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BIOLOGICAL CONTROL OF
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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. In the latter 1900's
Dr. Alex Calhoun, Director of the California Department of Fish and Game
spearheaded projects to use African ciclid fish to control mosquitoes and
chironomid midges in California waterways that successfully reduced the use
of insecticides and herbicides that were in widespread use for control. However, a group of over zealous
environmentalists later were opposed
to the introductions even though thorough research by marine biologists had
found no adverse affects on long established fish species. Indeed, the imported ciclids by retreating
to marine estuaries in winter contributed to the food supply of ocean fish
species. The
mosquitofish,
Gambusia 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 have 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 reducing both the number of predators
and malathion applications without lowering efficacy could further refine the
procedure. 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 \, 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, 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
; Geden 1984, Geden et
al. 1987, 1988; Geden & Axtell 1988) and that many biological
control agents of endophilous flies have not been thoroughly surveyed, nor
their potential adequately assessed (Mullens 1986, Mullens et al.
1986).
Exophilic Flies.--These species include
flies that persist in nature in the absence of humans, but whose populations
can increase dramatically as a result of certain human activities such as
providing more breeding habitat. They include several species in the genera Calliphora, Hippelates, Musca, Muscina, Phaenicia, Stomoxys. Some success has been
recorded with the use of natural enemies against the calliphorid species in California
and Hawaii, but attempts elsewhere in the world have not been effective (Bay et
al. 1976). The braconid parasitoid Alysia
ridibunda Say, indigenous to parts of the United States, was
released into an area of Texas new to its range and successfully parasitized
the blowflies Phaenicia sericata (Meigen), and a Sarcophaga species. However, the
parasitoid did not maintain control and became rare within a couple of years
(Lindquist 1940). The gregarious parasitoid T.
zealandicus may have considerable potential for biological control of
exophilic flies (Olton & Legner 1975 ).
The range of habitats utilized by this natural enemy is considered
unparalleled by any other fly parasitoid. However, extensive work with this
genus, from the standpoint of field use, has not been given the this genus
has not been given much attention. But one species, Tachinaephagus
stomoxcida Subba-Rao, provides overall permanent reductions of
Stomoxys in Mauritius
(Greathead & Monty 1982). The complex of problems
that confront field programs in biological control of exophilic flies has
clearly had a dampening effect on research in this area. The unforseen
problems associated with attempts to biologically control the eye gnat, Hippelates collusor (Townsend), in
California exemplify those problems. In the early 1960s, a concerted effort
was mounted to control this gnat with the use of both indigenous and exotic
parasitoids in orchards in southern California. About a dozen species and
strains were evaluated for several years. Some of the exotics established,
but eye gnat reductions were obvious only where cultivation practices were
curtailed (Legner et al. 1966,
Legner 1970 ).
Cultivation of the orchards buried the larvae and pupae of the eye gnat below
the search zone of the parasitoids and cultivation also removed vegetation
that offered the parasitoids protection and possibly nutrients (Legner 1968,
Legner & Olton 1969
, Legner & Bay 1970).
Buried eye gnats emerged from several centimeters below the soil surface and
thus continued to pose a serious problem (Bay et al. 1976). The recent discovery of a
group of genes, called wary genes, in parasitoids of
synanthropic Diptera affords greater opportunities for biological control
(Legner 1987b,
1988a,
1989).
Inheritance of quantitative behavior associated with gregarious oviposition
and fecundity in the South American parasitoid Muscidifurax raptorellus
Kogan & Legner (Kogan & Legner 1970)
is accompanied by unique extra nuclear influences which cause changes in the
oviposition phenotypes of females prior to the production of their progeny
(Legner 1987a
, 1987b;
1988a ).
Males can change a female's oviposition phenotype upon mating, by
transferring an unknown substance (Legner 1987, 1988a,c). Some genes in the female
apparently have the phenotypic plasticity to change expression under the
influence of substances in the male seminal fluid. The intensity of this
response depends on the genetic composition of the male and female. Full
expression occurs in the F1 virgin female (Legner 1987a ,
1988a ).
The mated female receives a message from the male after mating that expresses
his genome for the presence or absence of polygenes governing quantitative
behavior, such as fecundity. The discovery of this behavior in M. raptorellus has opened
questions into the nature of polygenic loci. The ability of the male
substance to switch loci on or off in the female suggests active and inactive
states for such lock. Polygenic loci generally have been thought to be coded
for a fixed kind of expression (Wright 1986). Greater importance may be
placed on liberated males during mass release strategies that seek seasonally
to accelerate and increase the magnitude of parasitism, because it may be
possible to convey directly to unmated females already resident in the
environment certain desirable strain characteristics. In the process of
hybridization, wary genes may serve to quicken the pace of evolution by allowing
natural selection to begin to act in the parental generation (Legner 1987a ,
1988a
). Tabanidae, or horseflies, although widespread and on occasion serious
pests and vectors of disease to livestock, have not received much attention.
Only one successful inundative release of the egg parasitoid, Phanurus emersoni Girault,
has been recorded (Parman 1928). Apparently, this effort was precipitated by
a severe outbreak of anthrax at the time and since this disease diminished
and other control tactics are available, interest in their biological control
has not been fostered. Flies associated with
cattle droppings, symbovine flies (Povolny 1971), have
received the most attention for biological control over the last two decades.
The primary targets for control have been the bush fly, Musca vetustissima Walker,
the hornfly, Haematobia irritans (L.), and the facefly, Musca autumnalis DeGeer
(Wallace & Tyndale-Biscoe 1983, Ridsdill-Smith et al. 1986,
Ridsdill-Smith & Hayles 1987). The primary emphasis of control has been
on habitat destruction through the use of introduced dung-burying scarab
beetles. Biological control through dung destruction has been reviewed by
Legner (1986).
Although the introduction of dung beetles has clearly aided agriculture by
reducing operating costs and increasing grazing areas through dung removal,
it has not had a great impact on the densities of flies in any area. As there
are no practical non-biological control methods to reduce fly numbers, and
the addition of more scarabs may actually exacerbate the problem, it is
thought that the most logical direction for research is to intensify world
wide searches for more effective natural enemies, especially predators and
pathogens. A number of pathogens have
been isolated from various species of muscids and some studies have been
conducted evaluating their role as control agents. For example, the exotoxin
of Bacillus thuringiensis Berliner has been
shown to reduce fly production under certain conditions. However, only a few
of these agents appear to show great promise for manipulative use (Daoust
1983a,b; Mullens 1986, Mullens et al. 1987a,b,c). Wasps (yellow jackets) are
widespread pests in recreational areas and in urban environments, yet no
extended efforts to control them biologically has ever been made. However, African honeybees, or "killer bees" [see
<killer.htm>]
as they frequently are called, have invaded North America from South America
through Mexico. Their first appearance in south Texas in spring of 1991 was
accompanied by an increase in attacks on humans, and they have since become
widespread in California and Arizona by 1999 (Legner, unpub. data; Taylor
1985). A public health problem may be expected within a year of the invasion
as people become aware of these bees and succumb to their attacks. However,
studies on honeybee behavior at higher latitudes in South America suggest
that the public health threat is not as great as these bees' notoriety
(Taylor 1985). Nevertheless, mosquito abatement districts in California will
undoubtedly be called upon for information about how to deal with the bees
and perhaps to exterminate feral colonies. Most of the characteristics
that distinguish African bees from European bees, such as aggressiveness,
early-day mating times, degrees of pollen and honey hoarding, etc. are
thought to be quantitative and, therefore, under the control of polygenic
systems. Unfortunately, because of difficulties inherent in studying
quantitative traits in honeybees, knowledge of this phase of their genetics
is scant. In fact Taylor (1985) acknowledge that there is an overall limited
understanding of honeybee genetics. Thus, we really cannot predict what will
occur following hybridization of African and European races because
practically all opinions are derived from their behavior in South America
(Kerr et al. 1982, McDonnell 1984, Rinderer et al. 1982, 1984; Taylor 1985).
Perhaps some indications can be obtained from other groups of Hymenoptera. A great deal of information
about hymenopteran quantitative inheritances has been gathered recently from
parasitic wasps in the genus Muscidifurax
that attack synanthropic Diptera, as previously discussed. If similar systems
prevail in honeybees, greater importance could be placed on drones because it
may be possible for African or European drones to convey directly to unmated
queens of either race some of their own racial characteristics. The rapid
Africanization of European bee colonies in South and Central America could be
explained partly by this process, although early-day mating of African drones
has been considered primarily responsible (Taylor 1985). It is admittedly
presumptuous at this time to infer similarities in the genetics of genera Apis
and Muscidifurax, and
the presence of wary genes in both. Some speculation seems justified where
similarities might exist, however, especially as there is general agreement
that permanent control of Africanized bees will probably involve genetic
manipulation and mating biology (The Calif. Bee Times 1988). If present, wary
genes could offer a means to the abatement of this potentially severe public
health pest. However, the possible occurrence of similar hybridization events
in honeybees, as has been observed in Muscidifurax,
would dictate extreme caution in setting into motion any processes that might
lead to the formation of new races. Available means for identifying hybridized
colonies and extirpating Africanized queens (Page & Erickson 1985, Taylor
1985) are tedious and imperfect. With the understanding that hybridization
events and wary genes of the kind found in Muscidifurax have yet to be substantiated in Apis, the following suggestions for
African bee abatement are tentative. Deployment of Wary Genes
in Abatement.--Wary genes could be used
to induce in queen bees immediate behavioral changes such as a reduced dispersal
tendency, greater susceptibility to winter cold, lower fecundity, or even a
preference for subsequent matings to occur in the afternoon when European
drones are most active. Africanized queens that
mate with different races of European drones might exhibit immediate
postmating depression in some cases, as was reportedly in some species of Muscidifurax (Legner 1988d).
However, the offspring of crosses between African queens and certain races of
European drones might be expected to show heterosis, expressed as increased
fecundity and stamina, while other crosses involving different races of
European bees might produce a negative effect. Crosses between hybrid queens
and hybrid males could result in superactive queens after mating, following
by even more highly active progeny, as was observed M. raptorellus (Legner, unpub. data). Selection favoring the
superactive hybrids would tend to guarantee the survival of both parental
races and a continuous formation of hybrid bees, as has been suggested for Muscidifurax (Legner 1988b ).
Such a process could direct events leading to the relatively rapid evolution
of a new race. A superiorly adapted race might displace Africanized bees and
prevail in the area. Of course this race also would have to display desirable
characteristics of honey production, pollination, and no aggression to be
acceptable. Mating European queens with
races of drones from feral northern European populations might cause such
queens to acquire increased winter tolerance and give rise to hybrids that
have even greater tolerances. On the other hand, having drones available that
possess a reduced winter tolerance could increase winter kill. The selection of appropriate
populations for intraspecific crosses is critical to avoid detrimental
outcomes from negative heterosis, or hybrid dysgenesis, as well as
undesirable positive heterotic behavior, such as an increased aggressiveness.
Preintroduction assessments are essential to reveal such tendencies (Legner
1988b). The introduction of alien
alleles into a population by hybridization utilizing naturally evolved
parental populations would probably be less risky than introducing genetically
engineered ones where no natural selection has acted priorly. Researchers
working to inject laboratory engineered products into natural populations
should consider what kind of behavior will be demonstrated once heterosis has
had a chance to act. Unless the engineered populations can be completely
isolated reproductively from resident wild populations, there is considerable
risk involved. A lot of other
possibilities could be imagined. However, the first step should involve a
more thorough understanding of honeybee genetics, and whether or not enough
similarity exists with known hymenopteran systems to derive safe and viable
strategies. Certain aspects of genetics are as yet unclear in Hymenoptera,
which was demonstrated with the discovery of paternal influences in males
(Legner 1989d). However, there is a clear rationale for pre-introduction
assessments as presently advocated for parasitic Hymenoptera (Coppel &
Mertins 1977, Legner 1986a,
1986b). Berg (1975), Bay et al.
(1976), Garcia & Huffaker (1979) and McCullough (1981) have reviewed
developments in biological control of mainly freshwater snails, especially as
they relate to the transmission of trematode parasites of humans and their
domestic animals. Discussion here is restricted to some pertinent points of
those reviews and to some developments that have occurred since their
completion. Predators.--Many general predators,
including species of fish, frogs, birds and certain aquatic insects, consume
fresh water snails. Domestic ducks have been used with some success in China
by herding them through rice fields to forage for food. However, of all these
general predators, only certain tilapine fishes have been given research
consideration as possible biological control agents. Fish in the genera Oreochromis, Sarotherodon, and Tilapia feed directly on snails
during various stages of their life cycle. This occurs primarily because the
feeding behavior of these fishes is frequently in the vegetation or detrital
zone that is also utilized for feeding by snails. Larger adult species of Oreochromis and Sarotherodon feed directly on adult
snails, but this predation has not been observed for Tilapia adults. Tilapia only consume snails
incidentally during their normal foraging on plant materials (Roberts &
Sampson 1987). Possibly the greatest
impact of these fish on snail populations is through competition for
resources. Roberts & Sampson (1987) stated that generally Tilapia compete directly with the
snails that feed on higher plants while Oreochromis
competes with snails that feed on algae.
In addition to competition for food, these fish alter the habitat and
therefore have a disruptive effect on the snails' life cycle. Certain species of sciomyzid flies are probably the most host specific
predators of snails. Several hundred species have been described, the larvae
of which depend on mollusks for food. Of six species that were studied for
biological control, two successful introductions have been recorded and those
were the release of Sepedon macropus
Walker and Sepedon sauteri
Hendel into Hawaii to control the intermediate host of the giant liver fluke
of cattle. Success of these releases was apparently shown by a reduction in
liver infections at slaughter houses (Bay et al. 1976, Garcia
& Huffaker 1979). Berg (1973) emphasized that because there are several
hundred species in this family with a wide range of biological attributes,
they offer great opportunity for matching a certain sciomyzid with the
appropriate ecotype snail. Unfortunately the scope of opportunities for use
of these flies for snail control has not been given the attention it
deserves. Antagonists.--Another approach for
control of snails has been through interspecific competition. The large
predatory snail Marisa cornuarietis
L., has been evaluated rather extensively Puerto Rico and has been shown to
be effective for control of Biomphalaria
glabrata Say, the intermediate host of human schistosomiasis, in
certain habitats, especially ponds. Suppression of B. glabrata by Marisa
is primarily due to competitive feeding and to incidental predation on the
immature stages of this snail (McCullough 1981). In Africa M. cornuarietis
eliminates three species of pulmonate snails (Biomphalaria sp., Bulinis
sp., and Lymnaea sp.) in
a water impoundment in northern Tanzania. Prior to release of M. cornuarietis, three pulmonate species in addition to a
melaniid snail, Melanoides
sp., existed in large thriving populations. Two years after the introduction
only M. cornuarietis
and the melaniid snail remained, the latter in population densities similar
to preintroduction levels (Nguma et al. 1982). No adverse
environmental effect was recorded in this situation; however, the authors
stressed that a careful examination of potential environmental risks should
be made before introduction to a new area. Another competitor snail, Helisoma duryi (Wetherby),
has shown promise for the control of B.
glabrata. Christie et al. (1981) working with the
ram's horn snail, H. duryi,
showed that it controlled B.
glabrata in artificial outdoor drains on the Caribbean island of
St. Lucia. The elimination of B.
glabrata may have been due to inhibition of reproduction by adults
and possibly to increased mortality of immature snails. The time required for
elimination was related to environmental temperature and the number of H. duryi initially released.
In Africa Madsen (1983) surveyed H.
duryi as an introduced species in an irrigation scheme in northern
Tanzania and found it restricted to just a few drains 10 years after it had
been established in the area. He noted that its failure to spread may have
been related to the routine molluscacide applications to the irrigation canal
system. Moens (1980, 1982) achieved
successful biological control of Lymnaea
truncatula Muller, an intermediate host of the trematode, Fasciola hepatica L. in
watercress in Belgium, with the predatory snail, Zonitoides nitidus Muller. Predation
was related to temperature, soil moisture and cover. It is obvious that the role
of biological control of snails as intermediate hosts of human diseases is
limited. As McCullough (1981) pointed out, it will be restricted to specific
situations and will rarely, if at all, have widespread applicability. In
addition it will play only a supportive role in almost all geographic areas
where schistosomiasis and other snail transmitted diseases exist. However,
this does not mean that biological control is not important. Indeed, any
method that reduces transmission of a disease in a self-sustaining fashion is
of major benefit. REFERENCES: [Please see <medvet.ref.htm>: [Additional references may be
found at MELVYL Library ] |
