Environmental risks of biological control
Non-target impacts can be very complex and unpredictable. A good example of this is the extinction of the large blue butterfly, Maculinea arion (L.) partly attributable to the biological control of rabbits in the UK using the myxoma virus (Wells et al. 1983). The butterfly larvae live in ants nests and feed on the brood of Myrrmica ants. Changing land use coupled with the rapid decline of rabbits in the UK caused many grassland habitats to revert to scrub with loss of suitable habitat for the ants. In New Zealand, the introduced braconid wasp, M. aethiopoides attacks several non-target weevil species including native broad-nosed weevils (Barratt et al. 2000). In native grassland sown with legumes to improve soil fertility, these weevils can cause severe damage to the developing legume seedlings. While parasitism by M. aethiopoides could be considered an added benefit, the native weevils are also weed seedling feeders and may play a role in controlling the seedling establishment of Hieracium (hawkweed), a serious agricultural and conservation weed in native grassland (Evans et al. 1994).
Biological control of weeds is generally assessed to be low risk if they do not directly attack non-target species, however, by evaluation of case studies Pearson and Callaway (2005) found that indirect effects can be demonstrated in some cases. They found that while difficult to predict, indirect non-target effects of host specific biological control agents were proportional to the biological control agents abundance, which was higher for moderately successful agents than those which were highly successful. They concluded that the most low-risk biological control agents are both highly effective, and host specific. Holt and Hochberg (2001) similarly concluded from their theoretical models that a biological control agent which is only moderately effective in controlling abundance of the target may be more abundant, and hence pose a greater risk to non-target species than a highly effective biological control agent. Clearly a case-by case analysis of risk is essential.
Another approach to investigating indirect effects of biological control agents has been the construction of food webs. Willis and Memmott (2005) used a weed biological control example to show that food webs can be used to demonstrate indirect effects of biological control agents. In the particular case discussed, the biological control agent served to increase the abundance, and change the community structure, of native parasitoids.
Another example, described in detail by Barratt et al. (2006) of unexpected indirect effects comes from weed biological control. A number of biological control agents were introduced into North America for Centaurea maculosa Lamarck (spotted knapweed) control. Two tephritid flies, Urophora quadrifasciata (Meigen) and Urophora affinis Frauenfeld became widespread and abundant, and the larvae overwinter in the galled flower heads until they pupate and emerge in the spring. This food resource has attracted the deer mouse, Peromyscus maniculatus which can consume several hundred Urophora larvae/day constituting >80% of its diet. Mouse populations have increased up to 3-fold and over-winter mortality of mice is greatly reduced in the presence of knapweed. However, a major concern raised by this indirect effect on deer mice is that they are the main carrier of Sin Nombre hantavirus, which can cause significant human mortality.
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.
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.
Evans A.A., Barratt B.I.P. and Ferguson C.M. (1994). Susceptibility of legume and Hieracium spp. seedlings to feeding by native broad-nosed weevils (Coleoptera: Curculionidae). Pp. 206-209 In: Proceedings of the 47th New Zealand Plant Protection Conference, A.J. Popay (Ed.) Waitangi Hotel, Pahia, N.Z., New Zealand Plant Protection Society Inc.
Holt R.D. and Hochberg M.E. (2001). Indirect interactions, community modules and biological control: a theoretical perspective. Pp. 13-37 In: Evaluating indirect ecological effects of biological control, E. Wajnberg, J. K. Scott and P. C. Quimby (Ed.) CABI Publishing, Wallingford, Oxon., UK
Pearson D.E. and Callaway R.M. (2005). Indirect nontarget effects of host-specific biological control agents: Implications for biological control. Biological Control 35: 288-298.
Wells S.M., Pyle R.M. and Collins N.M. (1983). Large blue butterflies. Pp. 451-457 In: The IUCN invertebrate red data book, (Ed.) International Union for Conservation of Nature and Natural Resources, Gland, Switzerland.
Willis A.J. and Memmott J. (2005). The potential for indirect effects between a weed, one of its biocontrol agents and native herbivores: A food web approach. Biological Control 35: 299-306.
Reducing the risk