SEE ALSO THE FOLLOWING ARTICLES

Agriculture / Biological Control, of Plants / Integrated Pest Management / Ladybugs / Wasps

Usually, this is achieved by the introduction of additional natural enemies (either new species or more of the same species) or by encouraging an increase in the abundance of local natural enemies by habitat modification.

FURTHER READING

Bigler, F., D. Babendreier, and U. Kuhlmann, eds. 2006. Environmental Impact of Invertebrates for Biological Control of Arthropods. Wallingford, UK: CABI Publishing. Clausen, C. P. 1978. Introduced Parasitoids and Predators of Arthropod Pests and Weeds: A World Review. Agricultural Handbook No. 480. Washington, DC: USDA. Greathead, D. J., and A. H. Greathead. 1992. Biological control of insect pests by parasitoids and predators: The BIOCAT database. Biocontrol News and Information 13(4): 61N–68N. Gurr, G., and S. Wratten, eds. 2000. Biological Control: Measures of Success. Dordrecht: Kluwer. Gurr, G. M., S. D. Wratten, and M. A. Altieri. 2004. Ecological Engineering for Pest Management: Advances in Habitat Manipulation for Arthropods. Ithaca, NY: Cornell University Press. Heinz, K. M., R. G. Van Driesche, and M. P. Parrella, eds. 2004. Biocontrol in Protected Culture. Batavia, IL: Ball Publishing. Neuenschwander, P., C. Borgemeister, and J. Langewald, eds. 2003. Biological Control in IPM Systems in Africa. Wallingford, UK: CABI Publishing. Van Driesche, R., M. Hoddle, and T. Center, eds. 2008. Control of Pests and Weeds by Natural Enemies: An Introduction to Biological Control. Oxford: Blackwell. Waage, J. K., and D. J. Greathead. 1988. Biological control: Challenges and opportunities. Philosophical Transactions of the Royal Society of London B 318: 111–128. Wajnberg, E., J. K. Scott, and P. C. Quimby, eds. 2001. Evaluating Indirect Ecological Effects of Biological Control. Wallingford, UK: CABI Publishing.

BIOLOGICAL CONTROL, OF PLANTS MICHAEL J. PITCAIRN California Department of Food and Agriculture, Sacramento

Plant populations are limited by many factors, including abiotic conditions, resource limitations, germination safe sites, plant-to-plant competition, predation (herbivory), pollination, and plant disease. The large and various groups of herbivores and diseases that consume or infect a particular plant are called its natural enemies, and the damage they impart due to their feeding or infection works together with the other limiting forces to maintain a plant’s population density around some reduced level. Biological control of invasive plants is a pest control method where the natural enemies of an organism are intentionally manipulated to further reduce its abundance.

BIOLOGICAL CONTROL STRATEGIES

Weed biological control efforts can be grouped into three different strategies: introduction, augmentation, and conservation. Introduction, or classical biological control, is the movement of selected natural enemies of a targeted plant species from its native range into the new area invaded by the weed. It is common for exotic weeds to lack natural enemies in their new area of invasion. When a plant is imported as an ornamental or crop plant, effort is taken to ensure it is free of insects, mites, and disease. Similarly, plants accidentally introduced are usually transported as seeds or pieces of stem or rhizome, plant parts too small to include or support natural enemies that require leaves or larger pieces of the plant to survive. If the plant escapes cultivation or is accidentally introduced and begins to spread, the reason for its success as an invader may be due to the difference in the level of herbivory it receives compared to plants native to the area, which are damaged and infected by their own group of natural enemies. This difference in the level of herbivory or disease has been proposed as one of the reasons that exotic plants become invasive and is called the “enemy release hypothesis.” Classical biological control involves the discovery of specific natural enemies in a plant’s native range, an evaluation of their safety (through host-specificity testing) and efficacy, and the study of their release and establishment in the invaded range. The objective is for the exotic natural enemies to permanently reduce the weed population. It is generally accepted that the weed will not to be eradicated and that both the weed and biological control agents will permanently persist, but at densities below economic or ecological threshold levels where the weed is no longer problematic. Classical biological control is the most common biological control method used against plants and should generally be part of an integrated pest management program. Augmentative biological control is the addition of natural enemies, either native or exotic, to provide a temporary boost to the background level of herbivory. Natural enemies released in an augmentative program are usually not expected to survive past their life spans or the growing season and often do not become permanently established. The released organisms are mass reared in laboratory cultures so that thousands are released at a time.

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Augmentative biological control was originally developed against insect pests in greenhouses and field crops, where it is economically feasible to produce thousands of parasitic or predatory insects on high value crops, especially if the pests are resistant to insecticides. There are very few examples of augmentative biological control being used on plants, probably because it is not cost-effective compared to herbicides, which are able to control broad classes of weeds. For invasive plants that infest large areas, augmentative strategies are not likely to be cost-effective. Some have called the use of sheep or goats an augmentative control activity, but the use of grazing is traditionally considered a cultural control method because the animals must be herded. Some plant diseases have been developed for use as bioherbicides and can be classified as augmentative control. Unlike insect agents, impacts from a bioherbicide may occur for several generations of the pathogen, but they usually do not extend beyond a single field season. Eight pathogens worldwide have been registered for use as bioherbicides against weeds.

An example is Collego, a commercial product consisting of spores of the fungus Colletoctricum gloeosporioides f. spp. aeschynomene, for control of northern jointvetch, a native leguminous weed in rice and soybean crops in the southeastern United States. Most of these products have not been economically viable because they are effective against a single weed species and must compete in a marketplace with broad-spectrum herbicides effective against many weed species. The use of plant pathogens as an augmentative biological control tool has great potential and needs to be explored further. Recently, a stem-boring wasp and a scale insect have been proposed for use in augmentative control releases against Arundo donax, a giant reed that has invaded the riparian community along the Rio Grande, the river that serves as a border between Mexico and the United States. Both insects are exotic and were obtained from Spain, where A. donax is native. The proposed objective is to rear hundreds of thousands of these species in a mass-rearing facility and then release them early in the growing season

STEPS IN A CLASSICAL WEED BIOLOGICAL

must be summarized and submitted for consideration to the regu-

CONTROL PROGRAM

latory authority before a permit will be issued. The review process can take months to years.

1. Target selection. Identify weed species using morphological and molecular techniques and identify area of origin. Resolve

5. Implementation. Upon approval for introduction, initial release

conflicts regarding the commercial or environmental value of the

and establishment of the biological control agent will occur in

target weed. Perform cost–benefit analysis.

field nursery sites, areas with high densities of the target weed located in climatic areas deemed optimal for the control agent.

2. Foreign exploration in weed’s area of origin. Examine litera-

Usually, only a few organisms (usually fewer than 1,000) are

ture and explore target weed’s native range to discover and col-

available for initial releases. Once they are established and their

lect potential biological control agents. When extensive, native

numbers increase, collections of surplus agents will be used

areas with the most similar climate to the invaded range should

to redistribute them throughout the invaded range. Regional

be identified as priority. Correct identification of all collected

redistribution can be facilitated through outreach events, such

material is critical for purposes of safety and project success.

as “field days” where local land managers and property owners

Plants closely related to the target weed should be examined in

are invited to visit the nursery site, learn the biology of the tar-

the native range to see if they are damaged by candidate control

get weed and control agent, and receive a small quantity of the

agents.

agent for release on their property.

3. Host specificity studies. All potential biological control agents

6. Post-release monitoring. Following their initial release, nurs-

should be subjected to a series of choice and no-choice tests.

ery sites should be monitored to determine whether the agent

Results will be used to predict field host range and potential

establishes, populations begin to increase, spread occurs into

risks to nontarget species after release of a control agent in the

nearby plant infestations, and the new populations support col-

invaded range.

lections for further redistribution. Generally, an agent is considered established once it has survived at least two consecutive

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4. Approval of agents by government regulatory agencies. Most

years after release. Monitoring should be performed to examine

major countries have enacted laws to regulate the introduction of

impact of the agent on the target plant population and the occur-

exotic plants and animals. These laws also regulate the introduc-

rence of any nontarget effects. This kind of monitoring is more

tion of biological control organisms. Results of host specificity tests

detailed and should occur for several years following release.

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along the critical areas of the Rio Grande, in an attempt to suppress growth of the reed. Conservation biological control is the manipulation of the habitat to encourage more activity by the local community of the pest’s natural enemies. This could include providing resources needed by the natural enemies (e.g., overwintering sites) and reducing interference by other control strategies, such as mowing or applying herbicides when they are likely to harm the weed’s natural enemies. This method is better developed for use against insect pests, such as the attraction of syrphid flies (hover flies) using certain flowering plants. Syrphid larvae are predators on aphids, and some control of aphids is achieved by the interplanting of Alyssum as a nectar subsidy among row crops such as lettuce. The use of conservation biological control needs to be more fully explored for control of weeds. CLASSICAL BIOLOGICAL CONTROL OF PLANTS

The objective in a classical biological control program is to locate host-specific natural enemies from a plant’s area of origin and introduce them into the plant’s invaded range. Those natural enemies identified for use in a plant’s invaded range are called biological control agents. All potential control agents are tested for safety prior to introduction, and a permit for their introduction is required from the appropriate regulating agency of the recipient country (see box). The goal is to establish permanent, self-sustaining populations of the biological control agent that increase to critical population levels and reduce the abundance or impact of the target plant. Control of a target weed can result from death of the attacked plant, but this is unusual. More commonly, control is achieved by the cumulative stress from nonlethal impacts that reduce

a plant’s reproduction, competitive ability, and growth rate (Fig. 1). It is common for a complex of natural enemies to be introduced against a target weed. Approximately 40 percent of past weed control projects introduced at least three exotic natural enemy species. A complex of agents is especially needed for weeds that are widely distributed throughout different climatic and geographic regions in the invaded range, are genetically variable, and have several modes of reproduction. HISTORY

The first recorded use of a natural enemy to control a plant population was the introduction of a cochineal insect to control the prickly pear cactus, Opuntia vulgaris, in Sri Lanka in 1863. Carmine red dye was produced using the cochineal insect, Dactylopius coccus, which can be grown on several species of Opuntia cactus. Both the cactus and insect are native to the tropical regions of North and South America and were introduced in the early 1800s to India and Australia for commercial production of carmine dye. Some cactus species became troublesome weeds, and it was discovered that another cochineal insect, Dactylopius ceylonicus, which had been mistakenly introduced as D. coccus into southern India, appeared to suppress populations of Opuntia vulgaris, one of the cactus species that had become a weed. In 1863, prickly pear pads infested with D. ceylonicus were transported from India to Sri Lanka where it established and substantially reduced the weedy cactus populations. The first classical biological control program in which a weed’s area of origin was explored for natural enemies was the program against Lantana camara in Hawaii in 1902. This woody shrub is a native of Mexico and was introduced into Hawaii as an ornamental. It built up

FIGURE 1 (A) Adult Galerucella calmariensis, a leaf beetle released as a biological control agent on purple loosestrife in northern California.

(B) Purple loosestrife plants damaged from feeding by the leaf beetle. (Photographs courtesy of Baldo Villegas, California Department of Food and Agriculture.)

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dense populations in a wide variety of habitats, displacing native vegetation. In 1902, the entomologist Albert Koebele, who was previously involved in the introduction of natural enemies for the control of the cottony cushion scale in California, searched the native range of Lantana in Mexico for natural enemies. His exploration efforts resulted in shipping 23 insect species to Hawaii, of which 14 were released and eight became established. These introductions resulted in successful control of Lantana in the drier lowland habitats of Hawaii; however, Lantana continues to be a problem in the wetter, upland habitats. The next major program was against a complex of Opuntia cacti that were rapidly invading rangelands in Australia. In 1912, two Australian scientists explored some of the native range of prickly pear cacti in South America and introduced five insects into Australia between 1913 and 1914. The cochineal insect, D. ceylonicus, successfully controlled O. vulgaris, but other species of Opuntia continued to spread, especially O. stricta and O. inermis. In 1920, a renewed effort was initiated with scientists searching Mexico, the southwestern United States, and Argentina for new natural enemies. The efforts resulted in the discovery of 48 different species of insects, 12 of which were released and established in Australia. The most important of these was the moth, Cactoblastis cactorum, which was introduced from Argentina in 1925. At the time, it was estimated that over 60 million acres were infested with prickly pear cactus. By 1933, less than ten years following its introduction, all of the large stands of cactus had been destroyed (Fig. 2). Control of prickly pear cactus by C. cactorum in Australia continues today.

In the United States, the first major weed biological control program was against Klamath weed (Hypericum perforatum, St. John’s wort) in California. Klamath weed is a European herbaceous perennial that became an invasive weed in Australia, South Africa, Chile, New Zealand, Hawaii, and western North America. It is toxic to livestock, and invaded rangelands and pastures could no longer be used for cattle and dairy production. Previously, scientists had introduced six insects into Australia, some of which proved successful in controlling Klamath weed. Bolstered by the success in Australia, scientists in California introduced four of the six insects between 1940 and 1950. The two most important insects were the chrysomelid beetles Chrysolina quadrigemina and C. hyperici. Larvae of these beetles burrow through the stems, and the adults feed on the foliage. Following their introduction, Klamath weed populations were reduced to less than 5 percent of their former abundance. Most local landowners at the time were involved in dairy production and credit the Chrysolina beetles with having saved their livelihood. In gratitude, they erected a monument to the beetles that sits in front of the Agricultural Commissioners Office in Humboldt County in northern California.

HOST SPECIFICITY TESTING

The risks associated with attack on nontarget plant species are reduced by selecting organisms with high host specificity—that is, those that damage only the target plant. Many insects and pathogens have long, coevolved

FIGURE 2 Before (A) and after (B) photographs of Opuntia inermis following release of Cactoblastis moths at a location in Queensland, Australia.

The “before” photograph was taken in October 1926; the “after” photograph was taken in October 1929. (From Dodd, A. P. 1940. The Biological Campaign against Prickly-Pear. Brisbane, Australia: Commonwealth Prickly Pear Board.)

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associations with their hosts and have developed high levels of host specificity. They search out and reproduce on only a few plant species and have proven to be safe when introduced into new areas. Prior to introduction, potential biological control agents are subjected to a series of tests to examine their host specificity. Upon establishment in a new habitat, a biological control agent will be exposed to hundreds of new plant species. It is not possible to test all plant species, and so methods have been developed to select a sample of plant species to best predict the host range of a potential biological control agent once it is released in the new region. A plant list is created, consisting of related genera, crop plants, and native species. Observations of control agents released in past programs have shown that those plants most closely related to the target weed are the most vulnerable to damage, and emphasis is placed on testing representatives of these species. This method of constructing a test list is called the phylogenetic method. Several types of feeding and oviposition tests are performed using all of the plant species listed for testing. If possible, it is important to reject a potential agent as early in the process as possible, to reduce costs and lost time. As a result, the most conservative tests (no-choice tests) are usually performed first. No-choice tests consist of enclosing an organism with a test plant, where it must either use the plant or die. Those plant species that are not fed on or in other ways damaged are considered to be unusable by the organism and are removed from further testing. The remaining plants are exposed to the potential control agent in a series of choice tests. In a choice test, the control agent can choose on which plants to feed, deposit eggs, or infect. Choice tests are performed in cages in a quarantine laboratory or in outdoor gardens in the native range of the target weed. Upon completion, the results of all tests are summarized and submitted to the appropriate governmental regulatory agency as a petition requesting permission to field release the organism. The costs of developing a classical biological control program are very high and can exceed $1 million and take five or more years per agent. The highest costs occur during the exploration and safety testing of potential biological control agents. Because of the high development costs, classical biological control is usually directed at weeds that infest large regions and produce significant negative impacts such as reducing forage plants in rangelands, poisoning livestock, displacing native plant and animal species by dominating

TABLE 1

Weed Species under Complete Biological Control in All or Part of Invaded Range

Acacia saligna Alternanthera philoxeroides Carduus nutans Centaurea diffusa Chondrilla juncea Chromoleana odorata Cordia curassavica Eichhornia crassipes Euphorbia esula Hypericum perforatum Lythrum salicaria Mimosa invisa Opuntia spp. Pistia stratiotes Salvinia molesta Senecio jacobaea Sesbania punicea Sida acuta Tribulus terrestris Xanthium occidentale

habitats, clogging water flow in irrigation canals, and modifying ecosystem services (Table 1). TYPES OF ORGANISMS USED FOR CLASSICAL BIOLOGICAL CONTROL OF PLANTS

Worldwide, there have been over 1,100 releases of biological control agents against 365 weed species in 75 countries. Most releases have occurred in five countries: the United States, Australia, South Africa, Canada, and New Zealand. Insects are the most common type of organism used, accounting for 98 percent of the species used. The other organisms consist of mites, nematodes, and plant pathogens. As a group, beetles (Coleoptera), moths (Lepidoptera), true bugs (Hemiptera), and flies (Diptera) are the most commonly used organisms, making up 65 percent of all species released. BENEFITS OF CLASSICAL BIOLOGICAL CONTROL OF WEEDS

Classical biological control is an attractive control method because, when successful, control is permanent and requires little human input thereafter. Ongoing expenditures for pesticides, labor, and specialized equipment are significantly reduced or removed altogether, saving enormous amounts of time and money. Over time, these cost savings accrue and can become substantial. For example, Klamath weed in the western United States has been successfully controlled since the 1940s following

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introduction of four exotic insects. The savings from not using herbicides or other control efforts was estimated at $5 million annually. Economic analysis of the biocontrol of leafy spurge, a noxious weed of rangeland in the north central United States, by introduction of several species of exotic Aphthona flea beetles, estimated the cost–benefit ratio to exceed 150:1, despite the high prerelease costs for the program’s development. Environmental benefits of classical biological control can include the reduction of pesticide use, an increase of biodiversity, a reduction of the occurrence of fire, and an increase in ecosystem services, such as increased water flow in irrigation canals and access to fishing in lakes and rivers. For some weeds, the immense size and spread of weed infestations preclude the use of chemical or other traditional control methods as both logistically and economically impossible. In such cases, classical biological control is especially valuable. Evaluation of success rates in classical biological control programs worldwide has been largely subjective. For those programs where the target weed is reduced to a fraction of its former abundance, such as occurred with Klamath weed in the western United States and Opuntia cactus in Australia, the level of success is obvious. However, for many programs, reduction of the target weed is not dramatic, and other control methods are still needed. Still, a reduction in control effort, such as using less herbicide or less frequent applications, may be considered a partial success. When programs identified as having had complete or partial success are combined, the success rate can be very high (Table 2), exceeding 80 percent in Australia, South Africa, and New Zealand.

of ultimate success, uncertain food web effects, and the inability to remove a control agent once it has been released. Classical biological control targets only one species and is not efficacious in habitats (e.g., cultivated crops) where many weed species need to be controlled. The introduction of a new exotic organism has the potential to cause both direct and indirect nontarget impacts. Direct impacts consist of feeding by a control agent on nontarget native, economic, or other desirable plant species. The risk of direct nontarget damage is reduced through the host-specificity tests that are performed prior to their introduction. Predictions of the realized host range from these tests have been mostly accurate. Reviews of past weed biological control programs report that, of nearly 400 species of control agents released worldwide, 12 (3%) have been recorded attacking nontarget plants. Of these, most are transitory, shortterm episodes of exploratory feeding on nearby plants that sometimes occurs when an outbreak population of a biocontrol agent has destroyed its local host population. However, there are two examples of potentially significant effects on nontarget plant species from biological control agents: the thistle seed head weevil, Rhinocyllus conicus, on native Cirsium spp. in the United States, and the cactus moth, Cactoblastis cactorum, on native Opuntia cacti in Florida and Mexico. The seed head weevil, R. conicus, was introduced from Europe to the United States during 1968 and 1969 for control of musk thistle (Carduus nutans, C. thoermeri). While there are no native North American Carduus species, there are two native genera (Cirsium and Sassaurea) in the same tribe Cardueae. Field host records in Europe and results from the prerelease hostspecificity testing suggested that four genera (Carduus, Cirsium, Sylibum, and Onopordum), all within the tribe Cardueae, can be used as hosts by R. conicus. Because none of the ornamental or agricultural crop species was damaged in the host-specificity studies,

DISADVANTAGES AND RISKS OF CLASSICAL BIOLOGICAL CONTROL

There are several disadvantages in a classical biological control project: high development costs, risks of damage to nontarget plant species, the lack of a guarantee

TABLE 2

Successful Weed Biological Control Programs Location

South Africa Hawaii Australia completed ongoing New Zealand

Total Weed Targets

Complete Success

Partial Success

Proportion of Total (%)

23 21

6 7

13 3

83 48

15 21 6

12 4 1

0 3 4

80 33 83

note: Reported number of weed biological control programs that have achieved complete (no other control options needed) or partial (reduced weed densities, some control options needed) success.

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and because many thistles (both native and exotic) were considered at the time to be weeds, release of this insect was approved. The target weed was successfully controlled at many locations; however, attack by R. conicus has been reported on over 20 native Cirsium species. The impact of this weevil on one native thistle, Cirsium canescens, has been studied in detail, and results showed that populations of this native thistle are seed-limited and that population densities are reduced following attack by this weevil. What has been learned from this program is that the error in the decision to release R. conicus was not due to a misjudgment of its predicted host range but to the societal view of the time that native species need not receive the same level of protection as agricultural crops and ornamental species. Social views on biodiversity have changed since the 1960s, and native plants are now seen as a valued resource worth protecting. Consistent with this change, both Canada and the United States have revoked all permits to collect and distribute R. conicus within their country’s borders. The second example of direct attack of a weed biological control agent on a new host is the cactus moth (C. cactorum) on native Opuntia cacti in southern Florida. In 1957 through 1960, the cactus moth was introduced into several islands in the Caribbean to control native Opuntia cacti that had infested pastures due to overgrazing. Several decades later, the moth accidentally spread into southern Florida, where it has been observed attacking native Opuntia cacti, including the endangered cactus Consolea (formerly Opuntia) corallicola. An even greater threat is the potential for attack on the much larger Opuntia flora of Mexico. The decision to release the cactus moth in the Caribbean was primarily economical, not ecological. Its release in Australia was ecologically sound, as there were no native cacti that were vulnerable to attack. In the Caribbean, the cactus moth was released into an ecological region that has a high diversity of Opuntia cacti, and, once it was established, was able to spread. The lesson learned from this project is that the degree of host specificity required of a biological control agent is dependent on the ecology of the region of introduction. Indirect nontarget impacts can occur through changes in the food web. If a biocontrol agent builds up high populations on a target weed but fails to control its host, then the biocontrol agent becomes an abundant new resource that can be exploited by generalist predators in the community. As a result, higher

abundance of generalist predators can lead to increased predation on desirable native species unrelated to the target weed system. For example, the fruit fly, Mesoclanis polana was introduced in 1996 as a seed predator of Chrysanthemoides monilifera (bitou bush), a perennial shrub that invaded the bush country of Australia. After introduction, M. polana developed moderate population levels, but seed destruction was too low to cause a decline in the host plant’s abundance. A few years after initial release, field observations found high rates of parasitism of M. polana by native parasitoid wasps, which normally attack several species of native insect seed predators. Recently, field observations have shown that species richness and abundance of the local native seed predators declined where the introduced biological control agent increased. Ineffective biological control agents that remain abundant in the community are most likely to have persistent, indirect negative effects. However, eventual achievement of successful control of the target weed will reduce populations of ineffective biological control agents, thereby reducing indirect nontarget impacts to acceptable levels. Biological control practitioners have developed an International Code of Best Practices, which provides a set of guidelines for individuals engaged in the biological control of invasive weeds. The code consists of 12 guidelines (Table 3) and covers all aspects of classical biological control, including prerelease and postrelease activities. The code attempts to incorporate the lessons learned from past projects and to help identify actions that reduce risk and enhance effectiveness. By following this code, it is hoped that the practice of biological control will continue to improve and remain a viable control option for invasive weeds in the future.

TABLE 3

The International Code of Best Practices for Classical Biological Control of Invasive Weeds

1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12.

Ensure that the target weed’s potential impact justifies the risk of releasing non-endemic agents Obtain multi-agency approval for the target weed Select agents with potential to control the target weed Release safe and approved agents Ensure that only the intended agent is released Use appropriate protocols for release and documentation Monitor impact on the target weed Stop releases of ineffective agents, or when control is achieved Monitor impacts on potential nontarget species Encourage assessment of changes in plant and animal communities Monitor interactions among biological control agents Communicate results to the public

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SEE ALSO THE FOLLOWING ARTICLES

Biological Control, of Animals / Enemy Release Hypothesis / Freshwater Plants and Seaweeds / Herbicides / Lantana camara / Pathogens, Plant / Weeds FURTHER READING

Carvalheiro, L. G., Y. M. Buckley, R. Ventim, S. V. Fowler, and J. Memmott. 2008. Apparent competition can compromise the safety of highly specific biocontrol agents. Ecology Letters 11: 690–700. Coombs, E. M., J. K. Clark, G. L. Piper, and A. F. Cofrancesco Jr. 2002. Biological Control of Invasive Plants in the United States. Corvallis: Oregon State University Press. Denoth, M., L. Frid, and J. H. Meyers. 2002. Multiple agents in biological control: Improving the odds? Biological Control 24: 20–30. Hoffman, J. H. 1996. Biological control of weeds: The way forward, a South African perspective (77–89). In C. H. Stirton, ed. Weeds in a Changing World International Symposium, November 20, 1995, Brighton, England. British Crop Protection Council Monograph no. 64. Farnham: British Crop Protection Council. Julien, M. H. 1997. Biological Control of Weeds: Theory and Practical Application. Canberra: Australian Centre for International Agricultural Research. Julien, M. H., and M. W. Griffiths. 1998. Biological Control of Weeds: A World Catalogue of Agents and their Target Weeds, 4th edition. Wallingford: CABI Publishing. McFadyen, R. E. C. 1998. Biological control of weeds. Annual Review of Entomology 43: 369–393. Rose, K. E., S. M. Louda, and M. Rees. 2005. Demographic and evolutionary impacts of native and invasive herbivores on Cirsium canescens. Ecology 86: 453–465. Van Driesche, R., M. Hoddle, and T. Center. 2008. Control of Pests and Weeds by Natural Enemies: An Introduction to Biological Control. Oxford: Blackwell Publishing.

BIOSECURITY SEE ECOTERRORISM AND BIOSECURITY

BIOTIC RESISTANCE HYPOTHESIS SEE INVASIBILITY

BIRDS NAVJOT S. SODHI National University of Singapore

Humans are responsible not only for creating a conducive environment for invasive species but also for introducing many of these species themselves. Worldwide, 1,400 attempts to introduce 400 bird species have been recorded. Approximately 70 percent of bird introductions have been to islands, although islands make up only

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about 3 percent of Earth’s ice-free land area. Just over half of global bird introductions have been to Pacific islands (notably to Hawaii) and to Australasia. Bird introductions do not always result in an established population. A case in point is the introduction of more than half a million common quail (Coturnis coturnix) to more than 30 states in North America between 1875 and 1958. Incredibly, this experiment failed. In the case of Australasia, of the 242 bird species introduced in the past two centuries, 32 percent established viable populations. BIRD INVADERS

Most bird introductions took place in the eighteenth and nineteenth centuries, during a period of major European colonization. Because of this, a large proportion of invasive (alien, exotic, or introduced) bird species originated from temperate regions. For instance, 60 percent of introduced birds in New Zealand originated from the Palaearctic and Australasian regions. Birds were introduced by settlers to various countries, predominantly for aesthetics, hunting, and biocontrol. Two-thirds of the species chosen for introduction have been from 6 (of 145) bird families: Anatidae (ducks), Columbidae (pigeons and doves), Fringillidae (finches), Passeridae (sparrows), Phasianidae (pheasants), and Psittacidae (parrots). This overrepresentation of certain families points to the reasons for these introductions. For example, ducks and pheasants were introduced for hunting, while finches, sparrows, and parrots were introduced as pets. Three bird species included among the 100 worst invasive species (see Appendix) are the European starling (Sturnus vulgaris), red-vented bulbul (Pycnonotus cafer), and common myna (Acridotheres tristis) (Fig. 1). The negative effects of invasive bird species on native biodiversity, ecosystems, and humans have been widely recognized and are briefly discussed below. Most longdistance bird introductions to new areas are the direct or indirect result of human activities, and social and economic factors are often as critical as biological factors in the introduction of exotic species. Activities such as logging and grazing further enhance establishment of exotics by creating optimal habitat for colonization (e.g., through range expansion). Agriculture can facilitate bird species invasions when pests in agroecosystems are exposed to agricultural practices for many generations, resulting in selection for characteristics that make them persist. It is possible that bird invasions will increase in the future owing to increase in human trade and traffic, and “global warming” may further facilitate species movements to new locations.

BIRDS

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