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Annotated bibliography

Laboratory host range testing

Weed biological control agents


Arnett A.E. and Louda S.M. (2002). Re-test of Rhinocyllus conicus host specificity, and the prediction of ecological risk in biological control. Biological Conservation 106: 251-257.
Rhinocyllus conicus was released in North America to control exotic thistles. It is now reducing seed production by multiple native North American thistle species. It was hypothesized that host specificity of R. conicus has changed since pre-release testing, providing an explanation for the unexpected magnitude of the documented ecological effects, however, this was not the case. The authors concluded that accurate prediction of the potential level of impact on native host plants in the field requires further ecological information in addition to host specificity.

Baars J.R. (2000). Emphasizing behavioural host-range: the key to resolving ambiguous host-specificity results on Lantana camara L. Proceedings of the X International Symposium on Biological Control of Weeds: 887-896
Candidate biological control agents presently under evaluation for release on L. camara in South Africa accept closely related native plant species. The results from host-range results of two natural enemies, Falconia intermedia (Hemiptera: Miridae) and Coelocephalapion sp. (Coleoptera: Brentidae) were compared to determine the influence these trials have on the interpretation of the accepted host-range. Results suggested that the natural host-range of a candidate biological control agent is best determined by focusing on behavioural factors influencing host acceptance. The implications of using trials that incorporate insect behaviour during host-specificity screening and risk analysis are discussed.

Balciunas J.K. (2004). Are mono-specific agents necessarily safe? The need for pre-release assessment of probable impact of candidate biocontrol agents, with some examples. Proceedings of the XI International Symposium on Biological Control of Weeds: 252-257
Biosafety is now often considered more important than efficacy. However, even a highly specific agent can have unpredictable adverse impacts especially if it becomes abundant on the target, but fails to reduce target weed populations. However, pre-release consideration of the proposed agent's probable efficacy is receiving increased attention. This is usually done overseas, in the native range of both the target weed and candidate agent and approaches used are reviewed. Pre-release impact assessments can also be performed in quarantine. The results of two "dosage" trials conducted with a gall-making fly that is being considered as a biological control agent for Cape ivy (Delairea odorata) are described. Plants exposed to both low and high densities of gall flies, were smaller, and had fewer leaves than the ungalled controls. Pre-release evaluations of a candidate agent's potential impact should lead to fewer ineffective agents being released, thereby making weed biocontrol more efficient, and reducing the possibility of negative indirect impacts on non-targets.

Berner D.K. (2010). BLUP, a new paradigm in host-range determination. Biological Control 53: 143-152
There has been increased focus on modernizing the approach from centrifugal phylogenetic testing to basing selection of test plants on molecular phylogeny rather than taxonomic classification. Mixed model equations (MME) and best linear unbiased predictors (BLUPs) have been used to determine the probable host-range of plant pathogens proposed for biological control of Russian thistle. The work focuses on evaluating disease severity on related plant species although the author describes how MME can be used with any biological weed control agent or target as long as the evaluation criterion is quantitative and variances and molecular genetic relationships among test species can be obtained. The author's objectives are to familiarize biological control researchers and regulators with some of the requirements and advantages of the MME and the use of the MME to construct test plant lists.

Blossey B. (1995). Host specificity screening of insect biological control agents as part of an environmental risk assessment. Pp. 84-89 In: Biological Control: Benefits and Risks, H.M.T. Hokkanen and J.M. Lynch (Ed.) Cambridge University Press, Cambridge, UK.

Blossey B. and Skinner L. (2000). Design and importance of post-release monitoring. Pp. 693-706 In: Proceedings of the X International Symposium on Biological Control of Weeds, N.R. Spencer (Ed.)

Briese D.T. and Walker A. (2008). Choosing the right plants to test: The host-specificity of Longitarsus sp (Coleoptera : Chrysomelidae) a potential biological control agent of Heliotropium amplexicaule. Biological Control 44: 271-285
Using the case of the root-feeding flea beetle, Longitarsus sp., a candidate agent for biological control of Heliotropium amplexicaule in Australia, this paper describes a new protocol, based on phylogeny, and refined by ecological and biogeographic similarities. Taxonomic nomenclature is de-emphasized in favour of strict phylogenetic relationships and the use of so-called "safeguard species" is abandoned. The testing showed that adult feeding extended to plant species with up to five degrees of phylogenetic separation from H. amplexicaule, indicating that there would be a moderate risk that more distantly related plants suffer some feeding damage by adult Longitarsus sp. when they co-occur with infestations of the target weed that have large flea-beetle populations. Longitarsus sp. was able to complete its life-cycle on plants related to the target weed by two degrees of phylogenetic separation or less, leaving indigenous Heliotropium and Tournefortia species at some risk of colonisation. While these species had different life-histories and/or only slightly overlapped with the actual and potential range of the target weed, a minority of reviewers were concerned that insufficient information was available on the dispersal abilities of Longitarsus sp. to dismiss this risk. Release was therefore not approved, although this was not unexpected, as the assessment was based on factors that modified the effects of host range alone. The new protocols highlighted problems of an overreliance on taxonomic nomenclature as opposed to actual genetic relationships. However, they also directed attention to knowledge gaps in biogeography and agent biology that might refine the assessed risk.

Cagnotti C., Mc Kay F. and Gandolfo D. (2007). Biology and host specificity of Plectonycha correntina Lacordaire (Chrysomelidae), a candidate for the biological control of Anredera cordifolia (Tenore) Steenis (Basellaceae). African Entomology 15: 300-309
The paper described host range testing for Plectonycha correntina Lacordaire (Coleoptera: Chrysomelidae), a proposed biocontrol agent for the Neotropical perennial climber, Anredera cordifolia (Tenore) Steenis (Basellaceae), an environmental weed in Africa and Australasia. Larvae and adults feed on the leaves. The host range was evaluated by no-choice larval survival tests and adult feeding and oviposition choice tests using 16 test plant species. The results indicated that the host range of P. correntina is restricted to the Basellaceae, with A. cordifolia as its primary host, and so P. correntina was considered a safe and promising biocontrol agent for Madeira vine in countries such as Australia and New Zealand where no other Basellaceae occur.

Cullen J.M. (1989). Current problems in host-specificity screening. Pp. 27-36 In: Proceedings of the VII International Symposium on Biological Control of Weeds, E.S. Delfosse (Ed.) CSIRO Publications, Melbourne.

Cullen J.M. (1997). Biological control and impacts on non-target species. Pp. 195-201 In: Proceedings of the 50th New Zealand Plant Protection Conference, M. O'Callaghan (Ed.) New Zealand Plant Protection Society Inc.
Analysis of examples of non-target impacts of weed biological control agents suggested that in most cases impacts are limited, but the potential exists for serious impacts. A risk analysis approach is advocated. Lack of relevant research data is a major problem.

Day M.D. (1999). Continuation trials: their use in assessing the host range of a potential biological control agent. Pp. 11-19 In: Host specificity testing in Australasia: towards improved assays for biological control, T.M. Withers, L. Barton-Brown and J. Stanley (Ed.) CRC for Tropical Pest Management, Brisbane.

Dhileepan K., Lockett C.J., Balu A., Murugesan S., Perovic D.J. and Taylor D.B.J. (2015). Life cycle and host range of Phycita sp. rejected for biological control of prickly acacia in Australia. Journal of Applied Entomology 139: 800-812.

Gerber E., Hinz H.L., Blossey B. and Bacher S. (2004). Two shoot miners as potential biological control agents for garlic mustard: should both be released? Proceedings of the XI International Symposium on Biological Control of Weeds: 108-112
Two shoot-mining weevils, Ceutorhynchus alliariae and C. roberti, both potential biological control agents for Alliaria petiolata in North America, show high temporal and spatial niche overlap. The comparison of attack levels as an indirect estimate of their potential to damage garlic mustard showed that C. alliariae was equally as effective in attacking garlic mustard alone as in combination with C. roberti, infact under experimental conditions, C. alliariae alone reached higher infestation levels than the mixed species but did not result in a higher impact on garlic mustard. Replicated releases of different combinations of the two species would provide a unique opportunity to test the conclusions from our pre-release investigations.

Grosskopf G., Wilson L.M. and Littlefield J.L. (2008). Host-range investigations of potential biological control agents of alien invasive hawkweeds (Hieracium spp.) in the USA and Canada: an overview. Proceedings of the XII International Symposium on Biological Control of Weeds, La Grande Motte, France, 22-27 April, 2007. pp552-557
Several European Hieracium species, e.g. Hieracium caespitosum Dumort. and Hieracium aurantiacum L., are noxious weeds in North America. A project for the biological control of alien invasive hawkweeds has therefore been initiated in 2000. Five European insect species investigated before their release in New Zealand and two additional gall wasps have been tested on North American test plants. The stolon-tip galling cynipid, Aulacidea subterminalis Niblett (Hym., Cynipidae) proved to be the most specific candidate attacking four Hieracium spp. in the subgenus Pilosella. The authors describe the results of their host-specificity tests.

Hill R.L. (1999). Minimising uncertainty - in support of no-choice tests. Pp. 1-10 In: Host specificity testing in Australasia: towards improved assays for biological control, W.T.M., L. Barton Browne and J. N. Stanley (Ed.) CRC for Tropical Pest Management, Brisbane, Australia.

Marohasy J. (1998). The design and interpretation of host-specificity tests for weed biological control with particular reference to insect behaviour. Biocontrol News and Information 19: 13-20.
Current host specificity procedures are reviewed and a new procedure proposed that takes into account mechanisms known to underlie the behavioural process of host plant finding and acceptance. This minimizes the risk of rejection of safe insect species or the release of potentially unsafe insect species for weed biological control. The period of time between the acceptance of the target weed and lower-ranked plant species by candidate biological control agents, can also be determined. This period may be as important a measure of specificity as the actual number of plant species susceptible to attack.

McEvoy P.B. (1996). Host specificity and biological pest control. BioScience 46: 401-405.
This review of host specificity and biological pest control is set out under the following headings: biological control organisms used to control weeds; biological control organisms used to control arthropods; and other aspects of biological control.

Olckers T. and Borea C. (2009). Assessing the risks of releasing a sap-sucking lace bug, Gargaphia decoris , against the invasive tree Solanum mauritianum in New Zealand. BioControl 54: 143-154
The South American tree Solanum mauritianum Scopoli (Solanaceae), a major environmental weed in South Africa and New Zealand, has been targeted for biological control, with releases of agents restricted to South Africa. The leaf-sucking lace bug, Gargaphia decoris Drake (Tingidae), has become established in South Africa with reports of severe damage. Host-specificity testing was carried out in South Africa in laboratory and open-field trials, with cultivated and native species of Solanum from New Zealand showed that none of the three native New Zealand Solanum species are acceptable as hosts. Some cultivars of S. melongena L. (eggplant) supported feeding, development and oviposition in the no-choice tests. Field trials and risk assessment indicate that the insect has a host range restricted to S. mauritianum. An application for permission to release G. decoris in New Zealand will be submitted to the regulatory authority.

Sheppard A.W., Van Klinken R.D. and Heard T.A. (2005). Scientific advances in the analysis of direct risks of weed biological control agents to nontarget plants. Biological Control 35: 215-226.
The strengths, weaknesses, and best practice for the different host specificity test types are now understood. Understanding the concept of fundamental host range and using this to maximize reliability in predicting field host specificity following release are still inconsistently understood or adopted. This needs to be consistently applied so the process of testing can follow a recognized process of risk analysis from hazard identification to uncertainty analysis based on the magnitude and likelihood of threats to non-targets. Modern molecular techniques are answering questions associated with subspecific variation in biological control agents with respect to host use and the chance of host shifts of agents following release. This review covers all these recent advances for the first time in one document, highlighting how inconsistent interpretation by biological control practitioners can be avoided.

Sime K.R., Daane K.M., Wang X.G., Johnson M.W. and Messing R.H. (2008). Evaluation of Fopius arisanus as a biological control agent for the olive fruit fly in California. Agricultural and Forest Entomology 10, 423-431.
The egg-prepupal parasitoid Fopius arisanus (Hymenoptera: Braconidae) was evaluated in quarantine facilities as a potential biological control agent for the olive fruit fly Bactrocera oleae (Diptera: Tephritidae) in California, U.S.A. F. arisanus will not attack Tephritidae that feed in inflorescences or galls but may pose risks to native Tephritidae that feed in fruit. The broad host-range of F. arisanus with respect to fruit-feeding Tephritidae may preclude its introduction to California, as may its low fecundity and its intrinsic competitive superiority over larva l-pupal parasitoids, which include specialists on B. oleae that are currently being introduced to California. High rates of direct mortality, however, point to potential uses in augmentative biological control.

Syrett P. (1996). Insects for biological control of broom (Cytisus scoparius) in New Zealand. Pp. 525-528 In: Proceedings of the 11th Australian Weeds Conference, Melbourne, Australia, 30 September - 3 October 1996, R. Shepherd (Ed.) Weed Science Society of Victoria Inc., Victoria, Australia.
A program to introduce insects for biological control of broom (Cytisus scoparius) in New Zealand began in 1981 and the progress in this programme is described.

Syrett P., Harman H.M. and Fowler S.V. (1995). Identification of risk to kowhai, a New Zealand native plant, Sophora microphylla Ait., from a potential biological control agent for broom, Cytisus scoparius (L.) Link. New Zealand Journal of Zoology 22: 305-309.

Vayssières J.F. and Wapshere A.J. (1983). Life-histories and host specificities of Ceutorhynchus geographicus (Goeze) and C. larvatus Schultze (Coleoptera: Curculionidae), potential biological control agents for Echium. Bulletin of Entomological Research 73: 431-440.

Vitou J., Skuhrava M., Skuhravy V., Scott J.K. and Sheppard A.W. (2008). The role of plant phenology in the host specificity of Gephyraulus raphanistri (Diptera: Cecidomyiidae) associated with Raphanus spp. (Brassicaceae). European Journal of Entomology 105: 113-119
Recent host records for Gephyraulus raphanistri (Kieffer), a flower-gall midge, indicate that it is restricted to Raphanus raphanistrum throughout Europe. This study tested host specificity of G. raphanistri in the field in Europe by manipulating host plant phenology of actual and potential hosts in the genera Raphanus and Brassica as part of a risk assessment of the insect as a potential biological control agent of R. raphanistrum, one of the most important weeds of crops in Australia. The high field specificity of this gall midge was shown to be driven by the synchrony of oviposition and flower availability, not host physiological incompatibility or behavioural unacceptability. Commercially grown brassicas are not suitable hosts because in the field they differ in flowering phenology from Raphanus raphanistrum. The overlap in the flowering phenology of the crop and weed in Australia makes this insect unsuitable as a biological control agent.

Wapshere A.J. (1974). A strategy for evaluating the safety of organisms for biological weed control. Annals of Applied Biology 77: 201-211.

Wapshere A.J. (1989). A testing sequence for reducing rejection of potential biological control agents for weeds. Annals of Applied Biology 114: 515-526.

Wheeler G.S., Mc Kay F., Vitorino M.D. and Williams D.A. (2013). Biology and host range of Omolabus piceus, a weevil rejected for biological control for Schinus terebinthifolius in the USA. Biocontrol 58: 693-702.

Withers T. and Barton-Browne L. (1998). Possible causes of apparently indiscriminate oviposition in host specificity tests using phytophagous insects. Pp. 565-571 In: Pest Management - Future Challenges: Proceedings of the 6th Australasian Applied Entomological Research Conference, M. Zalucki, R. Drew and G. White (Ed.) Brisbane, The Cooperative Research Centre for Tropical Pest Management.

Withers T.M. (1997). Changes in plant attack over time in no-choice tests: an indicator of specificity. Pp. 214-217 In: Proceedings of the 50th New Zealand Plant Protection Conference, M. O'Callaghan (Ed.) Lincoln University, NZ., New Zealand Plant Protection Society Inc.

Withers T.M. (1998). Influence of plant species on host acceptance behaviour of the biocontrol agent Zymogramma bocolorata (Col.: Chrysomelidae). Biological Control 13: 55-62.

Withers T.M., Potter K.J.B., Berndt L.A., Forgie S.A., Paynter Q.E. and Kriticos D.J. (2011). Risk posed by the invasive defoliator Uraba lugens to New Zealand native flora. Agricultural and Forest Entomology 13: 99–110.

Zwölfer H. and Harris P. (1971). Host specificity determination of insects for biological control of weeds. Annual Review of Entomology 16: 159-178.