta in C. tentans in France. Poinar omids collected from Florida was detected bv (1964) reported a new nematode, Orthomermis Federiciet al. (1973),and another virus closelv oedobranchus,parasitizing Srnittia sp. larvae in related to iridoviruses was found in C. plumosus England, a new speciesof Gastromernzrsparasi- in Wisconsin (Stoltz et al. 1968). tizing Tanytarsus larvae in California (Poinar Among fungi, the genus Coel,ornomycesis a and Ecke 1967),and another mermithid. I/y- pathogen of chironomids. Rasin (1929) reported dromermis conophaga,in Tanytarsus larvae in Coelomomyceschironomi in midge larvae. Later, California (Poinar 1968). There are several this fungus was also found in C. paraplumosus other reports indicating that many mermithids in Czechoslovakia(Weiser 1g76, Weiser ani have a variety of host chironomids in various V6vra 1964).Weiser and McCauley (1971)dis. parts of the world (Lewis 1.957,McCauley 1gT3, covered 2 Coelomomycesinfections of Chiron- Wtilker 1958, 1961, 1963, 1965; Welch and omidaein Marion Lake, British Columbia.Can- Poinar 1965).Welch and Poinar (196b), "highly Poinar ada,but their C. beirneiis now suspect,' (1981)and Petersen(1985) have discussedthe as a member of this genus and thought to be a role and use of nematodesin the regulation and protozoan (Couch and Bland 198b).The same control of insects of medical importance. authors also reported a new fungal species,Ber- In the USA, a monthly infection mte of Hy- tramia marionensis, parasitizing midge larvae dromermis contorta in C. plumosus ranged from (Weiser and McCauley 7974). 0 to 24.8%throughout the year (Johnson19bb1), The occurrenceof rickettsiae in midgesis rare. while in Germany, natural mermithid infections Richettsiellachironomi in C. decorus(G otz lg7 2) in Tanytarsus midges at certain times of the and a Richettsi.ella-llkeorganism in C. frornmeri year wereas high as l00Vo(Wiilker 1958,1961). (Federiciet al. 1976)have been reported. More recent investigations concerning mermi- The protozoan parasites of midge larvae are represented by microsporidia and ciliophores. Weiser (1961)discovered 16 species of micros- 'Johnson, A. A. poridia in 1955.Life history studieson liy- chironomids. Hilsenhoff and Lovett drornermis contorta (Kohn), parasite (1966) a nematode of found Th.elohania in a chironomid in Chirornmusplun'Losus (L.). Ph.D. thesis,Univ. Illinois. Lake Winnebago, WI. They reported that the Urbana. JUNE MnNe,cuNrnxrop Prsrlppnous Cnlnoxolr.ttone 265 thids of chironomidsare thoseof Chapmanand plication (10 kglha or 2.5ppm) gavethe highest Ecke (1969)in percolationponds in California, Ievel of control (E8%) after 2 wk of treatment. where the incidence of H. conophogoinfection In the golf coursepond, the rate of 3 kg/ha (0.5 in Tanytarsus reached 45% in a spring season. ppm) yielded 30-677oreduction of Chironomini, The authors concludedthat the parasite con- but Tanypodinae midgesremained generally un- trolled the midge populations for nearly 2 years affected. after the ponds were first flooded. Such inci- More recently,Rodcharoen et al. (1991)con- dences,however, are rarely observedin nature. ducted a number of field studies with B.t i. for Two microbial agents, Bacillus thuringiensis midge control in California. In ponds (each30 serovar.israelensis (B.t.i.) and Bacillw sphaeri- m2 at surfaceand 0.3 m deep),Vectobac'"'6A3 cus, have great larvicidal potential against some (aqueoussuspension containing 600 ITU/mg) at Diptera of medical importance (Ali and Nayar ratesof 11.2and 22.4kglha,yieldeda maximum 1986,Ali et al. 1981,1989a; Lacey et al. 1984, of 37 and 57% rcduction, respectively, of C. Mulla et al. 1982,1988). Of the 2 spore-forming decorus, C. fuluipillus and. Paralauterborniella bacteria, different B.t.i. formulations are cur- elarhistus midges during the 2-wk evaluation rently being used as larvicide of mosquitoesand period. In 3 separateman-made lakes (Wood- blackflies in various parts of the world (Kurtak ward Lake, Woodbridge North Lake and Lake et al. 1987,Majori et al. 1987,Merritt et al. 1989' Calabasas),ranging from 8.4 to 21.6 ha at sur- Mulla et al. 1985,World Health Organization face and 1.8 to 2.1 m in depth, different formu- 1982). Bacillus sphaericus,shown to be highly lations of B.t.i. at various rates were evaluated effectiveprimarily against Culer mosquitoes(AIi againstmidges. In WoodwardLake, ABG-6253 and Nayar 1986, Ali et al. 1989a, Mulla et al. (corngrit gtanules containing 200 ITU/mg) was 1988,World Health Organization1985), is pres- evaluatedat rates of 13.5,28 and 56 kg/ha in ently being investigatedand developedfor com- 1.4- to 2-ha separatesections (fingers) of the mercial use in mosquito control programs. The lake. These rates yielded 22, 83 and 9670conttol, potential for the 2 biocides in chironomid con- respectively,of C. decorusmidges at 2 wk post- trol has also been investigated(Ali 1981a,AIi treatment. Speciesof Tanypodinae (Procladius and Majori 1984,Ali and Nayar 1986,Ali et al. rnaculatus and Tanypus grodhausi) remained 1981,1985b; Rodcharoen et al. 1991).In labo- unaffected. In Woodbridge North Lake, a tech- ratory bioassays,the LCgovalues of G. paripes, nical powder(TP) of B.t.i., ABG-6164(contain- C. crassicaudatus,C. decorus and Tanytarsus ing 12,430ITU/mg), was tested at rates of 1.4 midges ranged from 4.56 to 47.02 ppm with and 2.8 kg/ha. Thesetreatments yielded 73 and different wettable powders (WP) and a flowable 877o conftol, respectively,of Chironomus sp. at concentrate (FC) of B.t i., including IPS-78 2-3 wk posttreatment.In Lake Calabasas,Vec- (WP), R-153-78(WP), ABG-6108(WP) and tobac'DTP containing 5,000ITU/mg was eval- SAN-402-WDC (FC), which had potenciesof uated at rates of 2.2, 4.5 and 6.7 kg/ha. These 1,000-3,500 international units of toxicity treatments resulted in a maximum control of 66, (ITU)/mg (AIi et al. 1981).The sameformula- 90 and 100%, respectively, of Chironomus tions of B.t.i. against Aedes aegypti and CuLex midges at 2-3 wk posttreatment. quinquefasciafuslarvae were highly active (LCgo The laboratory and field evaluations of B.t i. : 0.13-0.88ppm), revealing that chironomid have shown that this biocide is effective mostly midges,in general,are relatively less susceptible against Chironomine midges, although rather to B.t.i. than mosquitoes.In other laboratory high rates of treatment (at least 10x or higher studies (Ali and Majori 1984, AIi et al. 1985b), the rates establishedfor mosquito larvicidal ac- Bactimos@(WP), Vectobac@(WP) and Teknar@ tivity) are required to achievesatisfactory larval (FC) containing 1,500-3,500ITU/mg tested control of midges in some situations (Rodchar- against C. salinarius were shown to have LCso oen et al. 1991).The use of such elevatedrates values ranged between 5.07 and 38.26 ppm. of B.t.i. in midge control programsmay be pos- These results were comparableto those of Ali et sible in habitats ranging up to 50 or 100 ha, but al. (1981). would not be economical or practical in large Field tests were conducted in experimental lakes, such as Lake Monroe in Florida or in the ponds (each 24 m2 at surface and 0.5 m deep) Iagoon of Venice, Italy. Thus, there is a need to and in a golf coursepond (1 ha at surfaceand discovernew more toxic strain(s)of this biocide 0.6 m deep) in Florida with a WP formulation to be economically effective against chironomid of B.t.i., ABG-6108,containing 1,000ITU/mg Iarvae. (Ali 1981a).At t,2,3, 4 and 10 kglha,ABG- Studies on B. sphaerlcusagainst chironomids 6108gave 18-88% Iarval reductionsof Chiron- (Ali and Nayar 1986,Sinegre et al. 1990,Rod- omini and Tanytarsini midgesin the experimen- charoenet al. 1991)have shown that this bac- tal ponds. As expected,the highest rate of ap- terium remains ineffective against midge larvae 266 JounNlr,oF THEAunRrclrl Moseurro CoNrRorAssoclarrorl VoL.7,No.2

at mosquito control rates or even at very high Chen 1968,Legner et al. 1975a,Mezger 1962, "Ihe rates of treatment (11.2 and 22.4 ke/ha). Zur 1980).These studieshave shown that chi- LCssvalues of G. paripes and C. crassicaudatus ronomid larvae and pupae form a significant in the Iaboratory were >50 ppm for primary part ofthe diet offish, includingseveral sunfish, powders of strains 1593 and 2362of B. sphaeri- catfish, desertpupfish, young bass,carp, mos- cus (Ali and Nayar 1986).Thus, strains 1b9B quito fish, Tilapia and even gilthead seabream. and 2362 of B. sphoericusknown to be highly Only the carp appears to have been successful toxic to some mosquito larvae (Ali and Nayar in causing appreciable reductions of midges in 1986), do not offer any potential for midge field trials (Bay and Anderson 1965, Mezger control. 1967).Bottom-feeding fish, suchas catfish,may Macroinuertebratepredators.. Many macroin- also consume considerable numbers of midge vertebrates in various phyla are predaceouson larvae,but do not producesignificant reductions midge larvae and pupae in nature. For example, of midge nuisance in situations of large midge there are several reports of leeches(Bay 1964, populations where food supply of fish tends to Bennike 1943,Elliott 1973,Mann 1952),dra- be continuously replaced as it is consumed gonfly nymphs (Prichard 1964), and dytiscid (Hayne and Ball 1956). beetles and. Coelotanypusmidges (Bay 196a) The chironomid component in the diet of fish being predaceouson chironomids. Schuytema inhabiting a man-madereservoir in central Flor- (1977), in his review of biological control of ida was recently studied (A. Ali, unpublished). aquatic nuisances,included predators of chiron- Foregut contents of 14 speciesof fish taken from omids.Bay (1974)reviewed the subjectof midge the reservoir were examined. Of these, 3 species predation by invertebrates and discussed the of sunfish, Lepornis macrochiru,s(bluegill), /,. predator-preyrelationships of aquatic insects. megalntis(longear), and L. microlophus(redear), So far, however,most accountsin the literature and one species of catfish, Ictaluris sp., had concerning midge predators are qualitative lab- consumed appreciable numbers of chironomid oratory or field observationswhere predation by Iarvae and pupae. In the foregut of these 4 certain invertebrates on midgeswas noted. Very species,midge larvae and pupae comprised 42* few of these predators were subjectedto quan- 67% by volume, and 42-78% by wet weight, of titative experimentation against midges. the total food contents. The total number of The flatworm, Dugesia dorotocephala,is the midge larvae and pupae in the foregut of these most studied invertebrate predator of chiron- 10-25 cm long fish ranged from 4 to 45. Thus, omid larvae. Under laboratory and semifield ex- predatory pressureby the use of these fish could perimentalconditions, this planarianwas shown be increasedfor the possiblereduction of midges to be quite effective in reducing midges (Legner in somehabitats in Florida and elsewhere. et al. 1975b).Ali and Mulla (1983)evaluated D. Quantitative evaluations of fish in water dorotocephalaagainst chironomids in experi- spreading basins in the USA have shown that mental pondsduring 3 consecutivesummers. Of carp, Cyprinus carpio, and goldfish, Carassius the different rates (10,25,50 and 100planaria/ aurdtus, were effective in reducing midge popu- m2) used, the rate of 50 planaria/m2 reduced lations for a short time when stocked at 165- midge populations by 32-61% during the 3rd to 550kg of fish/ha (Bay and Anderson196b). Over the 8th wk post-introductionofthe predator.In the long term, however, factors such as pond these evaluations, the highest rate (100 plan- siltation, filamentous algaeand natural enemies aria/m2) did not produce the maximum reduc- tended to maintain larval populations at the tion of midge larvae. This was perhaps because same level as did the 2 fish species.When the the abundance of the flatworm after a certain fish were removed from the basins, midge larval level was checkedand regulatedby higher pred- populations increased only temporarily until ators in the food chain in these ponds. Since other controls interceded. The authors con- mass rearing of D. dorotocephalaseems feasible cluded that carp are less valuable for midge (Tsai and Legner 1977),this predator warrants control in large lakes and temporarily disrupted further developmentfor the biological control of habitats than in smaller sourcesof chironomid midges.Also, D. tigrina should be evaluated as nuisance.Carp have also beenused for the bio- a predator of midge larvae since its production logical control of midge larvae in Japan (Anon- and maintenance of large numbers are possible ymous 1974), but no quantitative data on their (Callahanand Morris 1989). effectivenessare available. It should be under- Predatory fish: There are numerous reports of stood that carp are prolific and aggressivefish. predation by fish on chironomid midges (Bay When introduced for midge control, they could and Anderson 1965, 1966; Ceretti et al. 198?, outcompete the desirable species of fish and Cook 1962,1964; Cook et al. 1964.Guziur 1976. becomea pest, inducing permanent and drastic Kajak et al. 1972,Kimball 1968, Kugler and alterations, similar to those produced by the JUNE 1991 MlNlcnunnt oF PESTIFEROUSCHIRONOMTDAE 267 mosquito ftsh (Garnbusiaaffinis) in pond eco- be partially effective in small (<1-20 ha) and systems(Hurlbert et al. L972).Introduction of closedhabitats. However, for satisfactory midge G. affinis had resulted in marked reduction of control in somesituations, other possibilitiesof zooplankton populations that fed upon phyto- control in the integrated approach would be plankton, thereby changing the water quality, required. Control of midges through the use of as heavy algal blooms resulted due to the ab- fish in large and open habitats, such as Lake senceof zooplankton.The possibility of indis- Monroe, FL, and the lagoon of Venice, Italy, criminate or preferential feeding of the intro- would be relatively less effective becauseof the duced fish on macroinvertebrate predators possibility of fish displacement,due to their free (midgepredators), which are more efficient than movement and migration. the fish in having accessto protective niches Chemical:The chemical control of midges by where midge Iarvaeprevail, may also disrupt the Iarviciding or adulticiding has primarily been trophic structure in the aquatic habitat. How- attempted in the USA and Japan (AIi 1980b, ever, in the presenceof predatory fish, such as Tabaru et al. 1987).A few scatteredand limited bass,the number of carp or other midge-preda- midge control studies (laboratory or field) have tory fish may be regulated,thus diminishing the beenmade in other countries,such as the United undesirableeffects produced by the latter. Kingdom (Edwards et al. 1964),Egypt (Abul- The possible use of mosquito fish for midge Nasr et al. 1970, Brown et al. 1961), France control was studied by Bay and Anderson (Sinegreet al. 1990),Italy (AIi and Majori 1984, (1966).They reportedthat although these fish Ali et al. 1985b)and others. A bibliographyof fed upon chironomid Iarvae and emerging chemical control of chironomidswas provided adults, no reduction in midge populations oc- by Grodhaus(1975). curred even when the predator biomass reached In the past 3-4 decades,the majority of chem- more than 276kg/ha. Cook et al. (1964)studied ical control work on midgesin the USA has been the impact of the fishery upon the midge popu- conductedin Florida (Patterson 1964,1965; Pat- lation of Clear Lake, CA, and found that chiron- terson and von Windeguth 1964a,1964b; Pat- omid larvae and adults comprised the bulk of terson and Wilson 1966,Patterson et al. 1966. the summer diet of mosquito fish, but suggested AIi 1981b,Ali and Chaudhuri 1988,Ali and Lord that these fish feed on chironomid larvae when 1980,Ali and Nayar 1985,1987; Ali and Stanley under food stress,concluding that mosquito fish 1981, AIi et al. 1987), Wisconsin (Hilsenhoff are of little or no value in chironomid midge 1959,1960, 1962) and California (AIi and Mulla control. 1976b,L977a, L977b,1978b; Ali et al. 1978,An- Legnerand Medved(1973) and Murray (1976) derson et al. 1964, 1965; Johnson and Mulla studied the use of exotic fish, such as Tilapia 1980,1981, 1982a; McFarland et al. 1962,Mulla spp. for midge control and found them to be and Darwazeh 1975, Mulla and Khasawinah highly predaceous on midge larvae. However, 1969,Mulla et al. 1971,1973, t974,1975,1976; Tilapia cannot withstand temperatures below Norland and Mulla 1975.Norland et al. 1974. 10-12"C and would die each winter, requiring Pelsueand McFarland 1971.Pelsue et al. 1974). removal of large numbers of dead fish from the Occasionalreports on chironomid control from midge breeding habitat, and their restocking other states,such as New York (Jamnback1954. during summer. Additionally, there is a great 1956), Maryland (Bickley and Ludlam 1968), environmental risk involved with the introduc- Illinois (Polls et al. 1975)and others also exist tion of exotic fishes.They interact and compete in the literature. with native fish and depauperatefish fauna, a Numerous laboratory and field studies on problem of great concern to fish and wildlife midge control were conducted in the past 2-3 biologists and conservation agencies.In several decadesin Japan (Inoue and Mihara 1975, Ka- instances, introduction of mosquito fish into mei et al. 1982, Kudamatsu 1"969,Ohno and Nevada (western United States) had adverse Shimizu 1982,Sato and Yasuno 1979,Tabaru effects on the native fish populations (Deacon 1975,1985a, 1985b, 1985c, 1985d; Tabaru et al. et al. 1964). Mosquito fish generally compete 1978,Tsumuraya et al. 1982a,1982b; Yasuno et effectively and may displace native species of al. 1982.1985). fish by consuming food and occupying their Insecticides against chironomids were first niches (Deaconand Bunnel 1970).These con- evaluated against midge larvae half a century siderations, thus, warrant great caution in ex- ago when Fellton (1940) used pyrethrins and ercising the introduction and stocking of exotic rotenone.These costly botanicals wereused only fishes that offer potential for control of pest for a very short time becauseofthe introduction insects. of organochlorines, orthodichlorobenzene and In general, the biological control of midges trichlorobenzenecompounds, which yielded sat- through the use of midge predatory fish would isfactory control of Chironorntts and,Procla.dius JounNa.r,oF THE AnpnrceN Moseurro CoNrRor, AssocrerroN VoL.7,No.2

midges (Fellton 1941). Subsequently,several to their large-scaleuse in the field. This method other organochlorines,such as DDT, DDD and was used to evaluate the OP insecticideschlor- dieldrin, afforded excellent control of midge lar- pyrifos, temephos, fenthion, malathion, phen- vae (Anderson and Ingram 1960, Anderson et thoate, ethyl parathion and methyl parathion al. 1964,Edwards et al. 1964, Flentje 1945b). against field-collected larvae from various hab- However,the problemof toxicity of organochlo- itats in southern California (AIi and Mulla rines to fish and other invertebrates in the food 1976b, 1977b, 1978b, 1980; Pelsue and Mc- chain (Hunt and Bischoff 1960),and the devel- Farland 1971). These studies showed that dif- opment of resistancein midge larvae (Lieux and ferent midge species manifested different de- Mulrennan 1956),diverted the focus of midge greesof susceptibility to the compoundstested. control to the use of organophosphate(OP) in- For example, Iarval populations of C. decorus secticides.Several of these compounds were and Tanytarsu.sspp. drawn from the Santa Ana evaluatedby Hilsenhoff (1959),who reported River spreadinggrounds were highly susceptible dichlorvos, trichlorfon, EPN, fenthion, mala- to chlorpyrifos and temephos (LCgo= 1.5 and thion and phosdrin to be highly toxic to C. 4.6 ppb, and 2.0 and 4.6 ppb, respectively),but plurnosus larvae. Granular malathion was con- Cricotopusspp. in the samehabitat weretolerant sidereda suitableinsecticide to control this spe- to all the OPs tested(LCeo : 0.L2-2.1ppm)(AIi cies (Hilsenhoff 1960,1962). and Mulla 1976b).Chlorpyrifos, temephos and In the early 1950sand 1960sin Florida, more phenthoate were also very effective againstChi- than 100chemical compoundswere evaluatedin ronon'utsutahensistaken from Silver Lakes with the laboratory and/or field as potential larvi- LCsovalues of 7.8,4.7 and 8.1 ppb, respectively. cides of G. paripes. Benzenehexachloride and This species,however, was tolerant to methyl the organophosphorusinsecticide EPN were the parathion and fenthion (LCr' : 0.47 and 1.16 most extensively used for midge control, but ppm, respectively) (Ali and Mulla 1977b).Chi- their use was generally discontinued by 1955, ronomus decoruswas most susceptibleto chlor- due to the development of resistance by midge pyrifos among all the OPs tested,but showed5- larvae(Patterson 1964,1965). Control measures 74x tolerance to chlorpyrifos, temephos and had to be substituted by the of fenthion use and malathion when comparedwith the susceptibil- temephos,and by adulticiding with thermal aer- ity of C. utahensisto these compounds.Larvae osol fogs (Patterson and von Windeguth 1964b, of Procladius spp. in Silver Lakes were the least Patterson et al. 1966).Fenthion as 1% granular susceptibleto temephos and the most to chlor- (G) applied at 0.22-0.28 kg Allha controlled G. pyrifos and phenthoate, while Cricotopus spp. paripes for 3-10 wk, dependingupon the time of were most susceptible to phenthoate and least the year; the duration of control was minimum to methyl parathion (Ali and Mulla 1977b). in summer (Patterson and Wilson 1966).Te- Against Iarval populations from another resi- mephos{l% G) appliedat 0.06kg Allha yielded excellentconfiol of.G. paripes. In the last decade, dential-recreational lake in southern California (Ali several laboratory and semifield (experimental et al. 1978),chlorpyrifos was highly toxic to (LCgo:3.1 ponds)studies on the evaluationoforganophos- Tanytarsusspp. ppb) andC. decorus = phates,pyrethroids and insect growth regulators (LCs6 1.4 ppb). Temephosand fenthion were (IGRs) (including chitin synthesis inhibitors also considerablyactive against Tanytarsus spp. : and juvenile hormone analogs) have been con- (LCeg 7.2 and,8.8 ppb, respectively),but ducted (Ali 1981b,Ali and Chaudhuri 1988, AIi against P. freemarui,temephos was totally inef- and Lord 1980, Ali and Nayar 1987, Ali and fective, as indicated by the LCgo value of >5 Stanley1981, Ali et al. 1987).The activity of an ppm. In the same study, fenthion showedpoor avermectin insecticide,abamectin, has also been activity against C. decorusas well as against P. tested in the laboratory against C. crassicauda- freernani, and malathion was also only slightly tus and G. paripes (Ali and Nayar 1985). How- toxic to P. freem,ani.In contrast to the midge ever, these studies remain of academicinterest susceptibility results from the Santa Ana River because no large-scale field trials using OPs, spreading grounds and the residential-recrea- pyrethroids or IGRs in actual midge problem tional lakes, chironomid fauna (mostly C. deco- habitats have been conducted in Florida in the rus, D. californicus and,Cricotoprrs spp.) inhab- past 2 decades. iting flood control channels, such as the Coyote Laboratory eualuations: Organophosph.orus Creek system draining Orange and Los Angeles lnruici.d.es.Mulla and Khasawinah (1969) devel- counties,CA (Ali et al. 1976a),were resistant to oped a useful laboratory method for larvicide most OPs, including chlorpyrifos, temephos, screeningand establishingsusceptibility levels fenthion and malathion (LCgo : 0.16-42.14 of field-collected or laboratory-colonized midge ppm) (AIi and Mulla 1980). Similar findings populations to the candidate compounds prior were reportedby Pelsueand McFarland (1971) JUNE1991 MeNncott,tnnr oF PESTTFER0USCHTRONoMIDAE 269 studying the midge problem earlier in the same habiting Village Grove Lake, CA, all 4 pyreth- channelsystem. roids were extremelytoxic (LCso: 0.025-0.058 More recently in Florida, chlorpyrifos, teme- ppb) (Ali et al. 1978).Decamethrin and its an- phos, fenthion and malathion were evaluated aloguewere also highly active against C. decorus against field-collected larvae of G. paripes and and P. freemani (LCeo: 0.76 and 0.5 ppb, and C. crassicaudatus from Lake Monroe, and 0.11and 0.36ppb, respectively).The pyrethroid against C. decoruscollected from 2 sewageoxi- FMC 35171 was also very effective against C. dation ponds in Sanford, FL (AIi 1981b). In decorus and P. freemani inhabiting Village these evaluations,G. paripes exhibited the most Grove Lake, but Pydrin was moderately active susceptibilityto malathion (LCso: 0.0079ppm) against C. decorus(LCs6 : 17 ppb) and,P. free- and the least to temephos(LCr' : 0.022ppm); mani (LCso= 47 ppb). Midge fauna (mostly C. C. crassicaudofuswas generallytolerant to these deconn, D. californicus, Cricotopusspp. and ?. OP insecticides with LCeevalues ranging from grodhausi) of flood control channels,such as the 0.14ppm (chlorpyrifos)to 0.48ppm (fenthion). Coyote Creek system and San Jose Creek, CA, Chironomusdecorus was also relatively resistant were also highly susceptibleto decamethrin and to thesecompounds (LCe. : 0.1-0.38ppm). its analogue, FMC-45497 (LCro : 0.13-12.0 In Italy, the laboratory activity of chlorpyri- ppb), but thesemidges showed lesser sensitivity fos, temephos,malathion and fenthion was de- to Pydrin (LCs1 : 33.0-420.0ppb) (Ali and termined for field-collected C. salinarius larvae Mulla 1980). from the saltwater lakes of Orbetello (Ali and In Florida, several new experimental pyreth- Majori 1984)and from the lagoon of Venice (Ali roids (e.s., FMC-30980, FMC-33297, FMC- et al. 1985b).Among the OPs used,temephos 35171. FMC-45497. FMC-45499 and FMC- was the most active [(LCno: 0.021ppm (lakes) 52703)were evaluated in the laboratory against and 0.027ppm (lagoon)1,but the rangeof activ- field-collected G. paripes, C. crassicauddttl.sand ity of all the OPs tested was narrow (LCro : C. decoruslarvae (AIi 1981b).These pyrethroids 0.021-0.091ppm), indicating that C. salinarius showeda very high level of activity against the populations in the Iakes and in the lagoon were 3 midge species,with LCgovalues ranging from susceptibleto these compounds. 0.26 to 13 ppb. Of the 3 species,G. paripes was From Japan, Kudamatsu (1969) had reported the most susceptible(LCeo : 1.3-9.8ppb), fol- on the Iarvicidal activity of someOP insecticides Iowed by C. decorus (LCno : 2.1-13.0 ppb). against field-collectedC. plumosus. Sato and Among the pyrethroidstested, FMC-45499 and Yasuno (1979) evaluated several insecticides FMC-52703were the 2 most toxic to the midge against larvae of C. yoshirnatsui, Polypedilum larvae. nubifer, Paratanytarsus partherngeneticus, Evaluations of the pyrethroids cypermethrin, Psectrocladius sp. and Procladius sp. These permethrin and deltamethrin against C. salinar- midges, except fot Proclndius sp., were suscep- ius larvae collected from the lagoon of Venice, tible to temephoswith LCsovalues ranging from Italy, indicated the superior activity of cyper- 0.0003to 0.015ppm. Tabaru (1985a)studied the methrin (LCeo- 0.34ppb) and permethrin (LCgo Iaboratory activity of chlorphoxim, chlorpyrifos, : 0.3 ppb) against this saltwater midge. Delta- chlorpyrifos methyl and temephos against C. methrin was 13-14x less toxic to C. salinarius yoshimatsui. The same author also developed (LCso : 4.3 ppb) when compared with cyper- and describeda unique criterion for determining methrin and permethrin (Ali et al. 1985b). midge larval mortality by observing the tube- Although most pyrethroids have proven to be building inability of intoxicated larvae provided far superior to OP compoundsin activity against with 0.1-mmglass beads. chironomid larvae, the pyrethroids at mosquito Pyrethroids: Several pyrethroids have been and midge larvicidal rates have a relatively low evaluatedin the laboratory against midge larvae index of safety to nontarget invertebrates and drawn from different habitats in California (AIi frsh (Mulla et al. 1978a,1978b). Therefore, the and Mulla 1978b,1980; Ali et al. 1978),Florida field useof pyrethroids as midge larvicideswould (Ali 1981b)and Venice,Italy (Ali et al. 1985b). be limited to midge problem habitats such as Evaluations made in California have shown that sewageponds and wastewater channels where decamethrin(FMC-45498) and its chloro ana- nontarget invertebrates and fish would be of logue FMC-45497 were highly active against C. minimal or no concern. utahensis, P. freemani and P. sublettei lawae Insect growth regulators:With the advent of drawn from Silver Lakes, with LCgovalues rang- insect juvenile hormone analogue and chitin ing from 0.13 to 0.77 ppb. Other pyrethroids, synthesis inhibitory insect growth regulators FMC-35171and Pydrinu(SD-43775), were rel- (IGRs) such as methoprene and diflubenzuron, atively less active against these species(Ali and respectively,additional materials for midge con- Mulla 1978b). Against Tanytarsus midges in- trol have become available. Mulla et al. (1974) 270 JounNer,oF THEArupRrclN Moseurro CoNrnol AssocrerroN VoL.7,No.2

evaluated several juvenile hormone analogue abamectin,and 1.82 ppb, diflubenzuron) (AIi IGRs, Altosido (ZR-515 or methoprene), R- and Nayar 1985). 20458,RO-20-3600 and RO-8-5497against OP- In Japan, the IGRs methopreneand difluben- resistant and OP-susceptiblepopulation s of Chi- zuronwere tested againstC. yoshimatsui (Kamei ronorn.r,ssp. larvae and found ZR-515 to be the et al. 1982,Tabaru 1985d).Both IGRs proved most effective.The same IGR at 0.05 ppm in- highly effective at concentrations of <0.001 ducedcomplete inhibition of adult emergencein ppm, but diflubenzuron showedsuperior activity Chironomus stigmaterus and ?. grodhausi col- over methoprene (Tabaru 1985d). Currently, lected from sewageoxidation ponds and exposed theseIGRs are being evaluatedin the laboratory in the laboratory. Ali and Lord (1980) described in Italy, against field-collectedC. salinarius from a laboratory bioassaytechnique for these IGRs the Venicelagoon (S. Della Sala,personal com- (having delayed effects) against midges, and munication). evaluated the chitin synthesis inhibitors diflu- It is obvious from the laboratory studies that benzuron,Bay SIR-8514and Stauffer MV-6?8, the levels of susceptibility of various midge spe- and the JHA Stauffer R-20458 against 2 nui- cies or generato different insecticidesvary con- sance midge speciesof Florida. In this study, siderably. Even the same species in different diflubenzuron and SIR-8514 caused 90Vo mor- geographicallocations may show different levels tality of C. decorusand G. paripes at 4-22 ppb, of susceptibility to a chemical. The existing var- the LCeo of MV-678 for the 2 species ranged iation of speciescomposition between habitats from 50 to 69 ppb, and R-20458 was the least further complicates the problem. Thus, each active with LCe6values of 0.24-03 ppm. In other habitat requires an independent approach for laboratory studies in Florida, several new ben- the chemical control of midges. zoylphenylureaIGRs (similar to diflubenzuron) FieLdstudies: Adult controL In the 1950sand were tested for activity against G. paripes and, 1960s,adulticiding was the principal means of C. decorus(Ali and Stanley 1981),and G.ponpes midge control in Florida. Malathion and mala- and C. tassicaudntus (AIi and Nayar 1987,Ali thion-Lethane or naled were used as thermal et al. 1987). The studies of Ali and Stanlev aerosol fogs. Application of these materials was (1981) revealed that the IGR UC-62644 was made from trucks, boats and airplanes. Low slightly more active than diflubenzuron against volume aerial sprays of malathion at 0.14-0.27 G. paripes and C. decorus (LCgovalues of 3.1 kg AI/ha were very effective. At the higher rate, ppb, G. paripes, and 5.7 ppb, C. decoruts)."Ihe malathion controlled G. paripes within 3 h and the control (Patterson respective LCee values with diflubenzuron for lasted for 4 days et al. 1966). Although these specieswere 4.1 and 6.0 ppb. More re- midge adulticiding proved ef- fective, fogginghas its limitations cently, another IGR, UC-84572, was shown to for controlling these insects.Presently, be evenmore toxic in the laboratory to G. paripes no specificinsecticide is registered (LCso: 0.58 ppb) and C. crossicau.datus(LCao : by the United States Environmen- tal Protection Agency for 1.99ppb) than diflubenzuronor UC-62644(Ali adulticiding midges. However, someOP compounds,pyrethroids and Nayar 1987).Four other benzoylphenylurea and other insecticides labeled for adult mosquito IGRs,UC-751 18, UC-7515 0, IJ C-787 2L and UC- control in the USA (Rathburn 1988) probabty 76724, showed an LCgo range of 4.b-2b.8 ppb reducesome adult midge populations when used against C. crassicaudaf,usand 3.1-34.2 ppb by mosquito control agenciesfor the control of against G.paripes. Among these,IJ C -7 67 2 4, was adult mosquitoesin some situations. Rathburn the most active against G. paripes (LCeo= 3.1 (1988) provided comprehensiveinformation on ppb) as well as C. crassicau.datus(LCro : 4.5 label recommendationsof 16-20 insecticidesfor ppb) (Ali et al. 1987). use as ultralow volume (ULV), low volume In addition to the IGRs, Ali and Nayar (19gb) sprays,ground applications, thermal aerosolsin have evaluated the laboratory activity of an ground applications and mists in ground appli- avermectin microbial pesticide, abamectin, cations in adult mosquito control programs.The against field-collected.C. crassicau.datusand G. label requirements for droplet size of ULV and paripes larvae. Since avermectins exhibit de- nonthermal aerosolsfor adult mosquito control layed toxicological (Wright effects 1984), the were also provided. Becauseof the rapidly es- activity of abamectin was comparedwith that of calating problem of midge nuisancein the USA, diflubenzuron, tested simultaneouslvas a stand- federal and/or state registration of some insec- ard. A comparisonof the LCsovalues revealed ticides as midge adulticides is needed. that abamectin was slightly superior in activity Insecticides as midge adulticides are used on to diflubenzuron against C. crassicau.d.atus(LCso a very limited basis in Japan (Y. Tabaru, per- = 1.63 ppb, abamectin, and 1.94 ppb, difluben- sonal communication). However, in Italy, aerial zuron) as well as G. paripes (LCsg : 1.b2 ppb, applications of deltamethrin and malathion are .,n1 JUNE 1991 MeNecrnanlr oF Ppsurrnous CHIRONoMIDAE the only means of control of adult C. salinarius (mostlyProcladius spp.). Temephos, in granular in and around Venice (F. D'Andrea, personal formulations, is the sole insecticideregistered communication). by the United StatesEnvironmental Protection Larual control: Organophosphoruslaruicides. Agency for use as a larvicide against nuisance A number of OP insecticides in different for- midges,and only in standing water situations. mulations were evaluatedin severalresidential- Among other OPs, fenthion at 0.56 kg AI/ha recreational lakes and in the Santa Ana River provided satisfactory midge control for >7 wk spreadingsystem in California by Ali and Mulla in Lake Calabasas,and for 4 wk in Spring Valley (1976b,t977a,1977b, 1978b), and Mulla et al. Lake, but remained ineffective in Westlake at (1971,1973, 1975). Chlorpyrifos at ratesranging 0.56 kg Allha (Mulla et al. 1971,1975). Mala- from 0.11to 0.28kg AI/ha gaveexcellent control thion and phenthoateapplied at 0.56 kg Allha, of tanypodine and chironomine midges in Lake yielded good control of midges for 2-3 wk in Calabasasand Westlake (Mulla et al. 1971, Spring Valley Lake; methyl parathion at the 1973),Spring Valley Lake (Mulla et al. 1975) same rate of application produced marginal and Silver Lakes (Ali and Mulla 1977b).The midgecontrol (Mulla et al. 1975). duration of control varied from 1 to 5 months, In Japan, in outdoor model streams,temephos dependingupon the rate oftreatment and nature and chlorphoxim applied at 2 and 5 ppm, re- of the habitat. In 4-5 m deep Spring Valley spectively, caused drastic larval reductions of Lake, when applied at 0.28 kg AI/ha, control Thienemanniella rnajuscula, P aratrichocladius lastedfor over 1 month (Mulla et al. 1975);while rufiuentris and Chironomus flauiplurnus, but in 1-2 m deep Lake Calabasas,chlorpyrifos at these speciesrecovered within 2-3 wk posttreat- 0.22k5 l\I/haprovided midge control for at least ment (Yasuno et al. 1985).In wastewater,te- 4 months (Mulla et al. 1971). The granular mephos has been successfully used at 2 ppm formulation gavebetter (magrritude)and longer- maintained for 20 min in the gutters to control Iasting control than the emulsifiable concen- C. yoshimatsui (Inoue and Mihara 1975).The trate formulation (Mulla et al. 1971, 1975). same rate of temephos and chlorpyrifos methyl Chlorpyrifos was also reported to provide satis- maintained for 30 min in the gutters, disinfect- factory control of C. raparius in sewagechannels ant tanks and effluent discharge channels of in Chicago,IL (Polls et al. 1975). sewagetreatment plants gave excellent control Field evaluations of temephos indicated that of C.yoshimatsui (Tabaru 1985b). Tabaru (1975) this OP insecticide was effective against some and Tabaru et al. (1978) reported satisfactory midge species in residential-recreational Iakes control of C. yoshim.atsuifor 3 wk in polluted and other midge habitats in California, but rivers by using temephosat rates of 0.69-1 ppm yielded control for shorter durations than chlor- maintained for 60 min; the insecticide was car- pyrifos, even though the rates of application ried up to 3,000 m downstream from the appli- were much higher than those employed for cation site. Chironomusyoshimatsui in another chlorpyrifos. In water percolation basins, teme- river was successfullycontrolled at rates of 0.9- phos at 0.27-0.38kg AI/ha gavea maximum of 2.0 ppm of temephos maintained for 60 min 78VoconftoI of midges (mixture of Tanytarsus, (Ohno and Shimizu 1982).In other studies,te- Chironomus and Procladiu.s)for 1 wk posttreat- mephosapplied at rates of 0.05-1 ppm provided ment (Johnsonand Mulla 1980).At higherrates excellent control of Polypedilum nubifer, Crico- (0.56-0.84 kg Allha) temephos controlled topusbicinctus, Chironomus kiiensis and Chiron- midgesfor 4-5 wk in Lake Calabasasand Spring omus tainanr"rsinhabiting eel culturing ponds Valley Lake (Mulla et al. 1971,1975), while at (Ohkura and Tabaru 1975,Yasuno et al. 1982). lower rates (0.17-0.28ke AI/ha) in the Santa Overall, the field studies on OP insecticides Ana River basinand in Silver Lakes,it produced against midges in the USA and Japan have similar results (Ali and Mulla 1976b, 1977b). indicated that chlorpyrifos, chlorpyrifos methyl, Later treatments of Silver Lakes with temephos temephos,chlorphoxim and a few other OP com- at 0.28 kg AI/ha producedcomplete control of pounds were effective against most nuisance Tanytarsus spp. for 2 wk, but Procladius spp. speciesof midges, suppressingthe Iarval popu- and C. decorus remained unaffected. Even lations for 2-b wk or longer at application rates higher rates of temephos(0.33 and 0.56 kg AI/ below 0.56kg AI/ha (USA) and <1-5 ppm (Ja- ha) failed to produce satisfactory control of C pan). Thesestudies were not intendedto eradi- decorusandProcladius spp. in the lake (Johnson cate midge larvae, but were implemented to re- and Mulla 1981).In Westlake, CA, temephos duce and maintain midge populations below the was also not effective at 0.56 kg AI/ha (Mulla levels at which they pose pest problems.Also, et al. 1971).Generally, temephos was effective the repeated and prolonged use of insecticides against Chironomini in most situations, but may result in buildup of resistance in midge causedonly slight or no mortality in Tanypodini Iarvae, as occurred in Florida due to the pro- 272 JouRrnl oFTHE AunRrclrl Moseurro CoNrRor,AssocrlrloN VoL.7, No. 2 longeduse of EPNand BHC (Lieux and Mul- fornia. Theseponds rangedfrom 0.25to 2.5 ha rennan1956), In somestorm drains and flood in surfacearea and <1 to 2.5m in depth.The control channels in California. most OPs. in- WP, appliedat 0.11and 0.28kg Allha, inhibited cludingchlorpyrifos and temephos,have become adult emergenceof Tanytarsus,Chironomlrs and ineffective against midge larvae even at 1.1 kg Procladius midges for 2 wk, while the granular AI/ha rate of treatment (Pelsueand McFarland formulation at the same rates effectively sup- 1971).In the Chicago area,C. raparius has de- pressedadult eclosionof thesechironomids for veloped resistance to chlorpyrifos due to the up to 4 wk after treatment. The duration of repeateduse of this OP insecticide (I. Polls, control resulting from the lower rate of treat- personalcommunication). In Silver Lakes, CA, ment of eachformulation was almost the same a considerable decline in the effectiveness of as producedby the higher rate. chlorpyrifos and temephoswas noted after re- Under semifieldconditions in shallowexper- peateduse ofthese compoundsagainst C. utah- imental ponds in Florida, a 257oWP and a l% ensis, C. decorus,P. freemani and P. sublettei granularformulation of SIR-8514at 56 and 112 (AIi and Mulla 1978b).Resistance levels in these g Al/ha gave excellent overall control of Tany- speciesto someother OPs not usedin the field forsus spp., G. holoprasinrzsand C. decorus also increased,indicating the phenomenon of midgesfor ca. 3 wk. Diflubenzuron25 WP at 28 cross-resistancewithin the OP group. and 56 g AI/ha was slightly more effective than The frequent and extensive use of temephos, SIR-8514and far more than MV-678 appliedat and to an extent fenthion, has causedthe devel- comparablerates (Ali and Lord 1980). These opment of resistance in C. yoshimotsui in the authors also showedthat SIR-8514at 70 g AII Kanda River, Tokyo (Ohnoand Okamoto1980). ha completely suppressedadult emergenceof Tabaru (1985c)has also indicateda widespread midges in a sewagepond for at least 10 days acquiredresistance to fenthion in C. yoshimatsui after treatment. In another study in the same collectedfrom 10 different rivers in Japan. How- ponds,a 25 WP formulationof the benzoylphen- ever, larvae from all of these rivers were suscep- ylurea IGR, UC-62644, was tested against tible to chlorpyrifos methyl, and temephos was midges at 25, 50 and 100 e Al/ha (Ali and still considered to be economically effective Stanley 1981). All 3 treatment rates produced against C. yoshirnatsuiin about 50% ofthe hab- excellent control of midges for more than 4 wk. itats exposedto the OP insecticide. Even the lowest rate (25 e Al/ha) induced 94- Insect growth regulators: Pioneering field 99% inhibition of midge emergenceduring the 4 studies on the use of IGRs for midge control are wk of the evaluation period. The WP of UC- thoseof Mulla and Darwazeh(1975) and Mulla 62644was also applied at 100 g AI/ha in a golf et al. (L974,1976)who reportedon the activity course pond in Florida, and gave good control of methoprene and diflubenzuron against (53-98%) of the predominant midge species, midges. These two IGRs, in different formula- Chironomuscarus,in the pondsduring the 4 wk tions, were evaluated in California in residen- ofevaluation (AIi and Stanley 1981).Less than tial-recreationallakes (Ali and Mulla 1977b,AIi 6 years ago another benzoylphenylurea IGR, et al. 1978,Mulla et aL 1974,1975, 1976), and UC-84572,became available for testing against in the Santa Ana River basin (Ali and Mulla midges.A 10 EC formulation of this IGR was 1977a).In these studies, methoprene at 0.28 kg evaluated at 1, 5 and 10 ppb AI in the experi- Allha controlled midgesfor 1-2 wk by inhibiting mental ponds in Florida. Diflubenzuron(Dimi- adult emergence(Mulla et aI. L974,1976),while lin 25 WP) at 10 ppb AI was simultaneously diflubenzuron at 0.11-0.28 kg AI/ha induced tested as a standard in ponds becauseof its large midge control for 4-8 wk at the highest rate of data base. Emergence of adult C. decorus, C. treatment (Mulla et al. 1976).In one study in stigmaterus, G. holoprasinus and Tanytarsini residential-recreational lakes in California, di- was inhibited by UC-84572as well as difluben- flubenzuron at 0.11 and 0.28 kg AI/ha com- zuron (Ali and Chaudhuri 1988).Even at 1 ppb, pletely suppressedemergence of Tanytarsus and UC-84572caused a maximum of g0% inhibition Procladius midges for 2 wk posttreatment, but of emergence of. C. decorus, 66Vo each of C. was not as effective against C. decorus(Johnson stigmaterus and G. holoprasinus, and 53% of and Mulla 1981).The samestudy indicatedthat Tanytarsini, 2 days after treatment. However, SIR-8514 applied at the same rates of difluben- the overall reduction of total adult midges at 1 zuron gave similar results. The authors sug- ppb ranged from 0 to 67% during the 28 days of gestedthat higher rates of application of the two posttreatment evaluation.The rate of 5 ppb gave IGRs may produce satisfactory control of C. completecontrol of G. holoprasinus,a maximum decorusin the lakes.Johnson and Mulla (1982a) 99% reductionof C. decorusand94% reduction evaluated2 formulations (25 WP and 0.5% G) each of C. stigmaterusand Tanytarsini, with an of SIR-8514in ponds on a golf coursein Cali- overall 96Voconftol of total chironomids. At 10 JUNE 1991 MANAGEMENT or PosrlrgRous CHIRoNoMIDAE ppb, UC-84572 causedcomplete inhibition of The IGRs, diflubenzuron and methoprene, adult emergencewithin 2 days posttreatment, havebeen used in Japanfor controlling C. yosh- Iasting for 2 wk for C. stigmaterus, l wk for C. imatsuL Treatments of 2 rivers with the former decorusand <1 wk for G. holoprasintzsand Tan- IGR at 1 ppm maintained for 60 min resulted in ytarsini. Diflubenzuron at 10 ppb also induced excellent control of C. yoshirnotsui for 3 wk. complete inhibition of adult midge emergence, Methoprene at the same dosageproved less ef- but it lasted for (1 wk for all midge species fective than diflubenzuron in the same river except for C. stigmatferus,which was controlled (Tabaru 1985d). In the gutters and discharge for X wk. A comparisonof the activity of UC- channels of sewagetreatment plants, metho- 84572with that of diflubenzuron applied at the prenewas applied at the ratesof 0.13and 4 ppm, samerate, 10 ppb, revealedthat UC-84572gen- but was effective against C. yoshimatsui only at erally producedslightly longer lasting control of the higher rate (Tsumurayaet al. 1982b). C. decorus,C. stigmaterus and G. holoprasinus The laboratory and field studies on IGRs than diflubenzuron. Emergenceof Tanytarsini, against midges have shown that many of these however,remained suppressed for longer periods compounds are highly effective against most of time in the ponds that were treated with chironomid species.These compounds are dif- diflubenzuron. ferent from insecticides.such as OP larvicides, In 1990, four formulations, liquid (Altosid in that they inhibit larval or pupal development pop- Liquid Larvicide or A.L.L.), granular (SAN 810 to the adult stage without reducing larval I 1.3 GR), Altosid pellet and Altosid XR (ex- ulations to the extent and magnitude of some tended residual) briquet of the juvenile hormone OP insecticides,such as chlorpyrifosand teme- (Ali Therefore, analogue IGR methoprene were evaluated for phos and Mulla I977a, t977b). of a decimating efficacy against midges including C. decorus,C. these compoundsmay have Iess important component of the food stigmaterus, G. holoprasinus,Polypedilun'L spp. effect on an IGRs also offer a goodpotential as and Tanytarsini in experimental ponds (each chain. The tools for control of midge species pond 24 m2 containing 0.5 m deep water) in additional resistant to OP insecticides. It has been docu- Florida (A. Ali, unpublished). In this study, mented that several of these IGRs, as well as A.L.L. at 2 rates 0.293 and 5.86 liters/ha, Bratr- OP larvicides, may have temporary or chronic ules at 13.0 kg/ha, pellets at 5.6 kg/ha and effects on nontarget aquatic biota coexisting briquets at the rate of 3/pond were each applied with midgelarvae (Ali and Mulla 1978c,1978d). to 3 separateponds. Three ponds were left un- Mulla et al. (1979)provided an excellentreview as controls.The A.L.L., granular,pellet treated of some 200 publishedpapers coveringthe ef- contained5.0, 1.3,4.0 and briquet formulations fectsofpredators, biocides, insecticides, and in- (S)-methropene, This and t.8% of respectively. sectjuvenile hormoneanalogue and chitin syn- study indicated that A.L.L. at 0.293 liters/ha thesis inhibitor growth regulators on nontarget remained ineffective, but at 5.86 liters/ha, it biota associatedwith a variety of mosquito hab- reduced emergenceof midges by 74-99% for 2 itats. However, the severe nuisance and eco- wk posttreatment. Midge emergencereturned to nomic problems posedby adult midgesand their pretreatment or higher levels in the 3rd wk after recently discoveredassociation with problems of treatment. The granular formulation reduced allergy in humans, warrant availability of new emergenceof midges ftom 6l-87% in the 2 wk tools, such as diflubenzuron and methoprene after treatment. The effectivenessof the gran- (particularly the pellet formulation), for midge ular formulation was totally lost in the 4th wk control in selectedhabitats. These IGRs should posttreatment. The pellet and the briquet for- be useful especially in polluted habitats where mulations produced greater control of midges impact on nontargetorganisms and the ecolog- for a longer duration as comparedwith the liquid ical balance of the habitat would be of minimal and the granular formulations. The pellet for- concern. In some situations, only partial areas mulation gave a maximum of 98% control at 3 of a habitat that support heavy populations of days after treatment, with the level of contro. larval midges need to be treated (Ali and Mulla gradually declining and fluctuating between 64 L977b). This practice would not only reduce and 90% for the 1-7 wk posttreatment. The some midge nuisance, but would also help in briquet formulation gave 66-96% control of quicker restoration of the lost nontarget inver- midges during 35 days posttreatment, with tebrates from the untreated areas. The toxic emergenceof adult midgesreducingby 98% after effects of the chemical used in these habitats 7 daysposttreatment. Generally, the pellet for- would also diminish soonerdue to dilution. mulation provided control equal or better than Presently, diflubenzuron has a state registra- the XR briquets with almost 1/4th the active tion (24c)for use againstmidges by the Califor- ingredient. nia Department of Food and Agriculture. Such JouRNu oFTHE Altnnrclu Moseurro Cournol Assocr.qtrorl VoL.7, No.2

a registration of diflubenzuronshould also be omid larvae, but most pyrethroids at mosquito consideredin other states. Also, methoprene and midge larvicidal rates would have a rela- warrants a similar registration. tively low index of safety to nontarget aquatic invertebratesand fish. SUMMARY The IGRs, methoprene,diflubenzuron and severalbenzoylphenylurea compounds (similar In many parts of the world, water bodies in to diflubenzuron), have shown superior activity urban and suburban areas exposedto intensive againsta variety of midge speciesin Japan and human use have becomeincreasingly eutrophic the USA. Somespecies exhibited an LCgovalue and favorable for the profuse breedingof chiion- <1 ppb to experimental benzoylphenylureas, omid midges. Some of these habitats support such as UC-84572.In the field, methoprene, larval densitiesin excessof 40,000/m,,resulting diflubenzuron,Bay SIR-8514and severalother in massiveemergences of adult midgesthat pose benzoylphenylureaswere highly effective, yield- a variety of nuisance,economic and occasionallv ing midge control for severalweeks at rates (0.8 medical problems for the nearby residents.In kg AI/ha. A new pellet formulation of metho- the past 2-3 decades,numerous habitats sup- preneat 0.22kg AI/ha suppressedemergence of porting primarily Chironomini speciesin the adult midges by 64-98% in experimental ponds USA, Italy and Japan have been the focus of for 7 wk posttreatment. Generally, diflubenzu- control studies. ron showed superior activity over methoprene A variety of chironomid control methods have in severalfield studies.The 2 IGRs are excellent been investigated in the past 2-3 decades,with candidates for controlling midges, particularly a majority dealing with chemical control. A the OP-resistantspecies, and warrant registra- number of parasites and pathogens,such as vi- tion in the USA. Diflubenzuron and methoprene ruses, rickettsiae, protozoans, nematodes and are presently being used in Japan for midge fungi have been reported from midges in differ- control. ent parts of the world but verv few of these Among biological control agents,Baciltus thu- microbial organisms have been subjected to ringiensis serovar. israel,ensis(B.t.i.) reduced massculturing and inoculating of natural breed- midge larvae to various degreesin some ponds ing sources for quantitative biological contro- and lakes. However, the application rates of assessments. Physical and cultural control B.t.l., neededfor the satisfactorycontrol (90% methodologiesof chironomids are also the least or higher) of midges,were at least 10x or higher explored. the rates establishedfor mosquito control; there- A large number of organochlorines, organo- fore, B.t.i. may have limited scopefor use in phosphates (OPs), pyrethroids and insect midge control programs. The flatworm, Dugesia growth regulators (IGRs) including juvenile hor- dorotocephalaand some fish (e.g.,carp, sunfish, mone analogues(e.g., methoprene) and chitin catfish, Tilapia and others) have been reportei synthesisinhibitors (e.g.,diflubenzuron) have to be effective in reducing midge larvae in some been evaluated in the laboratory and/or in the situations. Fish, as predators of midge larvae, field against nuisance speciesof midges in the however,are consideredto be partially effective USA and Japan. Among the OP compounds and only in small (20 ha or smaller)and closed tested, chlorpyrifos and temephos were gener- habitats. These predators would be lesseffective ally toxic to field-collectedlarvae of Chironomus in midge habitats covering several hundred or decorusand C. utahensls(Californi a), Glyptoten- thousandsof ha, particularly those that are con- dipes paripes (Florida), C. yoshimatsui and C. nected to river systemswhere they may be dis- plurnoas (Japan) and C. salinarius (Italy), but placed due to their free movement and migra- someof theseand a few other speciesof midges tion. More research on the development and in some situations in the USA and Japan were quantitativefield assessmentsof promisingpar- tolerant to temephos.There is also evidenceof asites,pathogens and predatorsof midgelarvae, cross-resistancein chironomidlarvae to the OP and the environmental implications and impact group.Presently, temephos is the only registered on trophic structure of these biological control midgelarvicide in the USA. Field studieson OP agentsin the aquatic environment is needed. insecticidesagainst midges in the USA and Ja- Midge habitats that spread over several pan have indicated that chlorpyrifos, chlorpyri- hundred or thousandsof ha demand exploration fos methyl, temephos, chlorphoxim and a few ofphysical and cultural control methods.In such other OP compounds causedappreciable larval habitats,the physicaland chemicalcomposition reductions fot 2-5 wk or longer at rate below of substratematerials and chemistry of the over- 0.56 kg AI/ha (USA) and <1-5 ppm (Japan). lying water in relation to spatial and seasonal Numerous pyrethroids have exhibited far supe- distribution of midge larval populations may rior activity than OP insecticidesagainst chiron- provide a clue to the conditions conducive to JUNE1991 MANAcEMENTop Pnsrrrenous CHIRoNoMIDAE 275 their proliferation, and the ecologicalbasis of Ali, A. and R. C. Fowler. 1985.A natural declineof midgeproduction. Their proliferation could then pestiferous Chironomidae (Diptera) populations be discouragedby manipulating their environ- from 1979 to 1984 in an urban area of central 68:304-311. ment. Information related to adult dispersalbe- Florida.Fla. Entomol. Ali, A. and J. Lord. 1980.Experimental insect growth patterns diel periodicity havior, of abundance, regulators against some nuisance chironomid of eclosion and attraction to light could also be midgesof centralFlorida. J. Econ.Entomol. 73:243- manipulated in some situations to reducemidge 249. nuisance more economically. Thusfar, very few AIi, A. and G. Majori. 1984.A short-terminvestigation studies on the larval ecologyand adult behavior of chironomid midge (Diptera: Chironomidae)prob- of pestiferous Chironomidae have been under- lem in saltwater lakes of Orbetello, Grosseto,Italy. taken. Mosq. News 44:17-21. Ali, A. and M. S. Mulla. 1975. Chironomid midge problem in water spreadingbasins and flood control ACKNOWLEDGMENTS channel in the Santa Ana River, OrangeCounty, California.Proc. Pap. Calif. Mosq. Control Assoc. This is Florida Agricultural Experiment Sta- 43:116-11?. tions Journal Series No. R-00920. Gratitude is AIi, A. and M. S. Mulla. 1976a. Substrate type as a expressedto Marshall Laird and an anonymous factor influencing spatial distribution of chironomid reviewer for their useful suggestionsthat im- midges in an urban flood control channel system. proved the quality of this article. Constructive Environ. Entomol. 5:631-636. criticism ofthis paperby John L. Capineraand AIi, A. and M. S. Mulla. 1976b.Insecticidal control of Donald R. Barnard and Kenneth E. Savageis chironomid midges in the Santa Ana River water also appreciated. I dedicate this article to my spreading system, Orange County, California. J. daughter and son, Khudejah Iqbal Ali and Umer Econ.Entomol. 69:509-513. Ali, A. and M. S. Mulla. 1976c.Chironomid larval Meraj Ali. density at various depths in a southern California water-percolation reservoir. Environ. Entomol. REFERENCES CITED 5:1077-1074. Ali, A. and M. S. Mulla. 1977a.Chemical control of Abul-Nasr,S., A. L. Isaand A. M. El-Tantawy.1970. nuisance midges in the Santa Ana River Basin, Controlmeasures of the bloodworms,Chironornus southernCalifornia. J. Econ.Entomol. 70:191-195. sp.,in rice nurseries.Bull. Entomol.Soc. Egypt, Ali, A. and M. S. Mulla. 1977b.The IGR diflubenzuron Econ.Ser. 4:127-33. and organophosphorusinsecticides against nuisance Ali, A. 1980a.Diel adulteclosion periodicity of nui- midgesin man-maderesidential-recreational lakes. sancechironomid midgesof central Florida. Envi- J. Econ.Entomol. 70:571-577. ron.Entomol. 9:365-370. Ali, A. and M. S. Mulla. 1978a.Chironomidpopulation Ali, A. 1980b.Nuisance chironomids and their control: changesin an intermittent water spreadingsystem. a review.Bull. Entomol. Soc.Am. 26:3-16. Mosq. News 38:386-392. Ali, A. 1981a.Bacillus thuringiensisserovar. israelensis Ali, A. and M. S. Mulla. 1978b.Declining field efficacy (ABG-6108) and somenontar- againstchironomids of chlorpyrifos against chironomid midges and lab- get aquatic invertebrates. J. Invertebr. Pathol. oratory evaluation of substitute larvicides. J. Econ. 38:264-272. Entomol. 7l:778-782. Ali, A. 1981b.Laboratory evaluationof organophos- Ali, A. and M. S. Mulla. 1978c.Effects of chironomid phate and new synthetic pyrethroid insecticides larvicides and diflubenzuron on nontarget inverte- againstpestiferous midges of central Florida. Mosq. in residential-recreational lakes. Environ. News41:157-161. brates Entomol. 7:21-27. Ali, A. 1989.Chironomids, algae, and chemical nu- of the IGR trients in a lentic systemin central Florida, USA. Ali, A. and M. S. Mulla. 1978d.Impact Acta Biol. Debr. Oecol.Hung. 3:15-27. diflubenzuron on invertebrates in a residential-rec- Ali, A. 1990. Seasonal changes of larval food and reational lake. Arch. Environ. Contam. Toxicol. feedingof Chlronomuscrassicoudatus Malloch (Dip- 7:483-491. tera: Chironomidae) in a subtropical lake. J. Am. Ali, A. and M. S. Mulia. 1979a.Diel periodicity of Mosq. Control Assoc.6:84-88. eclosionof adult chironomid midgesin a residential- Ali, A. and R. D. Baggs.1982. Seasonal changes of recreational lake. Mosq. News 39:360-364. chironomid populations in a shallow natural lake Ali, A. and M. S. Mulla. 1979b.Nuisance midge prob- and in a man-madewater coolingreservoir in cen- lem in southern California: chemical control strat- tral Florida.Mosq. News42:76-85. egies.Bull. Soc.Vector Ecol. 5:44-53. Ali, A. and P. K. Chaudhuri. 1988. Evaluation of a Ali, A. and M. S. Mulla. 1979c.Diel periodicity of new benzoylphenylurea insect growth regulator chironomid larval and pupal drift in an urban flood (UC-84572) against chironomid midges in experi- control channel system. Environ. Entomol. 8:902- mental ponds.J. Am. Mosq. Control Assoc.4:542- 907. 544. Ali, A. and M. S. Mulla. 1980.Activity of organophos- Ali, A. and R. C. Fowler.1983. Prevalence and disper- phate and synthetic pyrethroid insecticidesagainst sal of pestiferous Chironomidae in a lakefront city pestiferous midges in some southern California of centralFlorida. Mosq. News 43:55*59. flood control channels.Mosq. News40:593-597. 276 Jounrqer,oF THE AunRrcex Mosqurro CoNrRor,Assocrlrrox VoL. 7, No. 2

Ali, A. and M. S. Mulla. 1983. Evaluation of the Culicidae) to artificial Iight in the field. Proc. Calif. planarian, Dugesia dorotocephala,as a predator of Mosq.Vector Control Assoc.5?:82-88. chironomidmidges and mosquitoesin experimental Ali, A., B. H. Stanley and G. Majori. 198ba.Daily ponds.Mosq. News 43:46-49. abundance patterns of pestiferous Chironomidae Ali, A. and J. K. Nayar. 1985.Activity of an avermec- (Diptera) in an urban lake front in central Florida. tin insecticide,abamectin (MK-936), against mos- Environ. Entomol. l4:.780-7 84. quitoes and chironomid midgesin the laboratory. J. Ali, A., G. Majori, G. Ceretti, F. D'Andrea, M. Scat- Am. Mosq. Control Assoc.1:384-386. tolin and U. Ferrarese.1985b. A chironomid (Dip- Ali, A. and J. K. Nayar. 1986. Efficacy of Bacillus tera: Chironomidae)midge population study and sphaericus Neide against larval mosquitoes (Dip- laboratory evaluation of larvicides against midges tera: Culicidae) and midges (Diptera: Chironomi- inhabiting the lagoon of Venice,Italy. J. Am. Mosq. dae)in the laboratory.FIa. Entomol. 69:68b-690. Control Assoc.1:66-71. Ali, A. and J. K. Nayar. 198?. Laboratory toxicity of Anderson,L. D. and A. A. Ingram. 1960.Preliminary a new benzoylphenylurea insect growth regulator report on the chironomid midge project at the Los (UC-84572) against mosquitoes and chironomid Angeles County Flood Control District water midges.J. Am. Mosq. Control Assoc.3:809-811. spreadinggrounds on the Rio Hondo and San Ga- Ali, A. and B. H. Stanley.1981. Effects of a new insect briel River near Whittier. California. Proc. Pao. growth regulator, U C -62644,on target Chironomi- Calif. Mosq. Control Assoc.28:99-I03. dae and some nontarget aquatic invertebrates. Anderson,L. D., E. C. Bay and A. A. Ingram. 1964. Mosq. News41:640-649. Studies on chironomid midge control in water Ali, A., R. D. Baggsand J. P. Stewart.1981. Suscep- spreadingbasins near Montebello, California, Calif. tibility of someFlorida chironomids and mosquitoes VectorViews 11:13-20. to various formulations of Bacillus thuringiensis Anderson,L. D., E. C. Bay and M. S. Mulla. 1965. serovar.israelensis. J. Econ.Entomol. 74:672-677. Aquatic midge investigationsin southern California. Ali, A., M. S. Mulla and F. W. Pelsue.1976a. Chiron- Proc.Pap. Calif. Mosq.Control Assoc.33:31-33. omid midgeinvestigations in a concrete-lineddrain- Anonymous. 7974. A report on midge in the Kanda agesystem in southern California. Proc. Pap. Calif. River. Rep. Dept. SewerSyst., Metropolitan Tokyo, Mosq. Control Assoc.44:136-138. Tokyo. (In Japanese). Ali, A., M. S. Mulla and F. W. Pelsue.1976b. Removal Anthony, D. W. 1975. Use of viruses for control of aquatic pests. of substratefor the control of chironomid midgesin insect Environ. Prot. Agency, EPA- concrete-Iinedflood control channels.Environ. En- 600/3-75-100. tomol. b: /bb- /5tJ- Barthelmes, D. 1960.Tetraltymena parasitica (Penard 1922)Corliss 1952als Ali, A., J. K. Nayar and M. L. Kok-Yokomi. 1987. Parasit in Larven vom Chi- ronontus plumosrn. Typ. z. Evaluation of new experimental insect growth reg- F. Fischerei der. Hilf- swiss9 N.F:273-280. ulators against mosquitoes(Diptera: Culicidae) and Bay, E. C. 1964.An analysisof the "Sayule"(Diptera: midges (Diptera: Chironomidae) in the laboratory. Chironomidae) nuisance at San Carlos, Nicaragua, Proc. Calif. Mosq.Vector Control Assoc.55:81-86. and recommendationsfor its alleviation. W.H.O. Ali, A., S. R. Staffordand R. C. Fowler. 1984.Attrac- document,WHO/EBL/20. tion of adult Chironomidae (Diptera) to incandes- Bay, E. C. 1974.Predator-prey relationships among cent light under laboratory conditions. Environ. En- aquaticinsects. Annu. Rev. Entomol. \9:447-453, tomol. 13:1004-1009. Bay, E. C. and L. D. Anderson. 1965.Chironomid Ali, A., B. H. Stanley and P. K. Chaudhuri. 1986. control by carp and goldfish.Mosq. News 25:310- Attraction of some adult (Diptera: midges Chiron- J lo. omidae) of Florida to artificial light in the field. Fla. Bay, E. C. and L. D. Anderson.1966. Studies with the Entomol. 69:644-650. mosquito fish, Gambusia affinis, as a chironomid Ali, A., B. H. Stanleyand S. R. Stafford.1983. Short- control.Ann. Entomol. Soc.Am. 59:150-153. term daily emergenceof adult Chironomidae from a Beck,E. C. and W. M. Beck, Jr. 1969.Chironomidae natural lake and a man-made reservoir. Environ. of Florida. II. The nuisancespecies. Fla. Entomol. Entomol. L2:765-767. 52:1-11. Ali, A., M. S. Mulla, B. A. Federiciand F. W. Pelsue. Bennike,S. A. B. 1943.Contributions to the ecology 1977. Seasonal changes in chironomid fauna and and biology of the Danish freshwater leeches(Hi- rainfall reducingchironomids in urban flood control rudinea).Folia Limnol. Scand.2:1-109. channels.Environ. Entomol. 6:679-622. Bickley, W. E. and K. W. Ludlam. 1968.Insecticidal Ali, A., M. S. Mulla, A. R. Pfuntner and L. L. Luna. control of Glyptotendipesparipes in two Maryland 1978. Pestiferous midges and their control in a sewagelagoons. J. Econ.Entomol. 61:1454. shallow residential-recreational lake in southern Biever, K. D. 1965.A rearing technique for the colo- California.Mosq. News 38:528-535. nization of chironomidmidges. Ann. Entomol. Soc. Ali, A., M. S. Weaver and E. Cotsenmoyer.1989a. Am. 58:135-136. Effectiveness of Bacilhrs thurirqiensis serovar. ls- Biever,K. D. 1971.Effect of diet and competitionin raelensis(Vectobac 12 AS) and Bacillus sphaericus laboratory rearing of chironomid midges.Ann. En- (ABG-6232) against Culex spp. mosquitoes in a tomol.Soc. Am. 64:1116-1119. dairy lagoon in central Florida. Fla. Entomol. Brown,A. W. A., D. J. McKinley, H. W. Bedfordand 72:585-591. M. Qutubuddin. 1961. Insecticidal operations Ali, A., J. K. Nayar, J. W. Knight and B. H. 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Callahan,J. L. and C. D. Morris. 1987.Survey of 13 Federici.B. A.. W. L. Kramer and M. S. Mulla. 1976. Polk County, Florida, lakes for mosquito (Diptera: A disease tn Chironomus frommeri caused by a Culicidae)and midge(Diptera: Chironomidae) pro- Richettsiella-likeorganism. Proc. Pap. Calif. Mosq. duction.FIa. Entomol. 70:47 l-47 8. Control Assoc.44:123. Callahan,J. L. and C. D. Morris. 1989.Production Federici,B. A., R. R. Granados,D. W. Anthony and and maintenance of large numbers of Dugesia ti- E. I. Hazard.19?4. An entomopoxvirusand nonoc- grino (Turbellaria: Trachladida) for the control of cludedvirus-like particlesin larvae of the chiron- mosquitoesin the field.J. Am. Mosq.Control Assoc. omid.GoeLdichironomus holoprasinus. J. Invertebr. 5:10-14. Pathol.23:117-120. Ceretti, G., U. Ferrarese,A. Francesionand A. Bar- Fellton, H. L. 1940.Control of aquatic midgeswith baro. 198?.Chironomids (Diptera: Chironomidae) notes on the biology of certain species'J. Econ. in the natural diet of gilthead seabream (Sparus Entomol. 33:252-264. aurata L.\ farmed in the Venice lagoon.Entomol. Fellton, H. L. 1941.The use of chlorinatedbenzenes Scand. Suppl. 29:289-292. for the control of aquatic midges.J. Econ. Entomol. Chapman,J. and D. H. Ecke. 1969.Study of a popu- 34:192-194. lation of chironomid midges (Tanytorsus) parasi- Ferrarese,U. and G. Ceretti. 1989.Diel emergenceof tized by mermithid nematodes in Santa Clara Chironomus salinarius (Diptera: Chironomidae)in County,California. Calif. Vector Views 16:83-88. a Venice lagoon. Acta Biol. Debr. Oecol. Hung. Coffman,W. P. and L. C. Ferrington,Jr. 1984.Chi- 2:189-194. ronomidae.pp. 551-652.In: R. W. Merritt and K. Flentje,M. E. 1945a.Control and elimination of pest W. Cummins (eds.).An introductionto the aquatic infestations in public water supplies.J. Am. Water insects of North America. 2nd Edition. Kendall/ Works Assoc.37:1194-1203. Hunt Publ. Co.,Iowa. Flentje, M. E. 1945b.Elimination of midge fly larvae Cook, S. F., Jr. 1962.Feeding studies of the aeneus with DDT. J. Am. Water Works Assoc.37:1053. catfish, Coryd,orasaeneus on aquatic midges' J. Gad-El-Rab,M. O. and A. B. Kay. 1980.Widespread Econ.Entomol. 55:155-157. IgE-mediated hypersensitivity in the Sudan in the Cook, S. F., Jr. 1964.The potential of two native "green nimitti" midge Clad'otanytarsusI'ewisi (Dip- Californiafish in the control of chironomidmidges. tera: Chironomidae).I. Diagnosisby radioallergo- Mosq. News 24:332-333. sorbent test. J. Allergy CIin. Immunol. 66:190-195. Cook,S. F., Jr., J. D. Connersand R. L. Moore. 1964. Giacomin,C. and G. C. Tassi. 1988.Hypersensitivity midge popula- The impact of the fishery upon the to chironomid Chirornmus salinarius (non-biting California. Ann. tions of Clear Lake, Lake County, midge living in the lagoon of Venice) in a child with Entomol. Soc. Am. 57:.7Ol-707. serious skin and respiratory symptoms. BoIl. 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I (Diptera: Tendipedidae).A progressreporl. Mosq. Mulla, M. S., G. Majori and A. A. Arata. 1979.Impact News 16:201-204. of biological and chemical mosquito control agents Lewis, D. J. 7957.Observations on Chironomidaeat on nontarget biota in aquatic ecosystems.Residue Khartoum. Bull. Entomol. Res.48:155-184. Reviews7l:l2l-1,73. Lysenko,O. 1957.The possibilityof bacterialtransfer Mulla, M. S., H. A. Nawab-Gojrati and H. A. Dar- during the metamorphosisof the midge Chironomus wazeh.1978a. Biological activity and longevity of plumosus.Ceskoslovenenska Microbiol. 2:248-250. synthetic pyrethroids against mosquitoesand some (In Czech). nontargetinsects. Mosq. News 38:90-96. Magy, H. L 1968.Vector and nuisanceproblem ema- Mulla, M. S., H. A. Navvab-Gojratiand H. A. Dar- nating from man-made recreational lakes. Proc. wazeh.1978b. Biological activity and longevity of Pap. Calif. Mosq. Control Assoc.36:36-37. four speciesof freshwater fishes.Environ. Entomol. Majori, G., A. Ali and G. 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