Selecting biological control agents

Factors influencing host selection in the target range

Host finding cues and behaviour

Successful oviposition by either phytophagous insects or parasitoids follows host-searching behaviour that brings the female to the host. Parasitoids must locate hosts in a complicated and heterogeneous environment and on finding a possible host must make a range of reproductive decisions. The cues are often chemical stimuli emitted by the host insect and/or the host plant. Parasitoids tend to use the odour of invertebrate hosts only for short distance detection. While these direct stimuli are highly specific to the identity of the host, these make up only a small proportion of the biomass within the habitat, and so stimuli are difficult to detect at a distance. Instead, parasitoids often use chemicals associated with the host plant of the target, or the chemicals associated with insect damage to the host plant, insect saliva or insect frass to orient over longer distances. These indirect stimuli are easier to detect, but less reliable as an indicator of the presence of the true host. Turlings et al. (1991) found that these tritrophic stimuli engendered stronger behavioural responses in Cotesia marginiventris than the presence of its host. The response of parasitoids to mixtures of volatiles from plant and host can be complex.

The variety of behavioural cues seems endless. Some parasitoids orient to host pheromones (Godfray 1994), whereas Megarhyssa spp. react to stimuli from the fungus always associated with Sirex larvae, but not to the host larva itself (Spradberry 1970). Physical limitations such as size of nest hole can also influence which hosts are available to a parasitoid (Sands and Van Driesche 2004).

Godfray (1994) divides research into host location by parasitoids into two schools:

behavioural mechanisms or physiology: this approach has successfully revealed the complexity of the cues used in host location, how these can vary, and the importance of learning;
behavioural ecology: optimal foraging theory predicts feeding behaviour on the assumption of optimisation by natural selection.

Others (Vet and Dicke 1992) moved on from the concept of a 'hierarchy' of stimuli leading to parasitism (Vinson 1998) and proposed that a newly emerged parasitoid has a range of innate 'response potentials' to different stimuli and at any one time will respond to the stimulus with the greatest response potential. This makes response to hosts variable depending on where the parasitoid is, and sometimes otherwise strong behaviours might be bypassed. The response potentials can vary with experience, so that older parasitoids may respond differently from those that are newly emerged, and may differ depending on where the parasitoid finds itself. Responses vary with previous experience and between individuals and populations, on different plant hosts, and even with presence of other parasitoids. Many examples illustrate the extreme flexibility many parasitoids possess in the incorporation of new stimulus responses into their behavioural repertoire. The frass or cocoon of a Microplitis croceipes entrains the host-finding behaviour of the emerging adult, while other parasitoids are unaffected by their larval environment. This ability of parasitoids to learn the characteristics of their development site in this way is a means by which information can be inherited non-genetically � a form of cultural transmission (Godfray 1994). Once a host is found, parasitoids use a variety of optimal foraging strategies and patch leaving rules (Godfray 1994).

These are just a few of the myriad examples of how parasitoid behaviour can vary not only between but within species. Examples illustrate the extreme flexibility many parasitoids possess in the incorporation of new stimulus responses into their behavioural repertoire. Understanding how the candidate parasitoid behaves in different habitats and in different assemblages is important to the design and interpretation of reliable host range tests. Although difficult to design, oviposition tests should strive to include host-finding as well as host-acceptance behaviour (Barratt 2004, van Driesche and Murray 2004, Babendreier et al. 2005). The design of host range tests for parasitoids is discussed elsewhere.

For some parasitoids oviposition occurs away from the host stage. For example, the planidia and triungulin larvae of parasitic Diptera are either ingested by the foraging larva or are actively carried to the host. These agents are rare in biological control programmes and their behaviour is not discussed here.

It is tempting to think that predatory arthropods have a wider host range and therefore have less complex host-finding mechanisms. However, some coccinellids are relatively host specific, and may well be governed by similarly complex interactions. Causton (2004) noted reports that Icerya purchasi Maskell sequesters different alkaloids from different host plants, and this leads to different developmental performance in its predator Rodolia cardinalis Mulsant.

References

Babendreier D., Bigler F. and Kuhlmann U. (2005). Methods Used to Assess Non-target Effects of Invertebrate Biological Control Agents of Arthropod Pests. BioControl 50: 821-870.

Barratt B.I.P. (2004). Microctonus parasitoids and New Zealand weevils: comparing laboratory estimates of host ranges to realized host ranges. Pp. 103-120 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.

Causton C.E. (2004). Predicting the field host range of an introduced predator, Rodolia cardinalis Mulsant, in the Galapagos. Pp. 195-239 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

Godfray H.C.J. (1994). Parasitoids: Behavioural and Evolutionary Ecology. Princeton University Press, Princeton. 473 pp.

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.

Spradberry P. (1970). Host finding by Rhyssa persuasoria L. an ichneumon parasite of siricid woodwasps. Animal Behaviour 18: 103-114

Turlings T.C.J., Tumlinson J.H., Heath R.R., Proveaux, A.T. and Doolittle R.E. (1991). Isolation and identification of allelochemicals that attract the larval parasitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts. Journal of Chemical Ecology 17: 2235-2251

van Driesche R.G. and Murray T.J. (2004). Overview of testing schemes and designs used to estimate host ranges. Pp. 68-89 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.

Vet L.E.M. and Dicke M. (1992). Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37: 141-172

Vinson S.B. (1998). The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biological Control 11: 79-96