Biocontrol Science and Technology, Vol. 19, S1, 2009, 3Á22 REVIEW ARTICLE Improving the cost-effectiveness, trade and safety of biological control for agricultural insect pests using nuclear techniques Jorge Hendrichsa*, Kenneth Bloemb, Gernot Hochc, James E. Carpenterd, Patrick Greanye, and Alan S. Robinsona aJoint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture, International Atomic Energy Agency, Wagramerstrasse 5, A-1400 Vienna, Austria; bCenter for Plant Health Science & Technology (CPHIST), USDA-APHIS-PPQ, 1730 Varsity Drive, Suite 400, Raleigh, NC 27606, USA; cDepartment of Forest and Soil Sciences, BOKU Á University of Natural Resources and Applied Life Sciences, Vienna Hasenauerstrasse 38, A-1190 Vienna, Austria; dUSDA-ARS Crop Protection and Management Research Unit, Tifton, GA 31793, USA; e2770 Pine Ridge Road, Tallahassee, FL 32308, USA If appropriately applied, biological control offers one of the most promising, environmentally sound, and sustainable control tactics for arthropod pests and weeds for application as part of an integrated pest management (IPM) approach. Public support for biological control as one of the preferred methods of managing non-indigenous and indigenous pests is increasing in many countries. An FAO/ IAEA Coordinated Research Project (CRP) addressed constraints related to costly production systems for biological control agents, and the presence of accompanying pest organisms during their shipment. These constraints can be alleviated using nuclear techniques such as ionizing radiation or X-rays to reduce production and handling costs (e.g., by expanding the period of host suitability, increasing shelf life, avoiding unnecessary sorting steps before shipment, etc.), and to eliminate the risk of shipping fertile host or prey pest individuals or other hitchhiking pests. These nuclear techniques can also help to reduce the risks associated with the introduction of exotic biological control agents, which can become pests of non-target organisms if not carefully screened under semi-natural or natural conditions. Radiation is also a very useful tool to study host-parasitoid physiological interactions, such as host immune responses, by suppressing Downloaded By: [Hendrichs, Jorge] At: 16:18 4 November 2009 defensive reactions of natural or factitious hosts. Applied at a very low-dose, radiation may be used to stimulate reproduction of some entomophagous insects. Additionally, radiation can be applied to semi- or completely sterilize hosts or prey for deployment in the field to increase the initial survival and build-up of natural or released biological control agents in advance of seasonal pest population build-up. Finally, the work carried out under this CRP has demonstrated the feasibility of integrating augmentative and sterile insect releases in area-wide IPM programmes, and to utilise by-products from insect mass- rearing facilities in augmentative biological control programmes. This special issue provides an overview of the research results of the CRP. Keywords: biological control; radiation; biocontrol agents; weeds; irradiated host; prey; insects; nematodes; parasitoids; sterile insects; sterile insect technique; inherited sterility; F1 sterility *Corresponding author. Email: [email protected] First Published Online 18 June 2009 ISSN 0958-3157 print/ISSN 1360-0478 online # 2009 Taylor & Francis DOI: 10.1080/09583150902985620 http://www.informaworld.com 4 J. Hendrichs et al. Introduction Many pests, including arthropods and weeds, adversely affect agricultural produc- tion, and pre- and post-harvest losses of the order of 30Á40% are common (Yudelman, Ratta, and Nygaard 1998). Management of these pests still relies heavily on the use of pesticides with their associated limitations. For these reasons there is pressure to develop improved methods of pest control, with an emphasis on biologically and ecologically based tactics that can be applied as part of an area-wide integrated pest management (AW-IPM) approach (Vreysen, Robinson, and Hen- drichs 2007). If appropriately applied, biological control offers one of the most promising, environmentally sound, and sustainable tools for control of arthropod pests and weeds (van Lenteren, Bale, Bigler, Hokkanen, and Loomans 2006; van Driesche, Hoddle, and Center 2008). Public support for biological control as one of the preferred methods of managing non-indigenous and indigenous pests is increasing in many countries. There appear to be significant opportunities for increasing the use and cost-effectiveness of the application of classical and augmentative biological control through nuclear techniques for the production, shipping and release of biological control agents. Nuclear techniques are already applied in certain areas of entomology (Bakri, Heather, Hendrichs, and Ferris 2005a) and include the use of radiation sources for (1) studying sperm precedence, parasitoidÁhost interaction studies, etc., (2) post-harvest disinfestation for quarantine or phytosanitary security in support of agricultural international trade (IDIDAS 2004), and (3) insect sterilization as part of the application of the Sterile Insect Technique (SIT) (Dyck, Hendrichs, and Robinson 2005), where exposure to carefully selected irradiation doses of gamma or X-rays maximizes the induction of dominant lethal mutations in germ cells of pest insects, while minimizing other physiological changes (Bakri, Mehta, and Lance 2005b). Nuclear techniques in a wider sense also include the use of stable isotopes to study insect biology, behaviour, and physiology (IAEA 2009), although their use in biological control will not be considered here. In classical biological control, non-indigenous biological control agents, usually selected from the suite of parasitoids, predators and diseases that co-evolved with the pest, are introduced into the target area. One of the key concerns in this approach is Downloaded By: [Hendrichs, Jorge] At: 16:18 4 November 2009 the host specificity and host range of the introduced biological control agents. There are numerous examples of situations where introduced biological control agents have ‘jumped hosts’ (Follet and Duan 2000; Lockwood, Purcell, and Howarth 2001; Wajnberg, Scott and Quimby 2001), prompting some serious criticisms of this control method (Hamilton 2000; Louda, Pemberton, Johnson, and Follett 2003). In view of the growing awareness and concern, countries and their respective national plant protection organizations are increasingly implementing stringent environmen- tal risk assessment methods in order to screen potential biological control agents before release (van Lenteren et al. 2006). In cases where doubts remain about very promising natural enemies of weeds or insect pests, the release of such biological control agents that have been radiation-sterilized would enable a more definite and safe assessment of host specificity under natural conditions without any risk of permanent establishment. Inundative biological control involves the use of indigenous or non-indigenous biological control agents against indigenous or non-indigenous pests. These control Biocontrol Science and Technology 5 agents generally do not establish permanently, often because of adverse seasonal eco- climatic conditions in the area of introduction, and are mass-reared and released in very large numbers, often several times each season. Though the commercial biological control agent industry is growing, it still only represents a niche market with less than 3% of pest control sales (Cornell 2007). Regulatory, technical and other constraints on biological control have kept the market share relatively small. Challenges facing augmentative biological control include the high cost of production of biological control agents, adequate quality control and assurance, trade barriers and regulations that complicate shipping. Lack of enabling regulations probably has been amongst the most important barriers to the wider implementation of biological control globally. Appropriate regulations are needed that facilitate the importation and use of natural enemies. In many countries, ‘gatekeeper’ regulations place barriers in the way of efficient introduction of agents. However, the Secretariat of the International Plant Protection Convention, at the Food and Agriculture Organization of the United Nations (FAO) has developed and recently revised the International Standard for Phytosanitary Measures on ‘Guidelines for the export, shipment, import, and release of biological control agents and other beneficial organisms’ (ISPM No. 3) (FAO 2005), which should help to solve some of these problems and therefore increase cross-boundary trade in biological control agents. There are several ways in which nuclear techniques can improve the efficiency of augmentative biological control and the Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture initiated a 6-year Coordinated Research Project (CRP) entitled ‘Evaluating the Use of Nuclear Techniques for the Colonization and Production of Natural Enemies of Agricultural Insect Pests’ (Greany and Carpenter 1999) to address some of these aspects. For example, the cost of production may be decreased by simplifying the rearing process, increasing host suitability and shelf life, improving diets and dealing with disease and contamination. Possible trade barriers related to shipment of biological control agents include the accidental inclusion of fertile pest individuals or other hitchhikers, or the deliberate inclusion