History of Biological Control Programs in the United States

History of Biological Control Programs in the United States Department of Agriculture This history of biological control traces its start in the USDA to the 1880s; its progress includes the institution of biological control programs independently or in concert with the USDA. with the USDA. P. V. Vail, J. R. Coulson, W. C. Kauffman, and M. E. Dix T he history of biological control has been told many times but never limited specifically to the United States Department of Agriculture (USDA) role. Biological control (natural enemies and pathogens) has evolved gradually from limited programs to include programs in what are now three agencies within the USDA. Originally, when the USDA was small, biological control programs fell under the umbrella of the Department. Soon afterward, the USDA realized that native and exotic pests would be a continuing and increasing challenge as commerce and movement of people to the United States increased. Introductions of important agricultural and forest pests during this early period also had an impact. Thus, in 1881, a Division of Entomology (DE) was established within the USDA. Charles Valentine Riley (Fig. 1) was the first Chief of the DE and initiated classical biological control in the United States. Over time, the number of entomological studies of biological control agents increased. The biological control programs dealing with these studies would come under the administration of several Agencies within the USDA as well as Divisions and Units (Table 1). By 1971, three different USDA agencies were involved in biological control programs: (1) the Agricultural Research Service (ARS), which is the research arm of the USDA, covered basic and applied research and foreign exploration; (2) the Animal and Plant Health Inspection Service (APHIS) was committed primarily to action programs such as mass-rearing and release; and (3) the United States Forest Service (FS) was involved with the use of biological control for endemic and exotic forest pests. The evolution of programs and the significant contributions of these agencies of the USDA to biological control from 1881 through 1993 are discussed herein. Currently, about 60 USDA laboratories are conducting research on biological control, and the number of biological control projects exceeds 100 (USDA Current Research Information System project search, conducted in 1999). Programs conducted in the United States and at USDA laboratories on foreign soil also are discussed. There is voluminous literature on these subjects, only a few of which can be noted here. A detailed 645-page publication on the history of USDA research and development in biological control from 1881 through 1993, with an extensive bibliography, recently has been published by the USDA (Coulson et al. 2000). Most of the following discussion is excerpted from the above document. Only a few of the numerous references cited in the above publication are cited here. For the purpose of this publication, biological control is defined as the use of natural enemies (parasites [=parasitoids], predators, and pathogens) to regulate or control pests. Natural enemies for control of weeds also are considered. Various strategies have been used for the deployment of biological control agents. Involved in these discussions are two aspects of biological control: classical biological control, which involves the importation and release of exotic natural enemies to control pests (usually exotic), and augmentation, which includes enhancement of natural enemies through cultural techniques, environmental manipulation, and inoculative and inundative releases of beneficial insects. Examples include periodic (inoculative) releases of natural enemies with the expectation of season-long control and inundative releases of large numbers to provide immediate impact. Organisms AMERICAN ENTOMOLOGIST • Spring 2001 24 involved in inundative releases include insect pathogens/microbial control agents as well as beneficial arthropods. Biological control of noxious plants also is discussed. Much of this work was made possible through the USDA’s laboratories located on foreign soils throughout the world (Table 2). Classical Biological Control of Insects and Other Arthropods by the ARS Early programs began under the USDA’s DE and later Bureau of Entomology (BE), established in 1881. The first importation of an exotic braconid wasp parasite, Cotesia glomerata (L.), against the imported cabbageworm, Pieris rapae (L.), into the United States occurred in 1883 (Clausen 1978). The introduction of the famous predaceous vedalia beetle, Rodolia cardinalis (Mulsant), to control the cottony cushion scale, Icerya purchasi Maskell, followed in 1888 (Clausen 1978). The Department’s first large-scale biological control program did not begin until 1905 and involved explorations in Europe and Japan for natural enemies of the gypsy moth, Lymantria dispar (L.), and browntail moth, Euproctis chrysorrhoea (L.), introduced into New England. Despite establishment of several parasites and predators, satisfactory control of gypsy moth was not obtained, with the result that periodic natural enemy importation programs against this moth still occur. Control of the browntail moth was achieved, and many basic biological control concepts, principles, and procedures were developed as a result of this early importation program (Clausen 1956). The second major USDA importation program for natural enemies began in 1911 against the alfalfa weevil, Hypera postica (Gyllenhal), which was later to be one of the USDA’s most successful biological control programs (Coulson et al. 2000). A third major exploration program for natural enemies of the European corn borer, Ostrinia nubilalis Fig. 1. Charles Valentine Riley, First Chief of the USDA’s Division of Entomology from 1881 to 1894. Initiator of classical biological control programs in the United States. (Hübner), resulted in the establishment of a laboratory in France in 1919, the USDA’s first foreign laboratory. Description of the laboratories and programs in foreign countries are provided in Table 2. Other early importations included natural enemies from Malaya released in Cuba against the citrus blackfly, Aleurocanthus woglumi Ashby, which had been introduced into that country. Complete control of this pest in Cuba and elsewhere in the Caribbean was attained (Coulson et al. 2000). In 1934, the BE was combined with the old Bureau of Plant Quarantine to form the Bureau of Entomology and Plant Quarantine (BEPQ) (Table 1). Within the BEPQ, a Division of Foreign Parasite Introduction (DFPI) was formed, which was charged with the responsibility for exploration and importation of insect parasites and predators and, Table 1. History of Agencies Responsible for Biological Control Programs in the United States Department of Agriculture 1881–1993. Year 1881 1934 Location of Biological Control Programs Division of Entomology (DE); later, Bureau of Entomology (BE). Bureau of Entomology and Bureau of Plant Quarantine combine to Bureau of Entomology and Plant Quarantine (BEPQ). Division of Foreign Parasite Introduction (DFPI) formed in BEPQ; foreign laboratories established. Agricultural Research Service (ARS) established; BEPQ abolished. Entomology Research Division (ERD) formed. Forest Entomology moved from ARS to Forest Service (FS). Insect Identification and Parasite Introduction (IIPI) Research Branch formed; responsible for foreign laboratories, foreign exploration, and domestic quarantine receiving stations. Commodity-oriented Branches of ERD made responsible for biological control of pests. Animal and Plant Health Inspection Service (APHIS) established; Plant Protection and Quarantine (PPQ) division formed for action programs including biological control in concert with ARS. ARS reorganized, ERD and other Divisions abolished. Research directed now by Area offices and National Program Staff. FS National Center for Forest Health Management established; renamed Forest Health Technology Enterprise Team. 25 1953 1954 1971 1972 to present 1993 AMERICAN ENTOMOLOGIST • Volume 47, Number 1 Table 2. Foreign Biological Control Laboratories of the U.S. Department of Agriculture, 1919–1993. Dates of Operation 1919–1939 Name of Laboratory European Parasite Laboratory History of Laboratory Established at Auch, France, in 1919 for European corn borer investigations. Investigations expanded and laboratory moved to several locations in France. By 1936, a Division of Foreign Parasite Introduction (DFPI) laboratory was located at St. Cloud near Paris but closed in 1939 due to World War II. Personnel were moved to Montevideo, Uruguay. Various field laboratories for Japanese beetle and other fruit insects were established in Japan and Korea by 1922. These were consolidated at Yokohama, Japan, in 1932 and became a DFPI laboratory in 1934. Closed in November 1941 due to World War II. Established at Budapest, Hungary, in 1926. Became a DFPI Central European Investigations Laboratory in 1934. Closed and personnel moved to the DFPI European Parasite Laboratory in France in 1935. Established at Mexico City, Mexico, in 1928. Became a DFPI laboratory in 1934, and an Insect Identification and Parasite Introduction Research Branch (IIPI) laboratory in 1954. Closed at the end of 1957 when citrus blackfly program was terminated. A DFPI laboratory was maintained at Mayaguez, Puerto Rico, with special funds for study of insect pests of Puerto Rico. Funding terminated at end of 1936. A DFPI laboratory consisting of Division personnel from the laboratory in France was maintained at Montevideo, Uruguay. Closed in 1946 to re-establish the European Parasite Laboratory (EPL) in Behoust, France. The DFPI laboratory was reopened in France in 1947, becoming an IIPI laboratory in 1954. Moved to several locations in the Paris area; the last location was at Behoust, west of Paris. Closed in 1991 and consolidated with the IIPI Biological Control of Weeds laboratory to form USDA’s European Biological Control Laboratory (EBCL) in Montpellier, France. A laboratory for investigations of insect and weed pests was established at New Delhi, India, in 1952. It became an IIPI laboratory in 1954 and operated until 1958. Further biological control studies in the India-Pakistan area became possible by means of Public Law 480. An IIPI field station for study of natural enemies of the rangeland weed halogeton was established in Teheran, Iran, in 1956. Because of disappointing results there, the station was moved to Rabat, Morocco, in 1959 and closed in 1962. An IIPI laboratory was established in Rome, Italy, in 1959, to study natural enemies of rangeland weeds of the western United States. Closed in 1991 and consolidated with the IIPI European Parasite Laboratory to form USDA’s EBCL in Montpellier, France. A substation of the EBCL was continued in Rome. An IIPI laboratory was established in Hurlingham, Argentina, in 1962, to study natural enemies of aquatic weeds. Research gradually broadened to include terrestrial weeds and insect pests. Laboratory became the USDA’s South American Biological Control Laboratory (SABCL) in 1993, and research began to concentrate on insect pests. Re-established in 1975 at Sapporo, Japan, for control of gypsy moth. Research broadened to include other insect pests and weeds. In 1982, relocated to Seoul, South Korea. Closed in 1993. A substation of the Rome Biological Control of Weeds Laboratory (BCWL) was established in Thessaloniki, Greece, in 1980 for study of natural enemies of yellow starthistle and other weeds. Retained as a substation of the consolidated EBCL in 1991. Established in Beijing, Peoples Republic of China, in 1988. A collaborative effort of the Chinese Academy of Agricultural Sciences and ARS. Assists USDA and other USA scientists involved in study and collection of natural enemies of insect and weed pests in China. Established in Queensland, Australia, in 1989, for study and importation of natural enemies of the aquatic weed hydrilla and the weedy tree melaleuca (both native to Australia and introduced into the United States) and potential for study of natural enemies of other weed and insect pests of interest to both countries. Established at Montpellier, France, by consolidation of the EPL in Behoust, France, and the BCWL in Rome, Italy. Research on insect pathology began at the EPL. Two EBCL substations were retained in Thessaloniki, Greece, and Rome, Italy. 1922–1941 Asian Parasite Laboratory Gypsy Moth Laboratory 1926–1935 1928–1957 Insects Attacking Fruit Laboratory Temporary Puerto Rico Laboratory South American Parasite Laboratory European Parasite Laboratory 1935–1936 1940–1946 1947–1991 1952–1958 Indian Biological Control Laboratory 1956–1962 Insect Identification and Parasite Introduction Field Station Biological Control of Weeds Laboratory, Europe 1959–1991 1962–present Biological Control of Weeds Laboratory, South America Asian Parasite Laboratory Biological Control of Weeds Substation Sino-American Biological Control Laboratory 1975–1993 1980–present 1988–present 1989–present Australian Biological Control Laboratory 1991–present European Biological Control Laboratory See glossary of acronyms. 26 AMERICAN ENTOMOLOGIST • Spring 2001 later, natural enemies of weeds and plant and insect pathogens for other Bureau Divisions. Five existing or new laboratories in various parts of the world were managed under the DFPI between 1919 and 1940 (Table 2). USDA Laboratories still exist in the major areas of the globe (Table 2). Several USDA quarantine facilities were established in the United States to handle and clear imported beneficial species. Initially there were two, located at Moorestown, NJ, and Albany, CA. Today, USDA quarantine facilities are located in Newark, DE; Stoneville, MS; Albany, CA; Temple, TX; Frederick, MD; and Hamden, CT. USDA personnel also are located at quarantine facilities operated by states and universities. Table 3 provides a list of imported biological control agents, and their foreign origins, that have been used in USDA’s most successful classical biological control projects. The more significant accomplishments during 1934–1952 include complete control of the citrus blackfly in Mexico (and also Texas and Florida when the pest reached the United States in the 1970s), the European wheat stem sawfly, Cephus cinctus Norton, and Comstock mealybug, Pseudococcus comstocki (Kuwana), in the eastern United States, and substantial control of the larch casebearer, Coleophora laricella (Hübner), in New England. The USDA programs from 1888 through 1952 are discussed in some detail by Clausen (1956) (Fig. 2), a summary reference. In 1953, the ARS was established and the BEPQ was abolished. Regulatory functions were placed in the Divisions of Plant Quarantine (PQD) and Plant Pest Control (PPCD) under the ARS and research functions placed in the newly formed Entomology Research Division (ERD). Forest entomology, previously included in the BEPQ, was removed from the ARS and placed in the FS. A program review (Coulson et al. 2000) in 1953 of the ARS entomological research program indicated a major shift from research on chemical control to biological control was needed, and the ERD immediately increased research on alternative methods of pest control. In 1954, the Insect Identification and Parasite Introduction (IIPI) Research Branch was formed. It was given responsibility for conducting foreign exploration research and for directing work at, and maintaining all, ARS biological control quarantine-receiving stations in the United States. The commodity-oriented Branches of the ERD, in cooperation with the IIPI, were responsible for all aspects of biological control investigations that concerned pests within the scope of their responsibilities. The combination of parasite/predator research together with insect systematics in the IIPI was intended to facilitate maximum identification services for biological control and permit the use of USDA taxonomists in initial biological control surveys, collections, and field identifications. Three foreign locations initially reported to the IIPI: Mexico City (closed in 1957), New Delhi (closed in 1958), and the European Parasite Laboratory (EPL) near Paris in Behoust, France (Table 2). Stations at Moorestown, NJ, and Albany, CA, also reported to the IIPI. The New Jersey station received most of the parasite/predator shipments from the Indian and European stations. The Albany station was responsible mostly for receipt of shipments of natural enemies of weeds but also received insect parasites and predators from the European stations that were destined for use in western states. Besides quarantine clearance and natural enemy distribution activities, both stations also participated in research programs involving release and evaluation of exotic natural enemies in Glossary of Acronyms APHIS Animal and Plant Health Inspection Service (regulatory arm of the USDA) APL Asian Parasite Laboratory ARS Agricultural Research Service (research arm of the USDA) BCIRL Biological Control of Insect Research Laboratory, Columbia, MO BCL APHIS-PPQ Biological Control Laboratory BCWL Biological Control of Weeds Laboratory, Rome, Italy (established in 1959) BE Bureau of Entomology BEPQ Bureau of Entomology and Plant Quarantine BIRL Beneficial Insects Research Laboratory, Moorestown, NJ (moved to Newark, DE in 1973) Bt Bacillus thuringiensis Berliner, an insect pathogenic bacterium CANUSA Canada/United States Spruce Budworms Program DE Division of Entomology (formed in 1881) DFPI Division of Foreign Parasite Introduction EBCL European Biological Control Laboratory EPA U. S. Environmental Protection Agency EPL European Parasite Laboratory (now European Biological Control Laboratory in France) ERD Entomology Research Division FES Forest Experiment Station FIDR Forest Insect and Disease Research AMERICAN ENTOMOLOGIST • Volume 47, Number 1 Forest Pest Control Forest Pest Management Units of U. S. Forest Service FRES Forest and Range Experiment Station FS U. S. Forest Service IIBC International Institute of Biological Control, Great Britain IIPI Insect Identification and Parasite Introduction Research Branch (formed in 1954 by ERD) IPM Integrated Pest Management (a concept in which use of chemical pesticides is minimized and biological control, host plant resistance, scouting and others, are maximized) MDL APHIS-PPQ Methods Development Laboratory NBCI APHIS National Biological Control Institute NPV Nucleopolyhedroviruses (viruses infectious only to arthropods, primarily insects) PPQ APHIS Plant Protection and Quarantine PPQ-BCL APHIS-PPQ Biological Control Laboratories PPQ-MDL APHIS-PPQ Methods Development Laboratories PPQ-PPC Plant Protection Centers of APHIS PPQ SABCL South American Biological Control Laboratory SRQF Stoneville Research Quarantine Facility, Stoneville, MS (ARS facility) USACE U. S. Army Corps of Engineers USDA U. S. Department of Agriculture 27 FPC FPM Table 3. Examples of Successful Classical Biological Control for which ARS and Predecessor Agencies Largely were Responsible a,b Type of pest and Level of Control c Pest Species Insect – CEC Alfalfa blotch leafminer, Agromyza frontella (Rondani) Alfalfa weevil, Hypera postica (Gyllenhal) Crop Affected and Geographic Area of Control Alfalfa – Eastern United States Alfalfa – Eastern United States Natural Enemies Introduced and Country of Origin Chrysocharis punctifacies Delucchi (Hymenoptera: Eulophidae), Dacnusa dryas (Nixon) (Hymenoptera: Braconidae) – Europe Bathyplectes curculionis (Thomson) (Hymenoptera: Ichneumonidae) – California and Europe — Bathyplectes anurus (Thomson) (Hymenoptera: Ichneumonidae), Microctonus aethiopoides Loan (Hymenoptera: Braconidae), Oomyzus incertus (Ratzeburg) (Hymenoptera: Eulophidae) – Europe Tetrastichus julis (Walker) (Hymenoptera: Eulophidae), Anaphes flavipes (Foerster) (Hymenoptera: Mymaridae), Lemophagus curtus Townes, Diaparsis temporalis Horstmann (Hymenoptera: Ichneumonidae) – Europe Eretmocerus serius Silvestri (Hymenoptera: Aphelinidae) – Malaya — Encarsia opulenta (Silvestri) (Hymenoptera: Aphelinidae), Amitus hesperidum Silvestri (Hymenoptera: Platygasteridae) – India Allotropa burrelli Muesebeck (Hymenoptera: Platygasteridae), Pseudaphycus malinus Gahan (Hymenoptera: Encyrtidae) – Japan Rodolia cardinalis (Mulsant) (Coleoptera: Coccinellidae) – Australia Aphidius spp. (Hymenoptera: Braconidae), Aphelinus spp. (Hymenoptera: Aphelinidae) – France Cereal leaf beetle, Oulema melanopus (L.) Small grain – Eastern United States Citrus – Cuba, Mexico (later extended to Texas, Florida) Deciduous fruits – Eastern United States Citrus – California Small grains – Chile Citrus blackfly, Aleurocanthus woglumi Ashby Comstock mealybug, Pseudococcus comstocki (Kuwana) Cottony cushion scale, Icerya purchasi Maskell English grain aphid, Sitobium avenae (F.) and Metopolophium dirhodum (Walker) Eurasian pine adelgid, Pineus pini (Macquart) European wheat stem sawfly, Cephus pygmaeus (L.) Pea aphid, Acyrthosiphon pisum (Harris) Rhodesgrass mealybug, Antonina graminis (Maskell) Spotted alfalfa aphid, Theriophis maculata (Buekton) Insect – PEC d Alfalfa plant bug, Adelphocoris lineolatus (Goeze) Birch leafminer, Fenusa pusilla (Lepeletier) Euonymus scale, Unaspis euonymi (Comstock) Pine – Hawaii Wheat – Eastern United States Alfalfa – United States Range grass – Texas Leucopis obscura Haliday (Diptera: Chamaemyiidae) – France Collyria calcitrator (Gravenhorst) (Hymenoptera: Ichneumonidae) – Europe via Canada Aphidius smithi Sharma & Subba Rao – India — Aphidius ervi Haliday (Hymenoptera: Braconidae) – Europe Neodusmetia sangwani (Subba Rao) (Hymenoptera: Encyrtidae) – India Trioxys complanatus Quilis, Praon exoletum palitans Muesebeck (Hymenoptera: Aphidiidae) – Europe and Mid-East Alfalfa – United States Northeastern United States Birch – Northeastern United States Ornamentals – United States Peristenus conradi Marsh (Hymenoptera: Braconidae) – Europe Lathrolestes nigricollis (Thompson), Grypocentrus albipes Ruthe (Hymenoptera: Ichneumonidae) – Central Europe Chilorocus kuwanae Silverstri (Coleoptera: Coccinellidae) – Japan, South Korea — Cybocephalus nipponicus Endrody-Younga (Coleoptera: Cybocephalidae) – South Korea Peristenus digoneutis Loan (Hymenoptera: Braconidae) – Europe Tarnished plant bug, Lygus Northeastern lineolaris (Palisot de Beauvois) United States Insect – SEC Alfalfa weevil, Hypera postica Alfalfa – Western (Gyllenhal) United States Browntail moth, Euproctis Forest trees – chrysorrhoea (L.); gypsy moth, New England Lymantria dispar (L.); oriental moth, Cnidocampa flavescens (Walker); and satin moth, Leucoma salicis (L.); Bathyplectes curculionis (Thomson) (Hymenoptera: Ichneumonidae) – Italy Many hymenopteran and dipteran parasites – Europe and Japan 28 AMERICAN ENTOMOLOGIST • Spring 2001 Table 3. Continued Type of pest and Level c of Control Pest Species Crop Affected and Geographic Area of Control Natural Enemies Introduced and Country of Origin Chrysocharis laricienellae (Ratzeburg) (Hymenoptera: Eulophidae), Agathis pumila (Ratzeburg) (Hymenoptera: Braconidae) – Central Europe Diachasmimorpha longicaudata (Ashmead), Fopius vandenboschi (Fullaway) (Hymenoptera: Braconidae) – Malaya — F. arisanus Sonan) (Hymenoptera: Braconidae) – Indo-Malayan region Campoplex frustranae Cushman (Hymenoptera: Ichneumonidae) – Italy Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae) – Northeast United States Agasicles hygrophila Selman & Vogt (Coleoptera: Chrysomelidae), Vogtia malloi Pastrana (Lepidoptera: Pyralidae), Amynothrips| andersoni O’Neill (Thysanoptera: Phlaeothripidae) – Argentina Chrysolina quadrigemina (Suffrian), Chrysolina hyperici (Förster) (Coleoptera: Chrysomelidae) – Europe via Australia — Zeuxidiplosis giardi (Kieffer) (Diptera: Cecidomyiidae) – France Longitarus jacobaeae (Waterhouse) (Coleoptera: Chrysomelidae) – Italy — Tyria jacobaeae (L.) (Lepidoptera: Arctiidae) – France Aphthona cyparissiae (Koch), A. czwalinae (Weise) (Coleoptera: Chrysomelidae) – Central Europe — A. flava Guillebeau (Coleoptera: Chrysomelidae) – Italy and Hungary via Canada — A. lacertosa Rosenheim – Italy, Central Europe — A. nigriscutis Foudras (Coleoptera: Chrysomelidae) – Hungary via Canada — Oberea erythrocephala (Schrank) (Coleoptera: Cerambycidae) – Italy and Hungary — Hyles euphoribiae (L.) (Lepidoptera: Sphingidae) Switzerland and Hungary — Spurgia esula Gagné (Diptera: Cecidomyiidae) – Italy Galerucella calmariensis (L.), G. pusilla (Duftschmidt) (Coleoptera: Chrysomelidae); Hylobius transversovittatus (Goeze) (Coleoptera: Curculionidae) – Germany Bangasternus orientalis (Capiomont), Eustenopus villosus (Boheman), Larinus curtus Hochhut (Coleoptera: Curculionidae); Chaetorellia australis Hering, Urophora sirunaseva (Hering) (Diptera: Tephritidae) – Greece Larch casebearer, Coleophora Larch – New England laricella (Hübner) Oriental fruit fly, Bactrocera dorsalis Hendel Western pine tip moth, Rhyacionia bushnelli (Busck) Fruit – Hawaii Pine – Nebraska Woolly apple aphid, Eriosoma Apple – Northwestern lanigerum (Hausmann) United States Weed – CEC Alligatorweed, Alternanthera philoxeroides (von Martinus) Grisebach Common St. Johns-wort, Hypericum perforatum L. Tansy ragwort, Senecio jacobaea L. Weed – PEC d Leafy spurge e, Euphorbia esula L. Rivers, lakes – Southeastern United States Rangelands – Western United States Rangelands – Western United States Rangelands – Western Purple loosestrife f, Lythrum salicaria L. Yellow starthistle, Centaurea solstitialis L. Wetlands – Northern United States Rangelands – Western United States Weed – SEC Musk thistle, Carduus nutans L. Puncturevine, Tribulus terrestris L. Waterhyacinth, Eichhornia crassipes (von Martius) Solms-Laugach Pastures and Rangeland – Rhinocyllus conicus (Froelich) (Coleoptera: Curculionidae) – France United States —Trichosirocalus horridus (Panzer) (Coleoptera: Curculionidae) – Italy Rangelands – Western United States Rivers, lakes – Southeastern United States Microlarinus lareynii (Jac du Val), M. lypriformis (Wollaston) (Coleoptera: Curculionidae) – Italy Neochetina bruchi Hustache, N. eichborniae Warner (Coleoptera: Curculionidae); Sameodes albiguttalis (Warren) (Lepidoptera: Pyralidae) – Argentina a Many other federal, state, and university organizations and personnel (particularly the University of California and APHIS-PPQ) were involved in some of these programs. Many examples of “partial” economic control cited above and in the literature are not listed here. c CEC = complete economic control; SEC = substantial economic control; PEC = potential economic control. d Programs are too recent to predict complete economic control, but preliminary results indicate at least substantial control will result. e Canada Agriculture and International Institute for Biological Control are involved in the potential success of this program. f ARS involvement is chiefly limited to the initial stages of this program. b AMERICAN ENTOMOLOGIST • Volume 47, Number 1 29 Fig. 2. Curtis P. Clausen, Head of the Foreign Parasite Introduction Division of the USDA’s Bureau of Entomology and Plant Quarantine from 1934 to 1952. their respective areas. The projects are too numerous to mention here and the reader should refer to the larger document (Coulson et al. 2000) mentioned previously. The newly constructed Biological Control of Insects Research Laboratory (BCIRL) at Columbia, MO, was added to the IIPI in late 1964. The objectives of this laboratory were to develop and test new principles and methods of using parasites, predators, and pathogens against major insect pests. In 1958, the Foreign Agricultural Research Grant Program was initiated under authority of United States Public Law 480 (the Agricultural Trade, Development, and Assistance Act of 1954). To broaden the scope of the biological control program of the ARS, IIPI scientists became “cooperating scientists” on biological control and taxonomic projects worldwide. These projects concerned U.S. and foreign surveys for natural enemies of specific domestic crop pests, or certain ecological situations, and represented a considerable expansion of USDA’s biological control exploration program (Coulson et al. 2000) (Fig. 3). Significant accomplishments resulting from ARS biological control importation program during 1953–1972 included the control of three serious introduced pests: the cereal leaf beetle, Oulema melanopus (L.), a pest of small grains; the alfalfa weevil in the eastern United States; and the Rhodesgrass mealybug, Antonina graminis (Maskell), a pest of lawn and forage grasses in Texas. IIPI studies on cereal leaf beetle resulted in the discovery and importation of five species of hymenopteran parasites. Because there were no IIPI units within working distance of the pest populations, release and establishment work was conducted first under cooperative agreements with universities in Michigan and Indiana. In 1966, the ARS established a laboratory in Niles, MI (this became an APHIS-Plant Protection and Quarantine [PPQ] Laboratory in 1971), to release and further disseminate cereal leaf beetle parasites. By 30 1972, four of the European parasites were established in the United States (Table 3) and were being disseminated and established throughout the range of the beetle. Heavy crop losses reported during the late 1960s in the Midwest nearly were eliminated. Using APHIS field data in AGSIM, the empirical U.S. agricultural sector model, Wu (1993) calculated more than $168 million net present value of the program, with crop producers benefiting most. This was the first example in which a pest of an annual crop in a temperate continental area was controlled successfully by imported parasites. Previous successes had been with pests of perennial crops (Dysart et al. 1973, DeBach and Rosen 1991). In 1951, the alfalfa weevil, which had been present in the western United States since the early 1900s, was found in Maryland and by 1971 had spread throughout most of the eastern part of the country. It became the most important pest of alfalfa in the East, in most cases requiring regular insecticidal treatments to prevent total crop destruction. A parasite importation program began in 1957. By 1965, five hymenopteran parasite species were established in the New Jersey-eastern Pennsylvania area and began to disperse throughout the Middle Atlantic States. The New Jersey Department of Agriculture developed a strong parasite distribution program in cooperation with the ARS. By 1970, alfalfa weevil populations in New Jersey had decreased, and only 8% of farmers used insecticides for the weevil. An estimate of savings to farmers in 18 eastern states as the parasites’ range increased further was nearly $63.7 million annually by 1986. This is a considerable return for an estimated total cost of about $1 million for the ARS importation program. Following the APHIS Fig. 3. The parasitic wasp Diapetimorpha introita (Cresson) preparing to parasitize pupa of armyworm, Spodoptera sp. AMERICAN ENTOMOLOGIST • Spring 2001 parasite redistribution programs, economic benefits were calculated at $2.2 billion in 1987 dollar value (Bryan et al. 1993, Kingsley et al. 1993). The Rhodesgrass mealybug, an oriental species, first was reported in the United States in 1942 and quickly became a major pest of forage and lawn grasses in Texas. An early parasite importation program provided little control of this pest. In 1956, the ARS Indian station discovered an undescribed hymenopteran parasite (described later as Neodusmetia sangwani Subba Rao) attacking this mealybug. The parasite was introduced into Texas in 1959, and control of the mealybug quickly was demonstrated. Distribution of the parasite by the Texas Agricultural Experiment Station in the 1960s eliminated the mealybug as a pest of forage grasses in Texas by 1970. A 1979 cost:benefit analysis noted an annual savings of almost $17 million in reduced costs for turf grass maintenance alone and additional profits exceeding $177 million from increased cattle sales due to control in forage grasses. Total cost of the project in Texas was less than $200,000. The parasites also were established in Florida with nearly similar results (Dean et al. 1979, DeBach and Rosen 1991). Further Accomplishments of Classical Biological Control Accomplishments in addition to these three outstanding classical biological control programs during 1953–1972 also are noted in Table 3. The results of the USDA’s classical biological control program during this period produced estimated benefits of at least $300 million a year in 1993 dollars and continue to accrue (Coulson et al. 2000). These savings compare well with estimated total expenditures ($20 million) on research by both Federal and State agencies to find, establish, and utilize natural enemies of insect and weed pests from 1888 to 1972 and with the estimated $420 million spent annually on insecticides in the 1960s (Sailer 1973) (Fig. 4). During 1973–1993, the ARS classical biological control programs continued at the three established foreign laboratories in Europe and Argentina (Table 2) and at stations established during this period in Asia and Australia. The laboratories in Italy and Argentina (Table 2) continued to be devoted almost exclusively to biological control of weeds. However, in 1993, the mission of the Argentine laboratory, renamed the South American Biological Control Laboratory (SABCL), was changed to concentrate on insect target pests. The two biological control laboratories in Europe (France and Italy) were united at Montpellier, France, as the European Biological Control Laboratory (EBCL) in 1991. European research again concerned natural enemies of a large number of insect pests. The Asian Parasite Laboratory (APL) (Table 2) was reestablished in Sapporo, Japan, in 1975 with the help of special funds for ARS biological control research on the gypsy moth. In 1982, the APL was relocated to Seoul, South Korea, because of the need to conduct research on additional United States target pests. The station was AMERICAN ENTOMOLOGIST • Volume 47, Number 1 closed in 1993. To further biological control research and foreign exploration, agreements were made with China and the Soviet Union in the 1980s. A Sino-American Collaborative Biological Control Laboratory was established in Beijing 1988. Cooperative linkages later were established with agricultural institutions in several of the former Soviet republics. In 1989, an ARS laboratory was established in Queensland, Australia (Table 2), for study of natural enemies of aquatic/wetland weeds. The ARS Beneficial Insects Research Laboratory (BIRL) was relocated from Moorestown, NJ, to new, modern facilities at Newark, DE, in 1973 and continued quarantine clearance services and programs for several natural enemies of arthropod pests based primarily on material received from the programs of the EPL, EBCL, and APL. The BCIRL in Columbia, MO, was concerned largely with parasite/predator augmentation and insect pathology but also evaluated and released exotic insect parasites and predators and exotic weed-feeding insects. Foreign explorations resulted in the introduction of an eulophid egg parasite, Edovum puttleri Grissell, that has been studied at many locations for use in Colorado potato beetle, Leptinotarsa decemlineata (Say), parasite augmentation programs. The ARS Stoneville Research Quarantine Facility (SRQF) in Mississippi opened in 1973. Classical biological control research on insect pests of cotton and soybeans began at this location in 1978. In the early 1980s, the SRQF also served as a quarantine facility for the many explorations by state and federal entomologists involved in the U.S. Environmental Protection Agency (EPA)-supported Soybean Subproject of the Consortium for Integrated Pest Management. Other ARS facilities also were involved in research on introduced natural enemies of insect pests during 1973–1993. These included research on dung-breeding flies at College Station, TX (Fincher 1990); on lygus bugs (Ly- To further biological control research and foreign exploration, agreements were made with China and the Soviet Union in the 1980s. A Sino-American Collaborative Biological Control Laboratory was established in Beijing 1988. Fig. 4. Reece I. Sailer, Chief of the Insect Identification and Parasite Introduction Research Branch of USDA’s Agricultural Research Service, Entomology Research Division, from 1967 to its abolishment in 1972. 31 gus spp.) parasites at Tucson, AZ; on natural enemies of the pear psylla, Cacopsylla pyricola Foerster, and the apple ermine moth,2 Yponomeuta mallinellus Zeller, at Yakima (now Wapato), WA; on various citrus pests at Weslaco, TX, and Riverside, CA (closed in 1987); on introduced natural enemies of pecan and other arboreal aphids at Byron, GA; on imported parasites and predators of the recently introduced Russian wheat aphid, Diuraphis noxia (Mordvilko), at ARS facilities in Stillwater, OK, and Brookings, SD; and on sweetpotato whitefly, Bemisia tabaci (Gennadius), at Weslaco, TX. Research on an imported hymenopteran parasite of rangeland grasshopper eggs was conducted under a cooperative ARS-APHIS program at Sidney, MT. The proposed release of an exotic natural enemy against grasshoppers proved to be controversial, and studies were halted because of objections raised by ecologists to the introduction of exotic natural enemies against native pests. Biological control of other species of significance also was studied by the ARS during 1973–1993. The alfalfa blotch leafminer, Agromyza frontella (Rondani), was found in Massachusetts in 1968 and quickly spread throughout the northeastern United States and eastern Canada where it caused considerable reduction in alfalfa yield. The ARS discovered and imported 14 European hymenopteran parasites of the leafminer, three of which became established (Table 3). Insecticidal treatments to combat the leafminer threatened to upset the successful alfalfa weevil biological control program by decimating introduced alfalfa weevil parasites. The parasites provided excellent control of the pest by 1981 in Delaware and rapidly dispersed throughout the northeastern United States and into Canada. The need for insecticide treatments was eliminated. Annual savings of about $17.2 million in 1993 dollars due to yield increase have been estimated; this estimate does not include the cost of insecticide no longer applied (Hendrickson and Plummer 1983, Drea and Hendrickson 1986, DeBach and Rosen 1991). The Eurasian pine adelgid, Pineus pini (Macquart), first was found on the island of Hawaii in 1970 and spread rapidly through the other islands, causing severe damage to pines. Eradication attempts with chemicals failed, and requests for natural enemies were made to the ARS EPL (Culliney et al. 1988). The EPL collected natural enemies in France and shipped a dipteran predator of the adelgid to Hawaii, which became established, spread, and now provides effective control of the pest. In connection with the greenbug (aphid), Schizaphis graminum (Rondani), program, hymenopteran aphid parasites were sent by the EPL to Chile, Brazil, and Argentina for release against several species of grain aphids in those countries. Control of two of the aphids by the introduced parasites has been claimed in some areas of South America (Zuñiga 1985). 2 Common name not currently among common names of insects and related organism approved for use buy the ESA Committee -on Common Names of Insects. Several European hymenopteran parasites of lygus and other plant bug pests have been introduced by the ARS, and two species are firmly established in the northeastern United States. One has increased field parasitism rates of the tarnished plant bug, Lygus lineolaris (Palisot de Beauvois), to three times the previous rate provided by native parasites; the other has raised field parasitism of the alfalfa plant bug, Adelphocoris lineolatus (Goeze), by four times. Potential savings eventually, if adequate control of these two pests is obtained, may reach $60-130 million per year (Day et al. 1992). ARS research on hymenopteran parasites and predators of the euonymus scale, Unaspis euonymi (Comstock), was conducted at Newark, DE, and Beltsville, MD, using natural enemies introduced from the APL. Two beetle predators became established and have controlled the scale completely in many release sites in the United States (Hendrickson and Drea 1988). Augmentative Biological Control Of the two strategies for augmentation, environmental manipulation, and periodic releases, the latter has received the most attention of the USDA (Ridgway and Vinson 1977). Early large-scale augmentation attempts to control the boll weevil, Anthonomus grandis grandis Boheman, and house fly, Musca domestica L., utilized native parasites. Subsequent early programs used native ladybugs for aphid control in California; introduced predators against mealybugs in California; and a native parasite against the introduced oriental fruit moth, Grapholita molesta (Busck), in several states. Early USDA augmentation programs also included use of egg parasites against the range caterpillar, Hemileuca oliviae Cockerell, and pecan nut casebearer, Acrobasis nuxvorella Neunzig, and the large-scale culture and release of an imported tachinid parasite of the Mexican bean beetle, Epilachna varivestis Mulsant, that involved 19 states (Clausen 1956). Augmentation benefited from the mass-rearing techniques for parasitic wasps, Trichogramma spp., developed by University of California researchers by 1930. The major augmentation accomplishment during the 1930s and 1940s concerned the use of the native braconid parasite, Macrocentrus ancylivorus Rohwer, which attacked the newly introduced oriental fruit moth. The USDA mounted a large-scale release program in all infested areas of the eastern United States during 1929–1935; a 50% reduction of fruit injury frequently was reported (Clausen 1956). When the pest invaded California in 1942, this parasite became the first to be mass-reared and released in an attempt to eradicate or prevent further spread of a pest (Clausen 1956). Researchers at the University of California developed a low-cost, highly effective method for mass culture of this parasite, and millions were reared and released annually during 1944–1946 (Clausen 1956). Interest in augmentation, as well as in importation, waned in the early 1950s as highly effective insecticides were discovered and came into general use. In the 1960s, integrated pest management (IPM) AMERICAN ENTOMOLOGIST • Spring 2001 32 began growing in importance in pest control. Biological control is an important component of IPM programs. There was increasing awareness by biological control workers that not all insect pest problems in the United States were amenable to the classical importation approach. Many pests are native and have a full complement of natural enemies attacking them. Researchers also began to realize that the annual row crop agroecosystem was a difficult place for natural enemies to work without human assistance because of the disruptions that occur in such a system. Thus, in addition to importation, release, and conservation, augmentative and inundative strategies were investigated in more depth (Fig. 5). Much of the biological control research conducted by the ARS during 1953–1972 emphasized basic biological and ecological studies of parasites and predators that possibly could be used in augmentation or conservation programs aimed at arthropod pests. The feasibility of mass rearing large numbers of biological agents for immediate control of pests also was being investigated. The major targets of such research during this period included lepidopteran and hemipteran pests of cotton, lepidopteran pests of vegetables, and scale insect pests of citrus. Research on the use of easily reared Trichogramma egg parasites continued in the ARS and in other institutions in the United States, but utilization of these biological control agents was most intensive in other countries such as the USSR, China, and Mexico. ARS’ augmentative biological control research is discussed in detail in Coulson et al. (2000), which includes numerous references; only a few highlights are presented here. Massrearing developments allowed inundative releases of the common green lacewing, Chrysoperla plorabunda (Fitch), for control of the bollworm, Helicoverpa zea (Boddie), and tobacco budworm, Heliothis virescens (Fabricius), on cotton (Coulson et al. 2000). Many scientists within and outside of the ARS believed that environmental manipulation strategies could play an important role in biological control, but augmentative and inundative strategies also could be important depending on the species or complex of pest species of concern. Biological Control Insect Research Laboratory Combines Programs Beginning in late 1964, the BCIRL programs emphasized biological control of pests of cabbage and other cole crops. This research is particularly interesting because it combined parasite importation, periodic parasite releases, the use of both parasites and pathogens, and environmental manipulation techniques. In this program, two imported hymenopteran parasites, Cotesia rubecula (Marshall) and Trichogramma evanescens Westwood, were released periodically in cabbage along with fertile imported cabbageworm adults. The goals of the program were to (1) introduce more effective parasites, (2) increase parasite density and synchronize parasite populations with host populations, and (3) increase host density by reAMERICAN ENTOMOLOGIST • Volume 47, Number 1 Fig. 5. Predaceous bigeyed bug Geocoris punctipes (Say) feeding on nymphs of the whitefly Bemisia argentifolii Bellows & Perring. lease of fertile host adults to insure an adequate host supply for maintaining populations of the parasites. In treated plots, 96% of the cabbage plants produced grade A, No. 1 heads, whereas none of the plants in control plots produced marketable heads. When a nucleopolyhedrovirus (NPV) infectious to cabbage looper, Trichoplusia ni (Hübner), was applied and combined with release of Trichogramma egg parasites, the loopers were controlled. The bacterial insecticide Bacillus thuringiensis Berliner (Bt) was used to control other lepidopteran pests. Naturally occurring parasites, predators, and pathogens usually controlled aphids in the absence of chemical pesticides. This program is an excellent example of how a variety of biological control approaches can be integrated into an effective IPM program (Parker 1971, Biever et al. 1994). One of the major impediments to economical inundative release programs is the high cost of producing sufficient numbers of parasites or predators. A major factor in the production cost is the necessity of producing large numbers of hosts or prey. This realization led to efforts to develop in vitro rearing techniques for parasites and artificial diets for predators. ARS scientists developed an artificial diet for larvae and adults of the common green lacewing. This diet worked, but the presentation system was inefficient. Efforts to develop an encapsulation device for diets were more successful during this period, but equipment was costly and cumbersome, and sterility of the diet was a problem. Research of this type has continued (Coulson et al. 2000). Augmentation and conservation biological control received increased attention in the ARS beginning in 1973 as environmental concerns, pesticide regulations, and resistance to insecticides increased. 33 Many beneficial insects are dependent on semiochemicals to locate suitable habitats in which to locate hosts or prey. Research in this area has been conducted at ARS laboratories in Georgia, Florida, and Louisiana. Many of the IPM programs developed by the ARS and other institutions that were being adopted widely at the time basically were chemical pesticide management systems, which contributed toward insect control by conserving existing natural enemies. Much of ARS research related to augmentation was basic in nature (e.g., influences of semiochemicals on host or prey selection; basic biology, physiology, and nutrition; and development of mass production technology). Several large-scale tests involving augmentation of specific biological control agents were conducted. The ARS evaluated the technical feasibility of using a parasite to suppress sugarcane borer, Diatraea saccharalis (F.), populations in Louisiana and Florida and developed a mass-production technique (Coulson et al. 2000). Eulophid parasites imported from India and South America were studied for use in augmentation programs against the Mexican bean beetle and Colorado potato beetle, with some success, as were studies using artificially reared, predaceous, native lacewings against the bollworm/tobacco budworm complex in cotton (Coulson et al. 2000). Augmentation of other parasites against lygus bugs in cotton in Arizona, the boll weevil in Texas, and fruit flies in Hawaii also were tested. Laboratory and small-scale warehouse studies demonstrated that parasites can suppress pest populations in stored products (Coulson et al. 2000). Many studies have been conducted at ARS laboratories on augmentation of hymenopteran parasites to control flies breeding in dung, and many of the parasites now are being sold commercially to abate this problem (Coulson et al. 2000). Artificial Diets To reduce the cost of using natural enemies for augmentation programs, ARS laboratories in Arizona, Missouri, Florida, and Texas conducted considerable research in the development of artificial diets for predators and in vitro rearing techniques for parasites. At least 33 species of parasites have been reared with varying degrees of success on artificial diets (Coulson et al. 2000). One of the major new research efforts has been on the use of semiochemicals to manipulate the host and prey selection behavior of entomophagous insects (Tumlinson and Lewis 1991, Tumlinson et al. 1992). Many beneficial insects are dependent on semiochemicals to locate suitable habitats in which to locate hosts or prey. Research in this area has been conducted at ARS laboratories in Georgia, Florida, and Louisiana. The technical feasibility of augmenting several parasites and predators has been demonstrated. Improved techniques for rearing, storing, transporting, and releasing several organisms were developed. Knowledge of the basic biology and ecology of numerous parasites and predators and of the mechanisms of host and prey selection was increased. The ARS has increased research on development of economical mass-rearing systems, badly needed if augmentation as inundative releases is to be accepted widely. The Robert E. Gast Labo- ratory at Mississippi State University specifically was dedicated to developing efficient and economical methods for mass rearing of pest and beneficial species. The ARS leases part of this facility for its Biological Control and Mass Rearing Research Unit. Classical Biological Control of Weeds The first weed biological control program was established in Hawaii in 1902 for control of lantana, Lantana camara L. (Goeden 1978). Biological control of weed programs quickly developed in other areas of the world, notably Australia, but it was not until the 1940s that such research was conducted in the continental United States, first by the University of California and later by the USDA in cooperation with the University of California at Albany, CA (Goeden 1978). Research programs on biological control agents of weeds were included in the IIPI. Research on several weeds began at the EPL in 1947, and shipments of natural enemies were sent to the ARS station at Albany, CA. Initial target weeds at the EPL included common St. Johns-wort, Hypericum perforatum L., and gorse, Ulex europaeus L. The former also known as Klamath weed, a rangeland weed mildly poisonous to livestock, was introduced around 1900 into California, Oregon, and Washington and by 1944 occupied 809,388 ha of otherwise useful rangeland in California alone. After successful introduction and establishment of European natural enemies in Australia, a similar program was started in the United States in cooperation with University of California, and importations began from Australia in 1944 (Table 3). The Klamathweed beetle, Chrysolina quadrigemina (Suffrian), and a related species became established almost immediately and by 1950, millions of the beetles were collected in California for recolonization. By 1954, the weed in California was reduced to roadside habitats and now is estimated to be at less than 1% of its former abundance. California ranchers erected a monument in Humboldt County to the introduced beetles. The annual benefits of the program are estimated at $23 million over previous control costs plus weight gain in cattle (Huffaker and Kennett 1959, Goeden 1978, DeBach and Rosen 1991). Because most of the exotic California weeds studied were believed to be of Mediterranean origin, work shifted to a new Biological Control of Weeds Laboratory (BCWL) in Rome, Italy, established in 1959 specifically for the weed work (Table 2). During 1959–1972, target weeds at this new laboratory included over a dozen species common to the western United States (Table 3). Field stations were established in Teheran, Iran, and Rabat, Morocco, to study natural enemies of halogeton, Halogeton glomeratus (Stephen ex von Bieberstein) C. A. von Meyer (Table 2). Control of Rangeland Weeds Significant accomplishments of the research on rangeland weeds during 1953–1972 included establishment in the United States of a number of AMERICAN ENTOMOLOGIST • Spring 2001 34 European insect natural enemies of musk, Carduus nutans L.; plumeless, C. acanthoides L., Italian, C. pycnocephalus L., milk, Silybum marianum (L.) Gaertner, and Canada, Cirsium arvense (L.) Scopoli, thistles; tansy ragwort, Senecio jacobaea L.; gorse; Scotch broom, Cytisus scoparius (L.) Link; Mediterranean sage, Salvia aethiopis L.; and puncturevine, Tribulus terrestris L. The most successful results were obtained on tansy ragwort, musk thistle, and puncturevine. Tansy ragwort is a poisonous European weed in pastures and rangeland of the northwestern United States. Three European insect species were introduced successfully for control of tansy ragwort in the United States. Two of these, the cinnabar moth, Tyria jacobaeae (L.), and a flea beetle, Longitarsus jacobaeae (Waterhouse), primarily have been responsible for excellent control of this weed. Tansy ragwort has been reduced to less than 1% of its former densities at study sites in California and Oregon. Replacement vegetation chiefly has been native plants and more benign weeds. In Oregon, savings from the control of tansy ragwort have amounted to approximately $5 million annually, with an estimated cost:benefit ratio of 1:14 (Hawkes 1981, Pemberton and Turner 1990). Musk thistle is a serious pest of pastures and rangelands throughout the United States. Initial domestic research on European insects attacking musk thistle was funded under a cooperative agreement with the Virginia Polytechnic Institute and State University. A European seed weevil, Rhinocyllus conicus Fröelich, initially released in Canada, was tested by ARS scientists and established in Montana and Virginia; it later spread to other areas of the United States. The weevil substantially reduced musk thistle at many locations and also affected plumeless, milk, and Italian thistles (Andres and Rees 1995). Puncturevine is an introduced spiny weed of roadsides, noncultivated areas, cultivated crops, pastures, and rangeland throughout most of the United States. Two species of European weevils (Table 3) were introduced successfully from Italy and established and spread in California and in the southwestern and central states from Texas north to Nebraska. Of puncturevine-infested California counties surveyed in 1975, 32 reported a decrease in puncturevine populations as a direct result of the weevils. Estimated annual savings for California alone was $1.7 million. The one-time cost of the puncturevine project was estimated to be $360,000, one-fifth of the resulting annual benefits, which still are accruing (Huffaker et al. 1983). Control of Aquatic Weeds Beginning in 1959, ARS pioneered research on biological control of aquatic weeds (Coulson et al. 2000). Since 1899, the United States Army Corps of Engineers (USACE) has had the responsibility for controlling aquatic weeds in the nation’s navigable waterways; activities were expanded in 1945. As part of its expanded efforts, the USACE began to fund ARS research in 1959 to explore biological control of alligatorweed, Alternanthera AMERICAN ENTOMOLOGIST • Volume 47, Number 1 philoxeroides (von Martius) Grisebach, and waterhyacinth, Eichhornia crassipes (von Martius) Solms-Laubach, two of the most serious weeds of waterways in the southeastern United States, and subsequently funded research on other aquatic weeds. The ARS conducted surveys for natural enemies of these two weeds in South America, their place of origin, during 1960–1962. An ARS laboratory was established in Hurlingham, Argentina (Table 2), in 1962 to collect and study promising insect enemies. Three insect enemies (Table 3) of alligatorweed were introduced and established in the United States during 1964–1971. In 1970, the ARS established a laboratory in Gainesville, FL, to conduct research on biological control of these and other aquatic weeds in the Southeast. In 1972, an entomologist was stationed at the USDA Aquatic Weeds Research Laboratory in Fort Lauderdale to handle release and evaluation of natural enemies of alligatorweed and waterhyacinth in Florida. Two of the alligatorweed-feeding insects, a beetle and a moth (Table 3), spread rapidly after introduction throughout the southeastern United States, with spectacular results in some areas, and generally caused a substantial reduction in alligatorweed at many release sites. An early (1976) conservative estimate of the benefits of alligatorweed control in terms of reduced herbicidal treatments was $400,000 annually, with an estimated total ARS research cost of $1 million (Maddox et al. 1971, Coulson 1977). Results of a 1981–1982 survey of alligatorweed in 10 southern states conducted by the USACE showed that of the 39,255 ha problem weed in 1963, less than 400 ha remained in 1981. Research on biological control of aquatic weeds continued into the 1990s at the ARS Gainesville and Fort Lauderdale, FL, locations. In addition to natural enemies of alligatorweed and waterhyacinth, others were imported for control of the introduced weeds Eurasian watermilfoil, Myriophyllum spicatum L.; hydrilla, Hydrilla verticillata (L. fils) Caspary; and melaleuca, Melaleuca quinquenervia (Cavanilles Palop) Blake, established in Florida. Much of this research, including overseas surveys, was made possible via cooperative agreements with the University of Florida, USACE, and the Florida Department of Environmental Protection. Results of much of the research on biological control of aquatic weeds conducted at Florida locations are contained in many of the reports and miscellaneous papers of the USACE Aquatic Plant Control Research Program published by the Corps’ station in Vicksburg, MS, and other research papers cited in Coulson et al. (2000). The successes of the biological control of weeds program, from Klamath weed to alligatorweed and tansy ragwort, led to a marked expansion of effort in this area. From 1973 to 1991, the ARS laboratory in Rome, Italy, focused on biological control of the following weeds introduced into the United States from Europe: field bindweed, Convolulus arvensis L.; musk thistle; yellow starthistle, Centaurea solstitialis L.; Dalmatian toadflax, Linaria genistifolia dalmatica (L.) Maire & Petitmengin; 35 leafy spurge, Euphorbia esula L.; diffuse, Centaurea diffusa Monnet de Lamarck, and spotted, Centaurea maculosa Monnet de Lamarck, knapweeds, and others. A substation was also established in Greece in 1980 for study of the natural enemies of yellow starthistle and other weeds. The Rome laboratory and the EPL were consolidated in 1991 (Table 2) into the EBCL in Montpellier, France. Research at the new EBCL emphasized the introduced western weeds, leafy spurge, yellow starthistle, and knapweeds from 1991 to 1994. Studies on saltcedar, Tamarix ramosissima von Ledebaur, an introduced weedy tree in much of the southwestern United States, were begun in cooperation with the ARS laboratory in Temple, TX. Most of the natural enemies studied at the European laboratories were shipped to Albany, CA. Since 1988, shipments also have gone to the ARS in Temple, TX, and to Montana State University quarantine facilities in Bozeman, MT, for further study and release; and to APHIS personnel in Mission, TX, and Bozeman, MT. Other states and universities also have received material. During 1973–1993, research at the ARS laboratory in Hurlingham, Argentina (Table 2), focused first on biological control of aquatic weeds; candidate natural enemies resulting from these studies were sent to ARS laboratories in Florida. In 1993, the mission of this laboratory, renamed the South American Biological Control Laboratory (SABCL), was altered to include target insect pests. In 1989, a third overseas biological control of weeds labo- ratory was established, in Queensland, Australia, for the study of invertebrate natural enemies of aquatic and wetland weeds (Table 2). Targets of research there have been hydrilla and melaleuca. Quarantine Facilities Expanded From 1973 to 1985, the research program at Albany, CA, shifted from programs on aquatic weeds back to research on biological control of rangeland weeds. A new, expanded research quarantine facility for the laboratory was designed and constructed specifically for biological control and was occupied in 1986. In 1987, the spurge and knapweed projects at Albany and three biological control scientists were reassigned to Bozeman, MT, to emphasize introduction and evaluation studies on the control of these weeds, important to that area. Montana State University constructed new quarantine facilities to accommodate the needs of the transferred ARS personnel and university staff. One ARS scientist remained at Albany to continue research on yellow starthistle and other weeds. During 1988–1990, the Albany quarantine facility was shared with the APHIS biological control personnel importing natural enemies of leafy spurge provided by the ARS laboratory in Rome and other cooperators. The research program on rangeland weeds headed and coordinated by the Albany unit during 1958–1987 involved many ARS and state cooperators in several western states. The new ARS biological control of weeds unit in Bozeman, MT, coordinated activities on biological control of rangeland weeds of the northern states. Research focused on study and release of introduced natural enemies of spurge and knapweed, in cooperation with Montana State University, other western universities, Canada, and the APHIS (Fig. 6). The ARS research was funded in part by the Bureau of Land Management and Bureau of Indian Affairs of the United States Department of the Interior. Two new ARS biological control of weeds units were established in the early 1970s. One, located in Stoneville, MS, in association with the ARS laboratory in Rome, focused on the study of arthropod fauna of narcotic plants. A quarantine facility was constructed for use as a biological control of weeds and insects quarantine-receiving center. Studies on the biological control of pasture, row crop, and aquatic weeds of the Southeast by use of arthropods were conducted in Stoneville during 1972–1986. Biological control of weeds research in Stoneville later focused on use of indigenous plant pathogens. The second laboratory is located in Temple, TX. Research there has addressed biological control of native and introduced weeds and brush of southwestern rangelands by foreign insect control agents. The emphasis on native weeds was due to the existence of about 20 southwestern rangeland weeds and brush that are potentially controllable with biological control agents. This has been the only project worldwide devoted to classical biological control of native weeds in a continental area (DeLoach 1995). Much was accomplished in the AMERICAN ENTOMOLOGIST • Spring 2001 Fig. 6. Spurge hawkmoth larva, Hyles euphoribiae L., feeding on leafy spurge, Euphorbia esula L. 36 development of theory and application that demonstrated that biological control of native weeds is feasible if the target weeds and biological control agents are selected carefully. Information has been obtained on the host range, ecology, life history, and impact of native United States and South American natural enemies on the target and related weeds. The most important introduced weed in the Southwest is saltcedar. Beginning in 1987, an extensive review of the literature and analysis of the harmful and beneficial effects of this weed and of its potential for biological control was conducted in Temple, TX (Coulson et al. 2000). Surveys for natural enemies were conducted in southern Europe, North Africa, Turkmenistan, and China. Host-range testing of candidate agents began in 1991 by the ARS at the EBCL in France and by Israeli cooperators. As a result, two introduced insect species were proposed for release and have undergone quarantine testing in Temple, TX. The chrysomelid beetle Diorhabda elongata (Brullé) has now been released in field cages in the United States. Beltsville, MD, Program Initiated In 1974, research on biological control of weeds was initiated at Beltsville, MD, to take advantage of previous research on insect enemies of weeds established elsewhere in the United States for release against similar weeds in the Northeast. The potential for the biological control of other weed pests of northeastern pastures also was investigated. The last targeted weed for the Beltsville program was purple loosestrife, Lythrum salicaria L. After initial foreign exploration and funding of a fact-finding contract with the International Institute of Biological Control (IIBC), the Beltsville laboratory provided an early coordinating role in the program. Later, foreign and quarantine research on the biological control of this wetland weed was funded by the United States Fish and Wildlife Service. The overseas studies were conducted under contract by IIBC and the quarantine studies by scientists at Virginia Polytechnic Institute and State University. Three European beetles (Table 3) were imported and released in 1992 at several sites throughout the United States, and in Canada (Malecki et al. 1993). This part of the ARS program was terminated in 1993. Thirty-three new exotic weed-feeding invertebrates, including a nematode, were introduced into the United States during 1973–1994. Several of these projects have resulted in control of the weeds in portions of their ranges. The dramatic biological control of tansy ragwort throughout its range in California, Oregon, and parts of Washington matched the levels of control achieved in the earlier common St. Johns-wort program (Coulson et al. 2000). The improved control was primarily due to feeding of the earlier introduced ragwort flea beetle2 (see above). The Oregon Department of Agriculture has been instrumental in distributing the introduced ragwort insects throughout that state to the extent that they now pay some farmers to maintain ragwort to serve as a source of future beetle AMERICAN ENTOMOLOGIST • Volume 47, Number 1 collections. The Colorado and New Jersey Departments of Agriculture also distributed natural enemies introduced by the ARS to control thistles and other weeds. Intensive Implementation on Rangeland Pests Yellow starthistle is an annual weed from southern Eurasia that is highly invasive on rangelands and other environments in the far western states. Since the mid-1980s, three weevils and two tephritid flies have been introduced from Greece and have become established in the United States (Table 3). These five species attack the flowerheads and reduce reproduction. Leafy spurge (Table 3), from Eurasia, a perennial weed toxic to cattle, infests rangelands in the northcentral states and adjacent areas of Canada. Agriculture Canada, now Agriculture and Agri-Food Canada, and the IIBC initiated a biological control program against spurges in the 1960s. ARS joined the effort in the 1970s through research carried out at the Albany, CA, and Rome, Italy, laboratories, and in Bozeman, MT, by 1987. The APHIS has carried out an intensive implementation activity on this weed since the late 1980s. Eleven insects have been imported from Eurasia and released in the United States. Establishment is confirmed for seven, the most important being Aphthona flea beetles (Table 3). Reduction of leafy spurge is evident in many areas. Diffuse and spotted knapweed are biennial and perennial herbs, respectively, that are native to Eurasia and cause problems on rangelands in the northwestern United States and southwestern Canada. Biological control research on these weeds began in Canada in 1961; research by the ARS began in the 1970s. Twelve insects have been introduced into the United States against these two knapweeds. Of these, 10 (four tephritid flies, three weevils, a buprestid beetle, and two moths) were established in 1993. Their biological control potential appears good. Research on introduced weeds in Texas has resulted in the establishment of a mite, Aceria malherbe Nuzzaci, a promising natural enemy of field bindweed, as a result of previous research by the Albany laboratory. Prospects for control of saltcedar also are promising, although this has proven to be controversial (see pertinent chapters in Nechols et al. [1995] for progress on biological control of terrestrial weeds). In regard to aquatic weeds, waterhyacinth has been reduced to one-third of its former abundance in the Gulf Coast states by the activity of two weevils and a moth introduced from Argentina (Table 3). Asian and Australian natural enemies of hydrilla have been introduced, 1987–1991, but control of this weed has not been verified. A South American weevil, Neohydronomus affinis Hustache, first studied at the ARS laboratory at Argentina, was used by Australian and University of Florida researchers to successfully control waterlettuce, Pistia stratiotes L., in Australia and Florida (Dray et al. 1990). (Also see Center et al. [1990], Cofrancesco [1993], and Coulson et al. [2000] for progress on aquatic weeds.) 37 The ARS has been involved deeply since the 1960s in the development of the bacterium, Bt, by conducting basic and applied research on numerous insects and isolates (Dulmage and Aizawa 1982). Insect and Other Arthropod Pathogens The USDA has been involved in insect pathology/microbial control research since the early 1900s. Many research findings of the ARS have provided the information necessary to develop microorganisms as control agents of plant and animal pests and as prophylactic or therapeutic control methods for insect diseases in mass-reared pest and beneficial species such as the honey bee, Apis mellifera L. This summary covers highlights of many of the significant research findings in insect pathology and microbial control and the development of disease control methods. It describes research on insects of importance to food and crops, humans and animal, domesticated insects (i.e., honey bee), and forests. The USDA received early recognition for its research on insect pathology/microbial control. The research of L. O. Howard (1902) on biological control of grasshoppers with fungi was one of the first programs of the USDA to introduce exotic insect pathogens. In the early 1900s, an extensive project began on microbial control of the newly introduced Japanese beetle. Also the impact of pathogens on honey bees was recognized and research began on ways to ameliorate these problems. These early projects emphasized surveys, microbial control, epidemiology, pathology, and description of the relevant organisms. They provided important basic information for solving these problems. As mentioned by Steinhaus (1949), these projects provided the stimulus for modern day programs and the acceptance of insect pathology and microbial control as distinct disciplines. The developments of White and Dutky (1940) led to the first extensive use of an insect pathogen, the “milky” disease bacterium (Bacillus popilliae Dutky), for control of the Japanese beetle, Popillia japonica Newman. Until recently, this organism was produced commercially and used for control of the Japanese beetle. The studies of honey bee diseases also are considered to be classics. Programs on both of these problems continue to this day (Dutky 1992). These programs expanded to include numerous target pest species and virtually every type of insect pathogen. The establishment of insect pathology as a discipline combined with the foresight of E. F. Knipling led to the establishment of insect pathology and microbial control programs at many USDA-ARS locations throughout the United States beginning in the late 1950s, including the Insect Pathology Pioneering Research Laboratory in Beltsville, MD. In the 1950s and 1960s, the adverse effects of a protozoan, Glugea pyraustae (Paillot), and a fungus, Beauveria bassiana (Balsamo) Vuillemin, on European corn borer were demonstrated. The ARS also conducted early studies on the potential use of baculoviruses and bacteria for insect control. Research on all aspects of the mass production, efficacy, and safety of a nucleopolyhedrovirus, Helicoverpa zea SNPV, led to the first registration of a baculovirus for commercial use (Ignoffo and Couch 1981). Research on basic pathology, pro- duction, and efficacy of other baculoviruses also was conducted, i.e., cabbage looper, cotton bollworm/tobacco budworm, and Indianmeal moth, Plodia interpunctella (Hübner). At least 11 baculoviruses are now registered worldwide as microbial control agents. The ARS has been involved deeply since the 1960s in the development of the bacterium, Bt, by conducting basic and applied research on numerous insects and isolates (Dulmage and Aizawa 1982). More than 1,000 Bt isolates were propagated and screened against many target insects at various ARS laboratories (Dulmage et al. 1981). HD-1, a broadly used commercial strain, was identified as an agent with a high possibility for commercial use as a result of these studies. Other subspecies or isolates of this organism also are now used throughout the world to suppress insect pests of plants, animals, and humans. Numerous investigations on pathogens of insects affecting humans and other animals were conducted throughout the United States (Cantwell and Laird 1966). These investigations led to the isolation and development of several pathogens for population suppression and control of mosquitos and other aquatic Diptera (Hazard and Weiser 1968, Hazard et al. 1985, Sweeney et al. 1985). Research on Insect Pathology and Microbial Control Intensified During the 1960s and 1970s, the ARS had more insect pathology/microbial control specialists than any other institution in the world, conducting diverse research on a variety of pest species and pathogens. Intense research continued into the 1990s leading to a more thorough understanding of insect pathogens and their interactions with their hosts. Significantly more knowledge about their production and use as microbial control agents also was obtained. The first virus infecting plantfeeding mites was described from the citrus red mite, Panonychus citri (McGregor), by Tashiro et al. (1970). Two morphological types of nucleopolyhedroviruses, one with single virions within an envelope (SEV) and one with multiple virions within the envelope (MEV) were discovered (Heimpel and Adams 1966), which later led to the discovery of Autographa californica MNPV, a baculovirus having a broad host range that provided the potential to control several insect species (Vail et al. 1971). AcMNPV also replicates extensively in insect cell lines (Vail et al. 1973) and was the basis of the first plaque assay for an insect virus (Hink and Vail 1973). Intensive studies on insect cell-line nutrition and in vitro baculovirus production were conducted at numerous laboratories (Vaughn et al. 1977). This virus is now utilized as an efficient expression system for proteins and other compounds of biological and medical significance. Control of a number of economic insect species by baculoviruses was demonstrated, including cotton bollworm/tobacco budworm; fall armyworm, Spodoptera frugiperda (J. E. Smith); gypsy moth; Indianmeal moth; codling moth, Cydia pomonella (L.); cabbage looper; and others. In AMERICAN ENTOMOLOGIST • Spring 2001 38 1968, the ARS fire ant project began with a component for the development of microbial control agents. The microspordian Nosema locustae Canning became the first protozoan mass-produced and registered for use against rangeland grasshoppers (Henry 1971). ARS scientists contributed significantly to the knowledge and development of continuous in vitro insect cell cultures from insect species (primarily Lepidoptera, Orthoptera, and Coleoptera) that were capable of supporting reproduction of insect pathogens. Numerous studies were conducted on the efficacy of Bt, variety israeliensis de Barjac, for control of black flies and mosquitoes (Lacey 1983, Lacey and Undeen 1984). Several UV screens were developed to reduce sunlight inactivation of microbial control agents in efforts to increase efficacy through improved formulations (Shapiro et al. 1983). Autodissemination of an insect pathogen was recommended for reduction of populations of khapra beetle, Trogoderma granarium Everts, a storage pest (Burkholder and Boush 1974). Investigators at Beltsville, MD, demonstrated for the first time that spiroplasmas occurred in a number of insects, including members of the Coleoptera, Lepidoptera, Diptera, Homoptera, and Hymenoptera (Clark 1982, Hackett and Clark 1989). Insect Pathology Program Initiated at European Parasite Laboratory In 1981, an insect pathology program was initiated at the EPL in Rome to provide insect pathogens through foreign exploration for potential control of endemic and exotic pests introduced into the United States. The program gradually evolved and, in 1991, a permanent position for insect pathology research was established. This exploration and research program is now conducted at the EBCL in Montpellier, France. In concert with the EBCL, a Japanese beetle control program on the island of Terceira (Azores, Portugal) was implemented under the direction of USDA-ARS International Activities (Lacey et al. 1994). ARS scientists and A. W. Sweeney (from Australia) determined that a copepod was an essential intermediate host for a protozoan pathogen of mosquitoes, thus advancing the study of microsporidian ecology (Sweeney et al. 1985). A protozoan pathogen was isolated and described from specimens of the fire ant, Solenopsis geminata (F.), collected in South America (Knell et al. 1977). As a result of ARS research, Bt was registered for use on stored grains and a granulosis virus also provided high levels of control (McGaughey 1976, 1978). The same pathogens were studied as protectants of dried fruits and nuts with similar results (Hunter 1970, Hunter et al. 1977). The first documented case of resistance to Bt was described in the Indianmeal moth by the ARS Manhattan, KS, Laboratory (McGaughey 1985). As a result of the increased research, more microbial control agents were field tested. The pressure to provide suitable alternatives to chemical insecticides also was a factor influencing increased field testing. AMERICAN ENTOMOLOGIST • Volume 47, Number 1 Research was conducted with pathogens for areawide suppression of multicrop pests such as the cotton bollworm/tobacco budworm complex (Bell and Hardee 1994). Adjuvants to increase the effectiveness of microbial pesticides also were developed. While conducting research with optical brighteners as baculovirus protectants, high levels of synergism were observed between some of these compounds and baculoviruses (Shapiro and Robertson 1992). High variability in susceptibility between honey bee colonies to chalkbrood was found and stressors were defined. Captan, (Scotts, Ortho Group, Columbus, Ohio) was an effective control for chalkbrood when topically applied to hives. Selection for resistance to chalkbrood in a leafcutting bee, Megachile rotundata F., was demonstrated, and a rare protozoan, Malpighamoeba mellificae Prell, causing severe population reductions in the honey bee was identified. The world’s foremost collection of entomopathogenic fungi was started by R. S. Soper, Jr., and continued by R. A. Humber at the ARS Laboratory in Ithaca, NY. More than 3,200 isolates of more than 250 species now are in the collection (Humber 1992). In the 1980s and 1990s, nematodes were demonstrated to reduce populations of several agricultural and medical/veterinary pests and were produced by several private companies. Later, the EPA exempted entomopathogenic nematodes from registration based on the findings of a joint USDA-universityindustry effort (Gorsuch 1982). Hawaiian fruit fly populations could be reduced with soil drenches of nematodes (Lindegren 1990). Intensive research on gypsy moth rearing and virus production resulted in the production of 1.5 million insects in 100 days, which yielded 20,234 ha treatments with a 10-fold reduction in production costs (Bell et al. 1981). A large-scale test in El Salvador with microbials nearly eradicated an anopheline mosquito, Anopheles albimanus Wiedemann, malaria vector (Petersen et al. 1978). Simulation models were instrumental in guiding and evaluating studies on fungi infectious to grasshoppers. Beauveria bassiana (Balsamo) Vuillemin was found to move within corn plants and provide control of European corn borer (Bing and Lewis 1991). Entomopathogens will probably be used even more in the future because of environmental and consumer concerns. Research to protect beneficial species such as the honey bee and mass-reared insects from insect pathogens will also continue. The ARS has been among the leaders in basic insect pathology and microbial control since the early 1900s. The strong research base provided by the ARS and other research institutions will provide more practical and unique uses of insect pathogens for agricultural, forest, medical, and veterinary pests in the future. Biological Control in the USDA Forest Service, 1953–1993 Before 1953, the USDA-BEPQ was responsible for all biological control against native and exotic forest pests. In 1953, the USDA was reorganized and the responsibility for biological control of for39 est pests was transferred to the USDA-FS (Table 1). In the 1950s and 1960s, forest pests of local and regional importance were targeted for study and control (Schaffner 1959). Expertise for these efforts was expanded by the 1962 McIntire-Stennis Act, which authorized federal support for biological control research of forest pests at land grant universities. This Act did not provide for collection of natural enemies of major exotic pests in their place of origin. By 1965, 27 projects in Europe, the Far East, and South America targeted native parasites, predators, and pathogens of the gypsy moth; European pine shoot moth, Rhyacionia buoliana (Denis & Schiffermüller); balsam woolly adelgid, Adelges piceae (Ratzeburg); European elm bark beetle, Scolytus multistriatus (Marsham); and various sawflies by means of Public Law 480 funds (Table 4). Once ARS scientists at foreign laboratories collected the biological control agents, their identifications were verified and the agents shipped to the ARS quarantine facility in Moorestown, NJ (Newark, DE, after 1973) for clearance and biological evaluations. The exotic natural enemies were then sent to FS facilities for further evaluations, impact studies, rearing, and, if promising, were released. Table 4 describes some of the successful projects. Many releases were unsuccessful because of the low establishment rate of the natural enemies and the inability of these enemies to significantly impact pest abundance. A typical example is the unsuccessful release of balsam woolly adelgid, Adelges piceae (Ratzeburg), predators from Japan, China, India, Pakistan, and Europe into New England, North Carolina, Washington, and Oregon. Between 1970 and 1979, a number of events shaped the FS’s biological control programs in research and pest management: (1) publication of Silent Spring (Carson 1962) and related environmental publications; (2) concerns about pesticide pollution; (3) the 1972 ban of DDT; (4) concern about adverse impacts of exotic pests and their imported natural enemies; (5) development of the concept of IPM (Stern et al. 1959); (6) realization that focusing on a few key pests would produce greater gains than diversified efforts amongst multiple pests; (7) public and congressional call for the suppression of severe outbreaks of the gypsy moth, southern pine beetle, Dendroctonus frontalis (Zimmermann), and Douglas-fir tussock moth, Orgyia pseudotsugata (McDunnough); and (8) 1974 Congressional appropriation of more than $6 million to accelerate research and management programs for major forest insects and diseases (Shea 1985). In response to these events, the FS research and management programs on the gypsy moth, southern pine beetle, and Douglas-fir tussock moth were accelerated with a focus on coping with these pests on a long-term basis. IPM was emphasized over classical biological control research, and efforts increased on pheromones, pest impacts, pest biology, and chemical and microbial control of major insect pests. Biological control research emphasized understanding the impacts of natural enemies on pest population dynamics and developing 40 methods for utilization of microbial pesticides such as NPVs and Bt. NPVs were used successfully against the Douglas-fir tussock moth and several sawflies (Martignoni and Iwai 1977). Bt Berliner applications provided encouraging results against gypsy moth; spruce budworm, Choristoneura fumiferana (Clemens); forest tent caterpillar, Malacosoma disstria Hübner; and other defoliators (Abrahamson and Harper 1973). Parasites were released for control of the smaller European elm bark beetle and spruce budworm (Table 4). The “Gypsy Moth Expanded Research and Application Program” called for broad use of pesticides, increased foreign exploration for microbial control agents, and increased research to analyze and predict changes in pest populations. In cooperation with the ARS and APHIS, large quantities of a gypsy moth LdNPV were produced (Bell et al. 1981). The virus was registered by the EPA and applied aerially to gypsy moth outbreaks. Only a few exotic parasites [i.e., the chalcid wasp Brachymeria intermedia (Nees) and the braconid wasp Cotesia (=Apanteles) melanoscela (Ratzeburg); and two tachinid flies Blepharipa pratensis (Meigen) and Compsilura concinnata (Meigen)] were established with limited success after intensive trials. Augmentative releases of these and other parasites in the Northeast in combination with Bt or NPV applications also had mixed results. Because of problems ensuring parasite effectiveness after release, research was accelerated on selection and evaluation of isolates, strains, formulations, and application techniques for microbial pesticides (Doane and McManus 1981). The “Expanded Southern Pine Beetle Research and Application Program” focused on understanding population dynamics; salvaging beetle-killed trees, silvicultural techniques for prevention, and cut and leave techniques; developing integrated models for predicting impacts, population levels, and forest susceptibility; and developing survey and suppression techniques with pheromones and insecticides. Research on biological control agents was reduced unless viewed as critical to understanding the population dynamics of the pest or to predict population trends (Thatcher et al. 1981). The “Douglas-fir Tussock Moth Accelerated Research and Development Program” focused on developing effective suppression techniques with NPV and Bt, obtaining information on natural enemies needed to predict population levels, and impacts of the pest. Research in Corvallis, OR, concentrated on NPV development for microbial control (Martignoni and Iwai 1977). A baculovirus production facility was established in Corvallis, OR, which produced enough virus to treat 12,140 ha - 40,469 ha per year. Large-scale forest tests provided data to optimize NPV dosage and develop application strategies; EPA registration was received in 1976. Parasites and predators of Douglas-fir tussock moth also were identified and their impacts on pest populations assessed (Torgersen 1977, 1981; Mason and Overton 1983; Mason and Torgersen 1983; Mason et al. 1983). AMERICAN ENTOMOLOGIST • Spring 2001 Table 4. Examples of FS Biological Control Projects, 1953–1993 a Project Dates and FS Research Laboratories 1953–1979, Corvallis, OR 1953–1986, Ft. Collins, CO; Missoula, MT; Corvallis, OR 1953–1993, Orono, ME; Corvallis, OR; Odgen, UT; Lansing, MI; Flagstaff, AZ 1953–1993, New Haven, CN Level of Control b PEC Pest Species European pine shoot moth, Rhyacionia buoliana (Denis & Schiffermüller) Douglas-fir tussock moth, Orgyia pseudotsugata (McDunnough) Spruce budworms Choristoneura fumiferana (Clemens) and C. occidentalis Freeman Gypsy moth, Lymantria dispar (L.) Outcomes Rearing and release of the ichneumonid, Itoplectis quadricingulatus (Provancher), in Oregon. Thirty percent of the shoot borers at the release sites were parasitized. Parasite abundance in egg masses used to predict subsequent defoliation. Development and registration in 1976 of Biocontrol1Ô, the first virus registered in the United States for forest insects. Refinement of strains and formulations and improvement of Bt processing and application technology led to more effective control. SEC A series of field and laboratory trials and pilot tests in Maine, PEC Wisconsin, New Mexico, Montana, Oregon, and Washington that assessed and enhanced the effectiveness of Bt strains, formulations, dosages, and physical properties and improved application technologies resulted in increased efficacy and reduced damage levels. Augmented releases of the tachinid Blepharipa pratensis (Meigen) SEC in Pennsylvania increased B. pratensis abundance two-fold in areas where both the parasites and gypsy moth populations were declining. Refinement of Bt strains, formulations, dosages, and physical properties resulted in decreased impacts on nontarget organisms, significant foliage protection, and improved gypsy moth control. The development of effective nuclear polyhedrosis virus (LdNPV) formulations led to registration of Gypchek as a microbial pesticide. The subsequent identification of more virulent isolates and strains, development of “ready-to-use” Gypchek formulations, and development of improved application methodologies led to intervention tactics targeted to meet the needs of individual gypsy moth management programs. Demonstration that the braconid Cotesia (=Apanteles) melanoscela (Ratzeburg) can transmit lethal dosages of LdNPV opened new opportunities for transmission of LdNPV. The braconid Agathis pumila (Ratzeburg), the eulophid Chrysocharis SEC laricinellae (Ratzeburg), and three other parasitic species were collected in the northeastern United States and in Canada and released in Washington, Montana, and Idaho. The establishment, build up, and spread of A. pumila and C. laricinellae led to biological control of the casebearer. Importation of parasites from France, mass production, and successful release of the braconid Dendrosoter protuberans (Nees) in Missouri and Ohio. Twenty-three to 31 percent of the bark beetles in the release sites were parasitized. PEC 1953–1993, Missoula, Larch casebearer, MT; LeGrande, OR; Coleophora laricella Missoula, MT (Hübner) (Forest Health Protection); New Haven, CN 1960–1979, Delaware, OH European elm bark beetle, Scolytus multistriatus (Marsham) Elm spanworm, Ennomos subsignarias (Hübner); fall cankerworm, Alsophila pometaria (Harris); Oxydia trichiata (Guenée) 1960–1979, Research Triangle, NC Identification of the scelionid egg parasite, Telemonus droozi, that SEC caused the collapse of a Southeastern elm spanworm outbreak and the scelionid, T. alsophilae Viereck, that parasitized fall cankerworm eggs in Virginia led to a search for alternative geometrid hosts for these parasites and the development of storage and mass production techniques. Inundative releases of T. alsophilae against O. trychiata (Guenée), on Cupressus lusitanica Cyprus, in Columbia, South Africa, led to successful establishment. T. alsophilae was the first insect parasite to control a forest pests from a genus other than its original host. Augmentative release of the coccinellid Coleomegilla maculata (De Geer) in Mississippi met with limited success. Collection of the exotic ichneumonid Olesicampe benefactor Hinz, a parasite of larch sawfly in Minnesota, rearing in North Carolina, and release and establishment in Pennsylvania. After 8 years, approximately 59 percent of the sawflies were parasitized. Sawfly cocoons parasitized with the torymid Monodontomerus dentipes (Dalman) were collected in Wisconsin, and the parasite was mass-reared and released in North Carolina. The sawfly population collapsed due to the establishment of M. dentipes. PEC 1970–1986, Stoneville, MS 1970–1986, Research Triangle, NC Cottonwood leaf beetle, Chrysomela scripta Fabricius Larch sawfly, Pristiphora enrichsonii (Hartig) Introduced pine sawfly, Diprion similis (Hartig) PEC 1970–1993, Research Triangle, NC; Asheville, NC a b SEC This table identifies significant parasite and predator releases and microbial treatments; it does not summarize all biological control activities in the FS. A detailed discussion of FS biological control activities are in Coulson et al. (2000). CEC = complete economic control; SEC = substantial economic control; PEC = potential economic control. AMERICAN ENTOMOLOGIST • Volume 47, Number 1 41 Canada/United States Spruce Budworms Program Initiated (CANUSA) In 1977, a 6-year research, development, and application program actively explored the identity and role of natural enemies (predators, parasites, and pathogens) in regulating budworm populations and developed methods for suppressing spruce budworm populations with natural enemies (Winget 1985). Between 1980 and 1985, CANUSA research on the eastern spruce budworm, 2 Choristoneura fumiferana (Clemens); and western spruce budworm, C. occidentalis Freeman; concentrated on the role of native natural enemies on their population dynamics. Bird, spider, and ant predators proved influential in regulating budworm populations. Parasites proved less effective and inundative releases failed. For example, a trichogrammatid egg parasite, Trichogramma minutum Riley, was introduced successfully for control of spruce budworm in Maine. However, the parasite was not considered effective in regulating epidemic populations of this budworm because it parasitized less than 15% of the eggs. Field and laboratory trials on microbials by FS scientists and cooperators refined application techniques and formulations of Bt (Table 4). A 1984 international CANUSA symposium summarized research accomplishments, implementation activities, biological, chemical, and silvicultural control techniques and outlined management strategies that integrated available technology (Sanders et al. 1985). During the 1980s, parasites continued to be identified through foreign exploration for gypsy moth. Parasite and predator roles in regulating abundance of gypsy moth; larch casebearer; Douglas-fir tussock moth; and mountain pine beetle, D. ponderosae Hopkins, were assessed (Sesco 1992). Outcomes of this research were highly variable. For example, inundative releases of the gypsy moth braconid parasite Cotesia (=Apanteles) melanoscela (Ratzeburg) increased parasitism in Maryland but did not impact gypsy moth abundance and were unsuccessful in Vermont. An 18year FS study on the population dynamics of larch casebearer populations in Oregon identified the introduced ichneumonid Agathis pumila Ratzeburg as a key factor associated with reduced populations in this State. This study culminated a 50-year research and management effort by federal and state scientists in the Northwest, which was one of the most successful biological control efforts on a forest insect (Ryan 1985, 1990). Forest Insect and Disease Research Program Consolidated During this same decade, consolidation of Forest Insect and Disease Research (FIDR) programs resulted in significant losses of scientists working in biological control. In the Northwest, scientists were reassigned to western spruce budworm and Douglas-fir tussock moth programs. FIDR research units in Hamden, CT; Morgantown, WV; and Delaware, OH; cooperated with Forest Pest Management (FPM) units in West Virginia, New Hampshire, 42 and North Carolina to improve and implement biological management techniques for gypsy moth. In the South, a 5-year “Integrated Pest Management Program for Bark Beetles and Diseases of Southern Pines” was initiated in 1980 to complete research and transfer technical information from the “Expanded Southern Pine Beetle Research and Application Program.” This program developed an integrated southern pine pest management system for several species of bark beetles including the southern pine beetle; black turpentine beetle, Dendroctonus terebrans (Oliver); and Ips spp. and improved the accuracy of bark beetle population dynamics models (Branham and Thatcher 1985, Shea 1985). By 1986, approximately 13% of the FIDR research budget was devoted to biological control research with 75% of this budget for insect pests (Stewart 1989). In 1987, a 10-year plan was developed to guide FIDR into the twenty-first century. Research focused on pests of national concern and development of new technologies. Research priorities were as follows: (1) determination of how interactions among hosts, pests, natural enemies, and the environment influence the frequency and severity of pest outbreaks; (2) development of effective and environmentally safe microbial agents for insect pests; and (3) development of control tactics using parasites and predators through inundative or augmentative releases. In 1988, in response to congressional concern about the continued impacts of major forest pests, acid rain, and air pollution on forest health, the FS developed the strategic plan “Forest Health Through Silviculture and Integrated Pest Management.” The plan called for a monitoring program to identify areas of forest health concerns and the integration of forest and pest management practices. A 1990 Congressional amendment to the Cooperative Forestry Assistance Act of 1978 strengthened FS programs concerned with forest health monitoring, technology development, and promotion of management measures to protect forest health. In 1993, the strategic plan “Healthy Forests for America’s Future” was developed by the FS to address forest health problems. It emphasized ecosystem management in the National Forests and the integration of forest pest management. It also addressed congressional concerns about forests with increased susceptibility to drought, pest epidemics, wildfire, and introduced pests. The plan called for expanding biological control research: (1) to understand impacts of natural enemies on pest population dynamics and develop pest models and decision support systems to assist land managers in making management decisions; (2) to fill gaps in environmental data for Bt, develop other key microbes, and assess the impacts of pesticides and microbes on nontarget insects; (3) to explore the use of classical biological control including conservation and enhancement of natural enemies; and (4) to use resistant varieties of trees in cooperation with other USDA agencies (USDA Forest Service 1993a). In April 1993, a National Center for Forest Health Management was established in AMERICAN ENTOMOLOGIST • Spring 2001 Morgantown, WV: (1) to facilitate promotion, development, and use of technologies to sustain or enhance forest health, and (2) to advance understanding of forest health and effects of forest health technologies on forest ecosystems management goals. The biological control mission included introduction of exotic predators, parasites, and pathogens, or their augmentation; conservation or enhancement of native species; and evaluation of impacts of microbials and other pesticides on nontarget species such as parasites, predators, and their alternative hosts. In 1993, the Center funded research to evaluate the impacts of Dimilin, (Uniroyal, Bethany, Connecticut) and defoliation on nontargets; spread of the gypsy moth fungus Entomophaga maimaiga Humber, Shimazu, and Soper in the southern Appalachians; and formulation of Gypchek, (USDA Forest Service, Hamden, Connecticut) NPV for control of gypsy moth (USDA Forest Service 1993b, 1993c). As U.S. trade became more global during the 1980s and 1990s, the number of exotic pest introductions increased with the increased importation of foreign goods. Recent introductions, such as the Asian strain of the gypsy moth into North Carolina on birch logs imported from Russia and the European pine shoot beetle,2 Tomicus piniperda (L.), into the Midwest, are of serious concern because these introduced pests have few natural regulating factors in North American forests and could cause permanent and irreversible damage to the forest ecosystem. By 1992, identification of potential exotic pests and their biological control agents by the FPM and FIDR in collaboration with APHIS, ARS, and international organizations was rapidly becoming a high priority program within the FS. In 1992, the FS Quarantine Laboratory was established in Ansonia, CT, to accelerate research and development on biological controls for exotic forest pests and facilitate research with state, federal and international biological control programs. In conclusion, the last 40 years of the FS biological control programs evolved from diverse efforts on many pests and their natural controls to a focused research and management effort that targeted a few high priority pests. Early efforts focused on the identification and biology of native and exotic natural enemies, whereas later efforts focused on the influence of key natural controls on pest population dynamics and identification, importation, and release of exotic natural enemies. The long-term goal was to use these data and technology to develop strategies for managing both endemic and epidemic pest populations. Identification of microbial control agents and continual refinement of microbial technologies resulted in more effective control strategies and projects that continue to be a major focus of research and management efforts. The future role of biological control in the management of forest pests depends on public acceptance of long-term manipulation of ecosystems, successful reduction of impacts on nontarget organisms, and continued long-term support for research and management programs. AMERICAN ENTOMOLOGIST • Volume 47, Number 1 Animal and Plant Health Inspection Service, 1966–1993 The APHIS Biological Control Philosophy was stated by Robert Melland, APHIS Administrator, in 1992, “APHIS believes that biological control is preferable when applicable; however, we also recognize that biological control has limited application to emergency eradication programs. Whenever possible, biological control should replace chemical control as the base strategy for integrated pest management.” In 1972, the APHIS became the implementation agency for large-scale projects to suppress pest populations of agriculture and rangeland by the introduction of natural enemies (Table 5). Biological control operations within the APHIS are under Plant Protection and Quarantine (PPQ), which had its origins in 1966 in Niles, MI, with a program for implementing biological control of the cereal leaf beetle in the Midwestern states. It became a PPQ laboratory in 1972. During 1966–1976, biological control activities generally were restricted to large-scale rearing and distribution of natural enemies to combat major quarantine pests such as cereal leaf beetle, gypsy moth, and citrus blackfly. After 1976, the APHIS-PPQ, in cooperation with state departments of agriculture, expanded its biological control effort to include other economically important agricultural pests (Table 5). The role of PPQ in biological control is to implement projects that have been developed through the research of the USDAARS, IIBC, and universities. The projects emphasize importation-release and augmentation strategies. Biological control activities in the PPQ during 1972-1993 were conducted in three work units: (1) Methods Development Laboratories (MDL), (2) Biological Control Laboratories (BCL), and (3) the National Biological Control Institute (NBCI). Typically, the MDL would develop techniques for rearing, release, and evaluation of natural enemies; and the BCL would apply and refine these techniques in the laboratory and field. Evaluation activities included assessment of establishment, impact on the targeted pest, and, at times, economic impacts on agricultural sectors and consumers. Biological control activities were conducted at the following PPQ Laboratories: (1) the MDL at Otis Air Force Base, MA; Phoenix, AZ; Brownsville, TX (moved in 1983 to Edinburgh, TX); Gulfport, MS (later became a station under Phoenix); Hoboken, NJ (later merged with Oxford Plant Protection Center in Oxford, NC); and Whiteville, NC (later merged with Oxford, NC); (2) the BCL at Mission Air Base, TX, with a field station in Bozeman, MT; and (3) the BCL in Niles, MI. Since 1993, the Biological Control and Methods Development Laboratories have been renamed as PPQ Plant Protection Centers and are organizationally under the Center for Plant Health Science and Technology in Raleigh, NC. In 1990, the APHIS established the NBCI as part of the USDA’s commitment to implement biological control and IPM. The NBCI now is also administratively under the PPQ’s Center for Plant Early efforts focused on the identification and biology of native and exotic natural enemies, whereas later efforts focused on the influence of key natural controls on pest population dynamics and identification, importation, and release of exotic natural enemies. 43 Table 5. Examples of APHIS Biological Control Projects, 1973–1993 Project Dates and Locations 1963–1993+, Otis, Massachusetts; Niles, Michigan 1966–1979, 1993+, Niles, Michigan Pest Species Gypsy moth, Lymantria dispar L. Outcomes Numerous tachinid, ichneumonid, braconid, chalcid, and mermithid parasites reared and released (Reardon 1981); Bt tested; NPV developed. Rearing and establishment of three larval parasites, the eulophid Tetrastichus julis (Walker), ichneumonids Diaparsis temporalis (Thomson) and Lemophagus curtus Townes; and one mymarid egg parasite, Anaphes flavipes (Foerster). More than $168 million net present value of program (Wu 1993). Parasites redistributed to four western states in 1993. Aphelinid larval parasites [Encarsia opulenta Silvestri, E. clypealis (Silvestri), E. smithi (Silvestri), and Amitus hesperidum Silvestri] released and later recovered in Texas. Also released in Florida but only E. opulenta and A. hesperidium were recovered. Level of Control a PEC Cereal leaf beetle, Oulema melanopus L. CEC 1974–1975, Mission, Texas Citrus blackfly, Aleurocanthus woglumi Ashby PEC 1979–1984, Niles, Michigan; Otis, Massachusetts 1980–1991, Niles, Michigan; Otis, Massachusetts Mexican bean beetle, Epilachna varivestis Mulsant Alfalfa weevil, Hypera postica (Gyllenhal) Augmentative releases of eulophid larval parasite, Pediobius SEC foveolatus Crawford, in eastern and midwestern states contributed to reduced pest status in soybeans. Sixteen million parasites released in 38 states including CEC recovery of five larval parasites: the ichneumonids Bathyplectes anurus (Thomson), B. curculionis (Thomson) and B. stenostigma (Thomson); the eulophid Tetrastichus inrertus (Ratzeburg); the pteromalid Dibrachoides dynastes Foerster); and two braconid parasites of adults, Microctonus colesi Drea and M. aethiopoides Loan. Pest numbers lowered and pesticide use reduced by 73% (Kingsley et al. 1993). Economic benefits of $2.2 billion (1987 dollar value), a 91:1 benefit to cost ratio (White et al. 1995). Redistributed the aphelinid parasite Encarsia lahorensis (Howard) from Texas to southeastern states. Mass reared three braconid larval parasites, Apanteles flavipes (Cameron), Allorhogas pyralophagus Marsh, and Rhacanotus rosilensis Lal, at request of the Rio Grande Valley Sugar Growers Association (Martinez et al. 1988). Developed triploidy in white amur, or grass carp, as herbivore of Hydrilla. Developed use of leaf-galling nematode, Ditylenchus phyllobius (Throne) Filipjev, but not competitive with herbicides. Mass produced coccinellid egg predator, Coleomegilla maculata (De Geer) on diet of air-dried Mexican fruit fly eggs. Developed artificial diet for host adults to rear eulophid egg parasite Edovum puttleri Grissell. PEC PEC 1981–1985, Mission, Texas 1981–1991, Mission, Texas Citrus whitefly, Dialeurodes citri (Ashmead) Sugarcane borer, Diatraea saccharalis (F.), and Mexican rice borer, Eoreuma loftini (Dyar) 1981–1993+, Hydrilla, Hydrilla verticillata Whiteville, North Carolina (L. fils) Caspary 1982–1986, Mission, Texas 1985–1993+, Mission, Texas; Otis, Massachusetts Silverleaf nightshade, Solanum elaeagnifolium Cavanilles Colorado potato beetle, Leptinotarsa decemlineata (Say) SEC PEC SEC Health Science and Technology. Its mission is to promote, facilitate, and provide leadership for biological control. The NBCI communicates and publicizes significant activities, cosponsors and participates in meetings and exhibitions, encourages documentation of biological control releases and evaluations, and provides training and education in biological control. It also acts as a liaison between the APHIS and others in the biological control community such as other USDA agencies, universities, the National Plant Board, state departments of agriculture, special interest groups, the environmental community, industry, politicians, the media, and the international community. It is an objective advocate and brings biological control to 44 the attention of the media, environmental groups, scientists, administrators, elected representatives, and citizens. In 1989, the NBCI was named an APHIS Center of Excellence. Its major accomplishments have been as follows: (1) reviewing APHIS’ biological control policy; (2) updating APHIS’ procedures for movement and release of biological control agents; (3) developing training/educational materials for biological control; (4) managing cooperative agreements and grants program including Facilitation Project Grants, Implementation Grants, Postdoctoral Fellowships in Systematics; (5) sponsoring visiting scientists; (6) facilitating international biological control of high-risk pests to better safeAMERICAN ENTOMOLOGIST • Spring 2001 Table 5. Continued. Project Dates and Locations 1985–1993+, Mission, Texas Pest Species Diffuse and spotted knapweeds, Centaurea diffusa Monnet de Lamarck and C. maculosa Monnet de Lamarck European corn borer, Ostrinia nubilalis (Hübner) Outcomes Biological control with several beneficial insects offers ranchers solutions that are long-term and cost effective (Coulson et al. 2000). Beneficial species released included members belonging to Curculionidae, Buprestidae, Tephritidae, Gelechiidae, Pterolonchidae, Tortricidae, and Cochylidae. Biological control as part of IPM program utilizes several natural enemies. Beneficial species included tachinid larval parasite, Lydella thompsoni Herting; trichogrammatid egg parasite, Trichogramma ostriniae Pang and Chen; braconid larval parasite, Macroceutrus grandii Goidanich; ichneumonid larval parasite, Eriborus terebrans (Gravenhorst); protozoan pathogen Nosema pyrausta (Paillot); and fungal pathogen, Beauveria bassiana (Balsamo) Vuillemin. APHIS program participants released >15 million beneficial insects from five families (Aphidiidae, Encyrtidae, Coccinellidae, Syrphidae, and Chamaemyiidae) for control of Diuraphis noxia Mordvilko into 16 states, and four parasite species [Aphelinus albipodus Hayat and Fatima, Aphelinus asychis Walker, Aphidius colemani (Viereck), and Aphidius uzbekistanicus Luzhetzki] became established (Prokrym et al. 1998); coccinellids Scymnus frontalis (Fabricius) and Propylea quatuordecimpunctata (L.) were adapted to reducing pest numbers in rolled leaves of infested cereal grains (Kauffman and LaRoche 1994); IPM and biological control reduced pest populations below economic levels in most western states. Level of Control a CEC 1986–1993+, Mission, Texas PEC 1987–1993+, Niles, Michigan; Otis, Massachusetts Aphids and Russian wheat aphid Diuraphis noxia (Mordvilko) SEC 1988–1993+, Mission, Texas; Bozeman, Montana Leafy spurge, Euphorbia esula L. Released four chrysomelid flea beetles, Aphthona cyparissiae SEC (Koch), A. flava Guillebeau, A. lacertosa Rosenheim, and A. nigriscutis Foudras; a cerambycid beetle, Oberea erythrocephala (Schrank); and a cecidomyiid midge, Spurgia esula Gagné. Localized but expanding economic and ecological success (Bangsund et al. 1999, Hansen et al. 1997). Releases of larval braconid parasite, Diachasmimorpha longicaudata (Ashmead), into citrus in northern Mexico for fly-free zones. Identified isolates of Bt active against adults. Released >159,000 predators, the coccinellid Chilocorus kuwanae (Silvestri) and the cybocephalid Cybocephalus nipponicus (Endrody-Younga) in 22 states, with high establishment rates. Impact of C. kuwanae in three New England states was a 69% reduction in heavily infested plants, and economic benefits of $436,000 per year (Van Driesche et al. 1998). Release of aphelinid nymphal parasites Eretmocerus spp. and Encarsia spp. and geocorid predator Geocoris punctipes (Say). Tested formulations of a pathogen, Beauvaria bassiana (Balsamo) Vuillemin, in the laboratory and field. PEC 1990–1993+, Mission, Texas 1991–1993, Niles, Michigan; Otis, Massachusetts Mexican fruit fly, Anastrepha ludens (Loew) Euonymus scale, Unaspis euonymi (Comstock) SEC 1991–1993+, Mission, Texas; Phoenix, Arizona 1991–1993+, Phoenix, Arizona a Sweetpotato whitefly, Bemisia tabaci (Gennadius) Rangeland grasshoppers SEC SEC CEC = complete economic control; SEC = substantial economic control; PEC = potential economic control. guard U.S. agriculture and the environment from harmful, invasive species; (7) establishing an interagency center for biological control at Florida A&M University; and (8) being responsive to its Customer Advisory Panel comprised of 16 individuals from federal and state governments, universities, and the private sector. The APHIS will continue to promote biological control as a means to manage exotic species. Conclusions/Summary In the late 1800s, the USDA began conducting research on the possibilities of managing arthropod and other pests of humans, animals, agriculture, and forests. The possibilities of regulating AMERICAN ENTOMOLOGIST • Volume 47, Number 1 populations of these pests have developed from the early descriptive work on the impact of parasites, predators, and pathogens. Over time, more intensive research has been conducted on methods to manipulate and control pest populations as well as natural enemies to obtain partial or complete control. Many other research organizations, both public and private, have instituted biological control programs either independently or in concert with the USDA. Early studies provided control of pests by importation and release of exotic natural enemies to control either introduced or endemic pests and led to the considerable success of the extensive basic and applied research being con45 ducted today by the USDA, universities, states, and the private sector. Research on predators, parasites, and pathogens now includes weeds and arthropod pests of crops, livestock, humans, forests, stored products, and aquatic environments. Hostnatural enemy interactions are now being studied at the behavioral and biochemical level. The USDA and other institutions are learning more about mass rearing and release systems, methods to apply beneficial organisms, and genetic manipulation of the organisms to make them more effective. Hopefully, through these technological advancements, the use of beneficial organisms will increase, become more economically feasible, and provide predictable controls for key pests of importance to the United States. Acknowledgments We thank the many USDA agencies and individuals who have contributed not only to this article but also to the publication of Coulson et al. (2000), which provides the in-depth history of the biological control programs in the USDA. The current article is based on this 645-page document. We also thank the various reviewers whose comments helped to improve the manuscript. We greatly appreciate the efforts of Libby Fouse and Darlene Hoffmann of the USDA-ARS Horticultural Crops Research Laboratory, Fresno, CA; Ms. Fouse for her editing and word processing of the many drafts of the manuscript, and Ms. Hoffmann who was instrumental in literature searches and obtaining photographs used in this publication. References Cited Abrahamson, L. P., and J. D. Harper. 1973. Microbial insecticides control forest tent caterpillars. USDA For. Serv. Res. Notes 30-157. Andres, L. A., and N. E. Rees. 1995. Musk thistle, pp. 248–251. In J. R. Nechols, L. A. Andres, J. W. Beardsley, R. D. 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Proceedings, Fourth International Colloquim on Insect Pathology, College Park, MD. Vail, P. V., D. L. Jay, and W. F. Hink. 1973. Replication and infectivity of the nuclear polyhedrosis virus of the alfalfa looper, Autographa californica, produced in cells grown in vitro. J. Invertebr. Pathol. 22: 231– 237. Vaughn, J. L., R. H. Goodwin, G. J. Tompkins, and P. McCawley. 1977. The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera: Noctuidae). In Vitro 13: 213–217. White, R. T., and S. R. Dutky. 1940. Effect of introduction of milky diseases on populations of Japanese beetle larvae. J. Econ. Entomol. 33: 306–309. White, J. M., P. G. Allen, L. J. Moffitt, and P. O. Kingsley. 1995. Economic analysis of an areawide program for biological control of the alfalfa weevil. Am. J. Altern. Agric. 10:173–179. Winget, C. H. 1985. CANUSA: beginning to end, pp. 7– 13. In C. J. Sanders, R. W. Stark, E. J. Mullins and J. Murphy [eds.], Recent advances in spruce budworms research. Proceedings, CANUSA Spruce Budworm Research Symosium, 16-20 September 1984, Bangor, ME. Can. For. Serv.; USDA For. Serv. Wu, F. 1993. An econometric approach for measuring the benefits and cost of the biological control of the cereal leaf beetle. M.S. thesis, University of Massachusetts, Amherst. Zuñiga, S. E. 1985. Ochenta años de control biologico en Chile. Agric. Tecnica (Chile) 45: 175–183. Patrick V. Vail is a research entomologist and Director of the USDA-ARS Horticultural Crops Research Laboratory, Fresno, California 93727. His main research interests are insect pathogens of stored product pests with emphasis on baculoviruses, microbial control, and integrated pest management of storage and quarantine pests. Jack R. Coulson is head of the USDA-ARS Biological Control Documentation Center of ARS’ National Program Staff, at Beltsville, Maryland 20705. His main interests are development of the ROBO database, a computerized system for tracking the importation and release of exotic invertebrate and microbial biological control agents into the United States, and maintenance of the historical files of the Documentation Center. William C. Kauffman is an entomologist and biological control specialist at the USDA-APHIS-PPQ Niles Plant Protection Center, Niles, Michigan 49120. His specialized training and expertise are in field techniques for evaluating insect and weed biocontrol agents, taxonomy of parasitic Hymenoptera, predatory arthropod behavior, host specificity of candidate agents in classical biological control, and invasion biology and pest risk assessment of exotic pest organisms. Mary Ellen Dix is a Forest Health Specialist and Entomologist on the Forest Health Protection Staff of the U.S. Forest Service, State and Private Forestry, Washington, DC 20090. She is the staff specialist for sustainability and accountability and coordinates the invasive species detection program. AMERICAN ENTOMOLOGIST • Volume 47, Number 1 49