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Annotated bibliography

Post-release studies


Babendreier D. and Bigler F. (2005). How to assess non-target effects of polyphagous biological control agents: Trichogramma brassicae as a case study. Pp. 603-610 In: Second International Symposium on Biological Control of Arthropods, Davos, Switzerland, 12-16 September, 2005, M.S. Hoddle (Ed.) United States Department of Agriculture, Forest Service, Washington.
The risk assessment conducted for Trichogramma brassicae (Hymenoptera: Trichogrammatidae), an egg parasitoid used for control of the European corn borer in European countries is discussed. The main factors investigated were the potential of establishment, acceptance and parasitism of non-target butterflies under laboratory, field-cage and field conditions, the searching efficiency in non-target habitats, the dispersal capacities and the potential for effects on other natural enemies in maize. Although high parasitism of non-target butterflies and other natural enemies were observed under laboratory conditions, very few eggs of non-target species were attacked in the field, possibly because of low host searching efficiency, and limited parasitoid dispersal. It was concluded that the possibility of using invertebrate agents with a broad host range in inundative biological control should not be excluded, although a thorough environmental risk assessment should be performed prior to release.

Balciunas J.K. and Villegas B. (2007). Laboratory and realized host ranges of Chaetorellia succinea (Diptera : Tephritidae), an unintentionally introduced natural enemy of yellow starthistle. Environmental Entomology 36: 849-857
In 1999, Chaetorellia succinea (Costa) (Diptera: Tephritidae), an unintentional introduction from Greece, was considered for biocontrol of yellow starthistle, Centaurea solstitialis L., one of the worst weeds in the western United States. However, the host range of C. succinea had not been studied, and so the physiological host range was determined in the laboratory by exposing it under no-choice conditions to 14 potential Cardueae hosts. Two introduced weed species and the native American basketflower (Centaurea americana Nuttall) were found to be laboratory hosts, although yellow starthistle was highly preferred. Because Ch. succinea is already widespread throughout California, flower heads were collected from 24 potential host plant species in the field to determine the realized host range. Ch. succinea emerged only from the other two known hosts: Ce. melitensis and Ce. sulfurea. Our results suggest that American basketflower growing in the southwestern United States may also be at risk if Ch. succinea expands its range into that region.

Barratt B.I.P., Blossey B. and Hokkanen H.M.T. (2006). Post-release evaluation of non-target effects of biological control agents. Pp. 166-186 In: Environmental Impact of Arthropod Biological Control: Methods and Risk Assessment, U. Kuhlmann, F. Bigler and D. Babendreier (Ed.) CABI Bioscience, Delemont, Switzerland.
This paper deals with weed biological control agents, pathogens and parasitoids.

Barratt B.I.P., Ferguson C.M., Bixley A.S., Crook K.E., Barton D.M. and Johnstone P.D. (2007). Field parasitism of nontarget weevil species (Coleoptera : Curculionidae) by the introduced biological control agent Microctonus aethiopoides Loan (Hymenoptera : Braconidae) over an altitude gradient. Environmental Entomology 36: 826-839
The parasitoid, Microctonus aethiopoides Loan (Hymenoptera: Braconidae) was introduced into New Zealand in 1982 to control the alfalfa pest, Sitona discoideus Gyllenhal (Coleoptera: Curculionidae). Studies have shown that a number of nontarget weevil species are attacked in the field by this parasitoid. A field study was carried out over 6 years to investigate nontarget parasitism by M. aethiopoides over an altitudinal sequence from the target host habitat (alfalfa) into native grassland. Weevil densities were estimated, species identified, and dissections carried out to determine reproductive status and parasitism. Seven nontarget weevil species were found to be parasitized. Substantial nontarget parasitism was found at only one of the three locations, with up to 24% parasitism of a native weevil, Nicaeana fraudator Broun (Coleoptera: Curculionidae), recorded. Results are discussed in relation to weevil phenology.

Barron M.C. (2007). Retrospective modelling indicates minimal impact of non-target parasitism by Pteromalus puparum on red admiral butterfly (Bassaris gonerilla) abundance. Biological Control 41: 53-63
There is anecdotal evidence that populations of the New Zealand endemic red admiral butterfly Bassaris gonerilla (F.) have declined since the early 1900s as a result of the introduction of the generalist pupal parasitoids Pteromalus puparum (L.) and Echthromorpha intricatoria (F.). A discrete-time model for B. gonerilla population dynamics was constructed which suggested that the impact of non-target parasitism by P. puparum has been minimal, but that parasitism by E. intricatoria was estimated to have caused 30% suppression of B. gonerilla abundance. The model suggested that the presence of an overwintering larval generation of B. gonerilla provides a temporal refuge from the high levels of E. intricatoria parasitism, assuming that parasitism rates are independent of B. gonerilla density. This assumption appears valid for P. puparum parasitism, but may not be so for E. intricatoria.

Berg G., Grosch R. and Scherwinski K. (2007). Risk assessment for microbial antagonists: are there effects on non-target organisms? Gesunde Pflanzen 59: 107-117
Biological control of phytopathogenic fungi using antagonistic microorganisms is potentially environmentally friendly but possible non-target effects on ecologically important soil-microbes need to be considered. Serratia plymuthica HRO-C48 and Streptomyces sp. HRO-71 were applied to control the pathogen Verticillium dahliae on strawberry and potato, and the bacterial strains Pseudomonas trivialis 3Re2-7, P. fluorescens L13-6-12, S. plymuthica 3Re4-18 and the fungal antagonists Trichoderma reesei G1/8 and T. viride G3/2 were introduced to control Rhizoctonia solani on lettuce and potato. After BCA treatment we did not observe any long-term effect on the plant-associated microbes in any tested pathosystem. Therefore, no sustainable risks could be seen for the indigenous micro-organisms.

Carson W.P., Hovick S.M., Baumert A.J., Bunker D.E. and Pendergast T.H. (2008). Evaluating the post-release efficacy of invasive plant biocontrol by insects: a comprehensive approach. Arthropod - Plant Interactions 2: 77-86
A program is proposed to evaluate the post-release phase of biocontrol programs that use insect herbivores to control invasive plant species. The authors argue that randomized release and non-release sites should be followed up to evaluate the degree of success or failure, including (1) the abundance of the biocontrol agent, (2) the impact of the biocontrol agent on the target plant species, (3) the potential for non-target effects (4) the response of native species and communities to a reduction in the invasive species and (5) experimental reductions of the biocontrol agent are required to eliminate the chance that the putative impact of the biocontrol agent is not confounded with other causes. Six scenarios are described in which a biocontrol agent may decrease the abundance or vigor of the target plant species but not lead to successful control where native communities re-establish.

Fowler S.V., Gourlay A.H., Hill R.L. and Withers T. (2003). Safety in New Zealand weed biocontrol: a retrospective analysis of host-specificity testing and the predictability of impacts on non-target plants. Pp. 265270 in Proceedings of the XI International Symposium on Biological Control of Weeds, Canberra, Australia, 2003, J.M. Cullen, D.T. Briese, D.J. Kriticos, W.M. Lonsdale, L. Morin and J.K. Scott (Ed.).
A retrospective analysis showed that all weed biocontrol agents released in New Zealand were subjected to generally appropriate host-range tests, although there were several examples where significant plant species were not tested. The results have been used to focus field surveys on the most likely non-target plant species to be attacked by biocontrol agents in New Zealand. For example, Tyria jacobaeae (cinnabar moth) did feed on some Senecio species in the original host-range tests, so the occasional field attack on native New Zealand fireweeds such as S. minimus was predictable. To date, this is the only weed biocontrol agent in New Zealand (of the total of 32 established in the field since 1929) that has been recorded attacking a native non-target plant species in the field. There were two cases where test results did not predict potentially substantial non-target impacts: Bruchidius villosus (broom seed beetle) and Cydia succedana (gorse pod moth), attacking seed of nontarget, exotic Fabaceae. Limited replication and duration of tests, were among possible explanations for the failure to predict these impacts.

Groenteman R., Kelly D., Fowler S.V. and Bourdot G.W. (2008). Factors affecting oviposition rate in the weevil Rhinocyllus conicus on non-target Carduus spp. in New Zealand. Pp. 87-90 In: Proceedings of the XII International Symposium on Biological Control of Weeds, La Grande Motte, France, 22-27 April, 2007
Rhinocyllus conicus (Froehlich) (Coleoptera: Curculionoidae), oviposits on developing thistle flower buds and larvae feeding on the receptacle prevents seed development. The weevil attacks several thistle species, but prefers nodding thistle, Carduus nutans L. The effects of plant characteristics on oviposition preference and/or the size of emerging adult weevils were examined on three Carduus species. The results showed that larger, higher seed heads on larger plants were preferred for oviposition and larger seed heads supported the development of larger adults. Nodding thistle flowers over an extended period of time but the two winged thistle species offer additional oviposition opportunities three to four weeks before nodding thistle flowers. The adults emerging from the winged thistle species are likely to establish a second generation, enabling this normally univoltine weevil to sustain seasonally prolonged attack on nodding thistle.

Haines M.L., Martin J.-F., Emberson R.M., Syrett P., Withers T.M. and Worner S.P. (2007). Can sibling species explain the broadening of the host range of the broom seed beetle, Bruchidius villosus (F.) (Coleoptera : Chrysomelidae) in New Zealand? New Zealand Entomologist 30: 5-11
Following introduction into New Zealand for biological control of Scotch broom, Cytisus scoparius, the broom seed beetle, Bruchidius villosus, was found utilising tagasaste, Chamaecytisus palmensis, which was not predicted by host range testing. One possible explanation for these inconsistencies is that more than one species is included within the current concept of B. villosus. However, sequence data from the mitochrondrial gene COI showed a low level of sequence polymorphism (0.8%) between individuals of B. villosus suggesting that B. villosus is a single species with a broader host range than was predicted by host range tests.

Haines M.L., Syrett P., Emberson R.M., Withers T.M., Fowler S.V. and Worner S.P. (2004). Ruling out a host-range expansion as the cause of the unpredicted non-target attack on tagasaste (Chamaecytisus proliferus) by Bruchidius villosus. Proceedings of the XI International Symposium on Biological Control of Weeds: 271-276
This paper describes an investigation of the original host-testing procedures. Despite showing a strong preference for Scotch broom, the beetles tested in this study accepted Chamaecytisus proliferus for oviposition allowing us to rule out the possibility that a host range expansion has occurred.

Haye T., Goulet H., Mason P.G. and Kuhlmann U. (2005). Does fundamental host range match ecological host range? A retrospective case study of a Lygus plant bug parasitoid. Biological Control 35: 55-67.
Using the retrospective case study of Peristenus digoneutis (Hymenoptera: Braconidae) introduced in the United States for biological control of native Lygus plant bugs (Hemiptera: Miridae), laboratory and field studies were conducted in the area of origin to evaluate whether the fundamental host range of P. digoneutis matches its ecological host range. To confirm the validity of the fundamental host range, the ecological host range of P. digoneutis in the area of origin was investigated. Peristenus digoneutis was reared from 10 hosts, including three Lygus species and seven non-target hosts from the subfamily Mirinae. Despite the fact that laboratory tests demonstrated a high parasitism level in non-targets, ecological assessments in both North America and Europe suggest a much lower impact of P. digoneutis on non-target mirids. It was concluded that ecological host range studies in the area of origin provide useful supplementary data for interpreting pre-release laboratory host range testing.

Louda S.M. (2000). Rhinocyllus conicus - insights to improve predictability and minimize risk of biological control of weeds. Proceedings of the X International Symposium on Biological Control of Weeds: 187-193
This paper reviews information on the release of Rhinocyllus conicus to control Carduus spp. thistles in North America and suggests 8 lessons for future biological control efforts: (1) better a priori quantification of the occurrence and ecological effects of the weed; (2) improved ecological criteria to supplement the phylogenetic information used to select plants for pre-release testing; (3) increased assessment of potential direct and indirect effects when an agent looks promising but feeding tests suggest it is not strictly monophagous, (4) quantitative evaluation of the efficacy of the proposed biological agent (5) more evidence on alternative control methods; (6) expanded review, both prior to release and periodically afterward; (7) addition of post-release evaluations and redistribution control; and, finally, (8) a rethinking of the situations that qualify for the use of biological control releases.

Louda S.M. and Arnett A.E. (2000). Predicting non-target ecological effects of biological control agents: evidence from Rhinocyllus conicus. Proceedings of the X International Symposium on Biological Control of Weeds: 551-567
The significant non-target ecological effects of Rhinocyllus conicus on native species in the northcentral USA provides the opportunity to evaluate factors that might help predict direct non-target effects, and indirect effects mediated by trophic interactions. The relevance for biocontrol risk assessment of at least four important ecological relationships has emerged from these studies so far: (1) ecological and phylogenetic similarity of potential host plants; (2) synchrony of critical stages between insect and potential host plant(s), as well as acceptability; (3) population limiting processes of potential host plants; and, (4) overlap of feeding niche within the native guild of species dependent upon the host plants. In the selection of biocontrol agents, knowledge of the ecological relationships should help to quantify the risks inherent in deliberate introductions of new species.

Mafokoane L.D., Zimmermann H.G. and Hill M.P. (2007). Development of Cactoblastis cactorum (Berg) (Lepidoptera : pyralidae) on six north American Opuntia species. African Entomology 15: 295-299
The recent arrival and spread of Cactoblastis cactorum in North America has raised concerns for the native Opuntia species. The host range of the moths was examined in South Africa. Results showed that although O. ficusindica is the preferred host for C. cactorum in South Africa, the moth is nevertheless able to utilize several other species of Opuntia as hosts.

Morrison-Lloyd W. (2006). Post-release host-specificity testing of Pseudacteon tricuspis, a phorid parasitoid of Solenopsis invicta fire ants. BioControl 51: 195-205.

Paynter Q., Martin N., Berry J., Hona S., Peterson P., Gourlay A.H., Wilson-Davey J., Smith L., Winks C. and Fowler S.V. (2008). Non-target impacts of Phytomyza vitalbae a biological control agent of the European weed Clematis vitalba in New Zealand. Biological Control 44: 248-258
The agromyzid leaf-mining fly Phytomyza vitalbae, which was introduced into New Zealand as a biological control agent of the invasive vine Clematis vitalba L. (old man's beard; Ranunculaceae) has been recorded attacking two native Clematis species in New Zealand, particularly C. foetida but at lower incidence and levels of attack than the target. No-choice starvation tests indicated that non-target attack was a "spillover" effect that is unlikely to have a major detrimental impact on the non-target plants. Our results show that the prevalence of spillover onto non-target species was underestimated in pre-release testing and we discuss how host-range testing might be improved in the light of these findings.

Porter S.D., Valles S.M., Davis T.S., Briano J.A., Calcaterra L.A., Oi D.H. and Jenkins A. (2007). Host specificity of the microsporidian pathogen Vairimorpha invictae at five field sites with infected Solenopsis invicta fire ant colonies in northern Argentina. Florida Entomologist 90: 447-452
The microsporidian pathogen Vairimorpha invictae was evaluated for release in the United States as a biological control agent for imported fire ants. The host range of this pathogen was examined showing that Solenopsis invicta Buren fire ant colonies had high levels of infection (28-83%) at one site, but none were found in ants at other sites. The results of this study indicate that, in its native South American range, V. invictae is specific to Solenopsis fire ants.

Stanley J.N. and Julien M.H. (1998). The need for post-release studies to improve risk assessments and decision making in classical biological control. Pp. 561-564 In: Pest Management - Future Challenges: Proceedings of the 6th Australasian Applied Entomological Research Conference, M. Zalucki, R. Drew and G. White (Ed.) The Cooperative Research Centre for Tropical Pest Management.

Taylor D.B.J., Heard T.A., Paynter Q. and Spafford H. (2007). Nontarget effects of a weed biological control agent on a native plant in Northern Australia. Biological Control 42: 25-33
Pre-release laboratory tests predicted that Neurostrota gunniella, an agent released in Australia against Mimosa pigra, may occasionally use Neptunia spp. as hosts. However, it was not expected to persist on Neptunia spp., nor have a significant effect. N. gunniella has established widely and is now abundant on the target weed, which grows sympatrically with at least one species of Neptunia. Nontarget attack of Neptunia major in the field has been investigated, and although an average of 61% of N. major plants growing adjacent to M. pigra thickets had evidence of attack, this was relatively low. Where M. pigra was not present, use of N. major plants by N. gunniella was noticeably reduced or absent. Post-release results support the predictions made during prerelease studies of N. gunniella.

Withers T.M., Hill R.L., Paynter Q., Fowler S.V. and Gourlay A.H. (2008). Post-release investigations into the field host range of the gorse pod moth Cydia succedana Denis & Schiffermuller (Lepidoptera : Tortricidae) in New Zealand. New Zealand Entomologist 31: 67-76
The gorse pod moth Cydia succedana was released in New Zealand as a biological control agent against gorse Ulex europaeus L. in 1992 and is now widely established. Post-release evaluations of host range were undertaken using both laboratory assays and field collections on native and exotic plants related to gorse. Field surveys detected no attack on native New Zealand plant species. However, contrary to predictions based on pre-release host-range testing, several species of exotic Genisteae were shown to be hosts of C. succedana. Hypotheses to explain this unexpected non-target attack include a seasonal asynchrony between C. succedana and gorse flowering phenology, or that the original biocontrol introduction accidentally consisted of either two cryptic species or two populations with different physiological host range.

Zimmermann G. (2007). Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Science & Technology 17: 879-920
Metarhizium anisopliae (Metschn.) Sorokin is widely used for biocontrol of pest insects, and many commercial products are on the market or under development. This review summarises all relevant safety data for this fungus, which are necessary for the commercialisation and registration process. On the basis of the presented knowledge, M. anisopliae is considered to be safe with minimal risks to vertebrates, humans and the environment.

van Lenteren J.C., Loomans A.J.M., Babendreier D. and Bigler F. (2008). Harmonia axyridis: an environmental risk assessment for Northwest Europe. BioControl 53: 37-54
A recently designed, comprehensive risk evaluation method to evaluate the environmental risks of Harmonia axyridis showed that H. axyridis is a potentially risky species for Northwest Europe, because it is able to establish, it has a very wide host range including species from other insect orders and even beyond the class of Insecta. Its activities have resulted in the reduction of populations of native predators in North America, where it may develop as a pest of fruit. Current knowledge would lead to the conclusion that it should not have been released in Northwest Europe. In retrospect, the risks should have been sufficient to reject import and release of this species, but this was ignored. The case of Harmonia releases in Northwest Europe demonstrates an urgent need for harmonized, world-wide regulation of biological control agents, including an information system on risky natural enemy species.