Augmentation Biological Control

Microorganisms have been more amenable to laboratory culture and manipulation than arthropod natural enemies. As a result, most larger-scale commercial ventures into utilizing natural enemies have employed microorganisms, their genes, or gene products for development of bio-pesticides or transgenic crops. However, a small but growing industry has developed around the use of arthropods for augmentation biological control, and implementation of augmentation has increased significantly in recent years.

The augmentation of natural enemies is a practice that is widely recognized by the general public in the U.S. mainly as a result of widespread availability of arthropod natural enemies such as lady beetles (especially Hippodamia convergens Guerin-Meneville) and mantids through garden catalogs and nurseries (Cranshaw et al., 1996). The industry providing these organisms has grown tremendously in the past 20 years. Ridgway and Vinson (1977) reported 50 North American suppliers of natural enemies, while Hunter (1992) reported 95 suppliers and 102 different organisms sold for biological control. More recently, Hunter (1997) reported 142 commercial suppliers and over 130 different species of beneficial organisms, of which 53 are arthropod predators and 46 are parasitoids. The categories of organisms listed by Hunter (1997) included 17 predatory mites, 4 stored product pest parasites and predators, 17 aphid parasites and predators, 9 whitefly parasites and predators, 23 parasites and predators for greenhouse pests, 7 scale and mealybug parasites and predators, 12 insect egg parasites, 6 moth and butterfly larval parasites, 8 filth fly parasites, 4 "other" insect parasites, and 21 general predators. Anonymous (1998) lists biological control products and companies that provide them worldwide. The suppliers listed by Hunter (1997) and Anonymous (1998) do not reflect the "coun-tertop" sales of organisms such as ladybeetles and mantids by many local nurseries and some large discount home-improvement centers. Annual sales of natural enemies in the U.S. amount to approximately $9-10 million (U.S. Congress OTA, 1995), and approximately $60 million worldwide (Leppla and King, 1996).

Augmentative releases of parasitoids and predators are currently included in a variety of pest management programs around the world (Leppla and King, 1996). Although natural enemies are sold for suppression of pests in several different systems (e.g., manure management, urban environments, stored product protection, pastures and forests), detailed estimates of implementation are readily available only for food cropping systems. In Europe, approximately 40-60,000 ha of orchard, vineyard, and vegetable crops are treated with natural enemies annually (Bigler, 1991). Approximately 5000 ha of greenhouses worldwide utilize some form of augmentative biological control (van Lenteren et al., 1997). In the U.S., augmentative releases of natural enemies take place on approximately 10% of greenhouses, 8% of nurseries, 19% of cultivated fruit and nut acreage, and 3% of the cultivated vegetable acreage (U.S. Congress OTA, 1995). On one high-value crop, strawberries, beneficial mites are used for spider mite suppression on approximately 50-70% of acreage in California alone (U.S. Congress OTA, 1995). Egg parasitoids in the genus Trichogramma are the most widely produced and released arthropods in augmentative biological control. These parasitoids have several advantages, including relative ease of rearing and the fact that they kill their host in the egg stage before it causes feeding injury (Wajnberg and Hassan, 1994). Worldwide, approximately 20 species of Trichogramma are regularly used in augmentative biological control programs to control primarily lepidopterous pests in at least 22 crops and trees on an estimated 32 million ha (Li, 1994). Most of these species are released in large numbers, i.e., inundative releases, in order to rapidly suppress the target pest.

Although the practice of augmenting parasitoids and predators for insect management has seen modest but notable implementation throughout the world during the past two decades, impediments to increased implementation remain. These include the continued need for development of economically viable large-scale rearing technology, a lack of experimental data for release strategies to provide more predictable results, and the need for widespread adoption of effective mechanisms to ensure consumers receive quality products that perform as advertised.

Efficient mass production systems are necessary for augmentation of arthropods to become more commonly accepted as a pest management tool (Nordlund and Greenberg, 1994). A variety of impediments to these systems include a lack of artificial rearing media and systems for efficient delivery of artificial media, limited automation, as well as the need for properly designed facilities, effective quality controls, and improved management systems (Nordlund and Greenberg, 1994). As technology develops, however, especially in regard to rearing, this form of biological control may become more widespread in the future (Hoy et al., 1991; Moffat, 1991; Parrella et al., 1992; Nordlund and Greenberg, 1994; Leppla and King, 1996; Nordlund et al., 1998).

Although augmentation has been shown to be effective against a variety of pests and cropping situations, there is a lack of clear experimental data that supports the use of many of the arthropod natural enemies currently on the market. An example of conflicting data involves a 'product' that has been on the market for decades, the lady beetle H. convergens. Use of this beetle has long been considered ineffectual mainly as a result of concerns over dispersal of beetles following release (DeBach and Hagen, 1964). Recently, however, Flint et al. (1995) demonstrated that although H. convergens dispersal does occur, significant reductions of aphid numbers could be obtained in potted roses. The lack of clear or sufficient efficacy data has led to commercial suppliers making recommendations for the use of some products based on limited or anecdotal evidence. This situation has in turn prompted some growers to experiment with products on their own in order to find strategies that work for their specific situation.

Because of the lack of supporting data for many augmentation approaches, recommendations still cannot be made regarding rates and application methodologies that provide predictable results (Parrella et al., 1992). Several authors have called for development of predictive models to assist in implementation of augmentation biological control (Huffaker et al., 1977; Stinner, 1977; King et al., 1985; van

Lenteren and Woets, 1988; Ehler, 1990), but this has only rarely been done (see for example Parrella et al., 1992). There may be several explanations for the lack of experimental work supporting augmentation. One is certainly the tremendous logistical difficulties involved in conducting the large-scale, statistically valid, detailed studies that are required to effectively evaluate natural enemy augmentation (Luck et al., 1988). Another may be a perceived similarity between augmentative releases and the insecticide paradigm that has discouraged research interest in this area (Parrella et al., 1992).

Poor quality of released natural enemies or incorrect release rates can lead to unsatisfactory pest suppression and contribute to the unpredictability of augmentation biological control (Hoy et al., 1991). A variety of general approaches have been presented in the literature for quantifying the quality of commercially produced natural enemies (e.g., Boller and Chambers, 1977; King and Leppla, 1984; King et al., 1985; Bigler, 1991, 1994; Nicoli et al., 1994). Three components of insect mass production quality controls were identified in Bigler (1991) as (1) production control, monitoring general procedures of rearing processes (e.g., equipment maintenance and environmental conditions); (2) process control, monitoring quality of the unfinished product (e.g., % hatch, larval, and pupal weights, % pupation); and (3) monitoring quality of the final product (e.g., quantity, size, sex ratio, fecundity, and other biological and behavioral characteristics).

These tests, though necessary, can be very labor intensive and add to production costs. As a result, several authors have suggested relatively quick, inexpensive approaches to quality control testing that include flight-testing (Couillien and Gregoire, 1994; Dutton and Bigler, 1995; Doodeman et al., 1996; van Lenteren et al., 1996), DNA "fingerprinting" (Santiago-Blay et al., 1994), evaluation of host size (Purcell et al., 1994), "walking" ability (Vereijssen et al., 1997), and behavioral analysis (Lux and Bigler, 1991). A review of the current status of standardized quality control test for natural enemies sold for greenhouse pest management is presented by van Lenteren (1996a).

Although natural enemy producers and researchers can routinely conduct quality control tests, it may not be possible or desirable for consumers to conduct these tests themselves. Various efforts have been made to assist consumers in ensuring that they release quality products. Recommendations for using augmentative biological controls have begun to include suggestions for quick and easy quality control checks, such as in the use of Neoseiulus fallacis (Garman) on strawberries (e.g., Coop et al. 1997). In addition, several extension resources have been made available to assist the public in making informed consumer decisions regarding suppliers, and product quality and efficacy when purchasing natural enemies (e.g., Orr and Baker, 1997a, b; Knutson, 1998).

Very few independent studies have actually sampled the quality of commercially produced natural enemy "products" (Losey and Calvin, 1995; Fernandez and Nentwig, 1997; O'Neil et al., 1998; Schmidt, 1998). In general, what these studies highlight is that quality of commercial arthropod natural enemies received by consumers is frequently not satisfactory. It has been suggested that a solution to quality control concerns may lie in the development of regulatory legislation that includes provisions to govern quality of commercial natural enemies (van Lenteren, 1996b). There are currently very few countries that regulate the arthropods used in augmentative biological control (e.g., Martin and Wearing, 1990; Nedstam, 1994; Bigler, 1997; Blumel and Womastek, 1997).

Where government regulations do not exist, industry self regulation has in some cases been adopted that "includes quality control manuals with tests for production, process and product control, total quality management with shared authority and responsibility for quality, and the International Organization for Standards (ISO 9000) programme of full management" (Leppla and King, 1996). Institutional support for self-regulation comes from several public and private organizations (Leppla and King, 1996). Where government regulation of these organisms does exist, there are both advantages and disadvantages to the regulation process. Registration of macroorganisms used in augmentative biological control in Switzerland, for example, requires data on the organism's efficacy, and "bioecology," an assessment of risks to humans and the environment, and information on evaluation and registration in neighboring countries (Bigler, 1997). The advantages are that quality control protocols are followed, ineffective products are not marketed, and environmental and human hazards are assessed. However, higher costs associated with registration may delay or prevent implementation of products.

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