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BIOLOGICAL CONTROL OF PESTS OF MEDICAL
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Introduction The manipulative use of natural enemies for the control of
medical and veterinary invertebrate pests has been restricted largely to
various species of Diptera. Some work has been conducted on ants,
cockroaches, wasps, ticks, and snails, but work on these animals has been
limited. Here are reviewed the biological control agents that can be
manipulated, agents that have been used successfully, agents that are being
researched and agents that show at least some promise for successful
application. Bay et al (1976) indicate that medically important pests differ from
agricultural pests in fundamental ways: First, pests that affect humans are
usually in the adult stage while those that attack crops are usually in the
immature stage. This is of some advantage for control of medically important
pests since it allows the control action to be taken against the immatures,
thus eliminating the adult before it can cause problems. A second difference,
however, is not favorable as it relates to setting tolerance levels. Whereas,
an allowable number of pests (tolerance level) can be established for the
biological control of a crop pest, it is far more difficult to establish for
pests attacking humans. For example, an individual mosquito can be of great
annoyance and can precipitate a reaction for control. In addition, low
population levels of a vector may still transmit a disease and, therefore,
cannot be tolerated (Service 1983). However, setting tolerance levels for
veterinary pests would be more in line with those for agricultural pests. A
third difference, usually a distinct disadvantage for biological control, is
that the habitat utilized by medically important pests is frequently
temporary as opposed to that of an agricultural crop which is more permanent.
In the agricultural situation, natural enemies can coexist with pests and
thus may regulate the pest populations. Additionally, in many situations the
habitat exploited by the medically important pests is only an undesirable
extension of human activity. An example would be the cultivation of rice,
where the production of pests such as mosquitoes is usually of little concern
to the grower. Interest in biological control of medical pests and vectors had
its modest beginning in the late 1800's (Lamborn 1890). At that time the
possible use of dragonflies as natural enemies for the control of mosquitoes
was clearly recognized. However, as is true even today, the enormous
difficulties associated with the colonization and management of these insects
quickly extinguished any idea for the practical use of these predators for
mosquito control. In the early 1900's the mosquitofish, Gambusia affinis (Baird
& Girard), became stressed for biological control. This small fish, being
much easier to deal with than dragonflies, was quickly utilized and
transported throughout the world during the early decades of this century in
attempts to control mosquitoes (Legner & Sjogren 1984). The mosquitofish, G. affinis,
<PHOTO>, and a few other natural enemies were employed with some
vigor until the 1940's. All of these control measures were curtailed sharply
with the introduction of synthetic organic insecticides after World War II.
The convenience and quick killing power of these chemicals was so dramatic
for mosquitoes, flies and lice, that other control tactics were quickly
reduced to a minor role. Interest in biological control, arose again when the
succession of chemicals developed during the 1940s and 1950s began to fail,
due to the development of genetic resistance in vector and pest populations.
The biological control of medically important pests and vectors has made slow
progress since its revival, behind that which has occurred in agricultural
systems (Service 1983). This disparity is due to the problems of establishing
pest tolerance levels, and the temporary unstable habitats exploited by
medically important pests (Legner & Sjogren 1984). While progress in the development of biological control agents
has been substantial and work in progress appears promising, an overall
evaluation at this point is that biological control will rarely be a panacea
for medically important pests. However, with continued effort it can be a
major component in the overall strategy for the control of some of these
important pests (Legner & Sjogren 1984). The literature reviewed in this section according to major
taxonomic groups where some success has been achieved or where work is
currently being conducted are the mosquitoes, blackflies, synanthropic flies,
intermediate-host snails and cockroaches. Most effort has been directed
against mosquitoes because of the human disease agents they transmit.
Consequently, must of this section is devoted to mosquitoes. The successful widespread use of biological control agents
against mosquitoes will require a much better understanding of the ecology of
predator/prey and pathogen/host relationships (Service 1983). The
opportunistic characteristics of many species (i.e., their ability to exploit
temporary habitats, coupled with their short generation time, high natural
mortality, great dispersal potential, and other R-strategist characteristics)
pose difficult problems for any biological control agent. Mosquitoes
typically exploit many aquatic habitats. Often a biological control agent
will have a much narrower range of environmental activity than the target
species. Thus, in many situations a number of different biological control
agents and/or appropriate methods will be necessary to control even one
species of mosquito across its range of exploitable breeding sources.
Aquatic weeds in irrigation canals: Left =
Blythe, Center = All American Canal & Right: Coachella Valley, CA. Fish.--Several
species of fishes are used for the biological control of mosquitoes, and
these species together form the major successes in biological control.
Unfortunately, their usefulness is limited to more permanent bodies of water,
and even under these situations their impact on the target species has been
only partially successful. Bay et al (1976) point out that many species of
fish consume mosquito larvae, but only a few species have been manipulated to
manage mosquito populations. The mosquitofish, G. affinis, <PHOTO>, is the best known agent for mosquito control. This fish,
which is native to the southeastern United States, eastern Mexico and the
Caribbean area, was first used as an introduced agent for mosquito control
when it was transported from North Carolina to New Jersey in 1905 (Lloyd
1987). Shortly thereafter it was introduced to the Hawaiian Islands to
control mosquitoes which had been introduced during the 19th century. During
the next 70 years, the mosquitofish was transported to over 50 countries and
today stands as the most widely disseminated biological control agent (Bay
1969, Garcia & Legner 1999, Lloyd 1987). Many of these introductions were aimed at Anopheles species that were
transmitting malaria. Hackett (1937) described its usefulness in malaria
control programs in Europe. He commented that its effects were not sufficient
by themselves, but that the fish had a definite impact on the suppression of
the disease. Tabibzadeh et al. (1970) reported a rather
extensive release program in Iran and concluded that the fish was an
important component in malaria eradication. Sasa and Kurihara (1981) and
Service (1983) believed that the fish had little impact on the disease and
that most evidence is circumstantial. Gambusia
no longer is recommended by the World Health Organization for malaria control
programs, primarily because of its harmful impact on indigenous species of
fish (Service 1983, Lloyd 1987). The biological attributes of G.
affinis, namely a high reproductive capability, high survivorship,
small size, omnivorous foraging in shallow water, relatively high tolerance
to variations in temperature, salinity and organic waste, would seemingly
make this species an excellent biological control agent (Bay et al.
1976, Moyle 1976). However, whether this fish leads to effective mosquito
control at practical costs in many situations is still debated. Kligler's
(1930) statement that "... their usefulness as larvae-destroyers under
local conditions where vegetation is abundant and micro fauna rich enough to
supply their needs without great trouble, is limited. In moderately clear
canals, on the other hand, or in pools having a limited food supply, they
yielded excellent results ..." is probably one of the most accurate. In California this fish had been used extensively for control of
mosquitoes in various habitats (Bay et al. 1976). Many mosquito
abatement districts in the State have developed systems for culturing,
harvesting and winter storage of the mosquito fish to have enough available
for planting early in the spring (Coykendall 1980). This is particularly
important in the rice growing areas of California where early stocking
appears to be of critical importance for build-up of fish populations to
control mosquitoes during late summer. The results of the use of G. affinis in California rice
fields will be summarized below as an illustrative example of the mixed
successes achieved in the field. Rice cultivation in California continuously poses one of the most
difficult control problems for Anopheles
and Culex species. Hoy
& Reed (1970) showed that good to very good control of Culex tarsalis Coquillett could be achieved at stocking
rates of about 480 or more females per hectare, and Stewart et al (1983)
reported excellent control with a similar stocking rate against this species
in the San Joaquin Valley. Although Cx.
tarsalis appears to be
controlled effectively by G.
affinis, the control of its frequent companion in northern
California rice fields, Anopheles
freeborni Aitken, is less apparent. Hoy et al. (1971)
showed a reduction of An. freeborni
populations at various stocking rates of about 120 to 720 fish per hectare,
but the reduction was not nearly as striking as for Cx. tarsalis. These workers surmised that improvement in
control could be achieved by earlier season stocking, possibly multiple
release points in fields and a reliable source of healthy fish for stocking.
Despite an extensive research effort in mass culture, management and storage
for G. affinis by
the State of California (Hoy & Reed 1971), a mass production method has
not been satisfactorily achieved (Downs et al. 1986, Cech and
Linden 1987). Studies of G. affinis
for control of mosquitoes in wild rice show that relatively high stocking
rates can effectively reduce An.
freeborni and Cx.
tarsalis populations
within a three-month period (Kramer et al. 1987a). The
commercial production of wild rice, which is a more robust and taller plant
than white rice and requires only 90 instead of 150 days to mature, has been
increasing over the last few years in California (Kramer et al.
1987). In the above study, stocking rates of 1.7 Kg/ha (ca. 2400 fish/Kg)
released in 1/10 ha wild rice plots failed to show a significant difference
in reduction of mosquitoes from plots with no fish. A decrease in numbers of
larvae was noted just prior to harvest which suggested that the fish were
beginning to have an impact on mosquito numbers (Kramer et al.
1987). Numbers of fish in these plots, based on recovery after drainage, was
about 100,000 individuals per hectare (ca. 32 Kg/ha) or a density of about 10
fish per square meter. However, significant control was not achieved. During 1987 this study was repeated at the rates of 1.7 and 3.4
Kg/ha of fish. Results showed an average suppression of larvae (primarily An. freeborni) of <1 and
0.5 per dip for the low and high rate respectively, compared to control plots
which averaged >4.5 per dip. Fish densities in the 1987 study surpassed
those of 1986 by about two fold at the 1.7 Kg/ha rate and three fold at the
3.4 Kg/ha rate. It is believed that these greater fish numbers accounted for
the control differences observed in the second year, although mosquitoes were
not eliminated. Differences between test plots and control plots were first
observed eight weeks after the fish had been planted and mosquitoes remained
under control until drainage of the fields (Kramer et al.
1988). Davey & Meisch (1977a,b) showed that the mosquitofish at
inundative release rates of 4,800 fish per hectare, was effective for control
of Psorophora columbiae
(Dyar & Knab) in Arkansas rice fields. Fish released at the water flow
inlets dispersed quickly throughout the fields. This is an important
attribute for controlling species of Psorophora
and Aedes, whose hatch
and larval development are completed within a few days. A combination of
1,200 G. affinis
and about 300 sunfish (Lepomis cyanellus Rafinesque) gave
better control than either four times the amount of G. affinis or L. cyanellus
used separately. This synergistic effect reduces logistic problems associated
with having enough fish available at the times fields are inundated.
Blaustein (1986) found enhanced control of An. freeborni by mosquitofish in California
rice fields after the addition of green sunfish. He speculated that the
increased control was the result of the mosquitofish spending more time in
protected areas where mosquitoes were more abundant and the green sunfish was
avoided. The availability of fish for stocking fields either inundatively,
such as in Arkansas or for control later in the season as practiced in
California, has been a fundamental reason why fish have not been used more
extensively in rice fields. A unique use of the mosquitofish by inundative release was
reported by Farley & Caton (1982). The fish were released in subterranean
urban storm drains to control Culex
quinquefasciatus Say
breeding in entrapped water at low points in the system. Fish releases were
made following the last major rains to avoid having them flushed out of the
system. Fish survived for more than three months during the summer and were
found throughout the system. Gravid females produced progeny. However, no
mating occurred, and after the initial increase in numbers populations of
fish diminished as summer progressed. Reductions of mosquitoes from 75 to 94%
were observed for three months compared to untreated areas (Mulligan et
al. 1983). This control practice is now conducted on a routine basis
by the Fresno Mosquito Abatement District (J. R. Caton 1987, pers. comm.). Although G. affinis
has been useful for control of mosquitoes in a number of situations, clearly
there are drawbacks to its use. In fact, if today's environmental awareness
existed at the turn of the century, this fish probably never would have been
intentionally introduced into exotic areas (Pelzman 1975, Lloyd 1987). The
major objection to this fish has been its direct impact on native fishes
through predation, or its indirect impact through competition (Bay et al.
1976, Schoenherr 1981, Lloyd 1987). More than 30 species of native fish have
been adversely affected by the introduction of Gambusia (Schoenherr 1981, Lloyd 1987). Gambusia, a general predator, can also
substantially reduce zooplankton and thus lead to algal blooms in certain
situations (Hurlbert et al. 1972). Introductions of Gambusia have also reduced numbers
of other aquatic invertebrates coinhabiting the same waters (Hoy et al.
1972, Farley & Younce 1977, Rees 1979, Walters & Legner 1980
, Hurlbert &
Mulla 1981). The next most widely used fish for mosquito control is the common
guppy, Poecilia reticulata (Peters), <PHOTO>. It has been deployed successfully in Asia for the control
of waste water mosquitoes, especially Cx.
quinquefasciatus. Like
its poeciliid relative Gambusia,
it is native to the Americas (tropical South America). But, rather than being
intentionally introduced to control mosquitoes, it was taken to other parts
of the world by tropical fish fanciers. Sasa et al. (1965)
observed wild populations of this fish breeding in drains in Bangkok and
concluded from their observations that it was controlling mosquitoes common
to that habitat. The practical use of guppies is primarily restricted to
subtropical climates because of an inability to tolerate temperate-zone water
temperatures (Sasa & Kurihara 1981). However, their most important
attribute is a tolerance to relatively high levels of organic pollutants,
which makes them ideal for urban water sources that are rich in organic
wastes. In Sri Lanka, wild populations have been harvested and used for the
control of mosquitoes in abandoned wells, coconut husk pits and other sources
rich in organics (Sasa & Kurihara 1981). The fish occursin in India,
Indonesia and China and has been intentionally introduced for filariasis
control into Burma (Sasa & Kurihara 1981). Mian et al (1985) evaluated
its use for control of mosquitoes in sewage treatment facilities in southern
California and concluded that guppies showed great potential for mosquito
control in these situations. Exotic fish have also been used for clearing aquatic vegetation
from waterways [ <PHOTO1>, <PHOTO2>, <PHOTO3> ]which has resulted in excellent mosquito control. In the
irrigation systems of southeastern California, three species of subtropical
cichlids <PHOTO>, Tilapia
zillii (Gervais),
<PHOTO>, Oreochromis (Sarotherodon)
mossambica (Peters),
<PHOTO>, and Oreochromis (Sarotherodon) hornorum (Trewazas), <PHOTO>, were introduced and have become established over some 2,000
ha of Cx. tarsalis breeding habitat (Legner
& Sjogren 1984). In this situation, mosquito populations are under control by a
combination of direct predation and the consumption of aquatic plants by
these omnivorous fishes (Legner & Medved 1973, Legner 1978a, 1983 ; Legner & Fisher 1980; Legner & Murray 1981 , Legner & Pelsue 1983). As Legner & Sjogren (1984) indicate, this is a unique example of persistent biological
control and probably only applicable for relatively sophisticated irrigations
systems where a permanent water supply is assured, and water conditions are
suitable to support the fish (Legner et al. 1980). There is a
three-fold advantage in the use of these fish: (1) clearing of vegetation to
keep waterways open, (2) mosquito control and (3) a fish large enough to be
caught for human consumption. Some sophistication is necessary when stocking
these cichlids for aquatic weed control, which is often not understood by
irrigation districts personnel (Hauser et al. 1976, 1977; Legner 1978b). Otherwise competitive displacement may eliminate T. zillii, the most efficient weed
eating species (Legner 1986). Household storage of water in open containers has frequently been
the cause for outbreaks of human disease transmitted by Aedes aegypti (Linnaeus) in
less developed parts of the world. While conducting Ae. aegypti surveys in
Malaysia during the mid 1960s, Dr. Richard Garcia , <PHOTO>,of UC Berkeley observed what were apparently P. reticulata being utilized
by town residents for the control of mosquitoes in bath and drinking water
storage containers. The origin of this control technique was not clear but it
appeared to be a custom brought to the area by Chinese immigrants. Not all
residents used fish, but those that did had no breeding populations of Ae. aegypti.
Neng (1987) reported on the use of a catfish, Claris sp.,
for the control of Ae. aegypti
in water storage tanks in coastal villages of southern China. This fish was
considered appropriate since it was indigenous, edible, consumed large
numbers of mosquito larvae, had a high tolerance for adverse conditions and could be obtained
from the local markets. One fish was placed in each water source and later
checked for its presence by larval survey teams about every 10 to 15 days. If
fish were not found on inspection the occupant was told to replace the fish
or be fined. The investigation was conducted from 1981 to 1985, and surveys
over this period showed a sharp initial reduction in Ae. aegypti followed by a low
occurrence of the mosquito over the four-year study period. Outbreaks of
dengue were observed in neighboring provinces during this period, but not in
the fishing villages under observation. The cost of the program was estimated
to be about 1/15 that of indoor house spraying (Neng 1987). Alio et al. (1985) described another use of a local
species of fish for the control of a malaria vector similar to the method
reported by Kligler (1930). Oreochromis
sp., a tilapine, was introduced into human-made water catchment basins called
"barkits" in the semi arid region of northern Somalia. These small
scattered impoundments served as the only sources of water during the dry
season for the large pastoral population of the area. Anopheles arabiensis Patton, the vector of
malaria in that area, is essentially restricted to these sites. Release of
fish into the "barkits" dramatically reduced both the vector and
nonvector populations of mosquitoes rather quickly. Treatment of the human
population with antimalarial drugs during the initial phase of this two-year study,
combined with the lower vector population reduced the transmission rate of
malaria to insignificance over a 21 month period whereas the control villages
remained above 10 percent. Alio et al (1985) commented that the added
benefits of reduced vegetation and insects in the water sources was also
recognized by the local population. This resulted in community cooperation
and was expected to further benefit the control strategy by providing
assistance in fish distribution and maintenance as the program expanded to other
areas. The last two examples involve the use of indigenous over exotic
fish where feasible in vector control programs. There are other examples
where native fishes have been used in specialized circumstances (Kligler
1930, Legner et al. 1974 , Menon & Rajagopalan 1978, Walters & Legner 1980, Ataur-Rahim 1981 and Luh 1981). Lloyd (1987) argued that only
indigenous fish should be employed for mosquito control because of the environmental
disruption induced by exotics such as G.
affinis. However, he suggested that native fish should be analyzed
carefully for prey selectivity, reproductive potential and effectiveness in
suppression pest populations before attempting their use. Lloyd (1987) also
pointed out that a multidisciplinary approach involving fisheries biologists
and entomologists should be employed when developing indigenous fish for
mosquito control. However, in California where native pup
fishes in the genus Cyprinodon may afford a greater potential for
mosquito control under a wider range of environmental stresses than Gambusia (Walters & Legner 1980 & PHOTO), the
California Department of Fish and Game discourages their use on the basis
that unknown harmful effects might result to other indigenous fishes. There
is also the concern that certain rare species of Cyprinodon might be lost through
hybridization. Perhaps China's example of a multipurpose use of native fish for
mosquito control and a human protein source is the most resourceful strategy.
This application for mosquito control is not new. Kligler (1930) used a
tilapine fish to control Anopheles
sp. in citrus irrigation systems in old Palestine, where farmers cared for
the fish, consuming the larger ones. According to Luh (1981), the culture of
edible fish for the purpose of mosquito control and human food is not widely
encouraged in China. The old Chinese peasant custom of raising edible fish in
rice fields has received greater attention in recent times because of the
benefits made possible through this practice. The common carp, Cyprinus carpio Linnaeus, and
the grass carp, Ctenopharygodon idella Valenciennes, are most
commonly used. Fish are released as fry at the time rice seedlings are
planted. Fields are specially prepared with a central "fish pit"
and radiating ditches for refuge when water levels are low. Pisciculture in
rice fields, as noted by Luh (1981), has three major benefits: (1) a
significant reduction in culicine and to a lesser extent anopheline larvae,
(2) fish are harvested as food and (3) rice yields are increased apparently
by a reduction in competitors and possibly by fertilization of the plants by
fish excreta. Another group of fishes, the so-called "instant" or annual fishes, (Cyprinodontidae), <PHOTO>, which are native to South America and Africa, have been
considered as possible biological control agents for mosquitoes (Vanderplant
1941, 1967; Hildemann & Wolford 1963; Bay 1965, 1972; Markofsky &
Matias 1979). The relatively drought resistant eggs of these cyprinodontids, which allows them
to utilize temporary water sources as habitat, would seem to make them ideal
candidates for mosquito control. There is also some evidence that they do
impact mosquito populations in native areas (Vanderplant 1941, Hildemann
& Wolford 1963, Markofsky & Matias 1979). Research on the biology and
ecology of several species has been conducted; however, there are no
published accounts on the successful use of these fish in field situations.
In California the South American species Cynolebias
nigripinnis Regan and Cynolebias
bellottii (Steindachner), survived the summer in rice fields, but
no reproduction was observed over a three-year period (Coykendall 1980). It
was speculated that they may play a future role in California's mosquito
control program in temporary pools and possibly rice fields. C. bellottii was observed to
reproduce repeatedly and to persist in small intermittently dried ponds in
Riverside, California for eleven consecutive years, 1968-1979 (Legner &
Walters unpubl.). Four drying flooding operations over two months were
required to eliminate this species from ponds that were to be used for native
fish studies (Walters & Legner 1980). It seems logical, given the biological capability of surviving
an annual dry period, that these fish could be successfully integrated into
mosquito control programs, especially in newly created sources in geographic
areas where they naturally occur (Vaz-Ferreira et al. 1963,
Anon 1981, and Geberich 1985). Arthropods.--Numerous
species of predatory arthropods have been observed preying on mosquitoes, and
in some cases are believed to be important in controlling mosquitos (James
1964, Service 1977, Collins & Washino 1979, McDonald & Buchanan
1981). However, among the several hundred predatory species observed, only a
few have been used in a manipulative way to control mosquitoes. Dragonflies,
sometimes referred to as mosquito hawks, were one of the first arthropods to
be examined. Difficulties in colonization, production and handling have
restricted their use to experimental observation. It is unlikely that they
will ever be used extensively (Lamborn 1890, Beesley 1974, El Rayah 1975,
Riviere et al. 1987a). There are a few cases where the difficulties associated with the
manipulative use of arthropods has been at least partly overcome. More than
50 years ago, in a classic use of biological control, the mosquito Toxorhynchites, whose larvae are
predators of other mosquitoes, was released on several Pacific Islands in an
effort to control natural and artificial container breeding mosquitoes such
as Ae. aegypti
and Aedes albopictus (Skuse) (Paine 1934,
Bonnet & Hu 1951, Petersen 1956). The releases were not considered
successful, but the mosquitoes did establish in some areas (Steffan 1975).
Several reasons to explain why these releases failed were low egg production,
lack of synchrony between predator and prey life cycles, and selection of
only a relatively small number of prey breeding sites (Muspratt 1951,
Nakagawa 1963, Trpis 1973, Bay 1974, Riviere 1985). Although not apparently a suitable predator in the classical
sense, there is still interest in the use of various Toxorhynchites spp. for
inundative release (Gerbert & Visser 1978). Trpis (1981) working with Toxorhynchites brevipalpis
(Theobald) showed that the high daily consumption rate and long survival of
the larvae without prey made it a prime candidate for biological control use.
Observations on adult females indicated a 50% survivorship over a 10-week
period with a relatively high oviposition rate per female. All the above
attributes suggest that this species would be useful for inundative release
programs against container breeding mosquitoes. Studies by Focks et al (1979)
in Florida, working with Toxorhynchites
rutilis rutilis Coquillett, showed that this species had a high
success rate in artificial breeding containers. In a 12.6 hectare residential
area, about 70% of the available oviposition sites were located over a 14-day
period by two releases of 175 females. Mass culturing techniques have been
developed for this species and Toxorhynchites
amboinensis (Doleschall) (Focks & Boston 1979, Riviere et al.
1987b). Focks et al (1986), working with Toxorhynchites amboinensis, reported that
release of 100 females per block for several weeks, combined with ultra low
volume application of malathion, reduced Ae.
aegypti populations by about 96% in a residential area of New
Orleans. The Toxorhynchites
releases and not the insecticide treatment apparently accounted for most of
the reduction. These workers noted that the procedure could be further
refined by reducing both the number of predators and malathion applications
without lowering efficacy. Mosquitoes such as Ae. aegypti and Ae. albopictus, which breed in and whose eggs
are dispersed via artificial containers, pose major health hazards as vectors
of human diseases throughout much of the warmer climates of the world. The
massive quantities of containerized products and rubber tires which are then
discarded without care or stockpiled, have given these mosquito species a
tremendous ecological advantage. The recent establishment and extensive
spread of Ae. albopictus in the United States
underlines this point (Sprenger & Wuithironyagool 1986). The apparent
inability of governments to appropriately control disposal of these
containers and difficulties in location once they are discarded makes
inundative releases of Toxorhynchites,
either alone or in combination with other control tactics, a much more
plausible approach (Focks et al. 1986, Riviere et al.
1987a). Notonectids are voracious
predators of mosquito larvae under experimental conditions (Ellis &
Borden 1970, Garcia et al. 1974, Hazelrig 1974), and in
waterfowl refuges in California's Central Valley (Legner & Sjogren,
unpub. data). Notonecta undulata
Say and Notonecta unifasciata Guerin have been
colonized in the laboratory. In addition, collection of large numbers of
eggs, nymphs and adults is feasible from such breeding sites as sewage
oxidation ponds (Ellis & Borden 1969, Garcia 1973, Hazelrig 1975, Sjogren
& Legner 1974, Muira 1986). Some studies have been conducted on storage of
eggs at low temperatures, but viability decreased rapidly with time (Sjogren
& Legner 1989 ). At present, the most feasible use of these predators appears
to lie in the recovery of eggs from wild populations on artificial
oviposition materials and their redistribution to mosquito breeding sites.
Such investigations were carried out in central California rice fields by
Miura (1986). Floating vegetation such as algal mats and sometimes duck weed
(Lemna spp.) form protective refuges for mosquito larvae, and consequently
populations of mosquitoes can be high in the presence of notonectids (Garcia et
al. 1974). It appears that colonization and mass production costs,
coupled with the logistics of distribution, handling and timing of release at
the appropriate breeding site, are almost insurmountable problems for routine
use of notonectids in mosquito control. In addition to insect predators, several crustaceans feed on
mosquito larvae. Among these
are the tadpole
shrimp, Triops longicaudatus (LeConte), and several copepod
species. Mulla et al. (1986) and Tietze & Mulla (1987),
investigating the tadpole shrimp, showed that it was an effective predator
under laboratory conditions and speculated that it may play an important role
in the field against flood water Aedes
and Psorophora species
in southern California. Drought resistance in predator eggs is an appealing
attribute for egg production, storage and manipulationin field situations
against these mosquitoes. However, synchrony in hatch and development between
the predator and the prey is crucial if this is to be a successful biological
control agent for the rapidly developing Aedes
and Psorophora spp. In
addition, the tadpole shrimp is considered an important pest in commercial
rice fields. Miura & Takahashi (1985) reported that Cyclops vernalis Fisher was
an effective predator on early instar Cx.
tarsalis larvae in the
laboratory. These workers speculated that copepods could have an important
role in suppressing mosquito populations in rice fields because of their
feeding behavior and abundance. Another crustacean that has shown promise for more extensive
application is the cyclopoid predator, Mesocyclops aspericornis
Daday (Riviere et al. 1987b). This work has shown
reductions of Ae. aegypti
and Ae. polynesiensis Marks by more than 90%
after inoculative release of the organism into artificial containers, wells,
tree holes and land crab burrows. Although not able to withstand desiccation,
the rather small cyclopod predator has persisted almost 2.5 years in crab holes
and up to five years in wells, tires and tree holes under subtropical
conditions. This species can be mass produced, but its occurrence in large
numbers in local water sources allows for the inexpensive and widespread
application to mosquito breeding sites in Polynesia (Riviere et al.
1987a,b). The species is also very tolerant of salinities greater than 50
parts per thousand. The benthic feeding behavior of Mesocyclops makes it an effective
predator of the bottom foraging Aedes,
but limits effectiveness against surface foraging mosquitoes. Riviere et
al. (1987a,b) believed that the effectiveness against Aedes is due to a combination of
predation and competition for food. Perhaps the greatest utility of this Mesocyclops will lie in the control
of crab hole breeding species, such as Ae.
polynesiensis in the
South Pacific. Further investigations may uncover additional cyclopods that
can impact other mosquito species. The most important nonarthropod invertebrate predators to draw
attention for mosquito control are the turbellarian flatworms and a
coelenterate. Several flatworm species have been shown to be excellent
predators of mosquito larvae in a variety of aquatic habitats (Legner &
Medved 1974 , Yu & Legner 1976, Collins & Washino 1978, Case & Washino 1979, Legner 1977, 1979, Ali & Mulla 1983, George et al. 1983). Several
biological and ecological attributes of flatworms would seem to make them
ideal candidates for manipulative use. Among them are ease of mass
production, an overwintering embryo, effective predatory behavior in shallow
waters with emergent vegetation, on site exponential reproduction following
inoculation (Medved & Legner 1974 , Tsai & Legner 1977 , Legner & Tsai 1978, Legner 1979) and tolerance to environmental contaminants (Levy & Miller
1978, Nelson 1979). Collins & Washino (1978) and Case & Washino (1979)
suggested that flatworms, particularly Mesostoma,
may play an important role in the natural regulation of mosquitoes in some
California rice fields because of their densities and their predatory attack
on mosquito larvae in sentinel cages. Preliminary analysis using extensive
sampling showed a significant negative correlation between the presence of
flatworms and population levels of Cx.
tarsalis and An. freeborni (Case &
Washino 1979). However, these workers cautioned that an alternative
hypothesis related to the ecology of these species may have accounted for the
correlations. Later investigations by Palchick & Washino (1984),
employing more restrictive sampling, were not able to confirm the
correlations between Mesostoma and mosquito populations. However, the
enormity of the problem associated with sampling in California rice fields,
coupled with the complexity of the prey and predator interactions, make
further studies necessary before the role of this group of flatworms in rice
fields can be clearly established. The important attributes for manipulative use of flatworms
mentioned above raises the question of why they have not been developed
further for use in mosquito control. Perhaps the contemporary development of Bacillus thuringiensis var. israelensis DeBarjac (H-14), a
highly selective easily applied microbial insecticide, may have been at least
partially responsible for slowing further work and development of these
predators. Their mass culture must be continuous and demands skilled
technical assistants (Legner & Tsai 1978). Their persistence in field habitats may also depend on the
presence of other organisms, such as ostracods, which can be utilized for
food during low mosquito abundance (Legner et al. 1976). The coelenterates, like the flatworms, showed great promise for
further development and use in selected breeding habitats. Chlorohydra viridissima (Pallas) is
efficient in suppressing culicine larvae in ponds with dense vegetation and
this species also can be mass produced (Lenhoff & Brown 1970, Yu et
al. 1974a, 1974b, 1975). However, like the flatworms, work on these predators has
waned, perhaps for similar reasons as speculated for the flatworms. Microbial
pesticides can be employed over an extensive range of different mosquito
breeding habitats. Also, commercial production of flatworms and coelenterates
would be much more costly, and storage of viable cultures all but impossible. Fungi.--The most
promising fungal pathogen is a highly selective and environmentally safe
oomycete, Lagenidium giganteum Couch. First tested
for its pathogenicity to mosquitoes in the field by McCray et al.
(1973), it is applied by aircraft to rice fields (Kerwin & Washino 1987).
Lagenidium develops
asexually and sexually in mosquito larvae, and is capable of recycling in
standing bodies of water. This creates the potential for prolonged infection
in overlapping generations of mosquitoes. Lagenidium
may also remain dormant after the water source has dried up and then become
active again when water returns. The sexually produced oospore offers the
most promising stage for commercial production because of its resistance to
desiccation and long-term stability. However, problems in production and
activation of the oospores still remain (Axtell et al. 1982,
Merriam & Axtell 1982a,b, 1983; Jaronski & Axtell 1983a,b,c, Kerwin et
al. 1986, Kerwin & Washino 1987). Field trials with the sexual
oospore and the asexual zoospore indicate that this mosquito pathogen is near
the goal of practical utilization. Kerwin et al (1986) reports that the
asynchronous germination of the oospore is of particular advantage in
breeding sources where larval populations of mosquitoes are relatively low,
but recruitment of mosquitoes is continuous due to successive and overlapping
generations, as in California rice fields. The germination of oospores over
several months provides long-term control for these continuous low level
populations. In addition, the asexual zoospores arising from the oospore
infected mosquito is available every two to three days to respond in a
density dependent manner to suppress any resurging mosquito population. This stage
survives about 48 hours after emerging from the infected host. Kerwin et al. (1986) indicate that laboratory
fermentation production of the asexual stage of Lagenidium for controlling mosquitoes in the field is
approaching the development requirements and costs for the production of Bacillus thuringiensis israelensis. A distinct advantage of
this pathogen over the Bacillus
is its potential to recycle through successive host generations. The
disadvantage of the asexual stage is that it is relatively fragile, cannot be
dried and has a maximum storage life of only eight weeks (Kerwin &
Washino 1987). Thus, the focus of attention for commercial production is on
the oospore, which is resistant to desiccation and can be easily stored.
Axtell & Guzman (1987) have recently encapsulated both the sexual and
asexual stages in calcium alginate and reported activity against mosquito
larvae after storage for up to 35 and 75 days, respectively. Further
refinement in techniques of production and encapsulation might make this
approach a viable option for future commercial production and application. Limitations on the use of this pathogen include intolerance to
polluted water, salinity and other environmental factors (Jaronski &
Axtell 1982, Lord & Roberts 1985, Kerwin & Washino 1987). However,
there are numerous mosquito breeding sources where these limitations do not
exist and therefore one would expect to see this selective and persistent
pathogen available for routine mosquito control in the near future. The fungus Culicinomyces clavosporus
Couch, Romney & Rao, first isolated from laboratory mosquito colonies and
later from field habitats, has been under research and development for more
than a decade (Sweeney et al. 1973, Couch et al.
1974, Russell et al. 1979, Frances et al. 1985).
The fungus is active against a wide range of mosquito species and also causes
infections in other aquatic Diptera (Knight 1980, Sweeney 1981). The ease of
production with relatively inexpensive media in fermentation tanks is an
extremely desirable trait. However, problems in storage must be overcome if
this fungus is to be widely used. Perhaps a drying process, now being
investigated, will solve storage requirements (Sweeney 1987). Although the
fungus has shown high infection rates in field trials, dosage rates have been
high and appreciable persistence at the site has not been demonstrated
(Sweeney et al. 1973, Lacey & Undeen 1986, Sweeney 1983,
1987). Various species of Coelomomyces have been studied
over the last two decades for use in mosquito control. Natural epizootics
with infection rates in excess of 90% have been recorded. These fungi persist
in certain habitats for long periods; however, factors triggering outbreaks
in these situations are not well understood (Chapman 1974). Some field
testing has been done, but results have been highly variable (Federici 1981).
In general, difficulties associated with the complex life cycle of these
fungi have encumbered research on them. Federici (1981) and Lacey &
Undeen (1986) have reviewed the potential of these fungi for mosquito
control. Nematodes.--Among the
various nematodes pathogenic for mosquitoes, Romanomermis culicivorax Ross & Smith,
has received the most attention (Petersen & Willis 1970, 1972a,b, 1975;
Brown et al. 1977, Brown & Platzer 1977, Poinar 1979,
Petersen 1980a,b, Brown-Westerdahl et al. 1982, Kerwin &
Washino 1984). This mermithid, which is active against a wide range of
mosquito species, has been mass produced (Petersen & Willis 1972a) and
utilized in a number of field trials. The nematode was commercially produced
and sold under the name Skeeter Doom TMR, but according to Service
(1983) eggs showed reduced viability in transport and the product currently
is no longer sold. However, the nematode's ability to recycle through multigenerations
of mosquitoes and overwinter in various habitats, including drained,
harvested, stubble-burned, cultivated and replanted rice fields, are strong
attributes favoring its further research and development for biological
control (Petersen & Willis 1975, Brown-Westerdahl et al.
1982). Several field applications have shown good results and have included
both the preparasitic stage and post parasitic stages with the former more
applicable to the "quick kill" and the latter for more long-term
continuous control such as in California rice fields (Petersen et al.
1978a,b, Levy et al. 1979, Brown-Westerdahl et al.
1982). Some drawbacks to its widespread use include intolerance to low levels
of salinity, polluted water and low oxygen levels, predation by aquatic
organisms and the potential for development of resistance by the host
(Petersen & Willis 1970, Brown & Platzer 1977, Brown et al.
1977, Petersen 1978, Brown-Westerdahl 1982). However, these environmental
problems are not generally an issue for anopheline control. For control of
these species the cost of in vivo mass production clearly
stands as the major drawback for this pathogen. Perhaps its most plausible
use will be in specialized habitats integrated with other control strategies
(Brown-Westerdahl et al. 1982). Bacteria.--The spore
forming bacterial pathogen, Bacillus
thuringiensis var. israelensis (H-14), was isolated by
Goldberg & Margalit (1977) and the produced toxin has been shown by
numerous studies to be an effective and environmentally sound microbial
insecticide against mosquitoes and blackflies. Its high degree of specificity
and toxicity, coupled with its relative ease of production, have made it the
most widely used microbial product to date for mosquito and blackfly control.
Several formulations are currently available from commercial firms throughout
the world. Its efficacy under different environmental conditions and problems
associated with its use have been reviewed by Garcia (1986, 1987) and Lacey
& Undeen (1986). Another spore forming bacterium, Bacillus sphaericus Neide, has also shown great
promise as a larvacide against certain mosquito species (Mulla et al.
1984). In general, several strains of this pathogen show a much higher degree
of toxic variability among species of mosquitoes. Culex spp. appear to be highly
susceptible, whereas other species such as Ae. aegypti are highly refractory. Unlike the
ephemeral larvacidal activity of Bacillus
t. i. toxin, some strains of B. sphaericus have
shown persistence and apparent recycling in certain aquatic habitats
(DesRochers & Garcia 1984). For further detail see the recent review by
Lacey & Undeen (1986). Protozoa.--A large
number of protozoa have been isolated from mosquitoes and other medically
important arthropods (Roberts et al. 1983, Lacey & Undeen
1986). Of this assemblage the microsporidians have been studied
rather intensively. Due to their complex life cycle and the in vivo
production methods necessary for maintaining them, research on their
practical utility has been limited. However, as Lacey & Undeen (1986)
point out, if more information is developed on their life cycle, it may be
found that they could play a role in suppressing mosquitoes through inoculative
and augmentive releases in certain habitats. Among the other protozoa that show promise is the endoparasitic
ciliate, Lambornella clarki Corliss & Coats, a
natural pathogen of the treehole mosquito, Aedes sierrensis Ludlow. This pathogen has received
considerable attention over the last few years as a potential biological
control agent for container breeding mosquitoes (Egeter et al.
1986, Washburn & Anderson 1986). Desiccation resistant cysts allow
persistence of the ciliate from one year to the next. Currently, in vitro
production methods are being developed and small field trials are being
initiated to determine its efficacy and practicability for field use
(Anderson et al. 1986a,b). Viruses.--Numerous
pathogenic viruses have been isolated from mosquitoes and blackflies.
However, to date none look promising for practical use in control (Lacey
& Undeen 1986). SYNANTHROPIC DIPTERA These flies, the most important of which are muscoid species, can
be defined broadly as those most closely associated with human activities.
Breeding habitats very from the organic wastes of urban and rural settlements
to those provided by various agricultural practices, particularly ones
related to the management and care of domestic and range animals. Their
degree of relationship to humans varies considerably with the ecology and
behavior of the fly involved. Some are more often found inside dwellings (endophilic) while others remain mostly
outdoors (exophilic). The
discussion that follows separates these flies by their general endophilic and
exophilic habits, and is restricted to brief comments since the potential for
biological control of these flies has been reviewed (Legner et al.
1974, Bay et al. 1976, Legner 1986). Endophilic Flies.--Povolny
(1971) describes these flies as primarily dependent on human and domestic
animal wastes. Musca domestica
Linnaeus is by far the best known example. However, some Drosophila and Psychoda spp. also fall into this
category. Certain Fannia
spp. are more on the periphery but are also included here. The common housefly, Musca domestica, has been a
constant associate of humans over much of our modern history. Attempts to
control its populations by biological means have been extensive and on
occasion successful in special situations. More frequently they have failed
to reduce numbers to acceptable levels. It should be emphasized that control
of M. domestica
populations, as well as most other endophilic flies pestiferous to humans,
would be largely unnecessary if waste products produced by human activities
could be appropriately managed. Since this is not the case, efforts towards
the biological control of these species have continued. Starting around the turn of this century biological control of
these flies was attempted by the introduction of a broad range of different
natural enemies into areas where the flies presented problems. The Pacific
Islands were a focus of much attention with the introduction of dung beetles,
several parasitoids and predators during this period. It was believed that
the accidental introduction of an ant, Pheidole megacephala
F., combined with the introduction of the coprophagous dung beetle Hister chinensis Quensel, caused significant
fly reductions on the islands of Fiji and Samoa (Simmonds 1958). The Islands
of Hawaii had 16 introductions from 1909 to 1967 of which 12 established.
However, the exact role of these natural enemies in overall regulation of
flies on the islands is still not well understood (Legner et al.
1974 , Legner 1978c). Rodriguez & Riehl (1962) in California, used the novel and
successful approach of chicken cockerels as direct predators of fly larvae in
chicken and rabbit manure. However, this technique is utilized very little
today because of the threat that roving birds pose to the spread of avian
pathogens. Research over the last two decades has centered on the more highly destructive parasitoid and predatory species <PHOTO>. Examples, such as the encyrtid Tachinaephagus zealandicus Ashmead, five species of the pteromalid genus Muscidifurax, <PHOTO> and Spalangia sp. [for descriptions of parasitoids, please see <fly-par.htm> ]were evaluated for their capabilities of attacking dipterous larvae and pupae in various breeding sources <PHOTO>. They are believed to be capable of successful fly suppression if the right species and strains are applied in the right locality (Legner & Brydon 1966, Legner & Dietrick 1972, 1974; Morgan et al. 1975, 1977; Olton & Legner 1975, Pickens et al. 1975, Morgan & Patterson 1977, Rutz & Axtell 1979, Propp & Morgan 1985, Axtell & Rutz 1986, Legner 1988b, Mandeville et al. 1988, Pawson & Petersen 1988). Other approaches have included the use of pathogens and predatory mites, and inundative releases of parasitoids and predators (Ripa 1986). Although partially successful, none of these strategies have become the sole method for fly control, and the wrong choice of a parasitoid strain may have detrimental results (Legner 1988b). Instead, the focus is on integrated controls including other methods such as cultural, adult baiting and aerosol treatments with short residual insecticides. However, it is generally agreed that existing predatory complexes exert great influences on fly densities (Legner et al. 1975, 1980 |
