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BIOLOGICAL CONTROL OF ARTHROPODS
IN ROW & SHORT-TERM CROPS
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Introduction Biological control is most successful when used in stable perennial
agroecosystems (DeBach 1965, Huffaker & Messenger 1976, Luck 1981, Price
1981, Hokkanen 1985). Annual cropping systems are generally too unstable to
sustain delicate tritrophic level interactions (Kogan et al. 1999). When the
natural control of pest species has been upset by cultural operations and
chemical pest control, adequate levels of biological control are difficult to
restore. Yet, probably the majority of human food is produced from crops that
are annual or short term, and therefore deserve maximum attention for
alternatives to routine insecticide application. Many annual crop ecosystems
benefit from a high level of natural control, in particular when an ecosystem
has not been invaded by exotic pests that require the use of disruptive insecticides
(Wilson 1985). Turnipseed & Kogan (1983) suggested that indigenous
natural enemies are important in the regulation of minor phytophagous pests,
but it is their impact on the major pests that usually attracts attention.
However, when minor pests become important because of imbalances caused by
the overuse of insecticides, disaster often follows (Reynolds et al. 1982). Typically annual or short term crops in temperate zones begin with
soil preparation in late autumn and early spring, fertilization, preplant or
preemergence applications of herbicides, planting, cultivation and harvest.
In subtropical regions double or even multiple-cropping may be possible
within the yearly cycle. Rainfall distribution and temperature usually
determine optimal planting dates and the length of the growing cycle. In cold
high latitudes, soybeans must complete the cycle from planting to harvest in
about 90 days. In the subtropics, the use of 140-day varieties is not
uncommon (Hinson & Hartwig 1982). Throughout this cycle, soybean plants
accrue biomass at an exponential rate and undergo profound physiological
changes. The total above ground accumulation of biomass may reach 10 tons of
dry matter per ha., partitioned throughout the season into vegetative and
reproductive structures. As the cycle progresses, it is accompanied by a
parallel increase in architectural and microclimatic complexity within the
crop canopy and the underground structures that leads to the diversity and
proliferation of potential feeding niches or food resources for colonizing
herbivores. The availability of these resources is probably the most
important single factor in setting numerical limits on species packing in a
given community. Kogan (1981) summarized the dynamics of variation of food
resources in a typical annual field crop based on a soybean model. The
exclusively crop-dependent components of a herbvivore's feeding niche has
functional, spatial and temporal characteristics. Functional characteristics
are determined by the physiology of the plant and refer to the various plant
organs and tissues used differentially by various species of herbivores.
Spatial characteristics depend on the stratification of the aerial and
subterranean volumes of the plant and on the patterns of plants within
fields. Such stratification may cause nutritional variability within and
among plants (Denno & McClure 1985) or subtle but critical variability in
microclimate closely related to an insect's ecological preferenda. Both
functional and spatial characteristics vary in time, thus resulting in
profound differences in plant resources at various phenological stages of
development. The general pattern of the yearly ecological dynamics of a short
term crop is an initial more or less long phase of gradual geometric increase
in niche complexity and resource diversity open to herbivore occupancy,
followed by a sudden drop in diversity and complexity as plants senesce and
the crop reaches harvest maturity. This generalized pattern of crop dynamics
presents a scenario of changing opportunities to potential herbivore
colonizers and their complement of natural enemies. The instability of
tritrophic interactions under these conditions is one of the major obstacles to
classical biological control in short term crops. Colonization of Short
term Crops by Herbivores & Natural
Enemies.--Colonization
occurs both by herbivores and their natural enemies. The sources of
colonizing species are varied and according to the crop may include the
agroecosystem encompassing the crop (either a monoculture or a multiple crop
system) and the relative geographic location of interacting agroecosystems.
The first source of colonizers are well-adapted, host-specific, native
species that overwinter in or near the crop field. Corn rootworms, Diabrotica spp., overwinter as
eggs and colonize corn plants when the crop is grown without rotation with
nonhost crops (Krysan et al. 1987). In temperate zones the harsh winters
usually have a modulating effect on the survival of overwintering native
species and thus affect the size of colonizing populations. In the midwestern
United States, the bean leaf beetle, Cerotoma
trifurcata Forster, and the
Mexican bean beetle, Epilachna
varivestis Mulsant, overwinter
as adults in woodlots surrounding grain legume crop fields. The success of
colonization usually depends on the synchronization of the emergence of the
overwintered populations with the establishment of a host crop in fields
adjacent to hibernacula. When spring planting is delayed because of
insufficient or excess precipitation, the beetles may lack food or
oviposition sites, and colonization may fail. These species usually remain on
the crop, however, increasing gradually in succeeding generations if
environmental conditions are favorable. A second source of colonizers are polyphagous species, the
populations of which increase on wild plants or on temporarily more
attractive crops. These species migrate into a succession of crops as plants
reach a preferred stage of growth or as the crops on which they had resided
become unsuitable. The corn earworm, Heliothis
zea (Boddie) develops on
corn early in the season in North Carolina and produces two generations. When
second generation adults emerge, the corn is no longer suitable and the moths
disperse to such other crops as cotton, peanuts, tomatoes and late planted
soybeans at bloom. Waves of ovipositing moths often massive and generate
damaging larval populations (Stinner et al. 1977, Kennedy & Margolies 1985).
Also in this category are multivoltine species that arrive in small numbers
onto a crop at various times during the season and may or may not become
established. If they do their short life cycle and high reproductive rate
result in the build up of populations that may prove damaging (e.g., aphids,
whiteflies, leafhoppers and spider mites). A third group of colonizers are migrant species that overwinter
and reproduce early in the season in regions of subtropical climates.
Successive generations expand their geographic range from the overwintering
areas, generally following jet stream paths and the availability of suitable
hosts (Sparks 1979, Rabb & Kennedy 1979). An island biogeographical or dynamic equilibrium theory has been
proposed as a model for the colonization of annual crops by arthropods (Price
1976, Mayse & Price 1978, Price & Waldbauer 1982). However, it has
proven of small value in explaining or predicting patterns of colonization of
short term crops and its application has been criticized on both theoretical
and practical grounds (Rey & McCoy 1979, Liss et al. 1986, Simberloff
1986). Although detailed studies on the dynamics of crop colonization under
diverse cropping conditions ar few, those that exist suggest that the number
of colonizing species increases as the crop matures and that a lag occurs
between crop colonization by herbivores and subsequent colonization by
natural enemies (Price 1976, Mayse & Price 1978). It is important in the regulation of herbivore populations for
natural enemies to follow herbivore colonizers closely. The availability of
prey at an early stage of plant growth may determine the abundance of
predators at later stages when other prey species may be present. Anecdotal
accounts by soybean researchers in the southern United States (Harper et al.
1983) suggest that the green cloverworm, Plathypena
scabra (F.) an early season
herbivore, is a beneficial species because it serves as prey for the
predaceous hemipterans. Later in the season those predators help moderate the
population growth of such serious pest species as Heliothis zea,
Anticarsia gemmatalis (Hübner), and Pseudoplusia includens Walker. The green
cloverworm, however, is one of those migrant species that usually reach
midwestern soybean fields at critical stages of crop development, and it
therefore poses a potential threat in those areas. Recruitment of Crop
Colonizers.--The diversity of the arthropod community associated with
annual crops seems to depend mainly on the extent of the area planted to that
crop (Strong 1979). Plant architecture, however, influences the complexity of
available feeding niches, and these ultimately determine the complexity and
richness of those communities (Lawton 1978, Kogan 1981). Whether a crop is
introduced or native is also important. Kogan (1981) considered three sources
for species recruitment in introduced crops: (1) oligophagous species
associated with native plants that have taxonomic or chemical affinity with
the introduced crop, (2) polyphagous species capable of rapidly expanding
their host range as new food resources become available or replace previous
ones, and (3) oligophagous species that are associated with plants unrelated
to the crop and that may undergo gradual host shifts. Native crops have a
preponderance of host-specific, coevolved species and a full complement of
effective natural enemies. The colonization of introduced hosts by native
herbivores that originally fed on plant species closely related to the
introduced crop has resulted in some of the most serious pest problems on
record. The classic example is the Colorado potato beetle, Leptinotarsa decemlineata Say. Short term crops are recolonized annually by a herbivorous fauna
that varies spatially and temporally with the dynamics of the crop, the
characteristics of the ecosystem, and the spatial relationship of the crop
ecosystem to other adjacent or distant ecosystems. A complement of natural
enemies associated with those herbivores usually colonizes the crop after a
lag that is determined by the foraging patterns of the natural enemies and
the sources of the colonizers. The build-up of natural populations of enemies
depends on the availability of suitable prey or hosts. The nature and
complexity of this colonizing arthropod fauna depend on whether the crop is
native to or introduced into a region. Additionally, the colonizing fauna
depends on how long the crop has been under cultivation, increasing
exponentially for several growing cycles until it approaches a plateau
determined by the area planted to the crop and the complexity of the crop's
available feeding niches (Strong 1974, Lawton 1978, Kogan 1981). It is this rapidly changing and cyclically
disturbed habitat that poses the greatest obstacles to the success of
classical biological control in short term crops. Despite the inherent
ecological instability of these crops, however, most herbivore populations
are effectively regulated by a complement of natural enemies. This regulation
is most dramatically demonstrated when natural enemies are inadvertently
eliminated by broad-spectrum insecticides (Metcalf 1986). Natural Control in Short term Crops Short term crops in most growing regions of the world have a
diverse and abundant population of natural control agents, especially if the fields
have not been sterilized with broad spectrum pesticides. Predators.--Many surveys have been conducted using as the target
either the crop or particular species or guilds of species within a single
crop or the various crops in a region. One of the most extensive surveys of
natural enemies of any crop was conducted by Whitcomb & Bell (1964) in
Arkansas cotton fields. There were 600 species of predators representing 45
families of insects, 19 families of spiders and 4 families of mites found.
Other extensive surveys were done on spiders on soybean in other areas (Neal
1974, LeSar & Unzicker 1978). The number of unique species occurring at
each location far exceeded the number of species occurring in common at any
two locations combined or co-occurring at all locations. The spider community
of cotton in Arkansas was far richer than the spider communities of soybean
either in Florida or in Illinois. There were about as many species of spiders
common to Arkansas cotton fields and Illinois soybean fields as there were to
Arkansas cotton fields and Florida soybean fields, but there were three times
more species in common in those two comparisons than there were species
common to Florida and Illinois soybean fields. Although all three communities
had a diverse spider population, the spider community of cotton was much more
diverse. Species composition was more influenced by geographic location
than crop matrix. A similar comparison was made among surveys of carabids in
Illinois and Iowa corn fields (Dritschilo & Erwin 1982), in North
Carolina soybean fields (Deitz et al. 1976), and in Arkansas cotton fields
(Whitcomb & Bell 1964). In contrast to the spider fauna, the carabids
were much more localized. Only one species appeared in all three surveys, and
only 18 species co-occurred in any two agroecosystems. Such comparisons
suggest that crop communities have a rich fauna of predators and that many
species are probably well adapted to local conditions. Although the
effectiveness of this predaceous fauna has not been evaluated in detail,
resurgences of pests are often attributed to the disruption of such natural
control agents by broad spectrum pesticides (Shepard et al. 1977, Huffaker
& Messenger 1976). Parasitoids.--Assessments of naturally occurring parasitoids are
usually based on surveys of individual host species or guilds of hosts.
Extensive surveys have been conducted on the parasitoids of some of the major
pests of short term crops (e.g., Heliothis
zea, H. virescens,
Nezara viridula). Heliothis
zea and H. virescens
have been recorded in the United States from 235 plant species in 36 families
and are, therefore, highly polyphagous. A literature survey of the
parasitoids of these two species produced 60 species of Hymenoptera in six
families (Braconidae, Chalcididae, Eulophidae, Ichneumonidae, Scelionidae and
Trichogrammatidae) and 62 species of Diptera in four families (Muscidae,
Phoridae, Sarcophagidae and Tachinidae). The efficacy of natural control
agents in cotton in North America was assessed by Goodenough et al. (1986). A partial host record of N.
viridula showed that it is
also a highly polyphagous species, being recorded from 44 common cultivated
and wild hosts in 18 different plant families (Todd & Herzog 1980). Jones
(1988) surveyed the world literature for records of N. viridula
parasitoids and found 57 species in two Diptera and in five Hymenoptera
families. Species guilds, rather than single species, are often the object
of detailed studies. Comprehensive studies of parasitoids of lepidopterous caterpillars
in soybean in the United States were reviewed by Pitre (1983). Ten primary
parasitoids and 10 hyperparasitoids were recorded on cereal aphids in Europe
(Vorley 1986). In most cases extensive surveys of common herbivorous insects
of short term crops reveal the presence of a rich associated fauna of natural
enemies. However, many of those herbivores remain serious pests. Obviously
qualitative surveys reveal very little about the effectiveness of natural
enemies in population regulation. The enrichment of the complement of natural
enemies of short term crops through augmentive releases or through classical
biological control offer means to counteract this situation. Entomopathogens.--Entomopathogens are probably the most effective natural
control agents in explosive pest populations in short term crops. A good
example of the efficacy of a fungal pathogen in regulating lepidopterous
caterpillar populations is the fungus Nomuraea
rileyi (Farlow) Samson. This
fungus is primarily a pathogen of many species of lepidopterous larvae
(Ignoffo 1981). Natural epizootics frequently cause crashes of susceptible
host populations. Under favorable environmental conditions this fungus may be
the single most important mortality factor regulating populations of the velvetbean
caterpillar, A. gemmatalis, in soybean fields
in Brazil (Moscardi et al. 1984) and populations of the green cloverworm, P. scabra, in soybean in the midwestern United States (Pedigo
et al. 1982). The success of the soybean IPM program in Brazil was due, to a
great extent, to the correct assessment of natural epizootics of N. rileyi (Kogan et al. 1977, Kogan & Turnipseed 1987).
However, epizootics are often not predictable and are occasionally too late
in the growing season to prevent economic damage to the crop (Kish &
Allen 1978, Ignoffo et al. 1975, 1981, Fuxa 1984). Despite these adverse
characteristics of some epizootics, their dramatic natural has caused
substantial research to be directed toward using N. rileyi
as a biological control agent. Heliothis zea and H. virescens on cotton in the United States are infected by
many naturally occurring pathogens (Yearian et al 1986). The most common are:
Nomurea rileyi and Entomophthora
spp. fungi, Nosema heliothidis and Varimorpha necatrix, microsporidia, and the nuclear polyidrosis
viruses of H. zea and Autographa california
(Speyer). Although natural epizootics do occur, they are often inadequate to
maintain Heliothis spp.
populations below the economic injury level. Therefore, much effort has been directed
to developing manipulative methods to enhance entomopathogen efficacy. Classical Biological
Control in Short term Crops There are a few spectacular successes, which on examination again
show that the success of a biological control program cannot be predicted on
the basis of assumptions or preconceptions related to the ecological
instability of the crop (Hokkanen 1985). Southern Green
Stink Bug--Nezara
viridula (L.).--Southeast Asia
is considered the center of origin of this species (Yukawa & Kiritani
1965). The pest is presently found throughout the tropics and subtropics of
all continents. However, Hokkanen (1986) suggested that N. viridula
is of Ethiopian origin, based on records of polymorphism as well as the
number of host specific parasitoids in that region. Because it is an
immigrant pest of many important crops, many attempts to establish
parasitoids into newly invaded areas have been made. Programs in Hawaii and
Australia have been very successful (Caltagirone 1981), and importation and release
of natural enemies are currently being expanded in Africa, South America, New
Zealand, Taiwan and the United States (Jones 1988). The success in Australia
gives the greatest insight into the conditions for successful biological
control of this insect. Nezara viridula
was first recorded in Australia in 1913 and has since been the subject of
several successful biological control projects, mainly involving colonization
of the egg parasitoid Trissolcus
basalis imported from Egypt
and Pakistan. The early history of control by importation of natural enemies
was recorded by Clausen (1978), Caltagirone (1981) and Wilson (1960). Kogan
et al. (1999) updated this history and assessed factors that may have led to
the successful control of the pest in Australia. The pest spread to the Ord Valley in northwestern Australia in
1974, over a decade after the last introduction of parasitoids from Pakistan
to other parts of Australia. Within two years it had become a severe pest due
to its polyphagous habit that enables it do damage many vegetable and field
crops. Damage was so severe in sorghum that fields had to be abandoned. The
parasitoid, T basalis was reared in an
insectary and ca. 44,100 were released in fields in the Ord Valley. The host
population began to decline due to parasitism a few months later and good
control was obtained (Strickland 1981). Subsequent observations indicated
that the parasitoids were usually present regardless of the level of
abundance of the host population. Conditions that helped to maintain
populations of stinkbugs at low levels and prevented their upsurge following
their decline were explained by (1) the prevailing cropping system in the Ord
Valley involved diverse plant species that were infested by the stink bug at
different population levels. The parasitoids, therefore, were able to move
from centers of high host population to centers of low host populations,
thereby maintaining an overall low equilibrium position throughout the entire
spectrum of crops; and (2) in addition to N.
viridula, T. basalis attacked several other locally occurring
pentatomids and thus had a continuous supply of hosts (Strickland 1981). The success of T.
basalis as the parasitoid of
very mobile and polyphagous pest is attributable to a combination of the characteristics
of its own host range and the characteristics of the feeding range of its
host species. That combination guaranteed an environment that continually
provided fresh adult parasitoids capable of keeping the pest a low population
levels. As N. viridula is a major pest of
many short term crops in most parts of the world, efforts to control it by
means of natural enemies continue. According to Jones (1988), African and
Asian egg parasitoids in the genera Trissolcus,
Telenomus, and Gryon and six New World
tachinid adult parasitoids deserve consideration in biological control. The
tachinids are Trichopoda pennipes (F.), T. pilipes (F.), T.
giacomellii (Blanchard), T. gustavoi (Mallea), Eutrichopodopis
nitens Blanchard, and Ectophasiopis arcuata (Bigot). Melon Fly Dacus cucurbitae
Coquillet.--Native to the Indo-Malayan region, the melon fly was
first recorded in Hawaii in 1897. Prior to its invasion, cucurbit crops were
widely grown for local consumption and some were exported to California.
Following the introduction of the fly, growing cantaloupes became impractical
and the production of other melons, cucumbers and tomatoes was seriously
curtailed (Nishida & Bess 1950). Biological control of the melon fly was
undertaken by introducing Biosteres
fletcheri (Silv.) from
India. The parasitoids were mass reared in Hawaii, and field releases made in
1916 and 1917 resulted in their establishment. Two additional species Biosteres longicaudatus watersi
Full. from India and B. angeleti Full. from Borneo,
were introduced during 1950 and 1951, respectively (Clausen 1978). The 1916
and 1917 releases resulted in a 50% reduction of the melon fly populations,
and although the flies were still a pest, melons were again a profitable crop
in Hawaii (Fullaway 1920). Later the melon fly again became a severe pest
requiring multiple applications of insecticides and generating additional
control related research (Nishida & Bess 1950). Studies showed that the
change in parasitoid efficiency was probably associated with changes in land
use and agricultural practices (Newell et al. 1952, Nishida 1955). Because melons
and other perishable crops are available in the field for only a short
period, these plants form an unstable resource to which the biology and life
cycle of D. cucurbitae are well adapted.
Consequently, parasitoids of the fly must be able to follow the short-lived
and localized fly populations throughout their range if efficient control is
to be achieved. In Hawaii, control had been possible because the presence of Momordica balsamina, the fruits of which constituted a stable wild
host for D. cucurbitae and its parasitoids.
Changes in agricultural practices and increased land use, however, reduced
the areas where M. balsamina grew abundantly, thereby
reducing the reservoirs of the natural enemies and making it more difficult
for the natural enemies to reach the cultivated fields. The main fly
population now had its origin in culti9vated fruits where parasitization was
much lower than in the fruits of M.
balsamina: 1% for tomatoes,
0-16.5% for melons, and 0.2-6.5% for cucumbers vs. 20-37.8% for M. balsamina (Nishida 1955). Thus, a change in the diversity
of the habitat proved detrimental to this biological control project. Cereal Leaf Beetle--Oulema melanoplus (L.).--A native pest of cereals in Europe, cereal leaf beetle
was first recorded from Berien County, Michigan in 1962. According to Haynes
& Gage (1981), damaging populations in the area were probably present
since the 1940's. Expansion of the area infested by the cereal leaf beetle
occurred rapidly and the current range extends through much of the Midwestern
states to the East Coast. Strict interstage quarantines and treatment of
potentially infested bales of hay and grain were enforced. Eradication
efforts continued for about seven years, but were finally abandoned when the
spread of the beetle obviously could not be halted. Probably widespread
public opposition to the spray program influenced this decision. The cereal leaf beetle has one generation per year and
overwinters as unmated adults (Castro et al. 1965). With the spread of the
beetle out of control, research was initiated in several areas, including
sterile male techniques, behavioral control by means of attractants and
biological control by means of imported natural enemies. Clausen (1978)
summarized the biological control program. Initiated in 1963, the search for
natural enemies concentrated in France, Italy and Germany. From 1964 to 1967
five parasitoids were imported and four to become established were Tetrastichus julis (Walk.), Diaparis carinifer (Thomsen), Lemophagus
curtus Tow. and Anaphes flavipes (Foerster) (Haynes & Gage 1981). Mass releases of A.
flavipes were conducted in
the absence of more efficient natural enemies. Releases were made in Indiana
in 1966 and the parasitoid was recovered at most sites later in the same
season. As the beetle was not easily reared in the laboratory, cultures of
the parasitoid were maintained on beetles collected in the field. These
beetles were also used in the screening of wheat, oats, and barley lines and
varieties for resistance against the beetle. A parasitoid nursery was
established in Niles, Michigan for the redistribution of parasitoids reared
on field-infested populations. Populations were observed to decline since 1971, with causes for
the decline being attributed to a combination of such factors as
weather-related mortality, mortality due to introduced parasitoids, genetic
changes in beetle populations and changes in overwintering habitat (Haynes
& Gage 1981). Although sporadic outbreaks may require treatment,
populations of the beetle seem to have generally abated. This history
suggests that immigrant pests, after an initial period of explosive
expansion, may follow a pattern of adaptation within the agroecosystem that
results in an equilibrium state not as detrimental to the crop. Alfalfa Weevil--Hypera postica (Gyllenhal).--First found
in the United States near Salt Lake City, Utah in 1904, Hypera postica
is believed to have invaded from Europe (Titus 1907, 1910). The weevil was
confined to 12 western states until 1952 when it was detected in Maryland
(Bissell 1952). From Maryland it spread rapidly and is now found throughout
North America. There is one generation per year and winter is spent as
aestivating adults and as eggs. Eggs hatch in spring about the time that
alfalfa begins to grow. In the Midwest, larval feeding continues through May
when pupation occurs. After emergence adults leave the field for available
cover where they undergo summer aestivation. In autumn adults return to the
field and begin laying eggs (Manglitz & App 1957). Parasitoids were first introduced from Europe into the United
States in 1911, and by 1919 they were well established in many areas of the
western United States (Chamberlin 1924). Bathyplectes
curculionis (Thomson) is the
most widely distributed and most successful introduced parasitoid in the
Midwestern U. S. During the 1960's and 1970's, both B. curculionis
and B. anurus (Thomson) were released in Illinois by USDA
personnel and are now found in most midwestern populations of the weevil
(Dysart & Day 1976). A fungal disease of alfalfa weevil larvae was found in Ontario,
Canada in 1973 (Harcourt et al,. 1974), and was similar to that reported
active on cloverleaf weevil, Hypera
punctata (Arthur) by Arthur
(1886). The fungus is believed to be Erynia
phytonomi (Thomson) and
actually differs from that attacking cloverleaf weevil. It was found to
spread rapidly out of Ontario to other portions of North America (Muka 1976,
Puttler et al. 1978, Barney et al 1980, Los & Allen 1983, Nordin et al.
1983). It is now considered to be the major naturally occurring biological
control agent of the alfalfa weevil throughout most of its range (Carruthers
& Soper 1987). A similar fungus causes comparable mortality in Hypera variabilis in Israel (Ben Ze'ev & Kenneth 1982). Erynia phytonomi
overwinters in the soil as thick-walled resting spores that germinate in
springtime to produce germ conidia, which infect weevil larvae. Conidia
produced by infected larvae are responsible for the horizontal transmission
of the disease (Ben Ze'ev & Kenneth 1982). Younger larvae tend to produce
conidia and older larvae resting spores (Watson et al. 1980). Brown &
Nordin (1982) developed a detailed model of this disease and estimated that
the first incidence occurs in Kentucky after an accumulation of 220 to 290
degree days. Then the alfalfa weevil population has to reach a threshold
density in order to allow for sufficient horizontal transmission for an
epizootic. Brown & Nordin (1982) estimated this threshold to be 1.7
weevil larvae per stem. Mortality rates caused by the fungus are often quite
high (30-70%) at the time of peak larval occurrence and often 100% later in
the season (Morris 1985). It is restricted in effectiveness as a biological
control agent because it often appears late relative to currently recommended
harvest dates (Armbrust et al. 1985). Brown & Nordin (1982) proposed
using computer-directed harvest dates that are earlier than normally
recommended. The microenvironment in windrows promotes an earlier than normal
epizootic and reduces the need for insecticides. The appearance of the fungus as a major mortality factor after
the two above mentioned parasitoids were established poses the question of
how these all will now coexist, especially as they attack the larval stage.
About five days elapse from infection to death in diseased larvae and
parasitized larvae die within 10 days. Such time periods suggest that an
alfalfa weevil larva infected and parasitized simultaneously would probably
die from the fungus before the parasitoid completed its development. Field
studies indicate that the disease has a negative impact on the two
parasitoids (Los & Allen 1983, Loan 1981, Morris 1985). European Corn Borer--Ostrinia nubilalis (Hübner).--This insect is
believed to have been accidentally introduced in shipments of broom corn from
Europe in the area of Boston, Massachusetts in 1917 (Caffrey & Worthley
1927). Its range presently includes most of the major corn producing regions
of the United States. Between 1920-1930 24 species of parasitoids were
imported into the United States from Europe and the Orient, and by 1962 six
of these were established. Two of the introduced parasitoids, the tachinid Lydella thompsoni (Herting) and the ichneumonid Eriborus terebrons (Gravenhorst), usually parasitizes up to 50
percent of the borers in the Midwest during 1958-1963. However, in the 1960's
parasitism by the tachinid decreased rapidly and few, if any , can now be
found in the United States (Hill et al. 1978, Burbutis et al. 1981). Explanations to explain the decline of the tachinid center around
competition from the microsporidian Nosema
pyrausta. Presently the only
parasitoid commonly found in the Midwest is the braconid Macrocentrus grandii
(Goidanich), which is infected by N.
pyrausta and high levels of
mortality result (Andreadis 1980, 1982; Siegel et al. 1986). In Illinois in
1982 and 1983, M. grandii parasitized an average
of 19.5% of first generation corn borer larvae, but only an average of 5% of
second generation larvae . This is believed due to the fact that first
generation borer populations usually have a lower prevalence of Nosema than second generation
populations, and thus the parasitoid may avoid the disease by parasitizing
primarily first generation larvae. Paillot (1927) first described N. pyrausta
from European corn borers collected in France, and the pathogen was first
found by Steinhaus (1951) in the United States in larval European corn borers
from the Midwest. It now infects corn borers throughout most of their range,
and a high prevalence (up to 100%) have been reported from many states (Van
Denburg & Burbutis 1962, Hill & Gary 1979, Andreadis 1984, Siegel et
al. 1987). This microsporidian infects most body tissues, and infectious
spores are passed in the feces of infected larvae. Horizontal transmission
occurs when healthy larvae ingest sufficient numbers of spores, usually in
larval tunnels contaminated by frass from infected larvae. Although some
disease-induced mortality occurs when larvae are infected by oral ingestion
of spores, the most dramatic mortality occurs when transmission is
transovarial (Windels et al. 1976). Such larvae experience 30-80 percent
higher mortality than healthy larvae (Kramer 1959, Windels et al. 1976,
Siegel et al. 1987). Crashes usually occur after several years of rising corn
borer populations and when the prevalence of Nosema nears 100 percent. Because horizontal transmission
of infection in corn borer populations depends on the probability of healthy
larvae inhabiting a corn stalk with infected larvae, the initial infection
level of transovarially (vertical infection) infected larvae and the larval
population density are two of the most important variables affecting
infection levels in corn borer populations (Maddox 1987). Although in many areas of the United States N. pyrausta
is the most important biological mortality factor in corn borer populations,
it has little promise as a microbial insecticide because it is already widely
distributed. During some years the fungus Beauveria
bassiana causes considerable
larval mortality in central Iowa and west central Illinois by Marcos Kogan
and associates. Cassava Mealybug in Africa--Phenacoccus manihoti Matile-Ferrero.--A major food source for over 300 million people in
tropical regions of the world, cassava is an important root crop (Bellotti
& Schoonhoven 1985). Most production (80%) is concentrated in Brazil,
Indonesia, Nigeria, Zaire, India and Thailand. This plant is native to
tropical South America, and was introduced to the Congo basin in Africa in
the early 16th Century (Cock 1985). Although a perennial shrub reproducing
vegetatively, cassava roots may be harvested 7 to 18 months after planting.
Roots are harvested by pulling the stems and uprooting the whole plant. Mealybugs of the genus Phenacoccus
have been recorded in association with cassava in South America and Africa. Penaacoccus gossypii Towns. & Cock, P. grenadensis Green & Laing, and P. madeirensis
Green are polyphagous, but P
manihoti Matile-Ferrero
appears specific to cassava and the only species capable of producing severe
distortion of leaves. Another South American species was separated from P. manihoti and described as P. Herreni
Cox & Williams (Cox & Williams 1981). Mealybug damage seems to be a
recent phenomenon, but one that is increasing in areas where it had not
previously been found (Bellotti et al. 1985). This new pest status results
from an imbalance between the mealybug, the local cassava land race and the
existing natural enemies. The situation was particularly acute in Africa. Phenacoccus manihoti was first discovered
in Zaire in 1973 and spread into almost all other cassava growing areas of
the continent. The estimated losses caused by this species and another
explosive pest, cassava green spider mites, Mononychellus spp., were estimated at $2.0 billion per
year, and the pests affected an area about 5.5 million ha. (Neuschwander et
al. 1984). Control of the mealybug with natural enemies was attempted
following its recognition as an immigrant species (Cox & Williams 1981).
Surveys for native natural enemies associated with P. manihoti
in Gabon revealed that various guilds have incorporated the immigrant in
their host or prey range, but none were greatly efficient (Boussienguet
1986). The list included two primary parasitoids, four hyperparasitoids, nine
predators and eight parasitoids of the predatory species (Neuenschwander et
al. 1987). Extensive explorations for natural enemies were conducted in South
America. Between 1977 and 1981 the Commonwealth Institute of Biological
Control in collaboration with the International Institute For Tropical
Agriculture surveyed the tropical areas of central and northern South America
and found that the parasitoids Aenasius
vexans Kerrich, Apoanagyrus diversicornis (Howard), and Anagyrus spp. seemed to be
specific to the cassava mealybug (Cox & Williams 1981). In 1980 a species
of Diomus (Coccinellidae)
was imported and released in experimental fields (IITA 1981, 1985), and one
year later the encyrtid Epidinocarsis
lopezi (DeSantis), collected
in Paraguay by M. Yaseen, was imported to Nigeria and released at two sites.
The parasitoids were established and recovered from parasitized mealybugs.
(Lema & Herren 1985). The spread of E.
lopezi was spectacular; by
December of 1985 it had become established over 650,.000 km2 in 13
African countries (Neuenschwander et al. 1987). Exclusion experiments and continuous
monitoring demonstrated the efficiency of the parasitoid in regulating P. manihoti populations in Africa. IITA (1985) reported that
a significant reduction in population levels of the cassava mealybug had been
observed in all regions colonized by E.
lopezi. In those areas, the
mealybug was recorded at populations of 10-20 per terminal cassava shoot.
Prior to the establishment of the parasitoid peak populations in excess of
1,500 per shoot were common (IITA 1985). The successful importation and establishment
of E. lopezi gave further impetus to the biological control
program at IITA, and additional species of parasitoids and predators are
being released experimentally with various degrees of success (IITA 1987b). Detailed biological studies have been conducted on the
coccinellid Hyperaspis raynevali Mulsant (Kiyindou
& Fabres 1987), and the entomophthoraceous fungus Neozygites fumosa
(Speare) Remaudiere & Keller (Le Ru 1986). This successful biological
control program of cassava mealybug in Africa is probably one of the best
demonstrations of the potential of this tactic for IPM in short term crops.
However, other tactics are being used against this and other cassava pests,
including breeding of plant resistance, cultural control and the selective use
of pesticides (Cock & Reyes 1985). Other Systems (e.g., cotton).--Please consult
the case history series (CH-..) and the references for details on pink and
spotted bollworms in cotton. [ Please refer also to Related
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