Skip to main content
Log in

History and Future of Introduction of Exotic Arthropod Biological Control Agents in Spain: A Dilemma?

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The first documented introduction of an exotic invertebrate biological control agent (IBCA) in Spain occurred in 1908. Sixty-four additional species have been introduced since then. Information, both previously recorded and original data, on the species introduced for pest control is summarized. Most of the introduced IBCAs focused on citrus pests and homopterans clearly predominate among target phytophagous species. Success has been more frequent for IBCAs used in seasonal inoculative strategies (50.0% of cases) than in classical biological control programs (17.1% of cases). Concerns about potential non-target effects of such species are increasing, but post-release evaluation has often been insufficient to draw any conclusions about them. Most of the beneficial species introduced in Spain were parasitoids (n = 53), and the remaining species were predators (n = 12). Only four parasitoids are considered specialized monophagous natural enemies. The mean number of host species parasitized by parasitoids is 15.2, whereas the mean number of prey species attacked by predators is 21.2. Therefore, polyphagy appears to be quite common among the IBCAs that have been introduced in Spain. The rationale guiding many of these introductions in the past would not be acceptable nowadays. Since classical biological control is such a valuable strategy for pest control, straightforward protocols to evaluate exotic candidate species are urgently needed.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • J.R. Ables D.W. McCommas SuffixJr. (1982) ArticleTitleEfficacy of Podisus maculiventris as a predator of Ascogaster quadridentata on greenhouse cotton J. Ga. Entomol. Soc. 17 204–206

    Google Scholar 

  • Agustí, M. 1999. Citricultura. Mundi-Prensa, Madrid.

  • R. Albajes (2005) Control biològic: del control clàssic a la conservació J. Jacas P. Caballero J. Avilla (Eds) El control biológico de plagas y enfermedades Universitat Jaume I/Universidad Pública de Navarra Castelló, ES 31–47

    Google Scholar 

  • R. Albajes M.J. Sarasúa J. Avilla J. Arnó R. Gabarra (2003) Integrated pest management in the Mediterranean region: the case of Catalonia, Spain K.M. Maredia D. Dakouo D. Mota-Sánchez (Eds) Integrated Pest Management in the Global Arena CABI Publishing Trowbridge, UK 241–355

    Google Scholar 

  • Anonymous, 1923. Lucha biológica contra los parásitos de las plantas. Rev. Inst. Agric. Catalan S. Isidro LXXII 11: 226.

  • Y. Argov Y. Rössler (1996) ArticleTitleIntroduction, release and recovery of several exotic natural enemies for biological control of citrus leafminer, Phyllocnistis citrella, in Israel Phytoparasitica 24 33–38

    Google Scholar 

  • G.W. Barber (1936) ArticleTitleOrius insidiosus (Say.), an important natural enemy of corn earworm USDA. Tech. Bull. 504 24

    Google Scholar 

  • P. Barbosa S.M. Braxton A.E. Segarra-Carmona (1994) ArticleTitleA history of biological control in Maryland Biol. Control 4 185–243 Occurrence Handle10.1006/bcon.1994.1029

    Article  Google Scholar 

  • P. Barbosa A.E. Segarra-Carmona (1993) Criteria for the selection of pest arthropod species as candidates for biological control R.G. Driesche ParticleVan T.S. Bellows SuffixJr. (Eds) Steps in classical arthropod biological control Proc. Thomas Say Publications in Entomology ESA, Lanham, USA 5–23

    Google Scholar 

  • Beckwith, R.C. 2004. Forest pest leaflet 139. The Large Aspen Tortrix. http://www.fs.fed.us/r10/spf/fhp/leaflets/Fidl139.htm (24/05/04).

  • E.H. Beers J.F. Brunner M.J. Willett G.M. Warner (1993) Orchard pest management: a resource book for the Pacific North West Good fruit grower Yakima, USA

    Google Scholar 

  • M. Begon J.L. Harper C.R. Townsend (1990) Ecology. Individuals Populations and Communities EditionNumber2 Blackwell Science Taunton, MA, USA

    Google Scholar 

  • M.R. Berenbaum (1994) Bugs in the System. Insects and Their Impact on Human Affairs Helix Books. Adison-Wesley Publishing Company USA

    Google Scholar 

  • BOE [Boletín Oficial Del Estado]. 2004. Ley 43/2002 de 20 de Noviembre, de Sanidad Vegetal. BOE 21-11-02.

  • Boller, E.F., J. Avilla, E. Joerg, C. Malavolta, F.J. Wijnands and P. Esbjerg, 2004. Guidelines for integrated production. Principals and technical guidelines. 3rd ed. 2004. IOBC WPRS Bull./Bull. OILB SROP 27.

  • E.Z. Bouček R.R. Askew (1968) Hymenoptera, Chalcidoidea, Palearctic Eulophidae (Excl Tetrastichinae). Index of entomophagous insects Le François Paris, FR

    Google Scholar 

  • H.W. Browning (1994) Early classical biological control in citrus D. Rosen F.D. Bennett J.L. Capinera (Eds) Pest management in the subtropics. Biological control-a Florida perspective Intercept Andover, UK 123–128

    Google Scholar 

  • M. Carber P.A. Inkerman N.J. Ashbolt (1987) ArticleTitleAnagyrus saccharicola Timberlake (Hymenoptera: Encyrtidae) another biota associated with Saccharicoccus sacchari (Cockerell) (Homoptera: Pseudoccidae) in Australia J. Aust. Entomol. Soc. 26 367–368

    Google Scholar 

  • M. Casadevall E. Bordas R. Albajes (1979) ArticleTitleLa mosca blanca de los invernaderos, Trialeurodes vaporariorum, en el Maresme I. Estudios preliminares de control integrado en tomate An. INIA. Ser. Prot. Veg. 1 45–46

    Google Scholar 

  • C.E. Causton M.P. Lincango T.G.A. Poulsom (2004) ArticleTitleFeeding range studies of Rodolia cardinalis (Mulsant), a candidate biological control agent of Icerya purchasi in the Galápagos Islands Biol. Control 29 315–325 Occurrence Handle10.1016/j.biocontrol.2003.07.002

    Article  Google Scholar 

  • Charles, J.G. and D.J. Allan, 2002. An ecological perspective to host-specificitytesting of biocontrol agents. http://www.hortnet.co.nz/publications/nzpps/proceedings/02/02_037.pdf (25/10/04).

  • Charleston, D.S., R. Kfir, N.J. Rensburg van, B.N. Barnes, V. Hatting, D.E. Conlong, D. Visser and G.J. Prinsloo . Integrated Pest management in South Africa. In: K.M. Maredia, D. Dakouo and D. Mota-Sánchez (eds), Integrated Pest Management in the Global Arena. CABI Publishing, Trowbridge, UK. pp. 169–195.

  • M. Civantos (1997) Control de plagas y enfermedades del olivar Consejo Oleícola Interbacional Madrid, ES

    Google Scholar 

  • Cohen, I. 1975. From biological to integrated control of citrus pests in Israel. pp. 38–41. In: Citrus. Ciba-Geigy Ltd. Technical monograph No. 4. Basle, CH.

  • M.J.W. Copland H.A.S. Perera M. Heidary (1993) ArticleTitleInfluence of host plant on the biocontrol of glasshouse mealybug Bull. OILB/SROP 16 44–47

    Google Scholar 

  • Coulson J.R. 1992. Releases of beneficial organisms in the United States and territories-1982. U.S. Dept. Agric. Misc. Pub. 1505.

  • Coulson J.R., A. Carrel and D.L. Vincent, 1988. Releases of beneficial organisms in the United States and territories-1981. U.S. Dept. Agric. Misc. Pub. 1464.

  • V. Danon (1989) ArticleTitleBiological control of the European corn borer, Ostrinia nubilalis (Hübner), by Trichogramma pretiosum Riley Zast. Bilja 40 131–140

    Google Scholar 

  • F.F. Dicke J.L. Jarvis (1962) ArticleTitleThe habits and seasonal abundance of Orius insidiosus (Say.) (Hemiptera-Heteroptera: Anthocoridae) on corn J. Kan. Entomol. Soc. 35 339–344

    Google Scholar 

  • J. Eigelberg H. Hayek C. Lomer (2001) ArticleTitleSuggestions for unifying the terminology in biological control BioControl 46 387–400

    Google Scholar 

  • EPPO [European and Mediterranean Plant Protection Organization], 1999. EPPO Standards: Safe use of biological control. PM 6/1 (1): First import of exotic biological control agents for research under contained conditions. OEPP/EPPO, Paris, FR.

  • EPPO, 2000. EPPO Standards: Safe use of biological control. PM 6/2 (1): Import and release of exotic biological control agents. OEPP/EPPO, Paris, FR.

  • EPPO, 2004. http://www.eppo.org/QUARANTINE/biocontrol (16/9/04).

  • InstitutionalAuthorNameFAO [Food and Agriculture Organization] (1996) Normas internacionales para medidas fitosanitarias. Sección 1 – Reglamento para la importación. Código de conducta para la importación y liberación de agentes exóticos de control biológico FAO Rome, ITA

    Google Scholar 

  • J.V. Falcó S. Navarro S. Santiago M. Pérez-Hinarejos E. Garzón F. Beitia (2003) ArticleTitleAspectos biológicos de la cría en laboratorio de dos himenópteros parasitoides exóticos de Ceratitis capitata Phytoma España 153 173–174

    Google Scholar 

  • P. Fimiani (1971) ArticleTitleThe present state of biological control and possibilities of its use in problems concerning olives Ann. Fac. Sci. Agr. Univ. Studi Napoli, Portici 5 145–160

    Google Scholar 

  • J.H. Frank E.D. McCoy (1993) ArticleTitleThe introduction of insects into Florida Fla. Entomol. 76 1–53

    Google Scholar 

  • J.M. Fry (1987) Natural enemy databank CIB International Wallingford (UK) 185

    Google Scholar 

  • R. Gabarra J. Arnó O. Alomar R. Albajes (1999) ArticleTitleNaturally occurring populations of Encarsia pergandiella (Hymenoptera: Aphelinidae)in tomato greenhouses IOBC/WPRS Bull. 22 85–88

    Google Scholar 

  • F. García Marí R. Vercher J. Costa Comelles C. Marzal M. Villalba (2004) ArticleTitleEstablishment of Citrostichus phyllocnistoides (Hymenoptera: Eulophidae) as a biological control agent for the citrus leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Spain Biol. Control 29 215–226

    Google Scholar 

  • F. García Marí (2005) Control biológico de plagas en cítricos J. Jacas P. Caballero J. Avilla (Eds) El control biológico de plagas y enfermedades Universitat Jaume I/Universidad Pública de Navarra Castelló, ES 183–191

    Google Scholar 

  • AP. Garona G. Viggiani (1989) ArticleTitleNotizie preliminari sulla Comperiella lemniscata Compere & Annecke (Hymenoptera: Encyrtidae), parassitoide di Chrysomphalus dyctiospermi (Morg.) in Italia Redia 72 523–527

    Google Scholar 

  • A. Garrido J.J. Ventrura (1993) Plagas de los cítricos. Bases para el manejo integrado M.A.P.A. Madrid, ES

    Google Scholar 

  • Gómez, S. and M. Ferry, 1996. Problems of the introduction of the biological control in the palm grove in Elche (Spain), against the red scale of the date palm, Phoenicococcus marlatii Cockll. Conf. Intl. Transfers Technol. Lutte Biol. IOBC. 9-11/09/96. Montpellier. FR.

  • F. Gómez Clemente (1933) ArticleTitleEstación de Fitopatología de Valencia. Servicio Fitopatológico Agrícola Ministerio de Agricultura, Madrid, Memoria del Año 1932 47–64

    Google Scholar 

  • J.A. Goolsby A.A. Kirk D.E. Meyerdirk (2002) ArticleTitleSeasonal phenology and natural enemies of Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) in Australia Flda. Entomol. 85 494–498

    Google Scholar 

  • D.G. Hall F.D. Bennett (1994) Biological control and IPM of sugarcane pests in Florida D. Rosen F.D. Bennett J.L. Capinera (Eds) Pest Management in the Subtropics Andover UK 297–325

    Google Scholar 

  • Hernández, E. and A. Carnero, 2000. Enemigos naturales de la mosca blanca Bemisia tabaci en las Islas Canarias. http://entomologia.rediris.es/congresoiberico/resentaplicada (06/07/04).

  • B. Herting (1975) ArticleTitleLepidoptera, Part 1 (Microlepidoptera). A catalogue of parasites and predators of terrestrial arthropods. Section A. Host or Prey/Enemy Commonwealth Agricultural Bureaux, Commonwealth Institute of Biological Control 6 116–119

    Google Scholar 

  • H.A. Hespenheide (1991) ArticleTitleBionomics of leaf-mining insects Annu. Rev. Entomol. 36 535–560 Occurrence Handle10.1146/annurev.en.36.010191.002535

    Article  Google Scholar 

  • M.P. Hoffmann R.L. Ridgway E.D. Show J. Matteoni (1998) Practical application of mass-reared natural enemies: selected case histories R.L. Ridgway M.P. Hoffmann M.P. Inscoe C.S. Gleinster (Eds) Mass-Reared Natural Enemies: Application, Regulation, and Needs ESA Lanham, USA 268–293

    Google Scholar 

  • F.G. Howarth (2001) Environmental issues concerning the importation of non-indigenous biological control agents J.A. Lookwood F.G. Howarth M.F. Purcell (Eds) Balancing Nature: Assessing the Impact of Importing Non-native Biological Control Agents (an international perspective) Thomas Say Publications in Entomology: Proceedings, Entomological Society of America Lanham, MD, USA 70–99

    Google Scholar 

  • InstitutionalAuthorNameIAEA [International Atomic Energy Agency] (2003) Trapping Guidelines for Area-wide Fruit Fly Programmes IAEA Vienna, AUT

    Google Scholar 

  • IFAS [Institute of Food and Agricultural Sciences], 2004. Beneficial insects and mites. http://mrec.ifas.ufl.edu/lso/SCOUT/biological.htm(26/05/04).

  • D.J. Isenhour K.V. Yeargan (1981) ArticleTitlePredation by Orius insidiosus on the soybean thrips, Sericothrips variabilis, effect of the prey stage and density Environ. Entomol. 10 496–500

    Google Scholar 

  • J.A. Jacas A. Garrido A. Hermoso de Mendoza M.J. Verdú (1997) ArticleTitleLa estación de cuarentena del IVIA: un paso adelante en la protección de nuestros cultivos Comunitat Valenciana Agrària 10 57–62

    Google Scholar 

  • J.A. Jacas A. Urbaneja J.L. Ripollés (2005) El futuro del control biológico J. Jacas P. Caballero J. Avilla (Eds) El control biológico de plagas y enfermedades Universitat Jaume I/Universidad Pública de Navarra Castelló, ES 209–223

    Google Scholar 

  • Junta de Andalucía, 2004, Organismos de control biológico: Aphidius colemani. http://desaveal.ual.es/sifa/bio/org_biologicos/auxiliar.jsp?id=1 (31/04/04).

  • Junta de Andalucía, 2002. Informe 2002. Medio Ambiente en Andalucía. http://www.juntadeandalucia.es/medioambiente/ima2002/estadisticas/B06 ESPACIOS_ PROTEGIDOS_MUNDO.htm (16/06/04).

  • P. Katsoyannos (1996) Integrated insect pest management for citrus in northern mediterranean countries Benaki Phytopathological Institute Athens, GR

    Google Scholar 

  • Kenis, M. and K. Kloosterman, 1999. European parasitoids of the European False Webworm (Acantholyda erytrhocephala (L.)) and their potential for biological control in North America. 65–73 pp. In: A.M. Liebhold, M.L. McManus, I.S. Otvos and S.L.C. Fosbroke, (eds), Proceedings: integrated management and dynamics of forest defoliating insects; 1999 August 15–19; Victoria, CAN.

  • Z.R. Khan W.A. Overholt A. Ng’eny-Mengech (2003) Integrated pest management case studies from ICIPE K.M. Maredia D. Dakouo D. Mota-Sánchez (Eds) Integrated pest management in the global arena CABI Publishing Trowbridgem, UK 441–452

    Google Scholar 

  • E.F. Knipling (1995) Principles of insect parasitism analyzed from new perspectives. Practical implications for regulating insect populations by biological means USDA-ARS Greenbelt, MD, USA

    Google Scholar 

  • G.F. Knowlton (1944) ArticleTitleOrius feeding records Bull. Brook. Entomol. Soc. 39 84–85

    Google Scholar 

  • A. Lacasa J.M. Llorens (1998) Thrips y su control biológico (y II) Pisa Ediciones Alacant, ES

    Google Scholar 

  • P.L. Lambdin A.M. Baker (1986) ArticleTitleEvaluation of dewinged spined soldier bugs, Podisus maculiventris (Say), for longevity and suppression of the Mexican bean beetle, Epilachna varivestris Mulsant, on snapbeans J. Entomol. Sci. 21 263–266

    Google Scholar 

  • J. LaSalle I.D. Gauld (1993) Hymenoptera: Their diversity and their impact on the diversity of other organisms J. LaSalle I.D. Gauld (Eds) Hymenoptera and Biodiversity CAB International Wallingford, UK 1–26

    Google Scholar 

  • J. LaSalle J.E. Peña (1997) ArticleTitleA new species of Galeopsomyia (Hymenoptera: Eulophidae: Tetrastichinae): a fortuitous parasitoid of the citrus leafminer, Phyllocnistis citrella (Lepidoptera: Gracillariidae) Fda. Entomol. 80 461–470

    Google Scholar 

  • S. Laudonia G. Viggiani (1986) ArticleTitleNatural enemies of the citrophilus mealybug (Pseudococcus calceolariae Mask.) in Campania Boll. Entoml. Agr. Filippo Silvestri 43 IssueIDsuppl. 167–171

    Google Scholar 

  • T. Lewis (1973) Thrips. Their Biology, Ecology and Economic Importance Academic Press London, UK

    Google Scholar 

  • W.J. Lewis D.A. Nordlund H.R. Gross SuffixJr. W.D. Perkins E.F. Knipling J. Voegele (1976) ArticleTitleProduction and performance of Trichogramma reared on eggs of Heliothis zea and other hosts Environ. Entomol. 5 449–452

    Google Scholar 

  • E. Llácer A. Urbaneja J.A. Jacas A. Garrido (1998b) ArticleTitleCiclo biológico de Quadrastichus sp., parasitoide exótico del minador de las hojas de los cítricos Phyllocnistis citrella Stainton, en laboratorio Bol. San. Veg. Plagas 24 675–684

    Google Scholar 

  • E. Llácer A. Urbaneja R. Hinarejos J.A. Jacas A. Garrido (1998a) ArticleTitleIntroducción de Galeopsomyia fausta LaSalle, ectoparasitoide de pupas del minador de las hojas de los cítricos Levante Agrícola 343 159–164

    Google Scholar 

  • J.M. Llorens (1990a) Homóptera I: Cochinillas de los cítricos y su control biológico Pisa Ediciones Alicante, ES

    Google Scholar 

  • J.M. Llorens (1990b) Homóptera II: pulgones de los cítricos y su control biológico Pisa Ediciones Alicante, ES

    Google Scholar 

  • J.M. Llorens A. Garrido (1992) Homóptera III: moscas blancas y su control biológico Pisa Ediciones Alicante, ES

    Google Scholar 

  • J.A. Lookwood F.G. Howarth M.F. Purcell (2001) Balancing Nature: Assessing the Impact of Importing Non-native Biological Control Agents (An International Perspective) Thomas Say Publications in Entomology: Proceedings, Entomological Society of America Lanham, MD, USA

    Google Scholar 

  • J.E. Losey S.J. Fleischer D.D. Calvin W.L. Harkness T. Leahy (1995) ArticleTitleEvaluation of Trichogramma nubilalis and Bacillus thuringiensis in management of Ostrinia nubilalis (Lepidoptera: Pyralidae) in sweet corn Environ. Entomol. 24 436–445

    Google Scholar 

  • L. Lynch M.B. Thomas (2000) ArticleTitleNontarget effects in the biocontrol of insects with insects, nematodes and microbial agents: the evidence Biocontrol News Inform. 21 117–130

    Google Scholar 

  • M. Mani (1995a) ArticleTitleStudies of the natural enemies of oriental mealybug, Planococcus lilacinus (Ckll.) (Homoptera: Pseudococcidae) in India J. Entomol. Res. 19 61–70

    Google Scholar 

  • M. Mani (1995b) ArticleTitleStudies of the natural enemies of the wax scale, Drepanococcus chiton (Green) on ber and guava Entomon. 20 5–58

    Google Scholar 

  • M. Mani A. Krisnamoorthy S.P. Singh (1990) ArticleTitleThe impact of the predator, Cryptolaemus montrouzieri Mulsant, on pesticide-resistant populations of the stripped mealybug Ferrisia virgata (Ckll.) on guava in India Insect Sci. appl. 11 167–170

    Google Scholar 

  • M. Mani A. Krisnamoorthy G.L. Pattar (1995) ArticleTitleBiological control of the mango mealybug, Rastrococcus iceryoides (Green) (Homoptera: Pseudococcidae) Pest Manag. Hortic. Ecosyst. 1 15–20

    Google Scholar 

  • M. Mani A. Krisnamoorthy (1999) ArticleTitlePredatory potential and development of the Australian ladybird beetle, Cryptolaemus montrouzieri Muls. on the spiralling whitefly, Aleurodicus dispersus Russell Entomon. 24 173–176

    Google Scholar 

  • P. Mansilla R. Pérez F. Ruíz C. Salinero (1999) ArticleTitleAvetianella longoi Siscaro, parásito de huevos de Phoracantha semipunctata F.: primera evidencia de su presencia en España y bases para la práctica del control biológico del xilófago Bol. San. Veg. Plagas 25 515–522

    Google Scholar 

  • B. Massa M.C. Rizzo V. Caleca (2001) ArticleTitleNatural alternative hosts of Eulophidae (Hymenoptera: Chalcidoidea) parasitoids of the citrus leafminer Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) in the Mediterranean Basin J. Hymen. Res. 10 191–200

    Google Scholar 

  • Mau, R.F.L. and J.L. Martin, 1992. Crop Knowledge Master. Coccus viridis (Green). http://www.extento.hawaii.edu/kbase/crop/Type/c_viridi.htm (06/07/04).

  • R.G. Mercet (1921) Fauna Ibérica. Himenópteros Fam. Encírtidos Museo Nacional de Ciencas Naturales Madrid, ES

    Google Scholar 

  • J.P. Michaud (2002a) ArticleTitleClassical biological control: a critical review of recent programs against citrus pests in Florida Ann. Entom. Soc. Am. 94 531–540

    Google Scholar 

  • J.P. Michaud (2002b) ArticleTitleInvasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native ladybeetle, Cycloneda sanguinea Environ. Entomol. 31 827–835

    Google Scholar 

  • InstitutionalAuthorNameMinisterio de Agricultura, Dirección General de la Producción Agraria. (1975) Lucha biológica contra la mosca blanca mediante Cales noacki. Servicio de defensa contra plagas e inspección fitopatológica MAPA Madrid, ES

    Google Scholar 

  • MNCN [Museo Nacional de Ciencias Naturales]. 2004. Fauna Ibérica. http://www.fauna-iberica.mncn.csic.es/index.php (15/10/04).

  • J.P. Moner V.R. Petit J.M. Bernat (1988) La mosca de las frutas (Ceratitis capitata Wied.) Generalitat Valenciana-CAPA València, ES

    Google Scholar 

  • Mizell, R.I. 2003. Featured creatures. Harmonia axyridis. http://creatures.ifas.ufl.edu/beneficial/multicolored_Asian_lady_beetle.htm.

  • S. Nagarkatti P.C. Tobin M.C. Saunders A.J. Muza (2003) ArticleTitleRelease of native Trichogramma minutum to control grape berry moth Can. Entomol. 135 589–598

    Google Scholar 

  • C. Neale D. Smith G.A.C. Beattie M. Miles (1995) ArticleTitleImportation, host specificity testing, rearing and release of three parasitoids of Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) in eastern Australia J. Aust. Entomol. Soc. 34 343–348

    Google Scholar 

  • J.R. Nechols (2003) Fortuitous biological control R. Driesche ParticleVan (Eds) Proc. First Intl. Meeting of Biological Control of Arthropod Pests Honolulu, HI, U.S. Forest Service Morgantown, WV, USA 324–329

    Google Scholar 

  • P. Neuenschwander S. Michelakis E. Kapatos (1986) Tephritidae Y. Arambourg (Eds) Traité d’entomologie oléicole International Olive Oil Council Madrid, ES 115–159

    Google Scholar 

  • R. Nguyen F.D. Bennett (1994) Tea scale D. Rosen F.D. Bennett J.L. Capinera (Eds) Biological control – a Florida perspective. Intercept Pest Management in the Subtropics Andover UK 123–128

    Google Scholar 

  • J. Nonell (1936) ArticleTitleIntroducción y difusión del Aphelinus mali (Hald.) en España Bol. Patol. Veg. Entomol. Agric. VIII 179–186

    Google Scholar 

  • E.R. Oatman G.R. Platner (1985) ArticleTitleBiological control of two avocado pests Calif. Agric. 1985 21–23

    Google Scholar 

  • E.R. Oatman J.D. Pinto G.R. Platner (1989) ArticleTitleTrichogramma of Hawaii Pacific Insects 24 1–24

    Google Scholar 

  • A. Panis J.P. Marro (1978) ArticleTitleVariations in the behaviour of Metaphycus lounsburyi (Hym.: Encyrtidae) Entomophaga 23 9–18

    Google Scholar 

  • O. Peck (1963) ArticleTitleA catalogue of the Nearctic Chalcidoidea (Insecta: Hymenoptera) Can Entomol. (suppl.) 30 277

    Google Scholar 

  • T. Pina B. Martínez M.J. Verdú (2001) ArticleTitlePresencia en la Península Ibérica de Comperiella lemniscata (Hym.: Encyrtidae) sobre el piojo rojo de los cítricos, Chrysomphalus dyctiospermi (Hemiptera: Diaspididae) Bol. San. Veg. Plagas 27 29–34

    Google Scholar 

  • A. Polaszek G.A. Evans F.D. Bennett (1992) ArticleTitleEncarsia parasitoids of Bemisia tabaci (Hymenoptera: Aphelinidae, Homoptera: Aleyrodidae): a preliminary guide to identification Bull. Entomol. Res. 82 375–392

    Google Scholar 

  • M.A. Pomerinke P.A. Stansly (1998) ArticleTitleEstablishment of Ageniaspis citricola (Hymenoptera: Encyrtidae) for biological control of Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Florida Flda. Entomol. 81 361–372

    Google Scholar 

  • G.L. Prinsloo M.J. Samways (2001) Host specificity among introduced chalcidoid biological control agents in South Africa J.A. Lookwood F.G. Howarth M.F. Purcell (Eds) Balancing Nature: Assessing the Impact of Importing Non-native Biological Control Agents (an international perspective) Thomas Say Publications in Entomology: Proceedings, Entomological Society of America Lanham 31–40

    Google Scholar 

  • A. Raspi (1988) ArticleTitlePreliminary notes of the entomophages of Saissetia oleae (Oliv.) and Lichtensia viburni Sing. in olive groves of coastal Tuscany and western Liguria Frustula Entomol. 11 119–128

    Google Scholar 

  • A.C. Rivera S.S. Carbone J.A. Andrés (1999) ArticleTitleLife cycle and biological control of the eucalyptus snout beetle (Coleoptera: Curculionidae) by Anaphes nitens (Hymenoptera: Mymaridae) in north-west Spain Agric. Forest Entomol. 1 103–109

    Google Scholar 

  • M. Rose D. Rosen (1991–1992) ArticleTitleEretmocerus debachi n. sp. (Hymenoptera: Aphelinidae), an effective parasite of Parabemisia myricae (Homoptera: Aleyrodidae) Israel J. Entomol. 25–26 199–207

    Google Scholar 

  • D. Rosen P. Debach (1979) Species of Aphytis of the World (Hymenoptera: Aphelinidae). Series Entomologica 17 Israel University Press Jerusalem, IL

    Google Scholar 

  • J. Salas (1995) ArticleTitleOrius insidiosus (Hemiptera: Anthocoridae) su presencia en la región Centro Occidental de Venezuela Agronomía Trop. 45 637–645

    Google Scholar 

  • G. Salerno S. Colazza F. Bin (2002) ArticleTitleNezara viridula parasitism by the tachinid fly Trichopoda pennipes ten years after its accidental introduction into Italy from the New World BioControl 47 617–624 Occurrence Handle10.1023/A:1020521607677

    Article  Google Scholar 

  • InstitutionalAuthorNameServicio Fitopatológico Agrícola. (1933) Plagas del campo. Memoria del Servicio Fitopatológico Agrícola Ministerio de Agricultura y Pesca Madrid, ES

    Google Scholar 

  • SIFA (Servicio de Información Fitosanitaria de Almería). 2004, Organismos de control biológico. http://desaveal.ual.es/sifa/inicio.htm. (26/08/04).

  • Smirnoff, W., 1950. Sur la Bioecologie au Maroc de Rhizobius (Lindorus) lophantae Blaisd (Col. Coccinelidae). Rev. Pathol. Vég. Entomol. Agric. France. T. XXIX- N°4-Déc.

  • D. Smith G.A.C. Beattie R. Broadley (1997) Citrus pests and their natural enemies IOM in Australia. HRDC – Queensland Department of Primary Industries Brisbane, AUT

    Google Scholar 

  • L. Smith M.E. Cuéllar E.L. Melo (1996) ArticleTitleEvaluating Prey Preference by Several Phytoseiid Predators for Mononychellus tanajoa (Bondar) and M. caribbeanae McGregor (Acari: Tetranychidae) in Cassava Biol. Control 7 179–184 Occurrence Handle10.1006/bcon.1996.0082

    Article  Google Scholar 

  • Smith, S.M., J.R. Carrow and J.E. Lang (eds), 1990. Inundative release of the egg parasitoid Trichogramma minutum (Hymenoptera: Trichogrammatidae), against forest insect pests such as the spurce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae): the Ontario project 1982–1986. Mem. Entomol. Soc. Can. 153.

  • A. Soto F. Ohlenschlager F. García Marí (2001) ArticleTitleDinámica poblacional y control biológico de las moscas blancas Aleurothrixus floccosus, Dialeurodes citri y Parabemisia myricae (Homoptera: Aleyrodidae) en huertos de cítricos de Valencia Bol. San. Veg. Plagas 29 3–20

    Google Scholar 

  • P. Stáry (1975) ArticleTitleAphidius colemani Viereck: its taxonomy, distribution and host range (Hymenoptera, Aphidiidae) Acta ent. Bohemoslov. 72 156–163

    Google Scholar 

  • P. Stáry M. Cermeli (1989) ArticleTitleParasitoides (Hymenoptera, Aphidiidae) de áfidos en plantas cultivadas de Venezuela Bol. Entomol. Venez. N.S 5 77–80

    Google Scholar 

  • W.L. Sterling (1978) ArticleTitleFortuitous biological suppression of the boll weevil by the red imported fire ant Environ. Entomol. 7 564–568

    Google Scholar 

  • Stibick, J.N.L., 2003. Natural Enemies of True Fruit Flies (Tephritidae). http://www.aphis.usda.gov/ppq/manuals/pdf_files/Natural%20Enemies%20of%20True%20 Fruit%20Flies%20-%20July%208,%202003.pdf(05/09/04).

  • P. Stiling (1990) ArticleTitleCalculating establishment rates of parasites in classical biological control Amer. Entomol. 36 225–230

    Google Scholar 

  • P. Stiling (2004) ArticleTitleBiological control not on target Biol. Invasions 6 151–159 Occurrence Handle10.1023/B:BINV.0000022130.54793.b7

    Article  Google Scholar 

  • R.E. Stinner R.L. Ridgway J.R. Coppedge R.K. Morrison W.A. Dickerson SuffixJr. (1974) ArticleTitleParasitism of Heliothis eggs after field releases of Trichogramma pretiosum in cotton Environ. Entomol. 3 497–500

    Google Scholar 

  • InstitutionalAuthorNameSTSC (1987) Statgraphics User’s Guide Graphic Software System STSC Inc. Rockville, MD, USA

    Google Scholar 

  • R.J. Stuart S. Polavarapu (2000) ArticleTitleEgg-Mass Variability and Differential Parasitism of Choristoneura parallela (Lepidoptera: Tortricidae) by Endemic Trichogramma minutum (Hymenoptera: Trichogrammatidae) Ann. Entomol. Soc. Amer. 93 1076–1084

    Google Scholar 

  • M.A. Tamai G.J. Moraes Particlede C.A.D. Silva Particleda (1997) ArticleTitleSuitability of Brevipalpus obovatus as prey to Neoseiulus idaeus (Acari: Tenuipalpidae, Phytoseiidae) on cassava Syst. Appl. Acarol. 2 101–106

    Google Scholar 

  • Tenbrink, T., 1993. Crop Knowledge Master. Pseudococcus longispinus (targioni-Tozzetti). http://www.extento.hawaii.edu/kbase/crop/Type/p_longis.htm (06/07/04).

  • M.B. Thomas A.J. Willis (1998) ArticleTitleBiocontrol-risky but necessary? Trends Ecol. Evol. 13 325–329

    Google Scholar 

  • W.R. Thompson (1954) A Catalogue of the Parasites and Predators of Insect Pests. Section 2. Host parasite catalogue. Part III. Hosts of the Hymenoptera (Calliceratid to Evaniid) Commonwealth Agricultural Bureau, Commonwealth Institute of Biological Control Ottawa, CAN

    Google Scholar 

  • W.H. Thorpe (1931) ArticleTitleThe biology, post-empryonic development, and economic importance of Cryptochaetum iceryae (Diptera, Ahromycidae), parasitic on Icerya purchasi London Zool. Soc. Proc. 1930 929–971

    Google Scholar 

  • V.A. Trjapitzin (1989) Parasitic hymenoptera of the Family Encyrtidae of Palaearctics. Opredeliteli po faune SSR 158 158 Zoologicheskim Institutom Akademii Nauk SSR Leningrad, RU

    Google Scholar 

  • P. Troncho E. Rodrigo F. García-Marí (1992) ArticleTitleObservaciones sobre el parasitismo de los diaspinos Aonidiella aurantii (Maskell), Lepidosaphes beckii (Newman) y Parlatoria pergandei (Comstock) en un huerto de naranjos Bol. San. Veg. Plagas 18 11–30

    Google Scholar 

  • P.H. Twine R.J. Lloyd (1982) ArticleTitleObservations on the effect of regular releases of Trichogramma spp. in controlling Heliothis spp. and other insects in cotton Queensl. J. Agric. Anim. Sci. 39 159–167

    Google Scholar 

  • InstitutionalAuthorNameUC [University of California] (1991) Integrated pest management for citrus UC – Statewide IPM project – Division of Agriculture and Natural Resources publ. 3303 Oakland, CA, USA

    Google Scholar 

  • UC database [Universal Chalcidoidea Database. The Natural History Museum], 2004. http://www.nhm.ac.uk/entomology/chalcidoids/ (27/05/04).

  • UFL/IFAS (University of Florida/ Institute of Food and Agricultural Sciences), 2000. Featured creatures: Cotesia marginiventris. http://creatures.ifas.ufl.edu/misc/wasps/cotesia_marginiventris.htm (02/05/04).

  • A. Urbaneja E. Llácer O. Omás A. Garrido J.A. Jacas (2000) ArticleTitleIndigenous natural enemies associated with Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Eastern Spain Biol. Control 18 199–207 Occurrence Handle10.1006/bcon.2000.0830

    Article  Google Scholar 

  • A. Urbaneja J. Blom Particlevan der L. Lara R. Timmer K. Blockmans (2002) ArticleTitleUtilización de Cotesia marginiventris (Cresson) (Hym.: Braconidae) para el control biológico de orugas (Lep.: Noctuidae) en el manejo integrado de plagas en pimiento bajo invernadero Bol. San. Veg. Plagas 28 239–250

    Google Scholar 

  • A. Urbaneja E. Llácer A. Garrido J.A. Jacas (2003) ArticleTitleInterspecific competition between two ectoparasitoids of Phyllocnistis citrella (Lepidoptera: Gracillariidae): Cirrospilus brevis and the exotic Quadrastichus sp. (Hymenoptera: Eulophidae) Biol. Control 28 243–250 Occurrence Handle10.1016/S1049-9644(03)00104-X

    Article  Google Scholar 

  • USDA [United States Department of Agricutlure], 1984. Introduced parasites and predators relesaed in the US and territories. Section I. Part B. http://www.ars-grin.gov/nigrp/menu.html (06/07/04).

  • R. Driesche ParticleVan T.S. Bellows (1996) Biological Control Chapman and Hall New York, USA

    Google Scholar 

  • Van Driesche, R. and M. Hoddle, 1995. Natural Enemies for Suppression of Greenhouse Pests. http://www.umass.edu/umext/floriculture/fact_sheets/pest_management/enemy2.html. (15/09/04).

  • J. Vander Blom (2002) ArticleTitleLa introducción artificial de la fauna auxiliar en cultivos hortícolas Bol. San. Veg. Plagas 28 109–120

    Google Scholar 

  • J.C. Lenteren ParticleVan (Eds) (2003) Quality Control and Production of Biological Control Agents. Theory and Testing Procedures CABI Publishing Wallingford, UK

    Google Scholar 

  • J.C. Lenteren ParticleVan D. Babendreier F. Bigler G. Burgio H.M.T. Hokkanen S. Kuske A.J.M. Loomans I. Menzler-Hokkanen P.C.J. Rijn Particlevan M.B. Thomas M.G. Tommasini Q.-Q. Zeng (2003) ArticleTitleEnvironmental risk assessment of exotic natural enemies used in inundative biological control BioControl 48 3–38

    Google Scholar 

  • J.C. Lenteren ParticleVan C. Woets (1988) ArticleTitleBiological and integrated pest control in greenhouses Annu. Rev. Entomol. 33 239–269

    Google Scholar 

  • M.J. Verdú (1985) ArticleTitleEstablecimiento de Prospaltella elongata, parásito de serpeta fina Levante Agrícola 259–260 68–70

    Google Scholar 

  • P. Videllet R. Albajes R. Gabarra (1997) ArticleTitleHost-feeding activity of Encarsia pergandiella Howard on Bemisia tabaci (Gennadius) IOBC WPRS Bull. 20 147–153

    Google Scholar 

  • G. Viggiani (1975) La lotta biologica di tipo convenzionale Atti del X Congresso Nazionale Italiano di Entomologia Sassari, IT 161–187

    Google Scholar 

  • G. Viggiani (1994) ArticleTitleRecent cases of interspecific competition between parasitoids of the family Aphelinidae (Hymenoptera:Chalcidoidea) Norweg. J. Agric. Sci. suppl. 16 353–359

    Google Scholar 

  • Viñuela, E., P. del Estal, M. Arroyo, A. Adán , F. Budia, J.A. Jacas, V. Marco, 1992. Los artrópodos: características. Los Insectos: órdenes. Monografía 128. Universidad politécnica de Madrid. Escuela Técnica Superior de Ingenieros Agrónomos. Madrid, ES.

  • E. Wajnberg J.K. Scott P.C. Quimby (2001) Evaluating Indirect Ecological Effects of Biological Control CABI Oxon, UK

    Google Scholar 

  • I.M. White M.M. Elson (2004) Fruit Flies of Economic Significance: Their Identification and Bionomics CAB International–The Australian Center for International Agricultural Research Eastbourne, UK

    Google Scholar 

  • Wysoki, M. 1999. Thysanoptera in Israel, en: Abstracts of the 16th Conference of the Entomological Society of Israel. http://www.phytoparasitica.org/phyto/pdfs/1999/issue3/meet.pdf (16/10/03).

  • M. Wysoki M.A. Berg Particlevan den G. Ish-Am S. Gazit J.E. Peña G.K. Waite (2002) Pests and pollinators of avocado J.E. Peña J. Sharp M. Wysoki (Eds) Tropical Fruit Pests and Pollinators CABI Wallingford, UK 223–293

    Google Scholar 

  • Wysoki, M., W. Kutzlitzky, Y. Izhar, E. Swirski, S. Ben Yehuda, D. Hadar and S. Reneh, 1993. Successful acclimatation of Thripobius semiluteus, a parasitoid of Heliothrips haemorrhoidalis (Bouché) in Israel, In: Abstracts of the 10th Conference of the Entomological Society of Israel. http://www.phytoparasitica.org/phyto/pdfs/1997/issue2/MEET.pdf (16/10/03).

  • G.R. Young (2003) ArticleTitleLife-history, biology, host plants and natural enemies of the lilly pilly psyllid, Trioza eugeniae Froggatt (Hemiptera: Triozidae) Aust. Entomol. 30 31–38

    Google Scholar 

  • D.S. Yu J.E. Laing E.A.C. Hagley (1984) ArticleTitleDispersal of Trichogramma spp. (Hymenoptera: Trichogrammatidae) in an apple orchard after inundative releases Environ. Entomol. 13 371–374

    Google Scholar 

  • C.D. Zhu J. LaSalle D.W. Huang (2002) ArticleTitleA study of Chinese Cirrospilus Westwood (Hymenoptera: Eulophidae) Zool. Stud. 41 23–46

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Josep-Anton Jacas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jacas, JA., Urbaneja, A. & Viñuela, E. History and Future of Introduction of Exotic Arthropod Biological Control Agents in Spain: A Dilemma?. Biocontrol 51, 1–30 (2006). https://doi.org/10.1007/s10526-005-5808-3

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-005-5808-3

Keywords

Navigation