FILE <bc-25.htm> GENERAL INDEX [Navigate to MAIN MENU ]
[For educational purposes only; do not review, quote or abstract]
DISCOVERY,
IMPORTATION AND COLONIZATION
OF NEW NATURAL ENEMIES
(Contacts)
---- Please CLICK on desired underlined
categories [to search for Subject Matter, depress Ctrl/F ]: MAP Links
|
Problems Encountered by Explorers
from Universities |
||
Hazards Encountered in the Field
|
|
|
|
[ Please refer also to Selected Reviews & Detailed
Research ] Introduction The biological
control of pests with imported natural enemies involves the addition of new
biotic mortality factors to the pest's ecosystem. This practice is often
carefully scrutinized by regulatory agencies which strive to eliminate the
establishment of potentially harmful organisms. Biological control
researchers increasing seek more effective guidelines for judging a natural
enemy's capabilities before importation in order to accelerate biological
control success rates and to reduce project costs (Coulson 1981). The manner
by which biological control is achieved varies considerably among projects
and the various countries utilizing the technique; and there is a continuing
debate on proper procedures for selection of natural enemies and regulation
of their importation (Legner & Bellows 1999). The primary goal
of federal, state or university importation programs is the same, i.e., the
collection, safe transport, and quarantine processing, leading ultimately to
the colonization in the field of candidate biological control agents.
However, there are differences in the methods which are, or can be, used by
each entity. Perhaps the main factor in the United States is that the U. S.
Department of Agriculture (APHIS) either on its own initiative or in
concurrence with overriding dicta (as from the Environmental Protection
Agency) issues regulations regarding the importation and quarantine handling
of biological agents which the USDA (ARS), individual states and universities
are expected to follow. Of mutual
concern to the explorer/collector/shipper and government regulatory agencies
and quarantine personnel are the identification of target species and their
hosts, permits to import the material collected, packaging and labeling,
method of shipment, clearance at the port of entry by customs and
agricultural inspectors, and the quarantine facility itself. Most of the
technical and biological considerations relative to acquiring and shipping
biological agents remain much the same as those described for entomophagous
arthropods and /or weed feeders by Bartlett and van den Bosch (1964), Boldt
and Drea (1980), Coulson and Soper (1989), Klingman and Coulson (1983), and
for phytophagous (weed feeders) organisms by Schroeder and Goeden (1986). In
actual operation USDA (ARS) sponsored quarantine laboratories receive
shipments which usually originate from a USDA laboratory abroad where the
material has been screened for contaminants before being shipped to a primary
USDA quarantine facility in the United States, such as the laboratory at
Newark, Delaware, where further screening for unwanted organisms may occur
before the biological agent is forwarded to requestors in the field who may
or may not work out of a secondary quarantine facility where the biological
agent can be propagated or released directly into the field. State
departments of agriculture or universities usually send out members of their
staff as explorer/collectors, who typically do not have access to laboratory
facilities while in the field. As a consequence shipments sent to their
quarantine laboratories may contain more than one targeted pest species and
more than one natural enemy of each of these. They must then be segregated in
quarantine and studied through one generation (for newly introduced species)
before they can be released. Unsolicited extraneous material inadvertently
included may warrant further study in quarantine. If so, specific
arrangements must be made with APHIS PPQ regarding the handling of such
material. USDA collectors when abroad can utilize all available U.S.
governmental facilities (embassies, agricultural attaches, commissary,
vehicles, communication facilities, etc.) to expedite their missions. Thus
far U.S. state and university collectors abroad have only rarely been able to
avail themselves of similar federal cooperation even though their missions
were financed by public funds and their efforts would potentially accrue to
the benefit of agricultural crop production on a regional if not national
scale in the U.S. International
geo-political and socio-economic unrest may impact heavily on the success of
failure of foreign exploration missions. Terrorism in its broadest sense has
become a major deterrent to the search for biological agents in many areas of
the world. Colleagues in such areas or intermediary organizations (i.e.,
charging a fee for service), such as the Commonwealth Institute For
Biological Control, Silwood, UK, may be able to supply the desired beneficial
organisms, but experience has shown that biological control workers who know
what they need and who physically participate in the collecting process tend
to make a better showing in terms of successful introductions (Legner &
Bellows 1999).. A highly
important consideration is that during the last 25 years the number of
students trained in biological control and population ecology entomology
worldwide has been on the increase. The hope is that this expanding pool of
"applied ecologists" portends improved international cooperation
regarding greater use of the biological method of pest control. However, it
is anticipated that further legal constraints on biological control of pests
are, or will be, imposed by new and/or pending technical regulations
ostensibly aimed at protecting endangered species or the environment. These
regulations could severely hamper or preclude importation and field use of
new candidate natural enemies. Purpose and
Need The purpose for
exploration is to search for, import and colonize natural enemies of our
pests from areas where the pest is indigenous, or at least present in low
numbers because its natural enemies keep it in check. The need for
exploration is to protect our environment from needless or questionable use
of chemical pesticides, especially those with long half lives and/or broad
spectrum toxicity which can adversely affect non-target species and
beneficial organisms and ultimately the food chain within a wide range of
biologically diverse species. The basic goal
is to import species of strains presumed to be pre-adapted to areas targeted
for colonization of beneficial organisms. One tries for large founder numbers
in order to keep the gene pool as large as possible. Although traditionally
used for homopterous pests of perennial crops (DeBach 1964), it is
increasingly considered for non-homopterous and annual pests in agricultural,
urban and glasshouse environments. Extra agricultural uses in medical, forest
and household entomology are expanding. Environmental
concerns and laws, public opinion and resistance of arthropod and weed pests
to chemical pesticides are increasingly forcing a consideration and
implementation of non-chemical solutions of pest problems. Classical
biological control is a powerful and proven tool. The increasing threat that
federally mandated regulations may neutralize the importation and colonization
of new natural enemies by greatly slowing the process far beyond sound
biological protocols which have served applied biological control and society
for well over 100 years. Planning and
Preparation Funding.--There is a need for a long term stable commitment so
that chronic pest problems can be pursued. Ongoing search missions usually
require a minimum of 12 to 18 months of preparation, and the explorer must
have assurance that the funds will become available when the trip finally is
activated. Commodity groups
plus state funding can provide support for "brush fire" needs, but
coming up quickly with a qualified explorer or well planned biological
control campaign may be difficult to arrange on short notice. Experiment
station staff might use sabbatical leaves for extended studies abroad,
academic responsibilities permitting. Or, a full time person might be hired
to carry on broad biology field studies abroad, as is currently practiced by
the USDA, ARS in biological weed control. The Explorer/Collector.--The long tradition of classical biological control in
the University of California (beginning in 1923) has included exploration by
its academic and nonacademic staff. Initially this effort served mainly the
California citrus and subtropical fruit industries. In the late 1940's and
through the 1950's other crop systems began incorporating biological control
into their pest management programs. In California early notable biological
control successes of certain pests occurred in alfalfa (spotted alfalfa
aphid, alfalfa caterpillar, pea aphid), walnuts (walnut aphid), olives (Parlatoria
scale), and native pasture (Klamath Weed). Ongoing research with natural
enemies has resulted in partial to complete economic control of other pests
on natural those and other crops. The results are now obvious: in crop
systems which are managed from an ecological perspective, natural enemies
must be accorded high level consideration in the planning and implementation
of pest control practices...they cannot be ignored! Diplomacy by the explorer must be a primary concern. Explorers also must be aware that the
public they encounter in the field will invariably be ignorant of their
goals. In some cases, especially among
primitive societies, hostility may be
shown if the search and collection activities appear strange. When gifts such as fruit are presented to
the explorer, they must always be received graciously and with a minimum of
scrutiny. An example would be if one
is presented with oranges from a resident’s backyard, even though the fruit
may be crawling with insect life this should be ignored in the presence of
the bearer. Choosing the Explorer/Collector.--The explorer must have a broad knowledge of the target
pest and its known natural enemies, including their range, host plants,
biology, and taxonomy. The explorer must also be willing to travel, often
under adverse circumstances. Typically designated to perform this service are
academic or professional grade staff from state or federal agriculture
experiment station (usually scientists already working on the target pest or
its close relatives). Foreign Collaborators Because of their
own time commitments and responsibilities, it is usually not productive to
ask or expect foreign colleagues to search for and ship to the home
quarantine facility the desired natural enemies. However the cooperation of
colleagues or contacts in the area being contemplated for search is highly
important for maximizing the often compressed time frame within which an
explorer may be obliged to perform his/her assignment. Problems Encountered
by Explorers From Universities Because of
personal promotion constraints which require research, publication and teaching,
university academic appointees often cannot afford the time required to
thoroughly search for and study target natural enemies in the field, either
foreign or domestic (Legner & Bellows 1999).. Universities
also often set maximum limits for lodging expenditures, which although
usually based on the U. S. Government format, are frequently outdated and too
low, such that the explorer is faced with incurring personal expenses even
though granting agencies have provided ample funds. For expedient processing
of large field plant and insect samples, air conditioned spacious
accommodations with adequate lighting are essential even though such may
exceed the limits posed by institutions for reimbursement. A straight per
diem allowance without reimbursement by receipt tends to overcome the higher
charges which are equalized by lower cost accommodations en route or by some
nights spent in travel vehicles, tents, etc. A per diem allowance gives the
explorer flexibility to judge which is the most effective way to direct the
project. However, a punitive attitude
of incrimination has developed by “clerks” in some prestigious institutions
in dealing with a scientists expenses (e.g., the University of California). Choosing Targets
and Procedure Two schools of
thought are (1) narrowly targeted natural enemies based on available
information and (2) shotgun approach if information base is weak. The
procedure involves a literature search, taxonomy and the study of museum
material, or possibly voucher specimens from earlier trips dealing with the
same pest, correspondence with collaborators abroad in order to determine the
best season to search. The latter include referrals from colleagues, local
agricultural extension people, botanists, botanic gardens, nature preserves,
especially in the search area, and a letter of introduction from the host
country's Consulate to institutions for the temporary use of their
facilities. Permits are then
obtained which involve technical and bureaucratic requirements. Such permits
are required for importation to the home country (in the US the agency is
APHIS issuing PPQ 526 stickers), and often in the host country where
regulations govern the export of living or dead (museum) materials.
Individual states or provinces may impose further restrictions. Arrangements
must be made with the receiving quarantine laboratory. The explorer should
have a valid passport, necessary visas, immunization inoculations, letters of
authorization from the home institute, USDA and proper officials in the
country of search, showing names of cooperating institutions and/or
individuals collaborators. Field notes
should be taken of the names of contacts, villages, farms, host plants, other
pests noted, and possible sources of beneficial organisms for other crops,
etc. Maximizing Success
Potential and Reducing Risks A potential for
maximizing biological control successes is the placement of the various natural
enemy groups into different risk categories before proceeding with data based
decisions for introduction. Although the full impact of natural enemies which
have never been studied is impossible to accurately predict before
establishment (Coppel & Mertins 1977, DeBach 1964, 1974; Ehler 1979,
Miller 1983), and therefore involves empirical judgment, there is
nevertheless a strong desire that the process proceed with an educated
empiricism (Coppel & Mertins 1977, Ehler & Hall 1982, Legner 1986b). Whatever the
theory behind biological control by natural enemies, it is still one of the
most awesome weapons in our arsenal of pest management techniques. Because of
its relative permanency, mistakes cannot be readily corrected. Imported
organisms, once established, are not easily extirpated; and in some instances
their elimination is impossible altogether, regardless of the amount of
effort and funding. There is, therefore, some risk involved in any biological
control approach. But risks are a companion to life itself and any pest
management strategy involves some degree of risk, with alternatives to
importation of natural enemies undoubtedly being more formidable (Legner 1986b, Pimentel et
al. 1984). Trying to eliminate too much risk through government regulation is
not advisable as it can have the paradoxical effect of making life more
dangerous as well as more expensive and less convenient (see Huber 1983). The broad nature
of biological control including manipulation of vertebrates, arthropods and
pathogens, allows categorization of two major risk groups according to (1)
risks to the environment and health of humans and domestic animals, and (2)
risks of making wrong choices which may preclude or adversely affect
biological control at a later date. Environmental
risks are of especial concern in the biological control of weeds, where both
arthropods and pathogens are candidates for importation. The use of vertebrates
for biological control of terrestrial pests is loaded with potential risk and
is rarely practiced. An apparent desirable example is the common myna bird, Acritotheres
tristis L., importation from India to tropical areas for insect
control. However, mongoose, Herpestes auropunctatus birmanicus
(Hodgson), importation from India to tropical islands for rat, Rattus
spp., control and giant toad, Bufo marinus (L.), from America
to tropical islands and Australia for insect control have produced undesirable
side effects, either through numerical abundance or in the latter example by
predation of beneficial dung beetles (Macqueen 1975). Environmental
risks are minimized when vertebrates such as fish are imported to restricted
aquatic ecosystems for the biological control of noxious aquatic weeds,
mosquito habitats or mosquitoes and chironomids. Such fish can be studied
under natural conditions, but in isolation for adverse effects before being
widely disseminated. Yet, there are still possibilities that undesirable
unforseen behavioral and adaptive traits, such as spawn-feeding on other
desirable fish species, or an extension of subtropical species into temperate
climates (e.g., Gambusia spp.) may be expressed once populations are
allowed to establish broadly (Legner & Sjogren 1984). The risk of
making wrong choices of parasitic and predatory arthropods, especially host
specific ones, does not pose obvious environmental threats, as the outcome of
the establishment of an innocuous natural enemy is the pest density remaining
at status quo; although there is some theoretical debate on that issue (Ehler
1982, Turnbull 1967). However, wrong choices could possibly preclude the
achievement of maximum biological control (Force 1970, 1974; Legner 1986a), and add to
the list of failures, so that careful decisions are desirable (Franz 1973a,
1973b; Hughes 1973). The need for choosing the best biological control
candidates has generated considerable discussion and controversy over the
past 2 1/2 decades, and continues to stir controversy (Ehler 1976, 1982;
Huffaker et al. 1971, Legner 1986b, Turnbull & Chant 1961, Pimentel et al. 1984, van den
Bosch 1968, van Lenteren 1980, Watt 1965, Zwolfer 1971, Zwolfer et al. 1976).
However, the manner in which the best biological control candidates are
chosen is not clearly delineated for most groups of organisms (Coppel &
Mertins 1977, DeBach 1974, Pimentel et al. 1984); albeit there is a common
desire for prejudgment, if for no other reason than to expedite a biological
control success. Securing Natural
Enemies in the Native
Range Some of the most
dramatic successes in biological control, where the target pest's population
density is permanently reduced to below the economic threshold, involved the
introduction of one or two species of natural enemy (DeBach 1964, 1974;
Clausen 1978, Franz 1961a, 1961b; Franz & Krieg 1982, Hagen & Franz
1973, Luck 1982, van den Bosch 1971), in both stable and unstable habitats
(Hall et al. 1980, Ehler & Miller 1978). The usual procedure when a pest
species invades a new area is to seek natural enemies in its native home. The
first and most widely known biological control success, the cottony-cushion
scale, Icerya purchasi Maskell controlled by Cryptochaetum
iceryae (Williston) and Rodolia cardinalis (Mulsant),
followed that pattern (Quezada & DeBach 1973). The scale invaded
California and the natural enemies were found in its native range, southern
Australia. It seemed logical to follow the same format with subsequent
biological control efforts; and indeed this is still considered one of the
first approaches for a newly-invaded pest. However, using this approach
solely restricts the number and kinds of successes that can be realized. Searching Outside
the Native Range In many parts of
the world, especially Europe, Africa and much of Asia, there are numerous
native pests whose natural enemies are incapable of maintaining density
levels below the economic threshold under prevailing agricultural management.
What may be done other than costly and hazardous cultural and chemical
control? Pimentel (1963) and Hokkanen & Pimentel (1984) pointed out the
best approach for successful biological control. In many instances, the
natural enemies which caused significant drops in population densities of
organisms had never experienced evolutionary contact with their hosts. When
we consider other cases than those exemplified by the
host/parasitoid/predator relationship in cottony-cushion scale, we find
examples of great reductions of a population density by organisms that
originated in places other than the native home of the host. Such cases may
include the devastation of desirable native species by accidentally invaded
organisms. Well known examples to illustrate this phenomenon are the American
elm, Ulmus americana L., destroyed by the fungus, Ceratoystis
ulmi (Boisman) C. Moreau, of eastern hemispheric origin and vectored
primarily by the European beetle Scolytus multistriatus
(Marsham); the American chestnut, Castanea dentata (Marsham)
Borkhauser, practically eliminated by a fungus, Endothia parasitica
(Murriu) Anderson and Anderson, of Asian origin; and Asiatic citrus destroyed
by Icerya purchasi from Australia before biological control
efforts reduced the scale's density. There is a
history of successful biological control against invaded pests by organisms
actively secured in areas other than the native home. Famous examples are the
European rabbit, Oryctolagus cuniculus (L.), regulated by a
myxomytosis virus of South American origin and the black scale, Saisettia
oleae (Bernard), of probable northern African origin (D. P. Annecke,
pers. commun.), regulated by Metaphycus helvolus (Compere) from
extreme southern Africa. Also, the sugarcane borer, Diatraea saccharalis
(Fab.), of the Neotropics regulated by Apanteles flavipes
(Cameron) from northern India; the coconut moth, Levuana iridescens
Bethune-Baker, native to Fiji, regulated by a parasitoid, Bessa remota
(Aldrich) secured from Malaya; and Oxydia trychiata (Guenée) in
Colombia regulated by Telenomus alsophilae Viereck from eastern
North America (Bustillo & Drooz 1977, Drooz et al. 1977). Many other
examples exist (Pimentel 1963, Pimentel et al. 1984), which has led to some
speculation that the best natural enemies for biological control might
be those that have not experienced close evolutionary contact with the target
organism. The theory considers that the host and its natural enemies coevolve
to a balanced point where the host may exist at a relatively higher density
then where no coevolutionary balance has had a chance to evolve. Although the
examples of drastic impact on a host by natural enemies without recent
preevolutionary contact are numerous and impressive, there are equally
impressive and thorough examples of host reduction in which natural enemies
were obtained from the native home where coevolution has occurred. The
cottony-cushion scale and Comstock mealybug, Pseudococcus comstocki
(Kuwana) (Ervin et al. 1983) successes illustrate this clearly. Thus, we
would not want to deemphasize the native home as suggested by Hokkanen and
Pimentel (1984). In fact, in a recent analysis Hokkanen (1985) concluded that
there are no differences of biocontrol success according to the origin of the
pest, and that native hosts can be completely controlled by introduced
natural enemies exactly as exotic ones. However, as time goes on, one would
expect examples of the latter to drop proportionally because the former
include accidental invasions and random acquisitions, as well as planned
biological control attempts. There are some
antagonists to the approach endorsed by Hokkanen and Pimentel, especially
among the biological control of weeds researchers (Goeden & Kok 1986,
Schroeder & Goeden 1986). They argue that the record in the case of weeds
supports the native home approach most strongly. However, the record does not
seem wholly convincing evidence against Hokkanen's position, because
historically most biological weed control efforts emphasized the
native home in the search for natural enemies. Thus, statistically the
argument is biased and seems weak. Hazards & Awkward
Situations Encountered in the Field Researchers exploring for natural enemies in the field
frequently encounter situations that are hazardous or at least unpleasant. The account by Dr. Alfred Boyce of his discovery of the citrus
red scale parasitoid, Aphytis melinus in northern Pakistan clearly
illustrates this. Dr. Boyce had
obtained the original cultures from that region that was typically undergoing
intense political unrest. He was able
to bring out living cultures “in a hail of bullets” as he once described it
to Dr. Fred Legner. In his search
for natural enemies of common house and stable flies, Dr. Legner often found himself in awkward and even
dangerous circumstances, stemming from suspicions by local inhabitants of
techniques involved in the retrieval of host material from animal waste
habitats. Once in San Jose, Costa
Rica while processing samples of cattle manure for the presence off ly puparia
the director of the National Museum complained bitterly about such
“uncivilized” activity. In Central
Africa while searching for nests of the mountain gorilla, a prime breeding
site for Musca domestica, the Congo guides accompanying Legner and an
associate from Harvard University became suspicious about the collectors’
motives, probably suspecting witchcraft.
Legner’s Harvard companion who understood the local dialect alerted
the team to the unsettling remarks being made by the guides. This prompted an immediate cessation of
collection activity and a rapid return to base camp at Travelers’ Rest in
southwestern Uganda. That night
Congolese rebels stormed into the premises confiscating the area around the
bar; and after becoming quite drunk tore up the premises by breaking furniture
and urinating liberally around the place.
While exploring
in and around the area of Queen Elizabeth National Park in western Uganda,
the accommodations at the park had been pilfered such that there were no
mattresses on the beds, and the water faucets had been removed from outside
taps. At night elephants and hippos
converged on the area to obtain water seeping from the broken taps, which
precluded one’s ability to visit adjoining bathroom facilities. In the same area
of western Uganda while driving on a dirt road in tall grass country, a
mother elephant and her young crossed directly in front of the
automobile. After seeing the vehicle
the elephant returned to face the challenge!
A stand-off ensued whereby every time the car moved the elephant
returned with great agitation to ward off the intruder. Finally after part of an hour of this
conflict, Legner and his family who had accompanied him on this expedition,
made a quick dash ahead on the road to escape the irate elephant. One time the
automobile sustained a flat tire in a remote region of northern Uganda, where the dress code of
the inhabitants was sparse or nonexistent.
During the 20 minutes that it took to change the tire, people had
gathered in large numbers around the area to view the procedure. On completion and placing the damaged tire
into the trunk of the car, Dr. Legner was tapped on the shoulder by one of
the throng The man held up a
screwdriver that had mistakenly been left on the road bed, and in perfect
King’s English commented, “Sir, you left this on the ground!” In 1966 just
prior to the reign of Idi Amin, ominous drums were sounding in and around
Kampala, the research station that housed the researchers searching for
natural enemies of house flies and other pest insects. Local European residents talked frequently
of witch doctors predicting terrible events.
This made carrying on one’s collections difficult to say the least as
great efforts were made not to upset the inhabitants residing in remote
areas. A search in
Israel for fly breeding sites during late 1966 happened to take Dr. Legner
and colleague Dr. Dan Gerling to the border area between Israel and Jordan,
just north of Beersheba. A person was
noticed on the road ahead, and the custom was for motorists to offer rides to pedestrians. However, on closer examination it was
noted that the person was wearing the uniform of a Jordanian soldier, and no
ride was offered. That night they
learned that the road they had been driving on earlier in the day was booby
trapped, resulting in the death of several
Israeli patrol guards. This
started an immediate build-up of armed personnel in Beersheba and soon
afterwards led to the 6-day war.
Attempts to visit collection sites in the Sinai and Eilat were then
thwarted by Egyptian MIG jets that were strafing cars on the highways. Judgments of
Natural Enemy Capability Ways in which
the capabilities of a biological control agent are judged, as well as the
environmental threats, vary for different groups of organisms. If we consider
in descending order of environmental risk, the terrestrial vertebrates first,
followed by zoopathogens, phytopathogens, phytophagous arthropods,
terrestrial scavengers (e.g., scarab beetles), aquatic vertebrates and
invertebrates, and finally parasitic and predatory arthropods, it would be
logical to screen the first group more thoroughly than the last. However,
judgments of potential effectiveness would probably require more effort for
the last group and least effort for the first, because of problems in
measuring dispersal and other behavioral traits, as will be explained. Terrestrial Vertebrates.--such as the mongoose, myna bird and giant toad are more
readily observed in their places of origin because of their size, so their
attributes may be more easily viewed. However, they are also capable of
becoming conspicuous additions to the general landscape, and without natural
predators of their own may have the capacity to soar in numbers in the areas
of their introduction. Thus, they may pose the threat of becoming pests
themselves because of their numerical abundance and often nonspecific feeding
behavior, as well as the side effects this can have on native and other
desirable fauna and flora. Phytophagous Arthropods and
Phytopathogens.--have traditionally evoked the most thorough of preintroduction
studies to safeguard desirable plant species in the areas of introduction
(Ehler & Andres 1983. Goeden 1983, Harris 1973, Huffaker 1957, Klingman
& Coulson 1982). Host-plant specificity is strongly emphasized (Harris
& Zwolfer 1968, Zwolfer & Harris 1971). Past screening has been so
successful that among the numerous importations of beneficial phytophagous
arthropods and pathogens around the world (Julien 1982), there has never been
any widespread occurrence of harmful behavior shown by the organisms
imported. Rare reports of beneficial phytophagous arthropods feeding on
desirable plant species after importation (Greathead 1973), usually involved
temporary, geographically restricted alterations of behavior during the
establishment phase when the colony contracted in size due to its inability
to survive and reproduce on alternate host plants. Such dire reports have
been, nevertheless, magnified way out of proportion and cited out of context
as was done recently by Pimentel et al. (1984). Or an obscure wild plant or
recently cultivated variety or relative of a targeted weed may come under
attack by a phytophagous arthropod introduced earlier to combat the weed, as
presently has occurred in northern California with imported natural enemies
of Klamath weed, Hypericum perforatum L., and a species of Hypericum
used for roadside planting (Andres 1981). The benefits
derived from importation of phytophagous arthropods and phytopathogens are so
vast and levied against weeds that cannot be controlled effectively,
economically nor safely with any other strategy, that biological control will
continue to be a major effort. The risk involved has been and should continue
to be minimized by the extensive studies required prior to importation. Terrestrial Scavengers.--include scarab beetles that remove excess cattle dung
accumulated in grazing areas to improve pastures, and to control the
symbovine flies, Haematobia irritans (L.), Musca autumnalis
deGeer, and Musca vetustissima Walker, primarily. Although
dramatic successes have been achieved in the removal of dung by the
importation of several species of exotic scarabs in Australia, Hawaii,
California and Texas (Legner 1978a, Legner & Warkentin 1983, Macqueen 1975,
M. M. Wallace, pers. commun., Waterhouse 1974), there apparently have been no
widespread concurrent practical reductions of fly densities (Legner 1984, M. M. Wallace,
pers. commun.). In some instances fly densities may have actually increased
in the presence of established dung-burying scarabs. Although laboratory and
field experiments predicted practical fly reductions by the dung scattering
activities of the scarabs, in pastures several forces interplay to thwart
experimentally based predictions. Elimination of predatory arthropods and
increase of available larval breeding habitat could be two of the principal
causative factors (Legner & Warkentin 1983, Legner 1984). Terrestrial
organisms that alter large habitats, such as scarab beetles, are especially
risky biological control candidates because their activity may overlap
portions of the niche of other species so that potential disruptive
side-effects among organisms in different guilds exist. The outcome for
future symbovine fly control may be undesirable in that some potentially
regulative natural enemies, such as certain predatory arthropods, may not be
difficult to establish in the disrupted habitat (Legner 1986a). In California
and Texas the predatory staphylinid genus Philonthus is severely
restrained from colonizing the drier dung habitat created by Onthophagus
gazella F. (Coleoptera: Scarabaeidae) activity (Legner 1986b, Legner &
Warkentin 1983, Roth et al. 1983). Furthermore, various nongraminaceous
weed species often invade California irrigated pastures that sustain large
populations of exotic scarab beetles, so that mechanical pasture renovation
again is required (Legner & Warkentin 1983 ). Aquatic Vertebrates
and Invertebrates.--include herbivorous fish for biological aquatic weed
and arthropod control and Turbellaria and Coelenterata for arthropod control.
The minnows Gambusia and Poecilia are used worldwide in the
biological control of mosquitoes (Legner & Sjogren 1984, Legner,
Sjogren & Hall 1974). However, the threat
to endemic fish has caused widespread concern so that alternatives in the use
of native fishes are under consideration (Legner, Medved & Hauser 1975, Walters &
Legner 1980). Because fish
can be manipulated readily, the potential for resident species to increase
their effectiveness as natural enemies is greater than with terrestrial
organisms where widespread natural dispersion may have already covered most
possibilities. A group of cichlid fish has been
imported from Africa to the southwestern United States for the biological
control of mosquitoes, mosquito habitats and chironomid midges. Although the
degree of control achieved by the three species imported varied in different
parts of the targeted area, circumstances beyond the control of researchers
preempted a broader success. The fish species referred to are Tilapia zillii
(Gervais), Sarotherodon (Tilapia) mossambica (Peters),
and Sarotherodon (Tilapia) hornorum Trewazas, which were
imported to California for the biological control of emergent aquatic
vegetation that provides a habitat for such encephalitis vectors as the
mosquito Culex tarsalis Coquillet, and as predators of
mosquitoes and chironomid midges. Careful studies under natural, but
quarantine, areas in California showed that the different fish species each
possessed certain attributes for combating the respective target pests
(Legner & Medved 1973). Tilapia zillii was best able to perform
both as a habitat reducer and an insect predator. It also had a slightly
greater tolerance to low water temperatures, which guaranteed its survival
through the winter months in southern California, while t the same time it
did not pose a threat to salmon and other game fisheries in the colder waters
of central California. It was the superior game species and most desirable
for eating. Nevertheless,
the agencies supporting the research (mosquito abatement and county
irrigation districts) acquired and distributed all three species
simultaneously throughout thousands of kilometers of irrigation system, storm
drainage channels and recreational lakes. The outcome was the permanent and
semipermanent establishment of the two less desirable species, S. mossambica
and S. hornorum over a broader portion of the distribution
range. This was achieved apparently by a competitive superiority rendered by
an ability to mouth-brood their fry, while T. zillii did not
have this attribute strongly developed. It serves as an example of
competitive exclusion such as conjectured by Ehler & Hall (1982). In the
clear waters of some lakes in coastal and southwestern California, the
intense predatory behavior of S. mossambica males on the fry of
T. zillii could be easily observed, even though adults of the
latter species gave a strong effort to fend off these attacks. This outcome was
not too serious for chironomid control because the Sarotherodon
species were quite capable of permanently suppressing chironomid densities to
below annoyance levels (Legner, Medved & Pelsue 1980). However, for
control of higher aquatic weeds, namely Potamogeton pectinatus
L., Myriophyllum spicatum var. exalbescens (Fernald)
Jepson, Hydrilla verticillata Royle and Typha species,
they showed no capability whatsoever (Legner & Medved 1973). Thus,
competition excluded T. zillii from expressing its maximum
potential in the irrigation channels of the lower Sonoran Desert of
California and in recreational lakes of southwestern California. Furthermore,
as the Sarotherodon species were of a more tropical nature, they died
out annually in the colder waters of the irrigation canals and recreational
lakes. Although T. zillii populations could have been
restocked, attention was later focused on a potentially more environmentally
dangerous species, the white amur Ctenopharyngodon idella
(Valenciennes), and other carps. The substitution of T. zillii
in storm drainage channels of southwestern California is presently impossible
because the Sarotherodon species are permanently established over a
broad geographic area. Parasitic and
Predaceous Arthropods.--(Insecta and Acarina) are in a distinct category which
usually defies accurate prejudgment of biological control potential.
Theoretical guidelines based on laboratory studies and mathematical models
are not always useful to judge performance in nature. The extremely small
size of parasitic and predaceous arthropods, their high dispersal capacity,
unique sex determination mechanisms, differential response to varying host
densities and climate, distribution patterns and size, unreliable sample
techniques, dependence on alternate hosts and possibilities of rapid genetic
change at the introduction site (Attique et al. 1980, Eikenbary & Rogers
1973, Legner 1986b, McMurtry et al. 1978, Messenger 1971, Mohyuddin et al.
1981), make predictions of their performance highly uncertain. Even
sophisticated population models such as those developed for the winter moth, Operophtera
brumata (L.), could not predict the exceptional performance of the
tachinid parasitoid Cyzenis albicans Fallen against this host
in Canada (Embree 1971, Hassell 1969a, 1969b, 1978, 1980; Waage & Hassell
1982). Because risks to
the environment posed by parasitic and predaceous arthropods are very low, as
previously considered, the inability to predict their impact has not been a
major obstacle to their deployment in successful biological control. At the
same time selection of these biological control agents for importation has
not been unsophisticated and lacking in scientific judgment as was suggested
by van Lenteren (1980). There are valid scientific criteria for deciding
probable good candidates, which are especially useful for elimination of
those with little likelihood for success or which possess certain undesirable
characteristics such as hyperparasitism (Luck et al. 1981). Coppel &
Mertins (1977) proposed a list of 10 desirable attributes of beneficial
organisms to aid in assessment of their capabilities prior to widespread
dissemination, which are closely interrelated and difficult to separate.
Nevertheless, they categorize organisms and weigh their potential according
to a scientific plan. The list, obviously developed from efforts on prior
biological control projects, considers ecological capability, temporal synchronization,
density responsiveness, reproductive potential, searching capacity, dispersal
capacity, host-specificity and compatibility, food requirements and habits,
hyperparasitism and propensity for culture. Additional categories of
importance to a broad understanding of the niche of a potential biological
control agent are systematic relationships and morphological attributes
(e.g., fossorial structures, heavy sclerotization), and anatomical (e.g.,
type of spermatheca), and physiological attributes (e.g., synovigenic or
proovigenic), cleptoparasitism, and genetic data (e.g., number of founders,
collection locality, strain characteristics). Consideration of these
attributes in a more holistic approach to natural enemy acquisition is
desirable because it incorporates interrelations among qualifications which
cannot be detected from an accumulation of single, even well quantified sets
of data. Biological
control researchers have traditionally acquired data under these various
categories whenever possible, which has greatly aided in the interpretations
of the dynamics in biological control successes. However, there has not been
a systematized plan for data acquisition and storage, which can be attributed
to funding primarily. The collection
of facts in the different groups is meant not only to form a data base for
more accurate predictions of success, but also to raise biological control
pursuits to a more intercommunicative realm. The absence of a data collection
system in the past has unquestionably resulted in the loss of valuable
information about biological control organisms. Critics of a more
systematized data acquisition scheme point to the weaknesses of data secured
in experimental fashion, but overlook the fact that even incomplete data can
elevate one's understanding to the "educated empiricism" of Coppel
and Mertins (1977). Although there
is ever more room for additional information about the natural enemies of a
given host to help the foreign explorer, it is becoming increasingly possible
to appraise performance in nature. This knowledge comes from a combination of
laboratory and field studies both in the places of origin of the respective
natural enemies and at their introduction sites. For example, in
the parasitoids attacking endophilous synanthropic flies, we find the species
naturally distributed within certain ecological zones. Cooler, more humid
environments harbor different species and strains than those found in hot and
drier areas. Marked seasonal abundance, host and microhabitat preferences are
demonstrated by the different species (Legner 1986b). Thus, it is
possible to estimate which species is best suited for biological control in a
given area based on knowledge of its ecological requirements. Additionally,
accumulated information on temporal synchrony with the target hosts allows
for a high degree of certainty in the prediction of which species is most
capable of exerting a regulative effect on single host species in a
multi-host habitat (Legner 1986b). Data on density responsiveness, reproductive potential
under different ambient temperatures and RH, searching capacity in different
environments and strata of the host habitat, dispersal rates, host
specificity and parasitoid food requirements, systematics, synovigenic
characteristics, mass production and genetic variability provide a base from
which to judge the likely performance of particular species in different
areas. It also provides a means to properly sample for host destruction
(Legner 1986b). In Australia
there is a widespread opinion that predatory and parasitic natural enemies of
symbovine flies have been duly tested in biological control based on previous
attempts at introduction. However, basic information now available on species
that were tried, such as Aphaereta pallipes (Say), Aleochara
tristis Gravenhorst and Heterotylenchus, suggest that these
candidates were never suited to their targeted hosts in the introduced
environment. They were incapable of exerting much pressure against their
hosts because of different climatic
preferences (Legner 1986b). Research that
has been performed on the pink bollworm, Pectinophora gossypiella
(Saunders), navel orangeworm, Amyelois transitella (Walker),
and carob moth, Ectomyelois ceratoniae (Zeller) has already
laid the foundation for accurate decisions on which species of natural
enemies have a potential for reducing their respective host densities (Legner
1986b, Naumann &
Sands 1984, Sands & Hill 1982). Clues were found to which regions of the
world might be searched for additional candidates. A common
criticism of a systematized approach that there is lack of adequate funding,
suggests that a certain degree of adequacy in financial support ought to be
secured before new projects are embraced. More biological control researchers
are faced with the necessity for holistic studies with the outcome that basic
data are obtained more frequently. In a recent example, the biological
control of chestnut gall wasp, Dryocosmos kuriphilus Yasumatsu,
in Japan was guided largely by data acquired about the natural enemies in
their place of origin, China (Murakami & Ao 1980, Murakami et al. 1977).
Another example is the Comstock mealybug biological control success in
California (Meyerdirk & Newell 1979, Meyerdirk et al. 1981), which was
guided by basic research on natural enemies in Japan (Murakami 1966). Also,
the success of the North American egg parasitoid, Telenomus alsophilae,
against the South American geometrid, Oxydia trichiata
(Bustillo & Drooz 1977) was based on results of studies on the parasitoid
in North America (Fedde et al. 1979). Considerations on
Geographical Origin of the
Pest A well conducted
natural enemy introduction program requires an initial realistic appraisal of
the pest problem and the chances for success. Natural enemies are sought in
the native home of the pest and/or in an area which includes a climate
similar to that of destination. Species which restrict their attack to the
pest or a close relative of the pest are preferred, and those natural enemies
that possess the highest degree of preference for the pest are usually chosen
for final field release. During the search, natural enemies are collected
from all possible habitats to insure the inclusion of cryptic forms and
races. Special attention is given to the species of host plant on which the
pest is problematic. Biologies, host associations and species attributes are
ascertained automatically during the rearing and transfer process. The Nearctic
insect fauna is large, including 30 orders, 500 families and about 12,000
genera and 150,000 species (Ross 1953). Knowledge about the origin and
dispersal patterns of insects is in reality very spotty; therefore, the
origin and evolution of the North American insect fauna is largely a subject
to speculate and for making assumptions. It is generally held that the
Palearctic was the center or origin for many of the ancestors of new North
American insects. Although much
can be inferred about the past history of species from studies of their
present range and recent changes in distribution, the fossil records provide
the most objective. Although the staphylinid beetle Oxytelus gibblus
is presently restricted to the western Caucasus Mountains, the fossil records
show that this species was extremely abundant in Britain during the last
glaciation. The western Caucasus, then, probably represents the last stand
of the species rather than its place of origin. The carabid
subgenus, Cryobius, has its center of distribution in northeastern
Siberia and northwestern America. However, it was represented by a greater
number of species in western Europe during the Wisconsin glaciation, although
none are found there at the present time. The evolution of
the mosquito genus Culex has been studied through observations of
progressive changes in structures of the male genitalia. The genus apparently
spread through Africa where it gave rise to a leading line, guardi.
Seven different lines were formed, all but one remaining confined to Africa.
The exception, Culex pipiens L., which apparently spread to
India, produced new lines. Some of these eventually reached North America via
South America giving rise among others to the species Culex tarsalis
Coquillett. Were it not for the survival of connecting links in Africa and
Asia, we might think that this species group originated in South America. Much of our
native insect fauna is so old that we have no basis for even discussing its
place of origin. For biological control it suffices that this is the native
home. If species invade other areas and become pests, natural enemies ought
to be sought here. The concentration of species in a particular area may, in
fact, reflect more their common environmental needs than the center of
dispersal after relatively recent speciation in that area. A large complex of
natural enemies has been stated to indicate the site of longest residence
(native home) of a species, and especially if one or more natural enemies are
host specific. For biological
control it may not be necessary to pin-point the place of evolution of a
species but rather its place of recent origin in order to locate the
best natural enemies. "Recent" is a dubius term. It could be a few
hundred or thousands of years. However, natural enemy complexes efficient in
regulation of a targeted pest may evolve quicker than previously imagined, so
that paleoentomology may not be too important in biological control. The region of
origin of certain pest species is known without any doubt. Included are Icerya
purchasi, Hypericum (Klamath weed), Opuntia cactus in
India and Australia, rabbits in Australia, eucalyptus snout beetle, Dutch elm
disease, chestnut blight, olive scale, walnut aphid, navel orangeworm (Amyelois
transitella), grape leaf skeletonizer (Harrisina brillans
Barnes & McDunnough), and many more. The origin of other pests is open to
speculation, with the following examples illustrating some of the
difficulties involved. Saissetia oleae (Bernard), the black scale
on citrus, originally was believed to have originated in East Africa. Harold
Compere imported 30 species of parasitoids from East and South Africa during
1936-1937, with five becoming established in the United States. No
appreciable reduction in host density was caused by most species. However, Metaphycus
helvolus (Compere) from Capetown, South Africa proved to be very
successful in permanently lower black scale densities. The host scale is now
believed to have originated in northern Africa and not within the range of
its most effective parasitoid. Circulifer tenellus (Baker), the beet
leafhopper, is a serious pest of sugar beets, tomato and other crops as it
vectors the curly top virus. This leafhopper possesses strong migratory
habits, moving hundreds of miles each spring and early summer to cultivated
crops. Systematics have played an important role in determining the origin of
this insect. It was originally thought to be from Australia under the genus
name Eutettix. Parasitoids shipped from Australia failed to establish
in North America. Oman (1948) reclassified the leafhopper as Circulifer
and thought it originated in the arid portions of the Mediterranean and
Central Asian regions. A total of 36 shipments of parasitic material was
received during 1951-1954 (Huffaker 1954). Twelve parasitoid species were
involved, but the identity of all species is still not positive. Only two
released species were ever recovered as Lymaenon "A" and Polynema
"A." Further searches in Asia might be worthwhile. Heliothis zea (Boddie) has been described as several species due to a great
variability in color and markings. It is widespread within 40o N. to 49o S.
Lat. Originally it was thought to have originated in the West Indies because
of the fact that it feeds there particularly on American plant genera, such
as tomato, corn, etc. It is of rare occurrence in Europe and this would
indicate to some that it originated there where a better natural enemy
complex might exist. Various parasitoids were imported against it with some
Braconidae and Tachinidae showing some success after their discovery in
India. Native predators are presently thought to be most useful against H.
zea, but not usually to a satisfactory control level. Further searches
in Asia and possibly Africa might be worthwhile. Cydia
(Carpocapsa) pomonella (L.), the codling
moth, damages pome fruit and some stone fruits. This species was known in
Europe in ancient times (around the 4th Century B.C.). The codling moth is
widely distributed throughout the world, but it is still apparently of little
consequence in parts of China and Japan. Its northern limit is determined by
minimum heat in summer. The presence of the moth in America, Australia, South
America, South Africa and eastern U.S.S.R. is thought to be of recent
occurrence. Its probable point of origin is in the central Palearctic where
wild apples, Malus silvestris, occur. A long list of natural
enemies is known, which undoubtedly reflects the large number of researchers
who have studied this pest. Some natural enemies were introduced from Spain,
eastern North America and the Middle East to various countries, but only a
few became established without showing any control (Clausen 1978).
Considering the great importance of this insect, it is surprising that a
greater effort has not been made to control it biologically. In Europe, for
example, several potentially very effective parasitoids are kept from
expressing themselves fully due to hyperparasitism. The primary parasitoids
might be imported to America where their capabilities could be fully
expressed. Also, an intensive search in northern China, southern Siberia and
Japan might turn up some effective natural enemies. Aonidiella aurantii
(Maskell), the California red scale, is found between 40o N. and 40o
S. Lat., but it is at pest status only in the subtropics. This scale has a
wide host range but prefers citrus and roses. Using the last of three leads
for tracing the area of origin [ (1) the area where the preferred host originated--citrus,
(2) the area where the pest is present but kept at low densities by natural
enemies--the Far East, and (3) the area where an abundance of related species
exists--Neotropics], a search was begun in South America in 1934-1936, where
17 species of Chrysomphalus were reported. None of these were
effective in biological control. The Far East was searched subsequently, but
it took from 1905 to 1941 to establish a parasitoid, Comperiella bifasciata
Howard. Problems which hindered finding the right species included the sago
palm host plant approach for locating parasitoids, which failed because it
made host scales immune to attack. There were also numerous host
misidentifications. Aphytis lingnanensis Compere and A. melinus
DeBach were later successfully imported from the Far East. The resulting
success was attributed to the fact that parasitoids were sought from the
whole geographic range of the host in the East. Tetranychus spp. Tetranychid mites are pests of worldwide distribution
which are primarily found in the subtropics. There are 200-250 species of
economic importance, but there is limited information on the native home of
any species. Thee have been some inferences made on the native homes of the
European red mite, Panonychus ulmi (Koch) and citrus red mite (Panonychus
citri (McGregor), however (J. A. McMurtry, pers. commun.). Introductions of
predatory mites have been rather scanty, and should be continued before any
conclusions are drawn. Phytoseuilus persimilus Athan-Henriot
was released in periodic mass liberations, and has been successfully used to
prevent phytophagous mite outbreaks in greenhouses and on strawberries. Two
phytoseiid species were established on citrus mite pests in Israel, and 12
phytoseiids were released on avocado and 9 against citrus red mite in
southern California. Results are too recent in the California introductions
to determine permanency. Insecticide resistant strains of Typhlodromus
occidentalis Nesbitt have been produced and released in various
agroecosystems in California and Oregon (Croft 1970, Hoy et al. 1982). Phthorimaea operculella
(Zeller), the potato tuberworm, is presently cosmopolitan. Some
workers consider America to be the native area based on the origin of its
principal food plants, most of the wild progenitors of which originated in
South America. However, the first successful introduction against this
presumably American species was to France of Bracon gelechiae
Ashmead, where infestations were reduced. This parasitoid was later
successfully introduced in Australia, Asia, Africa and other portions of
North America. Other species are currently being tried and it is probable
that some new finds in South America will provide even greater control.
Nezara viridula (L.), the southern
green stinkbug, is probably of African origin. This pest is especially
important in tropical and subtropical areas of the world (Davis 1967). It
attacks 60 or more unrelated species of plants. The Egyptian parasitoid, Microphanurus
basalis (Wollaston) was successfully introduced into Australia, Fiji
and Hawaii, where it was effective only in the more tropical portions.
Further attempts should be made to secure parasitoids from the cooler
portions of the pest's range in Africa. Pectinophora gossypiella (Saunders), the pink
bollworm is now cosmopolitan. However, recent advances in the taxonomy of the
genus have placed its origin in the vast Australasian region. Importations of
natural enemies from the northwestern part of Australia and southeastern
Indonesia and Malaysia have just begun. But this was preceded by 60 years of
work with parasitoids that were secured from Europe, Africa and India,
yielding poor results (Common 1958, Legner & Medved 1979, Wilson 1972).
Unfortunately, some ignore this breakthrough in locating the probable area of
origin and hold the previous 60 years of failure as proof for being
unable to control pink bollworm biologically. Diptera of
Medical and Veterinary Importance, include the genera Musca, Fannia, Culex,
Aedes, and Anopheles, which are becoming more difficult to
control with insecticides and by cultural means. Emphasis is now being placed
on biological control. Unlike agricultural pests, medical and veterinary
pests are more difficult to evaluate because economic loss data is not
readily available. Therefore, although significant achievements have been
made with biological control of several species, the actual population drops
have not often been measured. [see Reviews] Future Direction
and Emphasis Hokkanen (1985b)
has recently addressed the question of "where do we go from here"
to maximize success in biological control. In a concluding statement,
Hokkanen (1985) considered the following: "Several
authors emphasize the importance of intellectual and material resources, as
well as a functioning institutional and administrative framework to any
successful biological control program. In a discussion about the factors
affecting establishment of exotic entomophages, van den Bosch proposed that
'a significant, perhaps even major, proportion of the introduced entomophages
never had a chance of establishment and never should have been introduced.'
He considered that biocontrol failures most often result from inadequate
information about the pest-natural enemy system, or from lack of persistence
in attempts, coupled with indifference in attitudes, as well as from
technical problems such as difficulties in propagating and liberating the
control agents." "Beirne
discussed these problems in greater detail, emphasizing inadequacies in
selection and shipment of parasitoids, inadequacies in colonization
procedures, and administrative constraints. The latter include financial
support, which tends to terminate when projects do not show signs of quick
success. Sailer added to this a discussion on the influence of economic
policy and national priorities in research, as well as organizational
structure of the importation agency and the increasing concern for
environmental protection." "DeBach
concluded that 'one thing is clear: highly trained professional entomologists
enthusiastically devoted to their science furnished the main ingredient for
success in case after case,' to which Sailer added 'almost without exceptions
these people had the opportunity to receive the kind of professional training
needed and the opportunity to be employed by organizations well suited, if
not designed, to facilitate their work.'" "These
authors clearly pointed out that much of the potential of classical
biological control remains to be realized, and will come about with adequate
infrastructure and resources. They also give examples of missed
opportunities, where the failure to appreciate the role and potential of
natural enemies in suppression of pests and the defects of program management
have prevented or greatly delayed the biological control of important
pests." "Classical
biological control introductions can be viewed as grand scale experiments,
which provide unique opportunities for developing and testing ecological
principles, as well as for gaining economic benefits. Detailed studies on
already existing results from past biocontrol attempts should be carried out
to improve our understanding of the factors that affect both the economic and
ecologic success in biocontrol. However, the chain of events and choices most
likely leading to biocontrol success in any project will hardly ever be a
dull routine that can be programmed into a computer: it takes experienced,
innovate scientists to identify the weak or missing links, and to put the
pieces of art together, scientifically." Past classical biological control successes have relied heavily
on the interaction with other international organizations, especially the
Commonwealth Institute of Biological Control with headquarters in Curepe,
Trinidad. Various permanent and
temporary laboratories of this organization existed in all parts of the
world. Researchers there would host,
assist and otherwise interact with those of the United States Department of
Agriculture and the University of California to obtain beneficial
species. As independence from the
British Commonwealth developed among the different countries that maintained
laboratories, local support for their continuance diminished, and in many
cases ceased entirely. This has
resulted in a greater than 90% decrease in classical biological control
activity worldwide. Natural enemies
for use in biological control may be categorized into separate risk groups.
Parasitic and predaceous arthropods fit into the lowest risk category, but
are the most difficult to study and to assess for potential success. The policy of certain countries, e.g.,
Australia, of requiring intensive studies on native organisms before allowing
them to be exported is especially devastating to the deployment of biological
control. A recent case of invading
Australian wood borers that attack eucalyptus in America has already caused
the death of over half of the trees in California, while the importation of
effective natural enemies continues to move at a crawl. Yet progress is being made with increased
attention to basic ecological and behavioral research. The rate of biological
control successes may drop initially as the style of "educated
empiricism" (Coppel & Mertins 1977) becomes more widely adopted, as
has apparently already begun (Hall & Ehler 1979, Hall et al. 1980).
Success rates could be expected to increase as the data base enlarges and
intercommunication possibilities expand. Certainly the trend will ever more
propel the activity of exotic natural enemy importation into a solid scientific
base. Exercise 25.1--List the steps you would take to initiate a foreign
exploration for natural enemies of an newly invaded pest insects in
California. Exercies 25.2--What if the pest were confined to northern Minnesota or
Maine? Exercise 25.3--How would you study potentially valuable natural enemies
before their introduction? Exercise 25.4--If following the introduction and establishment of two
natural enemy species the pest still remained at densities above the economic
threshold, what might be done to improve biological control? REFERENCES: [ Additional references may be found at MELVYL Library ] Andres, L. A. 1981. Conflicting interests and the biological control
of weeds. In: E. S. Del Fosse (ed.), Proc. 5th Intern. Symp Biological
Control of Weeds, 1980, Brisbane, Qld., CSIRO, Melbourne, Vic., Australia:
11-120. Arthur, A. P. 1966. Associative learning in Itoplectis conquisitor
(Say) (Hymenoptera: Ichneumonidae). Canad. Ent. 98: 213-23. Attique, M. R., A. I. Mohyuddin, C. Inayatullah, A. A. Goraya
& M. Mustaque. 1980. The present status of biological control of Chilo
partellus (Swinh.) (Lep.: Pyralidae) by Apanteles flavipes
(Cam.) (Hym.: Braconidae) in Pakistan. Proc. 1st Pakistan Congr. Zool., B:
301-305. Bartlett, B. R. & R. van den Bosch. 1964. Foreign exploration
for beneficial organisms. In: P. DeBach & E. I. Schlinger (eds.),
Biological Control of Insect Pests and Weeds. Chapman & Hall, London. Beddington, J. R., C. A. Free & J. H. Lawton. 1978.
Characteristics of successful natural enemies in models of biological control
of insect pests. Nature 273: 513-19. Beirne, B. P. 1980a. The human transport of insect parasites of
insects across the Northern Atlantic. Ent. Gen. 6: 267. Beirne, B. B. 1980b. Biological control: benefits and
opportunities. In: "Perspectives in World Agriculture."
Commonw. Agric. Bur., Slough, England. 307. Bellows, T. S., Jr. & T. W. Fisher, (eds) 1999. Handbook
of Biological Control: Principles and Applications. Academic Press, San
Diego, CA. 1046 p. Birch, L. C. 1971. The role of environmental heterogeneity in
determining distribution and abundance, p. 109-28. In: P. J. den Boer
& G. R. Gradwell (eds.), Dynamics of Populations. Center Agr. Publ. Doc.,
Wageningen. Boldt, P. E. & J. J. Drea. 1980. Packaging and shipping
beneficial insects for biological control. FAO Plant Protect. Bull., Vol.
28(2): 64-71. Bucher, G. E. & P. Harris. 1961. Food-plant spectrum and
elimination of disease of Cinnabar moth larvae, Hypocrita jacobaeae
L. (Lepidoptera: Arctiidae). Canad. Ent. 93: 931-36. Bustillo, A. E. & A. T. Drooz. 1977. Cooperative
establishment of a Virginia (USA) strain of Telenomus alsophilae
on Oxydia trychiata in Colombia. J. Econ. Ent. 70: 767-70. Carl, K. P. 1968. Thymelicus lineola (Lepidoptera:
Hesperidae) and its parasites in Europe. Canad. Ent. 100: 785-801. Carl, K. P. 1982. Biological control of native pests by
introduced natural enemies. Biocontrol News & Information 3: 191-200. Cheng, L. 1970. Timing of attack by Lypha dubia
Fall. (Diptera: Tachinidae) on the winter moth Operophtera brumata
(L.) (Lepidoptera: Geometridae) as a factor affecting parasite success. J.
Anim. Ecol. 39: 313-20. Clark, R. C., D. O. Greenbank, D. G. Bryant and J. W. E. Harris.
1971. Adelges piceae (Ratz.), balsam woolly aphid (Homoptera:
Adelgidae). Tech. Commun. Commonw. Inst. Biol. Contr. 4: 113-27. Clausen, C. P. 1956. Biological control of insect pests in the
continental United States. U. S. Dept. Agric. Tech. Bull. No. 1139. 151 p. Clausen, C. P. (ed.) 1978. Introduced parasites and predators of
arthropod pests and weeds: a world review. Agric. Handb. No. 48, U. S. Dept.
Agric., Wash., D.C. 545 p. Cock, M. J. W. 1986. Requirements for biological control: an
ecological perspective. Biocontrol News & Information 7: 7-16. Common, I. F. B. 1958. A revision of the pink bollworms of cotton
[Pectinophora Busck (Lepidoptera: Gelechiidae)] and related genera in
Australia. Aust. J. Zool. 6(3): 268-306. Coppel, H. C. & J. W. Mertins. 1977. Biological Insect Pest
Suppression. Springer-Verlag, Berlin, Heidelberg, New York. 314 p. Coulson, J. R. (ed.). 1981. Use of beneficial organisms in the
control of crop pests. Entomol. Soc. Amer. Publ. Proc. Joint American-Soviet
Conf., Wash., D.C., Aug 13-14, 1979: 62 p. Coulson, J. R. & R. S. Soper. 1988. Protocols for the
introduction of biological control agents in the United States. p. 1-35. In:
R. Kahn (ed.), Plant Quarantine. CRC Press, Boca Raton, Florida. Croft, B. A. 1970. Comparative studies on four strains of Typhlodromus
occidentalis Nesbitt (Acarina: Phytoseiidae). Ph.D. Thesis, Univ. of
Calif., Riverside. 92 p. Croft, B. A. & M. T. AliNiazee. 1983. Differential tolerance
or resistance to insecticides in Typhlodromus arboreus Chant
and associated phytoseiid mites from apple in the Willamette Valley, Oregon.
J. Econ. Ent. 12: 1420-23. Davis, C. J. 1967. Progress in the biological control of the
southern green stink bug, Nezara viridula smaragdula, in
Hawaii. Muschi (Suppl.): 9-16. DeBach, P. 1964. Successes, trends, and future possibilities (p.
673-713). In: "Biological Control of Insect Pests and
Weeds," P. DeBach (ed.). Reinhold Publ. Co., New York. 844 p. DeBach, P. 1974. Biological Control by Natural Enemies. Cambridge
Univ. Press, London-New York. 323 p. Drooz, A. T, A. E. Bustillo, G. F. Fedde & V. H. Fedde. 1977.
North American egg parasite successfully controls a different host in South
America. Science 197: 390-91. Ehler, L. E. 1976. The relationship between theory and practice
in biological control. Bull. Ent. Soc. Amer. 22: 319-21. Ehler, L. E. 1979. Assessing competitive interactions in parasite
guilds prior to introduction. Environ. Ent. 8: 558-60. Ehler, L. E. 1982. Foreign exploration in California. Environ.
Ent. 11: 525-30. Ehler, L. E. 1989. Environmental impact of introduced
biological-control agents: implications for agricultural biotechnology. In:
"Risk Assessment in Agricultural Biotechnology," J. J. Marois &
G. Bruening (eds.). Univ. of Calif., Div. Agr. & Nat. Res., Oakland, CA. Ehler, L. E. 1990. Introduction strategies in biological control
of insects. Crit. Issues in Biol. Contr., Chap. 6. 1990: 111-134. Ehler, L. E. & L. A. Andres. 1983. Biological control: exotic
natural enemies to control exotic pests (p. 395-418). In: "Exotic
Plant Pests and North American Agriculture," C. L. Wilson & C. L.
Graham (eds.). Academic Press, New York. 522 p. Ehler, L. E. & R. W. Hall. 1982. Evidence for competitive
exclusion of introduced natural enemies in biological control. Environ. Ent.
11: 1-4. Ehler, L. E. & J. C. Miller. 1978. Biological control in
temporary agroecosystems. Entomophaga 23: 207-212. Eichhorn, O. 1969. Natürliche Verbreitungsareale und
Einschleppungsgebiete der Weisstannen Wolläuse (Gattung Dreyfusia) und
die Möglichkeiten ihrer biologischen Bekämpfung. Z. angew. Ent. 63: 113-31. Eikenbary, R. D. & C. E. Rogers. 1973. Importance of
alternate hosts in establishment of introduced parasites. Proc. Tall Timbers
Conf. Ecol. Anim. Control Habitat Management 5: 119-33. Embree, D. G. 1971. The biological control of the winter moth in
eastern Canada by introduced parasites (p. 217-26). In:
"Biological Control", C. B. Huffaker (ed.). Plenum Press, New York.
511 p. Ervin, R. T., L. J. Moffitt, & D. E. Meyerdirk. 1983.
Comstock mealybug (Homoptera: Pseudococcidae): cost analysis of a biological
control program in California. J. Econ. Ent. 76: 605-609. Fedde, G. F, V. H. Fedde & A. T. Drooz. 1979. Biological
control prospects of an egg parasite, Telenomus alsophilae
Viereck, p. 123-27. In: Current Topics in Forest Entomology. Selected
papers from XV Intern. Congr. Entomol., U. S. Dept. Agric. For. Serv. Gen.
Tech. Rep. WO-8. 174 p. Fisher, T. W. & G. L. Finney. 1964. Insectary facilities and
equipment, p. 381-401. In: DeBach, P. (ed.), Biological Control of
Insect Pests and Weeds. Reinhold, New York. Force, D. C. 1970. Competition among four hymenopterous parasites
of an endemic insect host. Ann. Ent. Soc. Amer. 63: 1675-88. Force, D. C. 1974. Ecology of insect host-parasitoid communities.
Science 184: 625-32. Franz, J. M. 1961a. Biologische Schädlingsbekämpfung, p. 1-302. In:
P. Sorauer (ed.), "Handbuch der Pflanzenkrankheiten," Band VI. Paul
Parey Verlag, Berlin-Hamburg. 627 p. Franz, J. M. 1961b. Biological control of pest insects in Europe.
Ann. Eve. Ent. 6: 183-200. Franz, J. M. 1973a. Quantitative evaluation of natural enemy
effectiveness. Introductory review of the need for evaluation studies in
relation to integrated control. J. Appl. Ecol. 10: 321-23. Franz, J. M. 1973b. The role of biological control in pest
management. Bull. Lab. Ent. Agraria 30: 235-43. Franz, J. M. & A. Krieg. 1982. Biologische
Schädlingsbekämpfung, 3 Auflage. Verlag Paul Parey, Berlin-Hamburg. 252 p. Ghani, M. A. 1969. natural enemies of forage and grain legume
aphids in Pakistan. Ann. Rep. Commonw. Inst. Biol. Contr. Pakistan Sta. Rept.
(unpub.) Goeden, R. D. 1971. Insect ecology of silverleaf nightshade. Weed
Sci. 19: 45-51. Goeden, R. D. 1983. Critique and revision of Harris' scoring
system for selection of insect agents in biological control of weeds. Prot.
Ecol. 5: 287-301. Goeden, R. D. 1988. A capsule history of biological control of
weeds. Biocontrol News & Information. 9(2): 55-61. Goeden, R. D. & L. T. Kok. 1986. Comments on a proposed
"new" approach for selecting agents for the biological control of
weeds. Canad. Ent. 118: 51-58. Greathead, D. J. 1971. A Review of Biological Control in the
Ethiopian Region. Commonw. Inst. Biol. Contr. Tech. Commun 5. 162 p. Greathead, D. J. 1973. Progress in the biological control of Lantana
camara in East Africa and discussion of problems raised by the
unexpected reaction of some of the more promising insects to Seasamum indicum
(p. 89-92). In: Proc. 2nd Int. Symp. Biol. Contr. Weeds, P. H. Dunn
(ed.). Commonwealth Inst. Biol. Control Misc. Publ. 6. Gruys, P. 1971. Mutual interference in Bupalus pinarius,
p. 199-207. In: P. J. den Boer & G. R. Gradwell (eds.), Dynamics
of Populations. Center Agr. Publ. Doc., Wageningen. Hagen, K. S. & J. M. Franz. 1973. A history of biological
control. Ann. Rev. Ent. 18: 433-76. Hall, R. W. & L. E. Ehler. 1979. Rate of establishment of
natural enemies in classical biological control. Bull. Ent. Soc. Amer. 25:
280-282. Hall, R. W., L. E. Ehler & B. Bisabri-Ershadi. 1980. Rate of
success in classical biological control of arthropods. Bull. Ent. Soc. Amer.
26: 111-14. Harris, P. 1973a. Selection of effective agents for the
biological control of weeds, p. 29-34. In: Proc. 2nd Int. Symp. Biol.
Contr. of Weeds., Misc. Publ. Commonw. Inst. Biol. Contr. 6. Harris, P. 1973b. The selection of effective agents of the
biological control of weeds. Canad. Ent. 105: 1495-1503. Harris, P. & H. Zwolfer. 1968. Screening of phytophagous insects
for biological control of weeds. Canad. Ent. 100: 295-303. Harris, P., D. Peschken & J. Milroy. 1969. The status of
biological control of the weed Hypericum perforatum in British
Columbia. Canad. Ent. 101: 1-15. Hassan, S. 1970. The possible control of skeleton weed, Chondrilla
juncea L., using Puccinia chondrillina Bubak & Syd.
Proc. 1st Int. Symp. Biol. Contr. of Weeds, p. 11-14. Misc. Publ. Commonw.
Inst. Biol. Contr. 1. Hassell, M. P. 1969a. A study of the mortality factors acting
upon Cyzenis albicans (Fall.), a tachinid parasite of the
winter moth, Operophtera brumata (L.). J. Anim. Ecol. 38:
329-39. Hassell, M. P. 1969b. A population model for the interaction
between Cyzenis albicans (Fall.) (Tachinidae) and Operophtera
brumata (L.) (Geometridae) at Wytham, Berkshire. J. Anim. Ecol. 38:
567-76. Hassell, M. P. 1971. Parasite behaviour as a factor contributing
to the stability of insect host-parasite interactions, p. 366-79. In:
P. J. den Boer & G. R. Gradwell (eds.), Dynamics of Populations. Center
Agr. Publ. Doc., Wageningen. Hassell, M. P. 1978. The Dynamics of Arthropod Predator-Prey
Systems. Princeton Univ. Press, Princeton, New Jersey. Hassell, M. P. 1980. Foraging strategies, population models and
biological control: a case study. J. Anim. Ecol. 49: 603-28. Hassell, M. P. & H. N. Comins. 1978. Sigmoid functional
response and population stability. Theor. Pop. Biol. 14: 62-67. Hassell, M. P. & R. M. May. 1973. Stability in insect
host-parasite models. J. Anim. Ecol. 42: 693-726. Hokkanen, H. 1985a. Exploiter-victim relationships of major plant
diseases: implications for biological weed control. Agriculture Ecosystems
& Environment 14: 63-76. Hokkanen, H. M. T. 1985b. Success in classical biological
controls. CRC Crit. Rev. in Plant Sci., Vol 3(1): 35-72. Hokkanen, H. & D. Pimentel. 1984. New approach for selecting
biological control agents. Canad. Ent. 116: 1109-1121. Hokkanen, H. M. T. & D. Pimentel. 1989. New associations in
biological control: theory and practice. Canad. Ent. 121: 829-40. Howarth, F. G. 1985. Impacts of alien land arthropods and
mollusks on native plants and animals in Hawaii. In: "Hawaii's
Terrestrial Ecosystems: Preservation and Management," C. P. Stone &
J. M. Scott (eds.). pp. 149-178. Univ. of Hawaii Press, Honolulu. Hoy, M. A. 1985. Improving establishment of arthropod natural
enemies. In: "Biological Control in Agricultural IPM
Systems," M. A. Hoy & D. C. Herzog (eds.). pp. 151-166. Academic
Press, New York. Hoy, M. A., D. Castro & D. Cahn. 1982. Two methods for
large-scale production of pesticide-resistant strains of the spider mite
predator Metaseiulus occidentalis. Z. angew. Ent. 94: 1-9. Huettel, M. D. & G. L. Bush. 1972. The genetics of host
selection and its bearing on sympatric speciation in Procecidochares (Dipt.:
Tephritidae). Ent. Exp. Appl. 15: 465-80. Hughes, R. D. 1973. Quantitative evaluation of natural enemy
effectiveness. J. Appl. Ecol. 10: 321-51. Huber, R. D. 1973. Quantitative evaluation of natural enemy
effectiveness. J. Appl. Ecol. 10: 321-51. Huber, P. 1983. Exorcists vs gatekeepers in risk regulation.
Regulation 7(6): 23-32. Huffaker, C. B. 1957. Fundamentals of biological control of
weeds. Hilgardia 27: 101-157. Huffaker, C. B., P. S. Messenger & P. DeBach. 1971. The
natural enemy component in natural control and the theory of biological
control (p. 16-17). In: "Biological Control," C. B. Huffaker
(ed.). Plenum Press, New York. 511 p. Huffaker, C. B. 1954. Introduction of egg parasites of the beet
leafhopper. J. Econ. Ent. 47: 785-89. Huffaker, C. B., C. E. Kennett, B. Matsumoto & E. G. White.
1968. Some parameters in the role of enemies in the natural control of insect
abundance, p. 59-75. In: T. R. E. Southwood (ed.), Insect Abundance.
Blackwell, Oxford. Huffaker, C. B., P. S. Messenger & P. DeBach. 1971. The
natural enemy component in natural control and the theory of biological
control, p. 16-67. In: C. B. Huffaker (ed.), Biological Control.
Plenum Press, New York. Inman, R. E. 1970a. Problems in searching for and collecting
control organisms. Proc. 1st Int. Symp. Biol. Contr. Weeds, p. 105-08. Misc.
Publ. Commonw. Inst. Biol. Contr. 1. Inman, R. E. 1970b. Host resistance and biological weed control.
Proc. 1st Int. Symp. Biol. Contr. Weeds, p. 41-5. Misc. Publ. Commonw. Inst.
Biol. Contr. 1. Julien, M. M. (ed.). 1982. Biological control of weeds: a world
catalogue of agents and their target weeds. Commonw. Agric. Bur., Farnham
Royal, Slough, U.K. 197 p. Klingman, D. L. & J. R. Coulson. 1982. Guidelines for
introducing foreign organisms into the United States for biological control
of weeds. Weed Sci. 30: 661-67. 1978a Legner, E. F. 1978.
Natural enemies imported in California for the biological control of
face fly, Musca autumnalis DeGeer, and horn fly, Haematobia irritans (L.). Proc.
Calif. Mosq. & Vector Contr. Assoc., Inc. 46: 77-79. 1978b Legner, E. F. 1978.
Part I: Parasites and
predators introduced against arthropod pests. Diptera. In:
Introduced Parasites and
Predators of Arthropod Pests and Weeds: a World Review (C. P. Clausen, ed.), pp. 335-39; 346-55.
Agric. Handbk. No. 480, ARS, USDA,
U. S. Govt. Printing Off., Wash., D. C.
545 pp 1986a Legner, E. F. 1986.
The requirement for reassessment of interactions among dung beetles,
symbovine flies and natural enemies. Entomol.
Soc. Amer. Misc. Publ. 61: 120-131. 1986b Legner, E. F. 1986.
Importation of exotic natural enemies. In: pp. 19-30, "Biological Control of
Plant Pests and of Vectors of Human and
Animal Diseases." Fortschritte der Zool. Bd. 32: 341 pp. 1999 Legner, E. F.
& T. S. Bellows, Jr.. 1999. Exploration for natural enemies. In: T. W. Fisher & T. S. Bellows (eds.),
Chapter 15, p. 87-
101., Handbook of Biological Control:
Principles and Applications.
Academic Press, San Diego, CA
1046 p. 1973 Legner, E. F.
& R. A. Medved. 1973. Influence of Tilapia mossambica
(Peters), T. zillii (Gervais) (Cichlidae) and Mollienesia latipinna LeSueur (Poeciliidae) on pond
populations of Culex mosquitoes and
chironomid midges. J. Amer. Mosq.
Contr. Assoc. 33(3): 354-364. 1979 Legner, E. F.
& R. A. Medved. 1979. Influence of parasitic Hymenoptera on the
regulation of pink bollworm, Pectinophora
gossypiella, on cotton in the lower
Colorado Desert. Environ. Entomol.
8(5): 922-930. 1983 Legner, E. F.
& R. W. Warkentin. 1983. Questions concerning the dynamics of Onthophagus gazella (Coleoptera: Scarabaeidae) with
symbovine flies in the lower Colorado Desert of California. Proc. Calif. Mosq. & Vector Contr.
Assoc., Inc. 51: 99-101. 1984 Legner, E. F.
& R. D. Sjogren. 1984. Biological mosquito control furthered by
advances in technology and research.
J. Amer. Mosq. Contr.
Assoc. 44(4): 449-456. 1974 Legner, E. F., R.
D. Sjogren & I. M. Hall.
1974. The biological control
of medically important arthropods.
Critical Reviews in
Environmental Control 4(1):
85-113. 1975 Legner, E. F., R.
A. Medved & W. J. Hauser.
1975. Predation by the desert
pupfish, Cyprinodon macularius on Culex mosquitoes and benthic
chironomid midges. Entomophaga
20(1): 23-30. 1980 Legner, E. F., R. A. Medved & F.
Pelsue. 1980. Changes in chironomid breeding patterns in
a paved river channel following adaptation of
cichlids of the Tilapia mossambica-hornorum complex. Ann.
Entomol. Soc. Amer. 73(1): 293-299. Lucas, A. M.
1969. The effect of population structure on the success of insect
introductions. Heredity 24: 151-57. Luck, R. F. 1982. Parasitic insects introduced as biological
control agents for arthropod pests (p. 125-284). In: CRC Handb. Pest
Management in Agriculture, D. Pimentel (ed.). Vol II, CRC Press, Boca Raton,
Florida. Luck, R. F., P. S. Messenger & J. Barbieri. 1981. The
influence of hyperparasitism on the performance of biological control agents.
p. 33-42. In: D. Rosen (ed.), The Role of Hyperparasitism in
Biological Control: a Symposium. Univ. of Calif. Div. Agric. Sci. Macqueen, A. 1975. Dung as an insect food source: dung beetles as
competitors of other coprophagous fauna and as targets for predators. J.
Appl. Ecol. 12: 821-27. May, R. M. & M. P. Hassell. 1981. The dynamics of
multiparasitoid-host interactions. Amer. Nat. 117: 234-261. May, R. M. & M. P. Hassell. 1988. Population dynamics and
biological control. Phil. Trans. Roy. Soc. London B 318: 129-169. McMurtry, J. R., E. R. Oatman, P. A. Phillips and C. W. Wood.
1978. Establishment of Phytoseiulus persimilis (Acari:
Phytoseiidae) in southern California. Entomophaga 23: 175-79. Messenger, P. S. 1971. Climatic limitations to biological
controls (p. 97-114). In: Proc. Tall Timbers Conf. Ecol. Anim. Contr.
Habitat Manag. 3. Tallahassee, Florida. Meyerdirk, D. E. & I. M. Newell. 1979. Importation,
colonization and establishment of natural enemies on the Comstock mealybug in
California. J. Econ. Ent. 72: 70-73. Meyerdirk, D. E., I. M. Newell & R. W. Warkentin. 1981.
Biological control of Comstock mealybug. J. Econ. Ent. 74: 79-84. Miller, J. C. 1983. Ecological relationships among parasites and
the practice of biological control. Environ. Ent. 74: 79-84. Mohyuddin, A. I. 1971. Comparative biology and ecology of Apanteles
flavipes and A. sesamiae as parasites of graminaceous
borers. Bull. Ent. Res. 61: 33-9. Mohyuddin, A. I., C. Inayatullah & E. G. King. 1981. Host
selection and strain occurrence in Apanteles flavipes (Cameron)
(Hymenoptera: Braconidae) and its bearing on biological control of
graminaceous stem-borers (Lepidoptera: Pyralidae). Bull. Ent. Res. 71:
575-581. Murakami, Y. 1966. Studies on the natural enemies of the Comstock
mealybug. II. Comparative biology on two types of internal parasites, Clausenia
purpurea and Pseudaphycus melinus (Hymenoptera, Encyrtidae).
Bull. Hort. Res. Sta. Ser. A, 5: 139-163. Murakami, Y. & H.-B. Ao. 1980. Natural enemies of the
chestnut gall wasp in Hopei Province, China (Hymenoptera: Chalcidoidea).
Appl. Ent. Zool. 15: 184-86. Murakami, Y., K. Umeya & N. Oho. 1977. A preliminary introduction
and release of a parasitoid (Chalcidoidea, Torymidae) of the chestnut gall
wasp, Dryocosmos kuriphilus Yasumatsu (Cynipidae) from China.
Japan J. Appl. Ent. 21: 197-203. Naumann, I. D. & D. P. A. Sands. 1984. Two Australian Elasmus
spp. (Hymenoptera: Elasmidae), parasitoids of Pectinophora gossypiella
(Saunders) (Lepidoptera: Gelechiidae): their taxonomy and biology. J. Aust.
Ent. Soc. 23: 25-32. Oatman, E. R. and G. R. Platner. 1974. Parasitization of the
potato tuberworm in southern California. Environ. Ent. 3: 262-64. Oman, P. W. 1948. Notes on the beet leafhopper Circulifer tenellus
(Baker) and its relatives. J. Kansas Ent. Soc. 21: 10-14. Osborne, J. A. 1982. Efficacy of Hydrilla control and a
stocking model for hybrid grass carp in freshwater lakes. Off. of Exploratory
Res. (RD-675), U. S. Environ. Prot. Agency, Wash., D.C. 143 p. Pimentel, D. 1963. Introducing parasites and predators to control
native pests. Canad. Ent. 92: 785-92. Pimentel, D. 1973. Comments on present status of biological
agents. WHO/VBC/73.445. In: Conf. on the Safety of Biological Agents
for Arthropod Control. p. 9. Pimentel, D. 1980. Environmental risks associated with biological
controls, p. 11-24. In: B. Lundholm & M. Stackerud (eds.), Environmental
Protection and Biological Forms of Control of Pest Organisms. Ecol. Bull. 31,
Stockholm. Pimentel, D. 1988a. Improved success in biological control, p.
1-3. In: International Conference "Biological Control of Vectors
with Predaceous Arthropods." 7-10 Jan. Loyola College, Madras, India. Pimentel, D. 1988b. Improved success in biological control.
Bicovas 1: 90--3. Pimentel, D. & H. Hokkanen. 1989. Alternative for successful
biological control in theory and practice, p. 21-51. In: E. L. Kulhavy
& M. C. Miller (eds.), Potential for Biological Control of Dendroctonus
and Ips Bark Beetles. Center for Applied Studies, School of Forestry,
Stephen F. Austin St. Univ., Nacogdoches, Texas. Pimentel, D., C. Glenister, S. Fast & D. Gallahan. 1983. An
environmental risk assessment of biological and cultural controls for organic
agriculture, p. 73-90. In: W. Lockeretz (ed.), Environmentally Sound
Agriculture. Praeger Special Studies, N.Y. Pimentel, D., C. Glenister, S. Fast & D. Gallahan. 1984.
Environmental risks of biological pest controls. Oikos 42: 283-90. Price, P. W. 1972. Methods of sampling and analysis for
predictive results in the introduction of entomophagous insects. Entomophaga
17: 211-22. Pschorn-Walcher, H. 1973. Die Parasiten der gesellig lebenden
Kiefern-Buschhornblattwespen (Fam. Diprionidae) als Beispiel für Koexistenz
und Konkurrenz in multiplen Parasit-Wirt-Komplexen. Verh. deut. Zool. Ges.
(Jahresversammlung) 66: 136-45. Pschorn-Walcher, H. & H. Zwölfer. 1956. The predator complex
of the white-fir woolly aphids (Gen. Dreyfusia, Adelgidae). Z. angew.
Ent. 39: 63-75. Pschorn-Walcher, H., D. Schröder & O. Eichhorn. 1969. Recent
attempts at biological control of some Canadian forest insect pests. Tech.
Bull. Commonw. Inst. Biol. Contr. 11: 1-18. Quezada, J. R. & P. DeBach. 1973. Bioecological and
population studies of the cottony-cushion scale, Icerya purchasi
Mask., and its natural enemies, Rodolia cardinalis Muls., and Cryptochaetum
iceryae Will., in southern California. Hilgardia 41: 631-88. Ratcliffe, F. N. 1966. Biological control. Aust. J. Sci. 28:
237-40. Remington, C. L. 1968. The population genetics of insect
introduction. Ann. Rev. Ent. 13: 415-26. Ross, H. H. 1953. On the origin and composition of the Nearctic insect
fauna. Evolution 7: 145-58. Roth, J. P., G. T. Fincher & J. W. Summerlin. 1983.
Competition and predation as mortality factors of the horn fly, Haematobia
irritans (L.) (Diptera: Muscidae) in a central Texas pasture habitat.
Environ. Ent. 12: 106-109. Sailer, R. I. 1981. Elements of opportunity in biological
control. In: "Biological Control in Crop Production," G. C.
Papavizas (ed.). Granada Publ. Co., London. 419. Sands, D. P. A. & A. R. Hill. 1982. Surveys for parasitoids
of Pectinophora gossypiella (Saunders) (Lepidoptera:
Gelechiidae) in Australia. Commonw. Scien. Ind. Res. Org., Div. Ent. Rept.
No. 29: 1-18. Schröder. D. 1974. A study of the interactions between the
internal larval parasites of Rhyacionia buoliana (Lep.
Olethreutidae). Entomophaga 19: 145-71. Schroeder, D. & R. D. Goeden. 1986. The search for arthropod
natural enemies of introduced weeds for biological control--in theory and
practice. Biocontrol News and Information 7(3): 147-155. Sechser, B. 1970. Der Parasitenkomplex des Kleinen Frostspanners
(Operophthera brumata L.) (Lep., Geometr.) under besonderer
Berücksichtigung der Kokonparasiten. Teil I und II. Z. angew. Ent. 66: 1-35,
144-60. Sheldeshova, G. G. 1967. Ecological factors determining
distribution of the codling moth, Laspeyresia pomonella L.
(Lepidoptera: Tortricidae) in the northern and southern hemispheres. Ent.
Rev. 46: 349-61. Simmonds, F. J. 1949. Insects attacking Cordia macrostachya
(Jacq.) Roem & Schult in the West Indies. 1. Physonota alutacea
Boh. (Col., Cassididae). Canad. Ent. 81: 185-99. Simmonds, F. J. 1969. Commonwealth Institute of Biological
Control. Brief Resume of Activities and Recent Successes Achieved. Commonw.
Agr. Bureaux Publ. Ferozsons Ltd., Rawalpindi. 16 p. Smith, H. S. 1939. Insect populations in relation to biological
control. Ecol. Monogr. 9: 311-20. Taylor, T. H. C. 1937. The Biological Control of an Insect in
Fiji. An Account of the Coconut Leaf-Mining Beetle and its Parasite Complex.
Imp. Inst. Ent., London. 239 p. Turnbull, A. L. 1967. Population dynamics of exotic insects.
Bull. Ent. Soc. Amer. 13: 333-37. Turnbull, A. L. & D. A. Chant. 1961. The practice and theory
of biological control of insects in Canada. Canad. J. Zool. 39: 697-753. Turnock, W. J. & J. A. Muldrew. 1971. Pristiphora erichsonii
(Hartig), larch sawfly (Hymenoptera: Tenthredinidae), p. 175-94. In:
Biological Control Programs Against Insects and Weeds in Canada 1959-1968.
Tech. Commun. Commonw. Inst. Biol. Contr. 4. van den Bosch, R. 1968. Comments on population dynamics of exotic
insects. Bull. Ent. Soc. Amer. 14: 112-115. van den Bosch, R. 1971. Biological control of insects. Ann. Rev.
Ecol. Syst. 2: 45-66. van Lenteren, J. C. 1980. Evaluation of control capabilities of
natural enemies: Does art have to become science? Neth. J. Zool. 30: 369-381. Waage, J. K. & M. P. Hassell. 1982. Parasitoids as biological
control agents--a fundamental approach. Parasitol. 82: 241-68. 1980 Walters, L. L. & E. F. Legner. 1980.
Impact of the desert pupfish, Cyprinodon
macularius, and Gambusia affinis on fauna in pond
ecosystems. Hilgardia
48(3): 1-18. Wapshere, A. J. 1970. The assessment of the biological control of
organisms for controlling weeds. Proc. 1st Int. Symp. Biol. Contr. Weeds, p.
79-89. Misc. Publ. Commonw. Inst. Biol. Contr. 1. Waterhouse, D. F. 1974. The biological control of dung. Scien.
Amer. 230: 100-109. Watt, K. E. F. 1965. Community stability and the strategy of
biological control. Canad. Ent. 97: 887-895. Wilson, A. G. L. 1972. Distribution of pink bollworm, Pectinophora
gossypiella (Saund.), in Australia and its status as a pest in the Ord
irrigation area. J. Aust. Inst. Agric. Sci. 38: 95-9. Zwölfer, H. 1961. A comparative analysis of the parasite
complexes of the European fir budworm, Choristoneura murinana
(Hb.), and the North American spruce budworm, C. fumiferana
(Clem.). Tech. Bull. Commonw. Inst. Biol. Contr. 1: 1-162. Zwölfer, H. 1971. The structure and effect of parasite complexes
attacking phytophagous host insects (p. 405-18). In: "Dynamics of
Populations," P. J. den Boer & G. R. Gradwell (eds.). Cent. Agric.
Publ. Doc., Wageningen. Zwölfer, H. & P. Harris. 1971. Host specificity determination
of insects for biological control of weeds. Ann. Rev. Ent. 16: 159-78. Zwölfer, H., M. A. Ghani & V. P. Rao. 1976. Foreign
exploration and importation of natural enemies (p. 189-207). In:
"Theory and Practice of Biological Control," C. B. Huffaker & P. S.
Messenger (eds.). Academic Press, New York. 788 p. |