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Annotated bibliography

Pre-release prediction of host range and non-target impacts


Barratt B.I.P., Evans A.A., Ferguson C.M., McNeill M.R., Proffitt J.R. and Barker G.M. (1998). Curculionoidea (Insecta: Coleoptera) of agricultural grassland and lucerne as potential non-target hosts of the parasitoids Microctonus aethiopoides Loan and Microctonus hyperodae Loan (Hymenoptera: Braconidae). New Zealand Journal of Zoology 25: 47-63.
The paper describes a survey of the weevil fauna of pasture, lucerne and modified native grassland in parts of the southern South Island, Canterbury and the northern North Island of New Zealand, where the parasitoids Microctonus spp. are present to identify weevils with taxonomic and ecological affinities with the target hosts, and hence, potential non-target hosts.

Barratt B.I.P., Goldson S.L., Ferguson C.M., Phillips C.B. and Hannah D.J. (2000). Predicting the risk from biological control agent introductions: A New Zealand approach. Pp. 59-75 In: Nontarget effects of biological control introductions, P.A. Follett and J.J. Duan (Ed.) Kluwer Academic Publishers, Norwell, Massachusetts, USA.

Barratt BIP, Oberprieler RG, Barton D, Mouna M, Stevens M, Alonso-Zarazaga MA, Vink CJ and Ferguson CM. (2012). Could research in the native range, and non-target host range in Australia, have helped predict host range of the parasitoid Microctonus aethiopoides Loan (Hymenoptera: Braconidae), a biological control agent introduced for Sitona discoideus Gyllenhal (Coleoptera: Curculionidae) in New Zealand? Biocontrol 57: 735-750.

Casas J., Swarbrick S. and Murdoch W.W. (2004). Parasitoid behaviour: predicting field from laboratory. Ecological Entomology 29: 657-665.
The basic components of Aphytis melinus's response to California red scale (Aonidiella aurantii) were studied in the laboratory and validated in the field. Laboratory studies predicted foraging behaviour in the field with variable success; potential explanations for observed mismatch between laboratory and field and its possible larger implications are discussed.

Field R.P. and Darby S.M. (1991). Host specificity of the parasitoid, Sphecophaga vesparum (Curtis) (Hymenoptera: Ichneumonidae), a potential biological control agent of the social wasps, Vespula germanica (Fabricius) and V. vulgaris (Linnaeus) (Hymenoptera: Vespidae) in Australia. New Zealand Journal of Zoology 18: 193-197
Choice, non-choice, and host location tests using Sphecophaga vesparum indicated that brood of some Australian native Polistes, Ropalidia, and Trigona species would not be at risk from releases of the parasitoid in Australia. S. vesparum was approved for release in Australia and released in metropolitan Melbourne (Victoria) in December 1989, to act as a biological control agent against Vespula species

Fowler S.V., Barreto R., Dodd S., Macedo D.M., Paynter Q., Pedrosa-Macedo J.H., Pereira O.L., Peterson P., Smith L.Waipara N., Winks C.J. and Forrester G. (2013). Tradescantia fluminensis, an exotic weed affecting native forest regeneration in New Zealand: Ecological surveys, safety tests and releases of four biocontrol agents from Brazil. Biological Control 64: 323-329.

Gariepy T., Kuhlmann U., Gillott C. and Erlandson M. (2008). A large-scale comparison of conventional and molecular methods for the evaluation of host-parasitoid associations in non-target risk-assessment studies. Journal of Applied Ecology 45: 708-715
Host rearing and dissection are used to define the ecological host range of candidate biological control agents and assess host-specificity of parasitoids, however, molecular methods may also be useful, e.g. Lygus plant bugs, host rearing, dissection and multiplex polymerase chain reaction (PCR) analysis were compared for estimation of parasitism levels and parasitoid species composition in field-collected target and non-target Miridae. Parasitism levels estimated by conventional and molecular methods were similar but molecular analysis could detect parasitoids earlier than dissection and rearing. Molecular methods can provide more complete, parasitoid species composition information because the results are not confounded by the host and parasitoid mortality encountered in rearing. However, detection of a parasitoid in a host does not necessarily indicate survival to the adult stage. Beyond agent identification, molecular diagnostics can facilitate and expedite pre- and post-release studies on the ecological host range of parasitoids, potential non-target effects, host-parasitoid associations and trophic interactions.

Gassmann A., Tosevski I. and Skinner L. (2008). Use of native range surveys to determine the potential host range of arthropod herbivores for biological control of two related weed species, Rhamnus cathartica and Frangula alnus. Biological Control 45: 11-20
The buckthorn species, Rhamnus cathartica and Frangula alnus have become invasive in North America. The key question for biocontrol of teghse species was whether they are distantly enough related that they would not share the same arthropod complex in Europe, and, if so, which arthropod species would be less likely to use native North American buckthorns as hosts. Sampling in Europe indicated that the arthropod-species richness is higher on R. cathartica than on F. alnus and includes more species that are presumed to be host-specific at the species or genus level. At least 12 arthropod species were found exclusively on Rhamnus, some of which may be specific to R. cathartica and only one species was found exclusively on F. alnus.

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.

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.

Haye T., van Achterberg C., Goulet H., Barratt B.I.P. and Kuhlmann U. (2006). Potential for classical biological control of the potato bug Closterotomus norwegicus (Hemiptera: Miridae): description, parasitism and host specificity of Peristenus closterotomae sp. n. (Hymenoptera: Braconidae). Bulletin of Entomological Research 96: 421�431
The potato bug, Closterotomus norwegicus (Gmelin) (Hemiptera: Miridae) is an introduced pest of lucerne, white clover and lotus seed crops in New Zealand and a key pest of pistachios in California, USA. A total of eight parasitoids, including six from the genus Peristenus (Hymenoptera: Braconidae) and two hyperparasitoids from the genus Mesochorus (Hymenoptera: Ichneumonidae), were reared from C. norwegicus nymphs collected in northern Germany. With a proportion of more than 85% of all C. norwegicus parasitoids, Peristenus closterotomae (Hymenoptera: Braconidae), a new species, was the most dominant parasitoid, whereas other parasitoid species only occurred sporadically. Parasitism caused by P. closterotomae was on average 24% (maximum 77%). To assess the host specificity of parasitoids associated with C. norwegicus, the parasitoid complexes of various Miridae occurring simultaneously with C. norwegicus were studied. Peristenus closterotomae was frequently reared from Calocoris affinis (Herrich-Schaeffer), and a few specimens were reared from Calocoris roseomaculatus (De Geer) and the meadow plant bug, Leptopterna dolobrata (Linnaeus) (all Hemiptera: Miridae). The remaining primary parasitoids associated with C. norwegicus were found to be dominant in hosts other than C. norwegicus. Whether nymphal parasitoids may potentially be used in a classical biological control initiative against the potato bug in countries where it is introduced and considered to be a pest is discussed.

Hopper K.R. and Wajnberg E. (2006). The risks of interbreeding and methods for determination. In press In: Environmental Impact of Arthropod Biological Control: Methods and Risk Assessment, U. Kuhlmann, F. Bigler and D. Babendreier (Ed.) CABI Bioscience, Delemont, Switzerland.

Kimberling D.N. (2004). Lessons from history: predicting successes and risks of intentional introductions for arthropod biological control. Biological Invasions 6: 301-318.
The US National Invasive Species Management Plan (2001) calls for better screening methods for biological control agent introductions. Literature searches were used to develop a database of 13 life history traits and 8 descriptive variables for 87 insect biological control species in the United States. Models for predicting success in controlling a target species and likelihood of nontarget effects were developed using logistic regression. The most important life history traits for predicting success included host specificity, whether the agent was a predator or parasitoid, and number of generations per year. Traits important for predicting nontarget effects included sex ratio of progeny and the presence of native natural enemies.

Kuhlmann U., Mason P.G. and Greathead D.J. (1998). Assessment of potential risks for introducing European Peristenus species as biological control agents of native Lygus species in North America: a cooperative approach. Biocontrol News and Information 19: 83n-90n.
The pest status of Lygus species in North America and history of European collections and importations of Peristenus species into North America is described. Strategies and methods for host specificity testing of parasitoids are outlined and discussed in relation to the selection of non-target and native Lygus species for testing with Peristenus parasitoids. European Peristenus species are identified and their life histories outlined. It is concluded that cooperative research in Europe and North America is needed to assess the potential risks for the introduction of European Peristenus species for control of Lygus species in North America.

Lockwood J.A. (1993). Environmental issues involved in biological control of rangeland grasshoppers (Orthoptera: Acrididae) with exotic agents. Environmental Entomology 22: 504-518.
Neoclassical biological control with a parasitic wasp and an entomophagous fungus from Australia is now being applied to rangeland grasshoppers in the western USA, and it is predicted that there may be a number of possible nontarget impacts. Adverse effects include competitive suppression or extinction of both native biological control agents and nontarget acridids. Suppression of nontarget acridids may result in loss of biological diversity, existing control of weed species, release of otherwise innocuous acridid species from competitive regulation, disruption of plant community structure, suppression of essential organisms vectored by grasshoppers, and disruption of food chains and other nutrient cycling processes. Given that the value of the rangeland resource depends on the largely unknown ecological processes that underlie its sustainable productivity, there are a number of management techniques that offer a greater probability of success with a markedly lower likelihood of ecological and economic disruption than does neoclassical biological control.

Loomans A. and Van Lenteren J.C. (2005). Tools for environmental risk assessment of invertebrate biological control agents: a full and quick scan method. Pp. 611-619 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 International Standard for Phytosanitary Measures No. 3 (ISPM3) offers a framework for risk assessment and focuses specifically on the shipment, import, export and release of biological control agents. The major challenge in developing risk assessment methodologies is to develop protocols and guidelines that will prevent serious mistakes through import and release of potentially harmful exotics, while at the same time still allowing safe forms of biological control to proceed. A risk assessment methodology for biological control agents should integrate information on the potential of an agent to establish, its abilities to disperse, its host range and its direct and indirect effects on non-targets. A comprehensive risk evaluation method (full scan) for new natural enemies is proposed and, 'quick scan' method for natural enemies already in use.

McPartland J.M. and Nicholson J. (2003). Using parasite databases to identify potential nontarget hosts of biological control organisms. New Zealand Journal of Botany 41: 699-706
The authors propose that biocontrol researchers use internet-available databases to identify potential nontarget organisms that share parasites (biotrophic pathogens and pests) with target hosts, and add these organisms to test species lists. Marijuana (Cannabis sativa) has been targeted for biocontrol, and host range studies have focused upon the Moraceae. A list of Cannabis parasites was compared with database lists of pests and pathogens for hosts in the order Urticales. The databases revealed seven Cannabis biotrophic parasites that were shared by hosts in the family Urticaceae, one biotroph shared by a host in the Celtidaceae, and no biotrophs shared by hosts in the Moraceae, Cercropiaceae, or Ulmaceae. These results suggest that biocontrol host range studies of Cannabis parasites should focus on the Urticaceae and Celtidaceae as well as the Moraceae and that taxonomic relationships within the Uricales be reassessed.

Raghu S., Dhileepan K. and Scanlan J.C. (2007). Predicting risk and benefit a priori in biological control of invasive plant species: A systems modelling approach. Ecological Modelling 208: 247-262
In this study a simulation model is used to predict the risks and benefits of introducing the chrysomelid beetle Charidotis auroguttata to manage the invasive liana Macfadyena unguis-cati in Australia. Preliminary host-specificity testing of this herbivore indicated that there was limited feeding on a non-target plant, although the non-target was only able to sustain some transitions of the life cycle of the herbivore. The model included herbivore, target and non-target life history and incorporates spillover from the target to the non-target. The model predicted that risk to the non-target became unacceptable when the ratio of target to non-target in a given patch ranged from 1:1 to 3:2. By considering risk and benefit simultaneously, we highlight how such a simulation modelling approach can assist in making more objective decisions on the value of releasing specialist herbivores as biological control agents.

Sands D.P.A. and Van Driesche R.G. (2004). Using the scientific literature to estimate the host range of a biological control agent. Pp. 15-23 In: Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice, R.G. Van Driesche and R. Reardon (Ed.) USDA Forest Service, Morgantown, West Virginia.

Sheppard A.W. (1992). Predicting biological weed control. Trends in Ecology & Evolution 7: 290-291.

Solter L.F. and Maddox J.V. (1998). Physiological host specificity of Microsporidia as an indicator of ecological host specificity. Journal of Invertebrate Pathology 71: 206-216.

Taylor D.B.J., Heard T.A. and Jacob H.S. (2004). How effective is host testing at predicting non-target impacts of weed biological control agents in Australia? Pp. 91-94 In: 14th Australian Weeds Conference: Weed management: balancing people, planet, profit, B. M. Sindel and S. B. Johnson (Ed.) Wagga Wagga, New South Wales, Australia, 6-9 September 2004

Uygur S., Smith L.A., Uygur F.N., Cristofaro M. and Balciunas J.K. (2005). Field assessment in land of origin of host specificity, infestation rate and impact of Ceratapion basicorne a prospective biological control agent of yellow starthistle. BioControl 50: 525-541.

van Driesche R.G., Bellows T.S., Jr., Elkinton J.S., Gould J.R. and Ferro D.N. (1991). The meaning of percentage parasitism revisited: solutions to the problem of accurately estimating total losses from parasitism. Environmental Entomology 20: 1-7.
New analytical methods for obtaining stage-specific estimates of losses from parasitism for life-table, population dynamics, and evaluation studies are needed. Solutions considered include recruitment, stage frequency and death rate analyses. The rationale and methodology are presented and their usefulness for systems of varying types of biologies and sampling constraints is compared.

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.

Wheeler G.S., Pemberton R.W. and Raz L. (2007). A biological control feasibility study of the invasive weed-air potato, Dioscorea bulbifera L. (Dioscoreaceae): an effort to increase biological control transparency and safety. Natural Areas Journal 27: 269-279
The invasive weed Dioscorea bulbifera L. threatens the biodiversity of many natural areas in the southeastern United States. The authors propose that this weed will be a relatively safe target for biocontrol because of taxonomic and geographic isolation from desirable native and economic plant species. The family Dioscoreaceae is poorly represented in North America, north of Mexico, and the two native species that are sympatric with the weed are from a different subgeneric taxon than the weed. The West Indian and northern Mexican species, while more diverse, are also assigned to different subgeneric taxa, and are geographically isolated from the northern range of the weed. Further research pre-release needs to better delimit the geographic origin of the weed's North American population within its large native range to aid in the detection of suitable natural enemies. This will ensure that potential conflicts and risks can be judged and addressed during the projects to ultimately produce safer, more acceptable agents for biological control.