Skip to main content
SpringerLink
Log in

Lessons From History: Predicting Successes and Risks of Intentional Introductions for Arthropod Biological Control

  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The introduction of nonnative biological control agents into a new region is one of the several approaches to managing the deleterious effects of nonnative invasive species. Predicting outcomes of such introductions has proven difficult. The US National Invasive Species Management Plan (2001) calls for better screening methods for intentional introductions, including nonnative biological control agents for animal pests. To address this challenge, I searched current and historical literature to develop a database of 13 life history traits and 8 descriptive variables for 87 nonnative insect biological control species in the continental United States. Models for predicting success in controlling a target species and likelihood of nontarget effects (documented cases of attacks on native hosts, prey, or natural enemies) were developed using logistic regression. The most important life history traits for predicting success included host specificity, whether the agent was a predator or parasitoid, and number of generations per year. There was no information about nontarget effects in 50 of 87 cases. Traits important for predicting nontarget effects included sex ratio of progeny and the documented presence of native natural enemies. This quantitative approach, derived from a meta-analysis of historical data, can be useful in developing guidelines for intentional introductions and predicting ecological outcomes of a broader range of nonnative species in new environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aliniazee MT and Hagen KS (1995) Walnut aphid–Part 1 walnut aphid Chromaphis juglandicola (Kaltenbach) Homoptera: Aphididae. In: Nechols JR, Andres LA, Beasley JW, Goeden RD and Jackson CG (eds) Biological Control in the Western United States. Accomplishments and Benefits of Regional Research Project W-84, 1964–1989, Publication 3361, pp 140–141. University of California, Division of Agriculture and Natural Resources

  • Anbuthnot KD (1950) Status of European corn borer parasites in the United States. Journal of Economic Entomology 43: 422–426

    Google Scholar 

  • Anderson RC and Paschke JD (1968) The biology and ecology of Anaphes flavipes (Hymenoptera: Mymaridae), an exotic egg parasite of the cereal leaf beetle. Annals of the Entomological Society of America 61: 1–5

    Google Scholar 

  • Anderson RC and Paschke JD (1969) Additional observations on the biology of Anaphes flavipes (Hymenoptera: Mymaridae), with special reference to the effects of temperature and super parasitism on development. Annals of the Entomological Society of America 62: 1316–1321

    Google Scholar 

  • Angalet GW and Fuester R (1977) The Aphidius parasites of the pea aphid Acyrthosiphon pisum in the eastern half of the United States. Annals of the Entomological Society of America 70: 87–96

    Google Scholar 

  • Arnaud Jr PH (1978) A host–parasite catalog of North American Tachinidae (Diptera). Science and Education Administration, United States Department of Agriculture, Miscellaneous Publication No. 1319, Washington, DC, 860 pp

  • Arthur AP and Juillet JA (1961) The introduced parasites of the European Pine Shoot Moth, Rhyacionia buoliana (Schiff.) (Lepidoptera: Olethreutidae), with a critical evaluation of their usefulness as control agents. The Canadian Entomologist 93: 297–312

    Google Scholar 

  • Barratt BIP, Evans AA, Ferguson CM, Barker GM, McNeill MR and Phillips CB (1997) Laboratory non target host range of the introduced parasitoids Microtonus aethiopoides and M.hyperodae (Hymenoptera: Braconidae) compared with field. parasitism in New Zealand. Environmental Entomology 26: 694–702

    Google Scholar 

  • Boettner GH, Elkington JS and Boettner CJ (2000) Effects of a biological control introduction on three non target native species of saturniid moths. Conservation Biology 14: 1798–1806

    Google Scholar 

  • Brown NR and Clark RC (1957) Studies of predators of the balsam woolly aphid, Adelges piceae (Ratz.) (Homoptera: Adel-gidae). IV. Neoleucopsis obscura (Hal.) (Diptera: Chamaemyi-idae), an introduced predator in eastern Canada. The Canadian Entomologist 89: 533–546

    Google Scholar 

  • Burger TL (1977) Aeulophid wasp (Tetrastichus julis) parasite of the cereal leaf beetle, Oulema melanopus. Animal and Plant Health Inspection Service, United States Department of Agriculture. Cooperative Plant Pest Report 2: 494–495

    Google Scholar 

  • Burgess AF and Crossman SS (1929) Imported insect enemies of the gipsy moth and the brown-tail moth. United States Department of Agriculture Technical Bulletin 86, 148 pp

  • Burrell RW (1931) Dexia ventralis Aldrich, an imported parasite of the Japanese beetle. Journal of Agricultural Research 43: 323–336

    Google Scholar 

  • Carruthers RI and Petroff JK (eds) (1997) Proceedings of the Invitational Workshop on USDA Activities in Biological Control; Riverdale, MD and Washington, DC, United States Department of Agriculture, Agricultural Research Service 1997–2001, Washington, DC, 109 pp

  • Clancy DW (1944) Biology of Allotropa burelli, a gregarious parasite of Pseudococcus comstocki. Journal of Agricultural Research 69: 159–163

    Google Scholar 

  • Clark RC and Brown NR (1958) Studies of the predators of the balsam woolly aphid, Adelges piceae (Ratz.) (Homoptera: Adel-gidae). V. Laricobius erichsonii Rosen. (Coleoptera: Derodon-tidae), an introduced predator in eastern Canada. The Canadian Entomologist 90: 657–672

    Google Scholar 

  • Clausen CP, King JL and Teranishi C (1927) The parasites of Popillia japonica in Japan and Chosen (Korea), and their introduction into the United States. United States Department of Agriculture Bulletin 1429, Washington, DC, 56 pp

  • Clausen CP (1956) Biological control of insect pests in the continental United States. United States Department of Agriculture Technical Bulletin No 1139, Washington, DC, 151 pp

  • Clausen CP (ed) (1978) Introduced parasites and predators of arthropod pests and weeds: a world review. United States Department ofAgriculture, Agricultural Research Service, Washington, DC, USA, 545 pp

  • Clinton WJ (1999) Executive Order 13112. Invasive Species. The White House, Washington, DC, 5 pp

  • Colunga-Garcia M and Gage SH (1998) Arrival, establishment, and habitat use of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in a Michigan landscape. Environmental Entomology 27: 1574–1580

    Google Scholar 

  • Compere H (1931) A Discussion of the Parasites of Saissetia oleae (Bern.) Collected in Eritrea,247–255. University of California Press, Berkeley 5, Vol 5

    Google Scholar 

  • Cory JS and Myers JH (2000) Direct and indirect ecological effects of biological control. Trends in Ecology & Evolution 15: 137–139

    Google Scholar 

  • Cottrell TE and Yeargan KV (1998) Intraguild predation between an introduced lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae), and a native lady beetle, Coleomegilla maculate (Coleoptera: Coccinellidae). Journal of Kansas Entomological Society 71: 159–163

    Google Scholar 

  • Coulson JR, Vail PV, Dix ME, Nordlund DA and Kauffman WC(eds) (2000) 110 Years of Biological Control Research and Development in United States Department of Agriculture: 1883–1993.United States Department of Agriculture, Agricultural Research Service, Beltsville, Maryland, 645 pp

    Google Scholar 

  • Crossman SS (1922) Apanteles melanoscelus, an imported parasite of the gipsy moth. United States Department of Agriculture Bulletin No. 1028, 25 pp

  • Daane KM, Barzman MS, Caltagirone LE and Hagen KS (2000) Metaphycus anneckei and Metaphycus hageni: two discrete species parasitic on black scale, Saissetia oleae. Bio Control 45: 269–284

    Google Scholar 

  • Daane KM and Caltagirone LE (1999) A new species of Meta-phycus (Hymenoptera: Encyrtidae) parasitic on Saissetia oleae (Olivier) (Homoptera: Coccidae). Pan Pacific Entomologist 75: 13–17

    Google Scholar 

  • Dean HA, Schuster MF, Boling JC and Riheid PT (1979) Complete biological control of Antonina graminis in Texas with Neodusmetia sangwani (a classic example). Bulletin of the Entomological Society of America 25: 262–267

    Google Scholar 

  • DeBach P, Rosen D and Kennett CE (1971) Biological control of coccids by introduced natural enemies. In: Huffaker CB (ed) Biological Control. Proceedings of an AAASSymposium on Biological Control, held at Boston, Massachusetts 1969, 191–192. Plenum Press, New York

    Google Scholar 

  • Delucchi V (1954) Pullus impexus Muls. (Coleoptera: Coccinellidae), a predator of Adelges piceae (Ratz.) (Hemiptera, Adelgidae), with notes on its parasites. Bulletin of Entomological Research 45: 243–278

    Google Scholar 

  • Doane CC and Schaefer PW (1971) Field observations on the flight activity of Calosoma sycophanta (Coleoptera: Carabidae). Annals of the Entomological Society of America 64: 528

    Google Scholar 

  • Domenichini G (1966) Hymenoptera Eulophidae Palearctic Tetrastichinae. In: Delucchi V and Remaudiere G (eds) Index of Entomophagous Insects, 101. International Organization of Biological Control, Paris, France

    Google Scholar 

  • Dowden PB (1934) Recently introduced parasites of three important forest insects. Annals of the Entomological Society of America 37: 599–603

    Google Scholar 

  • Dowden PB (1935) Brachymeria intermedia (Nees), a primary parasite, and B. icompsilura (Cwfd.), a secondary parasite, of the gypsy moth Porthetria dispar L. Journal of Agricultural Research 50: 495–523

    Google Scholar 

  • Dowden PB (1962) Parasites and predators of forest insects liberated in the United States through 1960. United States Department of Agriculture Agricultural Handbook 226, Washington, DC, 70 pp

  • Drea Jr JJ and Hendrickson Jr RM (1986) Analysis of a successful classical biological control project: the alfalfa blotch leaf miner (Diptera: Agromyzidae) in the northeastern United States. Environmental Entomology 15: 448–455

    Google Scholar 

  • Drooz AT (1975) Mesoleius tenthredinis and other parasites of the larch sawfly in the eastern United States. Environmental Entomology 4: 645–650

    Google Scholar 

  • Drooz AT, Quimby JW, Thompson LC and Kulman HM (1985) Introduction and establishment of Olesicampe benefactor Hinz (Hymenoptera: Ichneumonidae), a parasite of the larch sawfly, Pristiphora erichsonii (Hartig) (Hymenoptera: Tenthredinidae), in Pennsylvania. Environmental Entomology 14: 420–423

    Google Scholar 

  • Drost YC and Carde CR (1992) Host switching in Brachymeria intermedia. Environmental Entomology 21: 760–766.

    Google Scholar 

  • Dyer LE and Landis DA (1997) Diurnal behavior of Eriborus terebrans (Hymenoptera: Ichneumonidae). Environmental Entomology 26: 1385–1392

    Google Scholar 

  • Ehler LE (1999) Critical issues related to non target effects in classical biological control of insects. In: Follett PA and Duan JJ (eds) Nontarget Effects of Biological Control, 3–13. Kluwer Academic Publishers, Boston, Massachusetts

    Google Scholar 

  • Elliott N, Kleickhefer R and Kauffman W (1996) Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia 105: 537–554

    Google Scholar 

  • Etzel LK, Hagen KS, Gonz' alez D and Ellington JJ (1995) Egyptian alfalfa weevil Hypera brunneipennis (Boheman) Coleoptera: Cur-culionidae. In: Nechols JR, Andres LA, Beasley JW, Goeden RD and Jackson CG (eds) Biological Control in the Western United States. Accomplishments and Benefits of Regional Research Project W-84, 1964–1989, pp 176–179. University of California, Division of Agriculture and Natural Resources, Publication 3361

  • Flanders SE (1944) Observations on Comperiella bifasciata, an endoparasite of Diaspine coccids. Annals of the Entomological Society of America 37: 365–371

    Google Scholar 

  • Flanders SE (1952) Biological observations on the parasites of the black scale. Annals of the Entomological Society of America 45: 543–549

    Google Scholar 

  • Flint ML (1980) Climatic ecotypes in Trioxys complanatus, a parasite of the spotted alfalfa aphid. Environmental Entomology 9: 501–507

    Google Scholar 

  • Frazer BD and Van den Bosch R (1973) Biological control of the walnut aphid in California: the interrelationship of the aphid and its parasite. Environmental Entomology 2: 561–568

    Google Scholar 

  • Gilstrap FE (1997) Importation biological control in ephemeral crop habitats. Biological Control 10: 23–29

    Google Scholar 

  • Godwin PA and Odell TM (1977) Alternate hosts of Blepharipa pratensis (Meigen). Northeastern Forest Experiment Station, Forest Service Research Note NE-245, 3 pp

  • Gould JR, Elkinton JS and Wallner WE (1990) Density-dependent suppression of experimentally created gypsy moth, Lyman-triadispar (Lepidoptera: Lymantriidae), populations by natural enemies. Journal of Animal Ecology 59: 213–233

    Google Scholar 

  • Gould JR, Elkinton JS and Odell TM (1992) Superparasitism of gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantri-idae), larvae by Parasetigena silvestris (Robineau-Desvoidy) (Diptera: Tachinidae). The Canadian Entomologist 124: 425–436

    Google Scholar 

  • Grinberg PS and Wallner WE (1991) Long-term laboratory evaluations of Rogas lymantriae: a braconid endoparasite of the gypsy moth, Lymantria dispar. Entomophaga 36: 205–212

    Google Scholar 

  • Hafez M and Doutt RL (1954) Biological evidence of sibling species in Aphytis maculicornis (Masi), (Hymenoptera, Aphelinidae). The Canadian Entomologist 86: 90–96

    Google Scholar 

  • Hagen KS (1962) Biology and ecology of predaceous Coccinellidae. Annual Review of Entomology 7: 289–326

    Google Scholar 

  • Hall RW and Ehler LE (1979) Rate of establishment of natural enemies in classical biological control. ESA Bulletin 25: 280–282

    Google Scholar 

  • Hawkins BA and Marino PC (1997) The colonization of native phytophagous insects in North America by exotic parasitoids. Oecologia 112: 566–571

    Google Scholar 

  • Heinz KM (1996) Host size selection and sex allocation behaviour among parasitoid trophic levels. Ecological Entomology 21: 218–226

    Google Scholar 

  • Hendrickson Jr RM and Plummer JA (1983) Biological control of alfalfa blotch leafminer (Diptera: Agromyzidae) in Delaware. Journal of Economic Entomology 76: 757–761

    Google Scholar 

  • Howard LO and Fiske WF (1911) The importation into the United States of the parasites of the gipsy moth and the brown-tail moth: a report of progress, with some consideration of previous and concurrent efforts of this kind. United States Department of Agriculture, Bureau of Entomology Bulletin 91, Washington, DC, 344 pp

  • Hoy MA (1976) Establishment of gypsy moth parasitoids in North America: an evaluation of possible reasons for establishment and non-establishment. In: Anderson JF and Kaya HK (eds) Perspectives in Forest Entomology, 215–232. Academic Press, New York

    Google Scholar 

  • Huber DM, Hugh-Jones ME, Rust MK, Sheffield SR, Simberloff D and Taylor CR (2002) Invasive pest species: impacts on agricultural production, natural resources, and the environment. Council for Agricultural Science and Technology, Issue Paper 20: 1–18

    Google Scholar 

  • Huffaker CB (ed) (1969) Biological Control. Plenum Press, New York, 511 pp

    Google Scholar 

  • Huffaker CB and Kennett CE (1966) IV. Biological control of Parlatoria oleae (Colvèe) through compensatory action of two introduced parasites. Hilgardia 37: 283–335

    Google Scholar 

  • Huffaker CB, Kennett CE and Finney GL (1962) Biological control of olive scale, Parlatoria oleae (Colvèe), in California by imported Aphytis maculicornis (Masi) (Hymenoptera: Aphelin-idae). Hilgardia 32: 541–636

    Google Scholar 

  • Huffaker CB, Kennett CE and Tassan RL (1994) The biological control of olive scale, Parlatoria oleae (Colvèe) by two aphelinid parasites. In: Rosen D (ed) Advances in the Study of Aphytis, 95–104. Intercept, Andover, UK

    Google Scholar 

  • Huffaker CB, Luck RF and Messenger PS (1977) The ecological basis of biological control. In: Packer JS and White D (eds) Proceedings of XV International Congress of Entomology, 1976, 560–586. The Entomological Society of America, College

  • Park, Maryland Ismail AB and Long GE (1982) Interactions among parasites of the larch casebearer (Lepidoptera: Coleophoridae) in northern Idaho. Environmental Entomology 11: 1242–1247

    Google Scholar 

  • Kennedy BH (1970) Dendrosoter protuberans (Hymenoptera: Braconidae), an introduced larval parasite of Scolytus multistriatus. Annals of the Entomological Society of America 63: 351–358

    Google Scholar 

  • Kennett CE, Huffaker CB and Finney GL (1966) III. The role of an autoparasite aphelinid, Coccophagoides utilis Doutt, in the control of Parlatoria oleae (Colvèe) through compensatory action of two introduced parasites. Hilgardia 37: 255–282

    Google Scholar 

  • Kim KC (1991) North American Non-Indigenous Arthropod Database. United States Department of Agriculture–Animal and Plant Health Inspection Service, http://www.invasivespecies.org/NANIAD.html

  • Kimberling DN, Miller JC and Penrose RL (1986) Distribution and parasitism of winter moth, Operophtera brumata (Lepidoptera: Geometridae), in western Oregon. Environmental Entomology 15: 1042–1046

    Google Scholar 

  • King BH (1987) Offspring sex ratios in parasitoid wasps. The Quarterly Review of Biology 62: 367–396

    Google Scholar 

  • Kolar CS and Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends in Ecology & Evolution 16: 199–204

    Google Scholar 

  • Krause SC, Fuester RW and Burbutis PB (1990) Competitive interactions between Cotesia melanoscelus and Glyptapanteles. flavicoxis (Hymenoptera: Braconidae): implications for biological control of the gypsy moth (Lepidoptera: Lymantriidae). Environmental Entomology19: 1543–1546

    Google Scholar 

  • Krombein KV, Hurd Jr PD, Smith DR and Burks BD (1979) Catalog of Hymenoptera in America north of Mexico. Volume 1. Symphyta and Apocrita (Parasitica). Smithsonian Institute Press, Washington, DC, 1198 pp

    Google Scholar 

  • Leppla NC and Delfosse ES (1995) The increasing significance of biological control and an overview of regulations governing biological control organisms. In: Fosbroke LC and Gottschalk KW (eds) Proceedings USDA Interagency Gypsy Moth Research Forum, 9–19. United States Forest Service, NE Forest Experiment Station General Technical Report NE-213, Delaware, Ohio

  • Liebhold AM and Elkinton JS (1989) Elevated parasitism in artificially augmented populations of Lymantria dispar (Lepidoptera: Lymantriidae). Environmental Entomology 18: 986–995

    Google Scholar 

  • Louda SM, Kendall D, Connor J and Simberloff D (1997) Ecological effects of an insect introduced for the biological control of weeds. Science 277: 1088–1090

    Google Scholar 

  • Louda SM, Pemberton RW, Johnson MT and Follett PA (2003) Nontarget effects–the Achilles' heel of biological control? Retrospective analyses to reduce risk associated with bio control introductions. Annual Review of Entomology 48: 365–396

    Google Scholar 

  • Luck RF (1986) Biological control of California red scale: case study. Ecological Knowledge and Environmental Problem-Solving. Concepts and Case Studies, 165–189. Board on Basic Biology, Commission on Life Sciences, National Research Council, National Academy Press, Washington, DC

    Google Scholar 

  • Luck RF (1995) California red scale Aonidiella aurantii (Maskell) Homoptera: Diaspididae. In: Nechols JR, Andres LA, Beasley JW, Goeden RD and Jackson CG (eds) Biological Control in the Western United States. Accomplishments and Benefits of Regional Research Project W-84, 1964–1989, 155–157. University of California, Division of Agriculture and Natural Resources, Publication 3361

  • Madden B (1996) Federal regulations impacting ARS biological control programs. Environmental Protection Agency, Office of Pesticides Programs. Report for Agricultural Research Service (unpublished), National Agricultural Library, Beltsville, Maryland

  • MathSoft (1999) S-Plus 2000 statistical software. Data analysis products division, MathSoft, Incorported, Seattle, Washington

    Google Scholar 

  • McEvoy PB and Coombs EM (1999) Biological control of plant invaders: regional patterns, field experiments, and structured population models. Ecological Applications 9: 387–401

    Google Scholar 

  • McFadyen REC (1998) Biological control of weeds. Annual Review of Entomology 43: 369–393

    Google Scholar 

  • Mohamed MA and Coppel HC (1986) Sex ratio regulation in Brachymeria intermedia, a pupal gypsy moth parasitoid. Canadian Journal of Zoology 64: 1412–1415

    Google Scholar 

  • Muesebeck CFW (1918) Two important introduced parasites of the browntail moth. Journal of Agricultural Research 14: 191–206

    Google Scholar 

  • Muesebeck CFW (1931) Monodontomerus aereus Walker, both a primary and a secondary parasite of the brown-tail moth and the gipsy moth. Journal of Agricultural Research 43: 445–460

    Google Scholar 

  • Muesebeck CFW and Parker DL (1933) Hyposoter disparis Viereck, an introduced ichneumonid parasite of the gipsy moth. Journal of Agricultural Research 46: 335–347

    Google Scholar 

  • National Management Plan: Meeting the Invasive Species Challenge (2001) National Invasive Species Council, Washington, DC, 74 pp

  • National Plant Board (1999) Safeguarding American plant resources (a stakeholder review of the APHIS-PPQ safeguarding system). Conducted by the National Plant Board at the request of the United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant, Protection, and Quarantine, Washington, DC, 173 pp

    Google Scholar 

  • Obrycki JJ, Giles KL and Ormord AM (1998) Interactions between an introduced and indigenous coccinellid species at different prey densities. Oecologia 117: 279–285

    Google Scholar 

  • Obrycki JJ, Elliott NC and Giles KL (1999) Coccinellid introductions: potential for and evaluation of nontarget effects. In: Follett PA and Duan JJ (eds) Nontarget Effects of Biological Control, 127–145. Kluwer Academic Publishers, Boston, Massachusetts

    Google Scholar 

  • Odell TM and Godwin PA (1979) Attack behavior of Parasetigena silvestris in relation to the gypsy moth, Lymantria dispar host density and behavior on Pinus sylvestris in Connecticut. Annals of the Entomological Society of America 72: 281–286

    Google Scholar 

  • Parker HL (1931) Macrocentrus gifuensis Ashmead, a polyembryonic braconid parasite in the European corn borer. United States Department of Agriculture Technical Bulletin 230, 63 pp

  • Peairs FB and Lilly JH (1975) Parasites reared from larvae of the European corn borer, Ostrinia nubilalis (Hbn.), in Massachusetts, 1971–1973 (Lepidoptera: Pyralidae). Journal of New York Entomological Society 83: 36–37

    Google Scholar 

  • Peterson EJ and Firko MJ (preparers) Environmental Assessment (1994) Field release of a nonindigenous predatory beetle (Calo-soma sycophanta) for biological control of gypsy moth. United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine (PPQ), Biological Assessment and Taxonomic Support, Riverdale, Maryland, 18 pp

  • Pimentel D, Lach L, Zuniga Rand Morrison D(2000) Environmental and economic costs of nonindigenous species in the United States. BioScience 50: 53–65

    Google Scholar 

  • Plant Protection Act (2000) Title IV of Public Law 106–224, 114 Stat. 438, 7 U.S.C. 7701-7772. Washington, DC, 20 pp

  • Pratt PD, Coombs EM and Croft BA (2003) Predation by phy-toseiid mites on Tetranychus lintearius (Acari: Tetranychidae), an established weed biological agent of gorse (Ulex europaeus). Biological Control 26: 40–47

    Google Scholar 

  • Price PW (1980) Evolutionary Biology of Parasites. Princeton University Press, Princeton, New Jersey, 237 pp

  • Pschorn-Walcher H and Zinnert KD (1971) Investigations on the ecology and natural control of the larch sawfly (Pristiphora erich-onii Htg.) (Hym.: Tenthredinidae) in central Europe. Part II. Natural enemies: their biology and ecology, and their role as mortality factors in P. erichsonii. Commonwealth institute of biological control, CAB (Commonwealth Agricultural Bureaux) Technical Bulletin 14: 1–50

    Google Scholar 

  • Quednau FW (1967) Notes on mating behavior and oviposition of Chrysocharis laricinellae (Hymenoptera: Eulophidae), a parasite of the larch casebearer (Coleophora laricella). The Canadian Entomologist 99: 326–331

    Google Scholar 

  • Reardon RC, Statler MW and McLane WH (1973) Rearing techniques and biology of five gypsy moth parasites. Environmental Entomology 2: 124–127.

    Google Scholar 

  • Reichard SH and Hamilton CW (1997) Predicting invasions of woody plants introduced into North America. Conservation Biology 11: 193–203

    Google Scholar 

  • Ruesink JL, Parker IM, Groom MJ and Kareiva PM(1995) Reducing the risks of nonindigenous species introductions. BioScience 45: 465–477

    Google Scholar 

  • Ryan RB (1997) Before and after evaluation of biological control of the larch casebearer (Lepidoptera: Coleophoridae) in the Blue Mountains of Oregon and Washington. Environmental Entomology 26: 703–715

    Google Scholar 

  • Salt G(1931) Parasites of the wheat-stem sawfly, Cepheus pygmaeus, Linnaeus, in England. Bulletin of Entomological Research 22:479–545

    Google Scholar 

  • SAS (1999) SAS 8.1 SAS Institute Inc., Cary, North Carolina

    Google Scholar 

  • Schaffner Jr JV (1934) Introduced parasites of the brown-tail and gipsy moths reared from native hosts. Annals of the Entomological Society of America 27: 585–592

    Google Scholar 

  • Schlinger EI and Hall JC (1959) A synopsis of the biologies of three imported parasites of the spotted alfalfa aphid. Journal of Economic Entomology 52: 154–157

    Google Scholar 

  • Schlinger EI and Hall JC (1960) The biology, behavior and morphology of Praon palitans Muesebeck, an internal parasite of the spotted alfalfa aphid, Therioaphis maculata (Buckton) (Hymenoptera: Braconidae, Aphidiinae). Annals of the Entomological Society of America 53: 144–160

    Google Scholar 

  • Schlinger EI and Hall JC (1961) The biology, behavior, and morphology of Trioxys (Trioxys) utilis, an internal parasite of the spotted alfalfa aphid, Therioaphis maculata (Hymenoptera: Braconidae, Aphidiinae). Annals of the Entomological Society of America 54: 34–45

    Google Scholar 

  • Schopf A (1991) The effect of host age of Lymantria dispar larvae (Lepidoptera: Lymantriidae) on the development of Glypanteles liparidis (Hym.: Braconidae). Entomophaga 36: 593–604

    Google Scholar 

  • Schuster MF (1965) Studies on the biology of Dusmetia sangwani (Hymenoptera: Encyrtidae). Annals of the Entomological Society of America 58: 272–275

    Google Scholar 

  • Schuster MF and Dean HA (1976) Competitive displacement of Anagyrus antoninae (Hymenoptera: Encyrtidae), by its ecological homologue Neodusmetia sangwani. Entomophaga 21: 127–130

    Google Scholar 

  • Simberloff D and Stiling P (1996) How risky is biological control? Ecology 77: 1965–1974

    Google Scholar 

  • Smith BC (1958) Development, feeding habits, and predator–prey relations of insect predators of the balsam woolly aphid, Adelges piceae (Ratz.) (Homoptera: Adelgidae), recently introduced into Canada. The Canadian Entomologist 90: 441–449

    Google Scholar 

  • Smith HD, Maltby HL and Jimenez EJ (1964) Biological control of citrus blackfly in Mexico. United States Department of Agriculture, Agricultural Research Service Technical Bulletin 1311: 1–30

    Google Scholar 

  • Smith HS and Compere H (1928) A Preliminary Report on the Insect Parasites of the Black Scale, Saisssetia oleae (Bernard) 231–334. University of California Press, Berkeley, Vol 4

    Google Scholar 

  • Stehr FW (1970) Establishment in the United States of Tetrastichus julis, a larval parasite of the cereal leaf beetle. Journal of Economic Entomology 63: 1968–1969

    Google Scholar 

  • Stehr FW, Gage PS, Burger TL and Montgomery VE (1974) Establishment in the United States of Lemophagus curtus, a larval parasitoid of the cereal leaf beetle. Environmental Entomology 3: 453–454

    Google Scholar 

  • Steinberg S, Podoler Hand Rosen D(1994) r and K strategies in parasitoids of diaspidid scale insects: Aphytis versus endoparasitoids. In: Rosen D(ed) Advances in the Study of Aphytis (Hymenoptera: Aphelinidae), pp 79–91. Intercept Limited, Andover, UK

    Google Scholar 

  • Stiling P (1990) Calculating the establishment rates of parasitoids in classical biological control. American Entomologist 36: 225–230

    Google Scholar 

  • Strand MR and Obrycki JJ (1996) Host specificity of insect parasitoids and predators. BioScience 46: 422–429

    Google Scholar 

  • Streams FA and Fuester RW (1967) Biology and distribution of Tetrastichus incertus, a parasite of the alfalfa weevil. Journal of Economic Entomology 60: 1574–1579

    Google Scholar 

  • Strong DR and Pemberton RW (2000) Biological control of invading species–risk and reform. Science 288: 1969–1970

    Google Scholar 

  • Syme PD (1977) Observations on the longevity and fecundity of Orgilus obscurator (Hymenoptera: Braconidae) and the effects of certain foods on longevity. The Canadian Entomologist 109: 995–1000

    Google Scholar 

  • Thomas MB and Willis AJ (1998) Biocontrol–risky but necessary? Trends in Ecology & Evolution 13: 325–329

    Google Scholar 

  • Thorpe WH (1933) Notes on the natural control of Coleophora lari-cella, the larch case-bearer. Bulletin of Entomological Research 24: 271–291

    Google Scholar 

  • US Congress, Office of Technology Assessment (1993) Harmful non-indigenous species in the United States OTA-F-565. United States Government Printing Office, Washington, DC, 391 pp

    Google Scholar 

  • US Congress, Office of Technology Assessment (1995) Biologically based technologies for pest control. OTA-ENV-636. United States Government Printing Office, Washington, DC, 204 pp

    Google Scholar 

  • United States Department of Agriculture (USDA) Forest Service, Northeastern Area State and Private Forestry, Forest Health Protection(1996) Hemlock Woolly Adelgid Newsletter, issue 4, 10 pp

  • United States Department of Agriculture (USDA), Agricultural Research Service. Biological Control Documentation Center. Releases of Beneficial Organisms (ROBO). Beltsville, Maryland, http://www.ars-grin.gov/nigrp/robo.html

  • Vail PV, Coulson JR, Kauffman WC and Dix ME (2001) History of biological control programs in the United States Department of Agriculture. American Entomologist 47: 24–50

    Google Scholar 

  • Vance AM (1932) The biology and morphology of the braconid Chelonus annulipes Wesm., a parasite of the European corn borer. United States Department of Agriculture Technical Bulletin 294, 49 pp

  • Van den Bosch R and Schlinger EI (1962) Initial field observations in California on Trioxys pallidus (Haliday), a recently introduced parasite of the walnut aphid. Journal of Economic Entomology 55: 857–862

    Google Scholar 

  • Van den Bosch R, Hom R, Matteson P, Frazer BD, Messenger PS and Davis CS (1979) Biological control of the walnut aphid Chromaphis juglandicola in California: impact of the parasite, Trioxys pallidus. Hilgardia 47: 1–13

    Google Scholar 

  • Waage JK (2001) Indirect ecological effects in biological control: the challenge and the opportunity. In: Wajnberg E, Scott JK and Quimby PC (eds) Evaluating Indirect Ecological Effects of Biological Control, pp 1–12. CAB International, New York.

  • Waage JK and Hassell MP (1982) Parasitoids as biological control agents–a fundamental approach. Parasitology 84: 241–268

    Google Scholar 

  • Walker MG (1940) Notes on the distribution of Cephus pygmaeus, inn., and of its parasite, Collyria calcitrator, Grav. Bulletin of Entomological Research 30: 551–573

    Google Scholar 

  • Wallner WE and Grinberg PS (1984) Suitability of the white-marked tussock moth (Lepidoptera: Lymantriidae) as an alternate host for the imported gypsy moth (Lepidoptera: Lymantriidae) parasite, Rogas lymantriae Watanabe (Hymenoptera: Braconidae). Environmental Entomology 13: 986–989

    Google Scholar 

  • Wellso SG (1982) Cereal leaf beetle under control. Biological control by wasps. Crops and Soils Magazine 34: 7–9

    Google Scholar 

  • Weseloh RM (1976) Reduced effectiveness of the gypsy moth parasite, Apanteles melanoscelus, in Connecticut due to poor seasonal synchronization with its host. Environmental Entomology 5: 743–746

    Google Scholar 

  • Weseloh RM (1985) Predation by Calosoma sycophanta L. (Coleoptera: Carabidae): evidence for a large impact on gypsy moth, Lymantria dispar L. (Lepidoptera: Lymantriidae), pupae. The Canadian Entomologist 117: 1117–1126

    Google Scholar 

  • Weseloh RM(1990) Experimental forest releases of Calosoma sycophanta (Coleoptera: Carabidae) against the gypsy moth. Journal of Economic Entomology 83: 2229–2234

    Google Scholar 

  • Wheeler Jr AG and Hoebeke ER (1995) Coccinella novemnotata in northeastern North America: historical occurrence and current status (Coleoptera: Coccinellidae). Proceedings of the Entomological Society of Washington 97: 701–716

    Google Scholar 

  • Williams DW, Fuester RW, Metterhouse WW, Balaam RJ, Bullock RH, Chianese RJ and Reardon RC (1993) Incidence and ecological relationships of pupal parasitism by Brachymeria intermedia in New Jersey populations of the gypsy moth. Entomophaga 38: 257–266

    Google Scholar 

  • Williamson MH (1996) Biological Invasions. Chapman & Hall, London, 244 pp

  • Williamson MH and Fitter A (1996) The characters of successful invaders. Biological Conservation 78: 163–170

    Google Scholar 

  • Wilson F (1938) Notes on the insect enemies of Chermes with particular reference to Pineus pini Koch, and P. tistrobi, Hartig. Bulletin of Entomological Research 29: 373–389

    Google Scholar 

  • Winnie WV and Chiang HC (1982) Seasonal history of Macro-centrus grandii (Hymenoptera: Braconidae) and Eriborus tere-brans (Hymenoptera: Ichneumonidae), two parasitoids of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae). Entomophaga 27: 183–188

    Google Scholar 

  • Wolfenbarger LL and Phifer PR (2000) The ecological risks and benefits of genetically engineered plants. Science 290: 2088–2093

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Forest Science, Oregon State University, 321 Richardson Hall, Corvallis, OR, 97331-5752, USA

    Diana N. Kimberling

Authors
  1. Diana N. Kimberling
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kimberling, D.N. Lessons From History: Predicting Successes and Risks of Intentional Introductions for Arthropod Biological Control. Biological Invasions 6, 301–318 (2004). https://doi.org/10.1023/B:BINV.0000034599.09281.58

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:BINV.0000034599.09281.58

Search

Navigation