DISCOVERY, IMPORTATION AND COLONIZATION
OF NEW NATURAL ENEMIES
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Problems Encountered by Explorers
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). It is well known that wild parasitoid populations exhibit seasonal and geographical differences in behavior and morphology. Therefore, collections meant for importation should optimally include isolates from diverse areas and different times of the year. Differences include aggressiveness, heat and cold tolerance, uniparentalism, gregarious versus solitary development, the number of eggs deposited into a single host, larval cannibalism intensity and parasitoid size. Detailed studies on Muscidifurax uniraptor, M. raptor and M. raptorellus demonstrate the great amount of diversity that can be found within one genus (fly-par.htm).
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).
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 assignments. Countries of the British Commonwealth have been especially helpful in locating beneficial species due to their maintenance of permanent research laboratories staffed with highly competent scientists.
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 sometimes 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 co evolutionary 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.
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 that 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?
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