Biological control not on target

Biological Invasions 6: 151 159, 2004. 2004 Kluwer Academic Publishers. Printed in the Netherlands. Biological control not on target Peter Stiling Department of Biology, University of South Florida, Tampa, FL 33620-5150, USA (e-mail: pstiling@chuma1.cas.usf.edu; fax: +1-813-974-3263) Received 20 May 2003; accepted in revised form 7 July 2003 Key words: biological control, non-target effects, parasitoids, predators Abstract Non-target effects of exotic biological control agents, parasitoids and predators, released worldwide to control insect pests, are becoming more apparent. This paper summarizes previously recorded information on the diet breadth of natural enemies released to control insect pests worldwide. It also summarizes the diet breadth of native parasitic hymenoptera in North America to determine whether the diet breadths of native and exotic parasitoids differ. Of released biocontrol agents, 48% were recorded as generalists (attacking more than one genus of host) and another 29.2% attacked more than one species in a genus. Only 22.5% were recorded as specialists on the target pests. This suggests that many natural enemies released in biocontrol programs against insect pests have broad diets and that non-target effects are likely. Data from native hymenoptera in North America also show that many species attack multiple host genera and species, with an average of 5.8 genera and 7.3 species attacked, indicating broad agreement with data from biological control releases. Introduction Biological control is a tremendously valuable weapon in the fight against insect pests and has usually been thought of as a safe alternative to chemical control (US Congress 1995; Onstad and McManus 1996). In the absence of detailed evidence to the contrary, many biocontrol workers view non-target effects as infrequent and unimportant. For example, Lynch et al. (2001) gathered together a mass of information on recorded non-target effects from biocontrol releases and argued that less than 10% of releases have led to population changes in non-targets. However, they noted that such effects have been looked for in only 1.5% of cases. Recently there have been a large number of documented non-target effects of biological control agents on native plants and animals (Howarth 1991; Elliott et al. 1996; Simberloff and Stiling 1996; Louda et al. 1997; Follett and Duan 1999; Boettner et al. 2000; Howarth 2000; Henneman and Memmott 2001; Stiling 2002). Biological control workers are beginning to heed the warning signs and some have even suggested a guilty until proven innocent approach about future releases of natural enemies (Strong and Pemberton 2000). Even well-behaved biological control agents, which do not normally attack non-target organisms, can have substantial indirect effects on native communities. For example, establishment of the biological control agent Urophora sp., the knapweed gall fly, on knapweed in Montana, which failed to control the knapweed, provided a bonanza of food for deer mice, which greatly increased in density and impacted local food webs (Pearson et al. 2000). Up until now, there have been few systematic attempts to determine when non-target effects may be considered likely. Entomologists have long been aware that many insects released in biocontrol programs are polyphagous and could have non-target effects (e.g. Perkins 1897; Tothill et al. 1930). Stiling (1990) documented that in 367 of 586 releases of parasitoids made worldwide against insect pests, 62.6% of the releases involved polyphagous species. Stiling (1993) later showed that lack of alternative hosts was frequently recorded as a

152 reason for failure in biocontrol (16.9% of 148 cases). To get some idea of the potential of non-target effects of natural enemies released against pests, I present information on the reported diet breadth of predators and parasitoids released against insect pests worldwide. I also examine the diet breadth of native parasitoids in the US which have been used in biological control campaigns in other countries. By comparing both sets of data I examine whether the reported diet breadth of species used in biological control represents a natural subset of native enemies in general. Materials and methods I examined reports in Clausen s (1978) review of biological control campaigns around the world to determine the reported diet breadth of released natural enemies. In this volume, for cases of successful biological control, where the enemy had become established, a fairly comprehensive report on the biology of the natural enemy was available. Diet breadth was assigned to one of three categories: specialists, species which had been reported to attack only the target pest; restricted to genus, species which had been reported to attack more than one species, but all in the same genus; and generalists, which had been recorded as attacking more than one genus. At the same time, the family of the enemy and the family of the target pest involved was recorded. To get an idea of the diet breadth of some natural enemies in their native communities, I examined the catalog of Krombein et al. (1979), who report on the diet breadth of parasitoids in the US, and crossreferenced it to species known by Clausen (1978) to have been used as biological control agents in areas outside the US. Both the numbers of recorded host species and host genera and the family of the enemy involved were recorded. Although both these catalogs are over 20 years old and may contain some errors, both were published at about the same time, are unlikely to contain systematic errors, and the biology of the species involved is unlikely to have changed drastically. Results and discussion One hundred and twenty instances were found that gave details of the diet breadth of natural enemies used in successful biological control campaigns (Table 1). Of these, a staggering 58, or 48.3%, were generalists (attacked more than one genus of host or prey), and another 35 (29.2%) attacked more than one species in a genus. Only 27 (22.5%) were recorded as specialists. Of course, for many of these species no nontarget effects are known, but absence of evidence is not evidence of absence. The present data lead us to believe that the chances of released enemies attacking non-target species of insect are more likely than not. Among the natural enemies with broad recorded diets were Coccinellids (87% recorded as generalists), Pteromalids (80%) and Tachinids (62%). Prominent Table 1. Diet breadth of exotic natural enemies released in biological control campaigns around the world and now established. Data from Clausen (1978). Natural enemy Family Host-affiliation HOMOPTERA Allotropa utilis Platygasteridae Genus Allotropa burrelli Platygasteridae Specialist Anagrus armatus Mymaridae Generalist Anagrus frequens Myrmaridae Generalist Anagyrus coccidivorus Encyrtidae Generalist Anagyrus pseudococci Encyrtidae Genus Aphelinus asychis Aphelinidae Generalist Aphelinus mali Aphelinidae Generalist Aphidecta obliterata Coccinellidae Genus Aphidoletes thompsoni Cecidomyiidae Genus Aphytis holoxanthus Aphelinidae Generalist Aphytis lignanensis Aphelinidae Generalist Aphytis lepidosaphes Aphelinidae Specialist Aphytis maculicoinis Aphelinidae Specialist Aphytis melinus Aphelinidae Generalist Aphytis mytilospidis Aphelinidae Generalist Blastothrix sericea Encyrtidae Genus Cerabunia myersi Encyrtidae Genus Chilocorus distigma Coccinellidae Generalist Chilocorus nigritus Coccinellidae Generalist Chilocorus politus Coccinellidae Generalist Coccophagus gurneyi Aphelinidae Generalist Coccophagus Eulophidae Specialist insidiator Coccophagoides utilis Aphelinidae Specialist Comperiella bifasciata Encyrtidae Generalist Cremifania Chamaemyiidae Genus nigrocellulata Cryptochaetum iceryae Agromyzidae Genus Cryptognatha nodiceps Coccinellidae Generalist Cryptolaemus Coccinellidae Generalist montrouzieri Cyrtorhinus fulvus Miridae Specialist Diversinervus elegans Encyrtidae Generalist Encarsia formosa Aphelinidae Specialist Eretmocerus serius Aphelinidae Genus

153 Table 1. Continued. Natural Enemy Family Host-affiliation Habrolepis dalmanni Encyrtidae Genus Hemisarcoptes malus Hemisarcopptidae Generalist Hungariella peregrina Encyrtidae Genus Hungariella pretiosa Encyrtidae Specialist Laricobius erichsonii Derodontidae Genus Leptomastidea Encyrtidae Generalist abnormis Metaphycus helvolus Encyrtidae Generalist Metaphycus lounsburvi Encyrtidae Genus Pauridia peregrina Encyrtidae Genus Praon exsoletum Braconidae Genus Prospatella berlesei Aphelinidae Specialist Prospatella opulenta Aphelinidae Genus Prospatella perniciosi Aphelinidae Specialist Pseudaphycus malinus Encyrtidae Specialist Pseudaphycus mundus Encyrtidae Generalist Pteroptrix smithi Aphelinidae Specialist Rhizobius ventralis Coccinellidae Generalist Rodolia cardinalis Coccinellidae Generalist Scutellista cyanea Pteromalidae Generalist LEPIDOPTERA Agathus pumila Braconidae Specialist Apanteles Braconidae Generalist circumscriptus Apanteles glomeratus Braconidae Generalist Apanteles harrisinae Braconidae Genus Apanteles hyphantriae Braconidae Generalist Apanteles lacteicolor Braconidae Generalist Apanteles melanoscelus Braconidae Specialist Apanteles rubecula Braconidae Specialist Ascogaster Braconidae Generalist quadridentata Bessa remota Tachinidae Generalist Blepharipa scutellata Tachinidae Specialist Calosoma sycophanta Carabidae Generalist Cedria paradoxa Braconidae Generalist Chelonus texanus Braconidae Generalist Chrysocharis Eulophidae Generalist laricinellae Compsilura concinnata Tachindae Generalist Diadegma cerophaga Ichneumonidae Generalist Doryphorophaga Tachinid Specialist doryphorae Eriborus terebrans Ichneumonidae Specialist Euplectrus plathypenae Eulophidae Generalist Eupteromalus Pteromalidae Generalist hemipterus Lespesia archippivora Tachinidae Generalist Lixophaga diatraeae Tachinidae Genus Lydella thompsoni Tachinidae Generalist Macrocentrus grandii Braconidae Specialist Macrocentrus homonae Braconidae Specialist Mericia ampelus Tachinidae Generalist Ooencyrtus kuwanai Encyrtidae Specialist Table 1. Continued. Natural Enemy Family Host-affiliation Pentalitomastix Encyrtidae Specialist nacoleiae Orgilus obscurator Braconidae Generalist Pteromalus puparum Pteromalidae Generalist Sturmia harrisinae Tachinidae Genus Temelucha interruptor Ichneumonidae Generalist Tetrastichus turionum Eulophidae Specialist Townsendiellomyia Tachinidae Specialist nidicola Trichogramma Trichogrammatidae Generalist japonicum COLEOPTERA Bathyplectes Ichneumonidae Genus curculionis Biolysia tristis Ichneumonidae Genus Campsomeris Scoliidae Generalist marginella Dexilla ventralis Tachinidae Generalist Dibrachoides druso Pteromalidae Genus Doryctes syagrii Braconidae Genus Micronotus aethiops Braconidae Generalist Patasson nitens Mymaridae Genus Plaesius javanus Histeridae Generalist Prorops nasuta Bethylidae Genus Prosena siberita Tachinidae Generalist Tetrastichus brontispae Eulophidae Genus Tetrastichus incertus Eulophidae Genus Tiphia parallela Tiphiidae Generalist Tiphia popilliarora Tiphiidae Genus Tiphia vernalis Tiphiidae Genus DIPTERA Aleochara bilineata Staphylinidae Genus Alysisa ridibunda Braconidae Generalist Chrysocharis gemma Eulophidae Specialist Spalangia drosophilae Pteromalidae Generalist Trybliographa rapae Cynipidae Genus HYMENOPTERA Chrysocharis Eulophidae Generalist laricinellae Collyria calcitraor Ichneumonidae Genus Pharomeris Braconidae Generalist phyllotomae HEMIPTERA Trichopoda pennipes Tachinidae Generalist Trioxys complanatus Braconidae Genus Trissolcus basalis Scelionidae Generalist THRIPIDAE Ceranisus brui Eulophidae Generalist ORTHOPTERA Larra bicolor Sphecidae Specialist Larra luzonensis Sphecidae Specialist Leefmansia bicolor Encyrtidae Genus MITES Typhlodromus rickeri Phytoseiidae Genus

154 Table 2. Diet breadth of exotic natural enemies known to be established and to attack species not in the same genus as the target prey. From Clausen (1978). No. Target pest Order Enemy Order Prey Location HOMOPTERA 1 Anasa tristis (squash bug) Coreidae Trichopoda pennipes Tachinidae A considerable number of coreidae and pentatomidae 2 Nezara viridula (southern green stink bag) Pentatomidae Trissolcus basalis Scelionidae A number of other pentatomidae Australia, New Zealand, Hawaii 3 Thrips tabaci Thripidae Ceranisus brui Eulophidae Three genera of thrips, kakothrips Hawaii (onion thrips) and taeniothrips 4 Aleurocanthus woglumi (citrus blackfly) Aleyrodidae Eretmocerus serius Aphelinidae Various blackfly species of Aleurocanthus Mexico, Cuba, South Africa 5 Eriosoma lanigerum Aphididae Aphelinus mali Aphelinidae A number other aphid genera Worldwide 6 Therioaphis trifolii Aphididae Aphelinus asychis Aphelinidae 20 or more species of Aphididae California (spotted alfalfa weevil) 7 Edwardsiana froggatii Cicadellidae Anagrus armatus Mymaridae Several Cicadellidae Tasmania (apple leafhopper) 8 Saissetia oleae (black scale) Coccidae Metaphycus helvolus Encyrtidae Many of the principal genera of soft scales Greece, California, Australia, Chile California 9 Saissetia oleae (black scale) 10 Saissetia oleae (black scale) 11 Peregrinus maidis (corn planthopper) 12 Aonidiella aurantii California red scale 13 Aonidiella aurantii California red scale 14 Aonidiella aurantii California red scale 15 Aonidiella aurantii California red scale 16 Pinnaspi buxi Diaspidid scale 17 Chrysomphalus aonidum Florida red scale 18 Chrysomphalus dictyospermi Dictyospernum scale Coccidae Diversinervus elegans Encyrtidae Most of the lecaniine scale genera Coccidae Scutellista cyanea Pteromalidae Wide variety of lecaniine scale insects, particularly those of the genera Saissetia, Lecanium and Ceroplastes Delphacidae Anagrus frequens Mymaridae Sugarcane leafhopper Hawaii Diaspididae Bifasciata comperiella Encyrtidae Aonidiella, Chrysomphalus and other species of armored scale USA California, Australia, Peru California Diaspididae Aphytis lignanensis Aphelinidae Three genera of scale insects California Diaspididae Aphytis melinus Four genera of scale insects Greece Diaspididae Chilocorus politus Coccinellidae Polyphagous, wide range of host scales Mauritius Diaspididae Chilocorus distigma Coccinellidae General predator of armored Seychelles and soft scales Diaspididae Aphytis holoxanthus Aphelinidae Aspidiotus and Diaspis Israel, Mexico Diaspididae Aphytis lounsbouryi Aphelinidae Aonidiella Italy

155 19 Lepidosaphes ficus Fig scale 20 Erococcus coriaceus Blue-gum scale 21 Icerya purchasi Cottony cushion scale 22 Dysmicoccus boninsis Grey sugarcane mealybug 23 Dysmicoccus brevipes Pineapple mealybug 24 Planococcus citri Citrus mealybug 25 Planococcus citri Citrus mealybug 26 Pseudococcus fragilis Citrophilus mealybug LEPIDOPTERA 27 Coleophora laricella Larch casebearer 28 Chilo suppresalis Asiatic rice borer 29 Lithocollitis messaniella Oak leaf miner 30 Porthetria dispar Gypsy moth 31 Porthetria dispar Gypsy moth 32 Stilpnotia salicis Satin moth 33 Nygmia phaeorrhoea Brown tail moth 34 Spodoptera exempta Nutgrass army worm 35 Spodoptera exempta Nutgrass army worm 36 Spodoptera exempta Nutgrass army worm 37 Laspeyresia nigricana Pea moth 38 Rhyacionia buoliana European pine shoot moth Diaspididae Aphytis mytilaspidis Aphelinidae Oyster shell scale California Eriococcidae Rhizobius ventralis Coccinellidae Many different kinds of coccids New Zealand Flatidae Rodolia cardinalis Coccinellidae Monophlebine scales California & 55 different countries Pseudococcidae Pseudaphycus mundus Encyrtidae Five genera of mealybugs Florida Pseudococcidae Anagyrus coccidivorus Encyrtidae Ferisia virgata Hawaii Pseudococcidae Cryptolaemus montrouzieri Coccinellidae Almost every kind of mealybug California & 40 other countries Pseudococcidae Leptomastidea abnormis Encyrtidae Five genera of mealybugs Hawaii, Eastern USA, Brazil Pseudococcidae Coccophagus gurneyi Aphelinidae Six species California, South Africa, New Zealand, Chile Coleophoridae Chrysocharis larcinellae Eulophidae Moth, sawfly and as a secondary parasite Canada Crambidae Trichogramma japonicum Trichogrammidae A number of lepidoptera Hawaii Gracillariidae Apanteles circumscriptus Braconidae Larvae of many gracillaridae New England Lymantriidae Compsilura concinnata Tachinidae Highly polyphagous, 200 host species New Zealand Lymantriidae Calosoma sycophanta Carabidae Other lepidoptera New England Lymantriidae Eupteromalus hemipterus Pteromalidae Primary and secondary parasite of many lepidoptera USA, Canada Lymantriidae Apanteles lacteicolor Braconidae A number of lepidoptera USA, Canada Noctuidae Euplectrus plathypenae Eulophidae Wide host range among lepidoptera Hawaii Noctuidae Chelonus texanus Braconidae Considerable number of lepidoptera Hawaii Noctuidae Lespesia archippivora Tachnidae Wide range of caterpillars Hawaii Olethreutidae Ascogaster quadridentata Braconidae A very large number of lepidoptera Canada Olethreutidae Orgilus obscurator Braconidae A considerable number of lepidopterous species USA, Canada

156 Table 2. Continued. No. Target pest Order Enemy Order Prey Location 39 Rhyacionia buoliana European pine shoot moth 40 Pieris rapae Cabbage worm 41 Pieris rapae Cabbage worm 42 Hapalia machaeralis Teak leaf skeletonizer 43 Ostrinia nubilalis European Corn borer 44 Plutella xylostella Diamond back moth Olethreutidae Temelucha interruptor Ichneumanidae Several families of lepidoptera USA, Canada Pieridae Pteromalus puparum Pteromalidae Wide range of pierids and nymphalids USA, New Zealand, Australia Pieridae Apanteles glomeratus Braconidae Many families of lepidoptera USA, New Zealand, Australia Pyralidae Cedria paradoxa Braconidae A wide range of lepidoptera Burma Pyralidae Lydella thompsoni Tachinidae Ostrinia penitalis and Papaipema nebris USA, Canada Yponomeutidae Diadegma cerophaga Ichneumonidae Nine moths from eight families New Zealand, Australia, Indonesia COLEOPTERA 45 Levuana iridescens Coconut moth beetle 46 Cosmopolites sordidus Banana root borer 47 Hypera postica Alalfa weevil 48 Anomala orientalis Oriental beetle 49 Phyllaphaga smithi Sugarcane scrub 50 Popillia japonica Japanese beetle 51 Popillia japonica Japanese beetle Zygaenidae Bessa remota Tachinidae Several other lepidopterous species Fiji Curculionidae Plaesuis javanus Histeridae Many soil- or trash-inhabiting insects Curculionidae Microctonus aethiops Braconidae A considerable number of species of Hypera and Sitona Scarabeidae Campsomeris marginella Scoliidae Six genera of scarab beetles Hawaii Scarabeidae Tiphia parallela Tiphiidae Five genera of scarab beetles Mauritius Scarabeidae Prosenia siberita Tachinidae Scarabeidae of several subfamilies USA Scarabeidae Dexilla ventralis Tachinidae Three genera of Scarabeidae USA Fiji, Jamaica, Mariana Islands, New Caledonia, Trinidad USA HYMENOPTERA 52 Heterarthrus nemoratus Birch leaf-mining sawfly 53 Heterarthrus nemoratus Birch leaf-mining sawfly Tenthredinidae Phanomeris phyllotomoe Braconidae Two genera of lepidoptera USA Tenthredinidae Chrysocharis laricinellae Eulophidae Two genera of lepidoptera USA DIPTERA 54 Calliphoridae spp. Blow flies 55 Hippelates spp. Eye gnats Calliphoridae Alysia ridibunda Braconidae Three genera of flies Australia, New Zealand Chloropidae Spalangia drosophilae Pteromalidae Two genera of flies USA

157 Table 3. Host specificity of native North American hymenoptera known to have been introduced from the US or other locations around the world as biological control agents. Data cross-referenced from Krombein et al. (1979) and Clausen et al. (1978). Family Genus Species No. genera No. species attacked attacked BRACONIDAE Heterospilus cephi 1 1 prosopidis 2 3 Bracon gelechiae 32 34 hebetor 10 10 mellitor 27 34 thurberiphagae 4 4 Rogas hyphantriae 1 1 laphygmae 2 4 Macrocentrus ancylivoris 16 16 delicatus 15 18 Ascogaster quadridentata 6 8 Apanteles bedelliae 6 7 harrisinae 1 2 hyphantriae 3 4 marginiventris 14 21 militaris 8 11 ICHNEUMONIDAE Itoplectis quadricingulata 21 25 Megarhyssa nortonii 3 3 Campoplex frustranae 1 2 phthorimaeae 3 4 Hyposoter exiguae 12 15 fugitivus 10 17 PTEROMALIDAE Muscidifurax raptor 5 5 EURYTOMIDAE Euryrtoma pini 3 5 ENCYRTIDAE Aphytis mytilaspidis 10 16 Coccophagus capensis 3 3 gurneyi 4 8 scutellaris 3 5 Prospaltella berlesei 1 1 brasiliensis 1 1 elongata 3 1 murtfeldtiae 3 3 Eretmocerus californicus 1 1 haldemani 4 5 portoricensis 1 1 Acerophagus pallidus 3 4 Metaphycus lounsburyi 1 1 luteolus 3 4 Pseudaphycus angelicus 3 5 mundus 3 4 Habrolepis dalmanni 2 3 Ooencyrtus johnsoni 3 3 EULOPHIDAE Euplectrus plathypenae 8 11 Elachertus hyphantriae 2 2 Ceranisus russellii 4 4 SCELIONIDAE Trissolcus murgantiae 1 1 PLATYGASTERIDAE Allotropha utilis 1 2

158 among the natural enemies with the most restricted diet were Encyrtids (42% specialists). Among the host or prey taxa, Lepidopterans had the largest number of recorded generalists released against them (58%). It was not possible to further quantify the diet breadth of generalists in terms of the number of genera they attacked as most often it was not given. However, it was clear that generalists were often very general because of statements such as recorded from a wide host range among the Lepidoptera, or considerable number of Lepidoptera, several families of Lepidoptera, a wide range of host scales, or almost every kind of mealybug (Table 2). Among the North American hymenoptera used in biocontrol programs, the mean number of genera of hosts attacked in native habitats was 5.8 ± 1.0 standard error (s.e.) and the mean number of species attacked was 7.3 ± 1.2 s.e. (Table 3). Most native parasitoids in North America used in biocontrol appear to have a fairly broad host range and are therefore unlikely to attack just one target species. Among the broader ranges found were those of Braconids, which attacked an average of 9.2 ± 2.3 s.e. genera and 11.1 ± 2.7 s.e. species and Ichneumonids, which attacked an average of 8.3 ± 3.1 s.e. genera and 11.0 ± 3.8 s.e. species. The recent finding of Hennemann and Memmott (2001), that most (83%) of the parasitoids reared from native Hawaiian Lepidoptera were originally imported as biological control agents shocked many in the ecological and entomological worlds. However, the data presented here and elsewhere show that successfully established biological control agents are more likely than not to attack non-target species and genera. Of course, many of the non-target genera attacked within the native range may not be present in other countries, but on the other hand some additional non-target species not present in the native country may be present in the area of release. Hawkins and Marino (1997) showed that at least 50 of 313 parasitoids released against insect pests in North America attacked nontarget species. This is not a feature peculiar to enemies released in biocontrol programs. Sheehan and Hawkins (1991) reported that for Canadian pimpline and metopiine wasps, the mean number of host species attacked was 9.92 and 4.29 respectively, and the mean number of host genera attacked was 7.64 and 2.86, respectively. From an extensive rearing program of Lepidoptera in the northeast United States, associated with the gypsy moth control program between 1915 and 1933, only 25 species of parasitoid were found to use just a single host while 49 species used 2 or more (Sheehan 1991). 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