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Introduction Elzen & King (1999) discussed the manipulation of
natural enemies for enhanced biological control. The successes in classical
biological control have provided the background and encouragement for efforts
in the manipulation of natural enemies. Such manipulations include
conservation, augmentation, habitat management and genetic manipulation.
During the 1980's there has been increased emphasis on the use of
semiochemicals to manipulate natural enemies, especially Hymenoptera
(Nordlund et al. 1981a). Also, insecticides are being stressed that minimize
direct toxic and sublethal effects to beneficial insects. The use of
biological control together with insecticides is encouraging. The enhancement of entomophage effectiveness has been
reviewed in various ways by Ridgway & Vinson (1977) and Ables &
Ridgway (1981). Propagation and release of entomophagous arthropods for use
in augmentation was discussed by King et al. (1984) and this practice in the
United States was reviewed by King et al. (1985a). Additionally the behavior
of liberated parasitoids and predators was discussed by Weseloh (1984). Lewis
& Nordlund (1985) stressed the importance of insect behavior in order to
enhance natural enemy effectiveness. Literature on semiochemicals was
discussed by Nordlund et al. (1981a,b; 1985) and Vinson (1975). Habitat
manipulation to enhance parasitoid activity was reviewed by Powell (1986). Entomophages may be potentially manipulated in many ways.
The concepts of inundative and inoculative releases were first mentioned by
DeBach & Hagen (1964). Inundative releases rely mainly on the agents
released, not their progeny, whereas inoculative releases rely upon a buildup
of the initial parasitoid populations so that immediate control is followed
by additional control wrought by progeny (Li 1984). Augmentative releases
have been described as supplemental releases, strategic releases, programmed
releases, seasonal colonization, periodic colonization and compensatory
releases (Ridgway et al. 1977, King et al. 1984, King et al. 1985a). Elzen
& King (1999) give examples demonstrating the feasibility of controlling
pests by augmentative releases of entomophages. Individual case studies were
presented by King et al. (1985a). Manipulation refers to those procedures that help the establishment
and activity of natural enemies. Manipulation of a natural enemy or its
environment may be justified if a definite need exists and a reasonable
assurance of success is possible. Certain factors associated with the habitat,
the host, or the natural enemy itself may render an
entomophagous organism ineffective as a biological control agent, but still
be subject to manipulation. The habitat may have certain adverse climatic factors,
such as heat, cold, low humidity or wind. Unattractive or otherwise
unsuitable host plants may be present, or there may be a scarcity of food or
water for adult natural enemies. Interspecific competition among natural
enemies. Pesticides may be present, or cultural practices may not favor
natural enemy activity. The host may lack synchronization with parasitoid
generations, or host plant resistance may not provide for hosts during
critical times. There may be host strains resistant to natural enemy attack,
or there may be periodic scarcities of suitable host stages. The natural enemy may exhibit an annual ovarian diapause
and migrate away from its hosts at certain times of the year (e.g.,
Coccinellidae), or its reproductive rate may be too low. It may exhibit an
adverse tendency to disperse, coupled with an inability to find mates at the
resulting low densities. Generally, manipulation of a natural enemy should only be
attempted if it involves some periodically occurring, unfavorable
environmental factor, a lack of some easily supplied requisite, or some
simple or minor, but correctable, intrinsic shortcoming. Manipulative Methods Employed Periodic
Colonization involves periodic releases of mass-produced or
field-collected natural enemies. Two types are inundative releases and
inoculative releases. The first type, inundation, has largely been employed
against the egg stage of univoltine pests. Control is largely the work of the
insects released, not their progeny. It has been called a biotic insecticide since host mortality is
more or less immediate, and there is no prolonged interaction between host
and natural enemy populations. This method is best employed against pests of
high value crops, against univoltine pests, or against multivoltine pests
that reach injurious levels during but one generation annually. The second, inoculation, is where the interaction between
host and natural enemy populations persists through more than one generation
of the natural enemy, and control is largely effected by the progeny of the
beneficial forms released. Inoculative releases may take the form of accretive
releases where small numbers of natural enemies are periodically released
against low density pest populations. Entomophagous insects and their pest
hosts may also be colonized concurrently in areas with a known history of
pest invasions or where hosts are too scarce to support natural enemies, this
in anticipation of pest invasions (e.g., Cryptolaemus
on citrus mealybugs in California). Selective
Breeding is not a practical method to date, but offers a
challenging field for research. Environmental
Manipulation may supply artificial structures which serve as shelters
or as nesting sites for natural enemies. Supplemental food for adult natural
enemies may be supplied. Alternate hosts may be supplied for beneficial
insects or their phytophagous hosts may be offered alternate host plants.
Artificially supplying suitable host stages when these are unavailable in the
field, and eliminating honeydew-feeding ants may also be effective. The
habitat may be modified to eliminate or reduce the adverse effects of
cultural practices, pesticides, dust deposits, etc. FURTHER DETAILS OF ENHANCING IMPACT Various examples in DeBach (1963) and Rabb (1962) describe
how the construction of nesting shelters encouraged high local populations of
Polistes wasps in cotton
fields in the West Indies and in tobacco fields in North Carolina, increasing
the total predation of injurious lepidopterous larvae. Nesting boxes provided for insectivorous birds in some intensively
managed European forests also resulted in increased predator densities and
protection from defoliating insects. Many adult natural enemies utilize
exudates from floral or extra-floral nectaries, as well as pollen, as sources
of nutrients and water. The culture or conservation of plant food sources in
the proximity of cropland and orchards has been found to enhance the
effectiveness of various natural enemies. Pollen is known to be an important
supplementary food for adult, aphid-feeding Syrphidae and Coccinellidae as
well as certain predacious mites. The long-practiced method of clean
cultivation for weed control may be undesirable from the standpoint
of removing wild plants infested with honeydew-producing insects or
containing nectaries. Colonization of alternative insect hosts may improve
synchronization between a pest and its natural enemies. Several benefits that
may be derived from this technique are: (1) the damping of extreme
oscillations in natural enemy and host population densities; (2) maintaining
functional natural enemy populations by providing a continuous food supply
during periods of low pest densities; (3) providing suitable overwintering
hosts; (4) promoting maximum distribution of the natural enemy; and (5)
reducing intra- and interspecific competition among natural enemies
(cannibalism and combat). Modifications of adverse cultural practices can improve
natural control because cultivation may kill soil-inhabiting beneficial
insects or pupating, non-subterranean natural enemies. Reduced or delayed
cultivation may reduce this mortality and also dust. Dust is especially known
to harm parasitoids and predators; it can be minimized by sprinkling, by
planting cover crops, by paving access roads or by holding cultivation to a
minimum. Properly timed irrigation may promote epidemics of fungal pathogens
of insect pests by providing the proper conditions of humidity in the
microenvironment. Improperly timed irrigation, on the other hand, may drown
or drive away beneficial insects. Trichogramma spp. have been extensively researched for inundation since
Flanders (1930) suggested that they offer a possible alternative to
insecticides. Comprehensive reviews on the use of Trichogramma were presented by Ridgway & Vinson
(1977), Ridgway et al. (1977) for use in the Western Hemisphere, by Huffaker
(1977) for China, by Belyarov & Smetnik (1977) for the Soviet Union, and
for augmentation in cotton by King et al. (1985). By 1985 Trichogramma spp. were the most
widely used entomophages for augmentation (King et al. 1985). Lepidopterous
pest control by mass rearing and release of Trichogramma spp. has carried out for many decades. The
pioneering research of Howard & Fiske (1911) and Flanders (1929, 1930) in
the United States stimulated research with Trichogramma spp. worldwide, and a number of successes in
reducing insect populations by augmentation with Trichogramma have been reported. Hassan (1982) and Bigler
(1983, 1984) reported 65-93% reduction in larval infestations of the European
corn borer following Trichogramma
releases during the 1970's in Germany and Switzerland. Voronin and Grinbert
(1981) reported positive reductions of pest such as Loxostege spp, Agrotis
spp., and Ostrinia species
following Trichogramma
releases. In China a significant reduction in populations were reported for Ostrinia spp., Heliothis spp. and Cnaphalocrocis spp., crop damage
being reduced (Li 1984). Oatman & Platner (1985) found that two common
lepidopterous pests of avocado in southern California, Amorbia cuneana
Walsingham and the omnivorous looper, Sabulodes
aegrotata (Guenée), could be
effectively controlled by liberations of 50,000 Trichogramma platneri
in each of four uniformly spaced trees per acre. At least three weekly
releases were required for control of S.
aegrotata, while two were
necessary for A. cuneana. Considerable success has been achieved in California with
the periodic introduction of cichlid fish and some invertebrate predators of
mosquitoes and midges in connection with biological control of aquatic weeds
and pestiferous insects [ Please refer to Research #1, #2, #3 ] Hassan (1982) obtained 65-93% reduction in larval
infestations of Ostrinia nubialis (Hübner) after four
years of releases in Germany. Reduction in insect density and crop damage in
several agroecosystems was also reported from China and the Soviet Union (Li
1982, Voronin & Grinberg 1981). Oatman & Planter (1971, 1978)
demonstrated the feasibility of augmenting Trichogramma pretiosum
to reduce damage in tomatoes caused by the tomato fruitworm, cabbage looper
and Manduca spp., although
they found that chemical control was also necessary for pests not susceptible
to T. pretiosum. Oatman et al. (1983) reported on an integrated
control program for the tomato fruitworm and other lepidopterous pests on
summer plantings of fresh market tomatoes in southern California in
1978-1979. Twice weekly applications of DipelR (delta-endotoxin of
Bacillus thuringiensis Berlinger var. kurstaki), plus twice weekly
releases of T. pretiosum, was compared with
weekly applications of methomyl. There were no significant differences in
fruit yield or size between the two control regimes. Methomyl adversely
affected predator populations, host eggs, and egg parasitization by T. pretiosum, whereas Dipel did not. In The Netherlands, Trichogramma
spp. have been utilized to develop biological control of Lepidoptera. Two
approaches there were (1) the selection of the best species and strains of Trichogramma (van Lenteren et al.
1982) and studies of the manipulation of Trichogramma
behavior. The first approach has been studied extensively, especially in Brassica spp. Inundative
releases of Trichogramma
were feasible for control of Mamestra
brassica on Brussels
sprouts, but control was not very effective at low host densities (van der
Schaaf et al.a 1984). Glas et al. (1981) reported reduction in larval
infestations of Plutella xylostella in cabbage crops.
Van Heinigen et al. (1985) summarized several years of work with Trichogramma releases. The
second approach (2) to Trichogramma
manipulation in The Netherlands involved examination of semiochemical
mediated behavior. These studies indicated that kairomones and volatile
substances released by adult female hosts (sex pheromones) were important in
foraging behavior of Trichogramma
(Noldus & van Lenteren 1983, Nodlus et al. 1986, 1987). Preintroductory
evaluation using the methods outlined by Wackers et al. (1987) may improve
prospects for augmentative release of specific strains of Trichogramma in The
Netherlands. It is evident that control can occur through augmentation
with Trichogramma spp. under
certain conditions. However, there have been variable results and cases of
insufficient pest control reported (King et al. 1985b). Trichogramma pretiosum
was tested in augmentative releases in Arkansas in 1981-82 and in North
Carolina in 1983 for management of H.
zea and H. virescens
in cotton. These releases failed to provide adequate control in 1981-82, but
in 1983 cotton fields treated by seven augmentative releases of T. pretiosum at 306,000 emerged adults/ha./release yielded
significantly more cotton than control fields which were not treated with
insecticides. Insecticidal control fields yielded more cotton than did
control of T. pretiosum release fields, which
led these researchers to conclude that management of Heliothis spp. in cotton by augmentative releases with
this parasitoid was not economically feasible (King et al. 1985b). However,
the greater yields obtained in North Carolina in 1983 in the T. pretiosum release fields supported the use of Trichogramma spp. In order to obtain consistent results, large numbers of Trichogramma spp. should be
released. However, in addition the effectiveness of Trichogramma may certainly be influenced by such factors
as, (1) the density and/or phenology of the pest, (2) the species or strain
of Trichogramma, (3) vigor
of the parasitoids, (4) method of distribution, (5) crop phenology, (6)
number of other natural control agents present, and (7) the proximity to
crops receiving insecticides and drift of insecticides into Trichogramma release fields
(King et al. 1985b). Trichogramma
spp. seem highly susceptible to most chemical insecticides, with lethal
effects resulting from direct exposure to spray applications, drift or
posttreatment contact with pesticide residues on foliage (Bull & Coleman
1985). It has been suggested that the inconsistent results in Arkansas and
North Carolina was due to chemical insecticides (King et al. 1985b). In order to effectively manipulate entomophages there must
be a thorough knowledge of the biology and host associations of the
organisms. Although such information may be gained through laboratory
studies, it is necessary that such data be followed by studies in the field.
Ideally a comparison of laboratory, field cage and field studies can provide
useful information which could be used to predict the impact of the natural
enemy on pest populations. In augmentation programs, the level of control achieved
may be influenced by many interacting factors. Primary factors include the
availability of hosts and host/parasitoid synchrony; conditions of weather
during release of entomophages, including the effect of environmental factors
on foraging; influence of habitat type; chemical pesticide usage, either
concurrent or not or adjacent; the fitness of laboratory reared parasitoids.
The use of augmentative releases is very complex, and the environmental
effects acting on released entomophages may be highly variable. Therefore,
studies must be planned that will be used to predict when and under which
specific situations biological control by augmentation may work. For example,
Microplitis croceipes (Cresson) efficiency
appears to be greater during summer on agricultural crops than in spring on
wild host plants. Fewer M. croceipes adult females were
required in a summer study as compared to an early spring study to achieve
comparable control of tobacco budworm in field cage experiments. All
parameters, biotic and abiotic should be explored in evaluating augmentation
release results. Augmentation of entomophages of row crop pests may be
implemented only after considerable effort has been expended to prove the
feasibility of this approach. Therefore, the efficiency and financial
benefits must be determined. Reliance on entomophages to control pests should
be limited to those situations where scientifically, environmentally and
economically sound procedures are available. Theory predicts that predator/parasitoid effectiveness can
be increased through propagation and liberation. Host/entomophage
interactions must be thoroughly studied, however before any program can be
relied upon. Such interactions may be assessed through studying the
functional response of the predator/parasitoid to host density and how this
relates to dispersal of the organism. Field evaluations must provide the data
necessary for defining the number of entomophages required for release per
unit area, and this together with mass production technology determines the
economic feasibility of the approach. Such fundamental knowledge as searching
rate, functional response, and efficiency could significantly add to the
predictability of success in augmentation efforts. Flight Chambers are useful tools for examining flight responses and
foraging patterns of parasitoids. Most designs presently in use are similar
to the wind tunnel of Miller & Roelofs (1978), which was used to study
moth flight. Nettles (1979, 1980) did a lot of work with the wind tunnel
flight responses of parasitoids in studies of Eucelatoria spp. These examined response of the parasitoid
to volatiles from the host and host habitat, and suggestions were made
regarding the use of Eucelatoria
attractants to increase parasitoid populations in the vicinity of Heliothis hosts. Drost et al.
(1986) examined the flight behavior mediated by airborne semiochemicals in M. croceipes and emphasized the importance of preflight
conditioning to the plant-host complex on positive searching responses of M. croceipes. Other research showed the M. croceipes
reared on hosts fed cowpea seedling leaves instead of artificial diet had an
increased percentage of oriented flights to odors of a cowpea seedling--H. zea complex in a flight tunnel. The increased response was
much stronger after adult females had searched a fresh host plant complex
(Drost et al. 1988). Elzen et al. (1986) evaluated the effects of cotton, Gossypium spp., cultivars and
species on the flight responses of Campoletis
sonorensis (Cameron) in a
study which found higher innate searching on glanded versus glandless
varieties. It was implied that volatile chemicals present in the glanded
varieties had a positive effect on parasitoid foraging in the wind tunnel
that was not produced by glandless cottons or Old World species.
Additionally, Elzen et al. (1987a) found strong innate responses by M. croceipes to cotton and further suggested that the
parasitoid responses represented fixed action patterns. Herard et al. (1988a)
conducted experiments with M.
demolitor which were similar
to those of Drost et al. (1986). Herard et al. (1988b) also described rearing
methods suitable for semiochemical studies. The wind tunnel flight chamber
has been further refined with the development of a novel system for injection
of semiochemical volatiles directly into the moving air (Zanen et al. in
press). Wind tunnels may aid in efforts to solve the mysteries of parasitoid
host habitat location and host location and provide insights which may allow
manipulation of parasitoid behavior. Wind tunnels are also ideal for the
early isolation of semiochemicals and for use in bioassay directed
fractionation and confirmation of synthetic chemical activity. Of course, laboratory assessments of entomophages must be
supported by field experiments. For example, field surveys have shown that
parasitization of Heliothis
spp. larvae varies greatly in space and time (Lewis & brazzel 1968,
Graham et al. 1972, Roach 1975, 1976; Smith et al. 1976, Burleigh &
Farmer 1978, Puterka et al. 1985, King et al. 1985). A summary of suggested
methods and steps in manipulation of semiochemical-mediated foraging behavior
is given in Nordlund et al. (1981a). Parasitization can vary spatially
due to variation in parasitoid host plant detection, search rate, or
retention of parasitoids on host plants. Host plant species and stage, host
density and weather are likely to affect all three processes. Parasitization
can vary temporally because of variation in host detection, searching,
retention, parasitoid natality or mortality. Research designed to gather
information to predict distribution of parasitization across host plants
under varying conditions could yield important information on the population
dynamics of hosts and parasitoids. These predictions are crucial to rational
conservation and augmentation of parasitoids. For example, the search rate of
M. croceipes in field cages was higher on Gossypium hirsutum L. in summer than on Geranium dissectum
L. in spring (Hopper & King 1986). However, this difference may arise
from different temperatures and not from different host plant species. In
field cages M. croceipes parasitized more
hosts on G. hirsutum than on Phaseolus vulgaris and more hosts on P. vulgaris
than on Lycopersicon esculentum (Mueller 1983).
However, it is unclear if these differences arose from differences in host
plant attraction or from differences in search rate. In field cage
experiments it was found that M.
croceipes parasitized a
significantly lower proportion of H.
virescens larvae on Geranium dissectum than on either Trifolium incarnatum
or Vicia villosa . The attraction of Compoletis sonorensis varies with host plant species (Elzen et al.
1983) cotton variety (Elzen et al. 1986), and the attraction to cotton
correlated with volatile chemical profile of the varieties (Elzen et al.
1984, 1985). The host plant species on which H. zea
has been feeding affects the response of M.
croceipes to nonvolatile kairomones
from its host. These data suggest that variation in parasitization found in
host plant surveys may arise from variation in attraction or retention of
wasps by semiochemicals directly or indirectly derived from the host plants.
Studies of host habitat preference may provide clues to the best habitat in
which to release parasitoids in augmentation. The effects of kairomones on
searching of pink bollworm parasitoids were studied by Chiri & Legner (1983, 1986), but no
effective means of deploying these chemicals for enhanced biological control
was found. In fact, their application may actually reduce parasitoid
effectiveness by confusion. Screening of the biological characteristics of entomophages has
been advocated (Sabelis & Dicke 1985, van Lenteren 1986). An example of a
predator currently used in IPM in Dutch orchards is Typhlodromus pyri
Scheuten. As note by Dicke (1988) despite the use of this predator, its
biology has not been thoroughly studied. Based on its response to volatile
kairomones it was later determined that T.
pyri prefers the European
red spider mite, Panonychus ulmi (Koch) to the apple rust
mite, Aculuc schlechtendali (Nalepa), which
was confirmed by electrophoretic diet analysis (Dicke & Dejong 1988). Field experiments may also provide insights into the
efficiency of a particular entomophage. For example, in field cages
containing Gossypium hirsutum or G. dissectum, M.
croceipes searching rate for
Heliothis zea and H. virescens
larvae did not depend on host density (Hopper & King 1986). In field
experiments on G. hirsutum, M. croceipes
parasitized a higher proportion of Heliothis
larvae in plots where host density was higher. Also, parasitoid aggregation
but not increased searching rate, caused the increased parasitization at high
host density which supports the linear functional response reported by Hopper
& King (1986). Some parasitoids have been shown to aggregate in areas of
high host density in laboratory experiments (Legner 1969, Hassell 1971,
Murdie & Hassell 1973, T-Hart et al. 1978, Collins et al. 1981, Waage
1983). Since host plant species vary in attraction and suitability for Heliothis, which can cause
variation in larval density, the spatial variations in Heliothis parasitization observed in field surveys may in
part result from parasitoid aggregation at high host densities. Several
parasitoid species are more attracted to plants on which hosts have fed than
to undamaged plants (Thorpe & Caudle 1938, Monteith 1955, 1964, Arthur
1962, Madden 1970< and mechanically damaged plants increase parasitoid
searching (Vinson 1975). Damaged terminals of G. hirsutum
attract more C. sonorensis than do undamaged terminals
(Elzen et al. 1983). Microplitis
croceipes is attracted to
wind borne odor of H. virescens frass and larvae
(Elzen et al. 1987), and M. croceipes responds to
nonvolatile kairomones produced by H.
zea (Jones et al. 1971,
Gross et al. 1975), H. virescens, and H. subflexa (Lewis & Jones 1971). Luck et al. (1988) suggested criteria for evaluating entomophages that are scheduled
for introduction. Experimental evaluation through life table analysis,
examination of percent parasitization, key factor analysis, and the use of
simulation models, may provide insights into the probability of success in
augmentation. Evaluation of entomophages may include introduction and
augmentation, and techniques using cages and barriers, removal of
entomophages, prey enrichment, direct observation and biochemical evidence of
entomophage feeding, and quantified experiments to gauge the impact of the
entomophages. Entomophages may be ineffective due to a lack of host
synchrony, temporal displacement in ephemeral systems, lack of protected
sites, lack of alternate hosts, adverse environmental conditions or influence
of pesticides, etc. Temporal synchrony between entomophage and pest, and
oscillations in populations have been documented by Varley & Gradwell (1974).
The influence of weather on parasitoid searching has, however, received
little attention. Often when natural control is not achieved it is due to the
lack of synchrony of entomophage and host in time. These complex
relationships make intervention at any one level difficult and less likely to
produce desirable results. An understanding of the effects of the pesticide component
is important (Croft & Brown 1975). Pesticide resistance in entomophages
was discussed by Croft & Morse (1979), and recommendations for changing
control practices to preserve entomophages were listed. Insecticide use in
cotton and the value of predators and parasitoids for managing Heliothis was reviewed by King
(1986), and results on Pectinophora
gossypiella were given by
Legner & Medved (1979 , 1981 ). The detrimental effects of pesticides on entomophages are
well documented, and it may be important to note that an underlying problem
in practical implementation of augmentation is the use of pesticides.
Unexpected problems may be encountered, even from pesticide drift, so that
basic toxicological studies may be required to determine if the entomophages
intended for use in augmentation have some degree of tolerance to the effects
of insecticides, especially as resurgence of primary and secondary insect
pests has been documented in some heavily sprayed monocultures (Huffaker
1971). Actions of insecticides on entomophages include not only those causing
direct mortality, but also those that act in indirect ways, or that alter
entomophage biology adversely. First and foremost, there are the obvious
direct lethal actions of broad spectrum insecticides, such as
organophosphates, on entomophages. Because entomophages have more specific
enzymes evolved for handling the toxins of their hosts they are much more
susceptible to broad spectrum insecticides than their hosts which have an
array of plant chemicals with which to contend (Krieger et al. 1971). The
occurrence of primary pest release and resurgence of a previously innocuous
secondary pest have been widely reported where insecticides selectively
destroy entomophages (DeBach & Bartlett 1951, Michelbacher et al. 1946,
Doutt 1984, Lingren & Ridgway 1967). For example, azinphosmethyl, a broad
spectrum organophosphate, selectively destroys entomophages in apple orchards
(Falcon 1971). On the other hand, chlordimeform was found less toxic than
some other insecticides to several species of entomophages (Platt &
Vinson 1977, Platt & Bull 1978). Sometimes insecticides do not kill entomophages, but they
may so affect them that normal behavior or reproduction is encumbered. Press et al. (1981) found the
permethrin and pyrethrin reduced the number of adult Bracon hebetor
Say produced when parental females were exposed to hosts and insecticides
simultaneously. Topical application of carbaryl on adult female Bracon hebetor results in reduced numbers of eggs that develop
from vitellogenic oocytes, and resorption of mature ova (Grosch 1975).
Residues of pyrethrin significantly reduce parasitization rates of T. pretiosum (Riley) on H.
zea eggs (Jacobs et al.
1984). Formamidines are especially recognized for their ability to disrupt
pest mating, reproductive and feeding behavior (Knowles 1982, O'Brien et al.
1985). Whether or not these compounds have such effects upon entomophages is
not well known. Parasitized hosts have been found to be more susceptible to
insecticides than nonparasitized hosts, thus preventing normal development of
immature parasitoids. Lymantria
dispar (L.) larvae
parasitized by Apanteles melanoscelus (Ratzburg) are
significantly more susceptible to carbaryl than nonparasitized larvae, and
more time is required for surviving parasitoids to develop (Ahmad & Forgash
1976). Fix & Platt (1983) found that H.
virescens larvae parasitized
by C. nigriceps are 1.42X more susceptible to methyl parathion,
and 2.5X more susceptible to permethrin than are treated unparasitized
larvae. These cases show how insecticides can have an additional, indirect
action on entomophages. Entomophage abundance may also be reduced when their hosts have been
decimated by insecticides. This was the case of the predator Orius insidiosus (Say) feeding on the cotton leaf perforator Bacculatrix thruberiella Bush in cotton
treated with chlordimeform. Numbers of O.
insidiosus steadily declined
when populations of the leaf perforator was reduced by chlordimeform sprays
(Lingren & Wolfenbarger 1976). Direct mortality is the most severe way
that insecticides can impact, chlordimeform may become important in certain
pest management strategies, due to the property of controlling pests
behaviorally and physiologically at low sublethal doses. Lo doses of
chlordimeform significantly decrease fecundity and egg viability of adult
female tobacco bollworms, and prevent moths from separating after mating
(Phillips 1971). Although chlordimeform decreased the number of eggs laid by
Lepidoptera, it is not clear whether reduced fecundity was caused by
interference with ovarian development or with oviposition behavior
(Hollingworth & Lund 1982). Chlordimeform also reduces fecundity in the
cotton aphid, Aphis gossypii Glover (Ikeyama &
Maekawa 1973) and in the cattle tick, Boophilus
microplus (Masingh &
Rawlins 1979). Feeding behavior is upset by chlordimeform in larval tobacco
cutworms, Spodoptera litura F. (Antoniosus &
Saito 1981), armyworm, Leucania
separata Walker (Watanabe
& Fukami 1977) and in cockroaches, Periplaneta
americana L. (Matsumura
& Beeman 1982). But the effects of chlordimeform vary with species and
there is much selectivity between species and stages for actual acute
toxicity; some insects are very sensitive and others are immune, as in the
case of adult boll weevils (Wolfenbarger et al. 1973). Additional evidence
for the suitability of chlordimeform for some pest management strategies is
given by Platt & Vinson (1977), who found that chlordimeform is ca. 100X
less toxic to the parasitoid C.
sonorensis than
organophosphates similar to azinphosmethyl. By controlling pests at sublethal
doses, the problem of pest resistance may be lessened. Dittrich (1966) found
that chlordimeform is effective against some pests that have already become
resistant to organophosphate and carbamate insecticides. The work with Trichogramma
augmentation may provide clues for other species of entomophages. From
1981-83 King et al. (1985) collected Heliothis
larvae from insecticide treated and untreated cotton fields and found 1/3rd
of the larvae were parasitized, particularly by the braconid M. croceipes. These levels of parasitism of M. croceopes were greater than any reported in cotton since
the advent of organochlorine insecticides in the 1940's (King 1986). As M. croceipes has been commonly found in cotton in the SE
United States (King et al. 1985) and due to the apparent tolerance of this
parasitoid to some commonly used insecticides (King et al. 1985, Powell et
al. 1986, Bull et al. 1987), augmentation releases of the parasitoid are
anticipated in the future (King 1984). This parasitoid was recently exposed
to insecticides commonly used in cotton using a spray tower (Elzen et al.
1987b). Direct treatment with the pyrethroid fenvalerate, a mixture of the
formamidine chlordimeform plus fenvalerate, and the carbamate thiodicarb resulted
in nearly 100% survival of both sexes at both the lowest and highest field
rates recommended for these insecticides. The organophosphate acephate and
the carbamate methomyl were extremely toxic to adult M. croceipes,
causing 100% mortality at the lowest recommended field rates. Marking studies have shown that lady beetles, lacewings, syrphid
flies and parasitic wasps fed on nectar or pollen provided by borders of
flowering plants around farms. Many insects were shown to have moved 250 ft.
into adjacent field crops. The use of elemental marker rubium also showed
that syrphid flies, parasitic wasps and lacewings fed on flowering cover
crops in orchards and that some moved 6 ft. high in the tree canopy and 100
fleet away from the treated area. The use of nectar or pollen by beneficial
insects helps them to survive and reproduce. Thus, planting flowering plants
and perennial grasses around farms may lead to better biological control of
pests in nearby crops (Long et al. 1998). The
effectiveness of resident
insect predators as biological control agents of peach twig borer was tested
in a series of field experiments. It was shown that the native gray ant, Formica
aerata was the most common and effective generalist predator. Treatments
with native gray ant present had significantly lower peach twig borer
abundance and peach shoot damage. Ant population densities were studied in
seven commercial orchards. However, results showed that although this ant is
found in most peach and nectarine orchards, its abundance was not clearly
associated with any single cultural practice and may be difficult to
manipulate (Daane & Dlott 1998). Spray tower treatment of Microplitis croceipes
with insecticides applied directly to the insects was followed in another
study by exposure of parasitoids to plants which were sprayed in the spray
tower. Parasitoids were then caged on these plants and mortality observed
after 24 hrs. The fenvalerate/chlordimeform mixture caused 10-23% mortality,
with thiodicarb causing a similar percent mortality, whereas methomyl caused
significantly high mortality, ranging from 23-70%. It is probable that the
use of thiodicarb as an ovicide and larvicide for Heliothis control will increase in the future because of
resistance to pyrethroids, and fortunately M. croceipes
seems relatively tolerant to this insecticide. Useful information for models to predict the impact of
entomophages on reducing herbivore induced damage or plant stress is obtained
by monitoring and sampling entomophages that are indigenous or released by
augmentation. Modelling of population interactions requires accurate tools to
determine absolute densities of entomophages and pests. Monitoring
entomophage populations, particularly parasitoids, may be complicated by
factors such as lack of a stable sex ratio, movement (females must forage for
often patchily distributed hosts), weather, and lack of synchrony with host
populations. However, monitoring methods to evaluate parasitoid populations
have been suggested. The most reasonable approach to this problem would
involve estimating population numbers from captures of males or females in
traps baited with an appropriate attractant, such as sex pheromone. Powell
(1986) suggested that monitoring systems be explored using some volatile host
or host habitat attractant to trap female arthropods, thereby capturing the
agent responsible for doing the parasitizing, and perhaps obviating any
problems which may arise from an unstable sex ratio. There has been no system developed whereby a parasitoid
can be monitored with sex pheromone for decision making in an agricultural
crop. Although much effort has been expended in the field of insect sex
pheromones, few studies have resulted in identification of parasitoid sex
pheromones. Robacker & Hendry (1977) identified neral and geranial from
female Itoplectis conquisitor (Say), and
demonstrated that these chemicals were attractive to males in the laboratory.
Eller et al. (1984) identified and demonstrated the field effectiveness of
ethyl palmitoleate, a female sex pheromone of Syndipnus rubiginosus
Walley, a parasitoid of the yellowheaded spruce sawfly, Pikonema alaskensis
(Rohwer). Powell & King (1984) showed that males of M. croceipes were attracted to virgin females in the field,
and diurnal activity of males and females was
found to differ. From these observations it was believed that knowledge of
parasitoid activity periods would be important in developing techniques for
sampling parasitoid populations in the field. Subsequently it was determined
that SentryR wing traps (Albany International) were more effecting
in capturing M. croceipes males than were
Pherocon II traps (Zoecon). Studies in unsprayed cotton in 1984 revealed that
wing traps baited with living virgin females could be used to estimate
parasitoid populations, and recently M.
croceipes mating behavior
and sex pheromone response were reported by Elzen & Powell (1988), and a
tentative identification of the female-produced sex pheromone has been made. Control guidelines often recognize the impact of
entomophage populations on pest populations (Rude 1984). But, explicit
instructions for using entomophages in decision making are lacking, and where
present are used with reservation. Two exceptions are Michelbacher &
Smith (1943) who recommended that insecticide control decisions in alfalfa
for Colias eurytheme Boisduval be made
only after determining that the number of Apanteles
medicaginis Muesebeck
present was capable of maintaining the pest under control and Croft (1975)
reported on a decision making index for predicting the probability of
adequate control of a phytophagous mite that would occur depending ont the
predator/prey ratio per apple leaf. Vertebrates & invertebrates used in pest aquatic
insect control are more easily monitored because of their size and
confinement [ Please refer to Research #1, #2, #3 ]. Pheromone traps baited with living virgin females attracted large numbers
of male cereal aphid parasitoids when placed in cereal fields (Powell &
Zhang 1983). Aphidius rhapalosiphi DeStef and Praon volure Haliday males were caught in separate traps baited
with females. Monitoring may be useful in this situation to achieve maximum
impact when the parasitoid/aphid ratio is particularly high, especially early
in the season (Powell 1986). Methods for isolating sex pheromones (Golub
& Weatherston 1984), as well as bioassay directed fractionation,
identification (Heath 7 Tumlinson 1984), and synthesis (Sonnet 1984) are
detailed. These methods are adaptable for identification of parasitoid
pheromones (Elzen & Powell 1988). Entomophage culture is treated extensively in a different
section , as previously discussed. It is obvious that efficient and cost
effective methods of rearing entomophages must be developed if augmentative
releases are to be feasible. Large numbers of beneficial insects may be
employed in greenhouses, field cages and laboratory studies. Thousands of
entomophages available at unpredictable times, may be required for commercial
augmentation. Considerable attention has been devoted to development of
techniques to produce quality entomophages in large numbers (King &
Leppla 1984). The genetic implications of long term laboratory rearing of
insects are vast (Bouletreau 1986, Mackauer 1976). Powell & Hartley
(1987) described techniques for producing large numbers of parasitoids
efficiently. These researchers adapted a multicellular host rearing tray
technique (Hartley et ala. 1982) to rear M.
croceipes and some other
parasitoids. Techniques reduced parasitoid harvest time by 1/2 and
simultaneous release of nearly 17,000 wasps was possible using low
temperature storage. Powell & Hartley (1987) also noted several factors
that were important for maintaining this large scale rearing program, and
which may be applicable to other programs. Included were (1) a continuous
host supply, (2) use of environmental chambers to alter developmental rates
of hosts and parasitoids, (3) constant appropriate environmental conditions,
(4) sanitary rearing conditions with flash sterilization of diet, (5) use of
laminar flow hoods, (6) autoclaving reusable supplies, (7) disinfecting work
areas, (8) acid or antibiotics in water or food, (9) adequate technical
support, space and equipment. Elzen & King (1999) show a list of
beneficial insects that have been reared for augmentative purposes by the U.
S. Department of Agriculture. Costs.--King et al. (1985) cited costs for release of Trichogramma pretiosum to control Heliothis spp. at US$7.68/ha.
per application. This cost compared well with the cost of a commonly used
pyrethroid, fenvalerate, at US$16.18/ha when applied at 0.11 kg/ha. The
pyrethroid had to be applied only once for every two to three parasitoid
applications. However, the development of resistance to pyrethroids by Heliothis (Luttrell et al.
1987) and to dimethoate by Lygus
lineolaris Paisot de
Beauvois (Snodgrass & Scott 1988), and in general, possible development
of resistance, makes augmentation attractive. In Vitro Rearing.--Augmentation may be commercialized only for selected organisms
for which suitable diets and storage methods are developed. Artificial
rearing would offer possibilities, but as is discussed in the section on
Entomophage Nutrition, this technology is poorly developed. Various groups
have made progress in in vitro rearing of parasitoids
nevertheless. Over 22 entomophage species have been reared in vitro. Several Hymenoptera (1 ectoparasitoid, 4 pupal
parasitoids and 4 species of Trichogramma)
and 3 species of Diptera have been cultured with varying success (King et al.
1984). Predators have been reared on artificial diets, notably Chrysopa carnea Stephens (Vanderzant 1973, Martin et al. 1978).
While there have been numerous successes in oviposition stimulant
identification or partial rearing (Nettles & Burks 1975, Nettles 1982),
definite development of a feasible in
vitro rearing system for
entomophages has yet to be developed. Presently most parasitoids are
expensive to rear, and the costs involved would preclude mass rearing in vivo preparatory to thrifty augmentation efforts. Although
considerable advances have been made in in
vivo rearing, the advances
have not been achieved with in
vitro rearing to such an
extent. The work of Wu et al. (1982) illustrates an instance in which a
completely synthetic artificial host egg was produced which contains no
insect derivatives, and supports Trichogramma
oviposition and development. Greany et al. (1984) suggested that mass rearing
of Trichogramma using
completely artificial hosts would soon become economical, however. Hymenopterous larval endoparasitoids have not been successfully
reared to the adult stage on artificial diet. However, Cotesia marginiventris
and M. croceipes have been reared on artificial media through the
first instar. Larval endoparasitoids have evolved complex mechanisms that
interact with the host's internal dynamics and organs without damaging this
environment or causing untimely death of the host. The function of these
interacting factors must be understood for in vitro
rearing of larval endoparasitoids to become a reality. Developments in
artificial rearing of entomophages on artificial diet may allow production of
sufficient numbers of individuals to practically implement the further
evaluation of entomophages in biological control. Parasitoids which have been reared to the adult stage on
artificial media include the larval ectoparasitoid Exeristes roborator
(F.) (Thompson 1982), the endoparasitoids of eggs: T. pretiosum
Riley (Hoffman et al. 1975) and T.
dendrolimi (Wu et al. 1982);
of larvae: Lixophaga diatreae (Towns) (Grenier et
al. 1978) and Eucelatoria bryani Sabrosky (Nettles et al.
1980), and of pupae: Brachymeria
lasus (Walker) (Thompson
1983), Pachycrepoideus vindemiae Rondani (Thompson et
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and Pteromalus puparum L. (Hoffman &
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