Classical Biological Control Ecological Justification

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People routinely move species such as crop plants and ornamentals across natural barriers such as mountain ranges or oceans that would otherwise limit their spread. These plants may carry with them small, unrecognized infestations of pest insects. In some cases, the plants themselves may spread and become damaging. Both invasive plants and insects often escape their specialized natural enemies when they cross geographic barriers and establish in new locations. This allows these species to reach abnormally high densities and become damaging pests. Classical or importation biological control is based on the premise that the pest was originally limited to lower densities in its area of origin by specialized natural enemies, that these control agents are missing in the invaded area, and that densities of the pest in the invaded area can be reduced by importing the missing specialized natural enemies. Two recent biological control success stories from Africa, the control of cassava mealybug

(Phenacoccus manihoti) and water hyacinth (Eichhornia crassipes) illustrate these processes.

cassava mealybug Cassava (Manihot esculenta) is a tropical shrub that produces starchy tubers used much like potatoes, as a staple food source. The crop is a native of the Americas, but it is now a basic crop in all tropical countries, from Asia to Africa. In the 1970s, an unknown species of mealybug appeared on cassava in West Africa and spread rapidly throughout the cassava belt of tropical Africa. In this region, cassava was a basic food for some 200 million people. Within a few years, cassava crops began to fail as plants suffered extreme damage from high-density mealybug populations. Because the pest was clearly an exotic invader in Africa, importation biological control was seen as a means to suppress it. Furthermore, this method was chosen because it offered the possibility of providing permanent control that would not require the region's cash-poor farmers to repeatedly buy expensive pesticides and application equipment.

Cassava mealybug was believed to be from the Americas, the area of origin of the crop plant. The pest, however, was initially an unknown species. Therefore, no one knew where it could be found in South or Central America. With international funding, a cassava mealybug control project was organized. Crop protection laboratories in Africa (the International Institute of Tropical Agriculture in Benin) and South America (Centro International de Agricultura, in Colombia) worked with the Commonwealth Institute of Biological Control in Trinidad (now CABI-Bioscience, a private biological control organization in the United Kingdom) to find the pest, locate specialized natural enemies attacking it, import natural enemies to quarantine laboratories in the United Kingdom, and ship pure cultures of natural enemies on to Africa for release and evaluation in the effort to control the cassava mealybug.

Initial efforts were frustrated by an inability to find the pest in the Americas. Eventually, cassava mealybug and its parasitoid, the encyrtid wasp Epidinocarsis lopezi, were found in Paraguay. Upon release of this parasitoid, control was rapidly achieved. The parasitoid has spread (both naturally and from releases made by entomologists) throughout the cassava region, covering more than 26 countries. In 95% of the region, this single parasitoid has achieved stable, permanent control of this pest.

The net result of this project has been to increase food security in a region that frequently experiences food shortages. A pest has been controlled permanently (for nearly 20 years now in some areas), at no recurring cost, with no use of contaminating pesticides, and no damage to native plants or wildlife.

water hyacinth E. crassipes is both a plant used in ornamental fish ponds and the world's worst aquatic weed. Its beautiful lavender flowers have led people to take it far from its native range in the Amazon basin of South America. Wherever water hyacinth has been introduced into subtropical or tropical climates, it has escaped into the wild, forming gigantic mats that clog rivers and cover over bays and ponds. Among the many places invaded by water hyacinth is Lake Victoria in East Africa. The pest was first recorded there in 1980 and by the mid-1990s some 12,000 ha of weed mats had clogged bays and inlets around the lake. Economic losses resulted for fisheries (the mats impede the launching of boats and the use of nets) and for waterworks and hydroelectric power plants. Ecologically, the weed threatened one of evolution's greatest products—the radiation of cichlid fishes in the lake, some 200 to 400 species of endemic fish that have evolved in the lake. These fish, often separated by mating habits based on bright colors, were threatened by hybridization among species induced by low light under weed mats, where color-based visual recognition mating systems could not be sustained.

Controls efforts recommended to the governments of the affected countries (Uganda, Kenya, and Tanzania) included applying herbicide to the mats, using harvester boats to cut the mats, and releasing specialized herbivorous insects. Two weevils, Neochetina eichhorniae and N. bruchi, known to be specialists on water hyacinth from earlier work in Florida, were chosen for release. In 1995 Uganda was first to release biological control insects against the weed, followed by the other two countries in 1997. On the Ugandan shore, weed mats began to show damage and disappear by late 1998. By 1999 some 75% of the mats had died and sunk into the lake. Neochetina weevils also produced dramatic results on a water hyacinth infestation in Kenya in only a few months in 1999 (Figs. 1 and 2).

Description of the Process

The following steps are typical of importation biological control projects.

1. Choice of the target pest. There should be broad social agreement that the species chosen as targets of importation biological control are pests and need to be reduced in density. Targets should be species that are strongly regulated by natural enemies in their native ranges, and these species should be missing in the areas invaded by the pest.

2. Pest identification and taxonomy. Correct identification of the target pest is essential. Mistakes at this stage cause project delays or failure. If the pest is an unknown species, its nearest relatives need to be identified, for this information can provide clues to the pest's likely native range.

3. Identification of the native range. The region in which the pest evolved needs to be identified to facilitate the search for specialized natural enemies that evolved with the pest. Several criteria can be used, including the center of the geographic range of the pest, the area where the principal host plant of the pest evolved, regions where the pest is recorded to occur but remains at low densities, and regions with the largest numbers of species closely related to the pest.

4. Surveys to collect natural enemies. Natural enemy collection, or foreign exploration, needs to be done extensively over the range of locations and habitats where the pest is found naturally, and in the proper seasons. Surveys of natural enemies in the invaded area are unlikely to locate effective natural enemies but are needed to identify any natural enemies that may already be present because of their own natural invasion of the region.

FIGURE 1 Water hyacinth infestation at a yacht club in Kisumu, Kenya, weevils at the yacht club in Kisumu, Kenya, December 16, 1999. May 6, 1999. (Photograph courtesy of Mic Julien.) (Photograph courtesy of Mic Julien.)

5. Importation to quarantine. Promising natural enemies collected in surveys need to be shipped to quarantine laboratories, where they can be colonized and maintained on the pest for further study.

6. Host specificity and biology studies. To promote selection of safe species for importation, the biology and degree of host specificity of each candidate biological control agent must be determined through a mixture of field observations in the area of origin and laboratory studies in quarantine before release into a new area is approved.

7. Release and colonization in the field. Releases need to be made at numerous locations where the target pest is present, and over extended periods, until efficient means to establish the natural enemies in the invaded area have been discovered or until it is clear that the agents are unable to establish. Once established, natural enemies are further redistributed throughout the range of the pest.

8. Evaluation of efficacy. Field experiments in the invaded area comparing pest density in plots having and lacking the introduced natural enemy are needed to measure the degree to which the natural enemy is able to reduce the density of the pest.

9. Documentation of benefits. Economic and ecological consequences of the project need to be recorded and published.

Extent of Successful Use

Following introductions of natural enemies, pest densities may be reduced, sometimes by 90 to 99% or more. This has been achieved for a variety of kinds of pest insects, including caterpillars, sawflies, aphids, scales, whiteflies, and mealybugs. Over the past 125 years, some 1200 projects of insect biological control have been attempted. Of these, 60% have resulted in a reduction of the pest's density. In 17% of projects, no further controls were needed and control was complete. Introductions of specialized herbivores have been attempted against about 133 species of invasive plants and, of these, 41 species (31%) have been completely controlled.

Economics

Importation biological control is an activity conducted by governments for the benefit of society. Funds for such work are typically provided by governments but may come from grower organizations representing particular crops in a region. Costs of projects are concentrated at the beginning of the work, as costs to search for and study new candidate natural enemies are high. Use of biological control agents of proven value in new locations (where need arises because of the continued spread of the pest into new regions) is cheaper, as much of the initial work need not be repeated and known natural enemies can quickly be introduced. Benefits of successful projects accrue indefinitely into the future, and benefit-to-cost ratios of past projects have averaged 17:1, with some projects reaching as high as 200:1. In successful programs, control is permanent and does not require continued annual investments to sustain the benefits, in contrast to other forms of pest control (e.g., pesticide applications). This makes the method particularly attractive for the protection of natural areas and of crops in countries with resource-poor farmers. Biological control also promotes good environmental stewardship of farmlands in developed countries.

Safety of Natural Enemy Importations

Insects may be released as natural enemies of either invasive plants or invasive insects. Both biological weed control and biological insect control show a very high level of safety to human health and to the health of all other vertebrates. There are three safety issues when insects (herbivores, predators, or parasitoids) are imported to a new region: identification of unwanted contaminants, recognition of organisms damaging to other biological control agents, and potential damage to nontarget species (e.g., native insects or plants) in the area of release by natural enemies with broad host ranges.

The first two safety concerns are addressed by the use of quarantine facilities, which are designed to prevent the unintentional release of new species into the environment following importation. In quarantine, desired natural enemies are separated from miscellaneous insects that might have been accidentally included in the package by the collector, as well as from extraneous plant materials and soil inadvertently sent along.

A taxonomist then confirms the species identification of the organism and ensures that all individuals collected are the same species. Voucher specimens are deposited with an entomological museum for possible future reference. Natural enemy identification indicates either the name of the organism or, sometimes, that it is a species new to science and has not yet been described. New species can usually be placed in a known genus, for which some biological information may exist. A sample of the natural enemies is also submitted to a pathologist to determine whether they carry any microbial or nematode infections. If they do, they are either destroyed or, if possible, treated with antibiotics to cure the infection. This group of field-collected, healthy individuals is then bred in the laboratory on the target host. This series of steps eliminates any undesirable parasitoids (for herbivores attacking weeds) or hyperparasitoids (for insect agents) that might exist in the collected material and, if established, could damage the biological control project by reducing the efficacy of imported natural enemies. For insect parasitoids, rearing for one generation on the target host excludes the possibility that a hyperparasitoid has been obtained by mistake, since such agents typically do not breed on the host itself because they use the natural enemy as nutrient source.

The third safety concern—potential attack on nontarget species after release—requires that scientists estimate the host range of the natural enemy proposed for release and that this information be carefully evaluated as part of the decision whether to release the species from quarantine. For both weed and insect biological control agents, estimation of an agent's host range is based on several sources of information, including the hosts known to be attacked by the agent in the region from which it is collected, any species of interest that occur with the agent in its home range but are not attacked, and data from laboratory tests. For herbivorous insects released for weed biological control, these laboratory tests include studies of the adult's preference for where it lays its eggs, the immature feeding stages' preferences to eat various plants, and the ability of these plants to sustain normal growth of the agent's larvae to maturity. Similar tests can be applied to the study of parasitioids (i.e., both oviposition preferences and survival of the immature stages on a given host). For predators, oviposition preferences may sometimes exist; feeding preferences of both adults and larvae must be measured.

Estimation of host ranges of herbivorous insects used against weeds began in the 1920s, evolving from initial testing of local crops only to a phylogenetically based attempt to define the limits of the host range by testing first plants in the same genus as the target weed, then plants in the same tribe, and finally plants in the same or other families. This process has been highly successful in avoiding the introduction of insects whose host ranges are wider than initially thought. Attacks of introduced herbivores on nontarget plants have largely been limited to other species in the same genus. Also, some attacks were forecast by quarantine studies and judged acceptable by agencies granting permission for release, rather than being unforeseen attacks. Of 117 species introduced into North America, Hawaii, or the Caribbean for biological weed control, only one species (the lacebug Teleonemia scrupulosa, introduced into Hawaii in 1902 against the shrub Lantana camara) has attacked nontarget plants that were neither in the same genus as the target weed, nor a very closely related genus (for the lacebug, the native shrub Myoporum sandwicense).

Estimation of host ranges of parasitoids and predators introduced for biological control of insects began in the 1990s, in response to changing views on the ecological and conservation value of native nontarget insects. Techniques for making estimates of arthropod natural enemy safety are less well developed than those for herbivorous biological control agents. A few examples of harm from parasitoids or predaceous insects to nontarget insects have been reported. Importation of generalist species that have broad host ranges should be avoided because of such potential to harm native insects.

Laws governing biological control importations exist principally in New Zealand and Australia. Laws in the United States regulate importation of herbivorous insects used against weeds but do not currently regulate importation of parasitoids or predators.

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