Annual Reviews www.annualreviews.org/aronline Annu. Rev. Entomol. 1991. 36:485-509 Copyright © 1990 by Annual Reviews Inc. All rights reserved ENVIRONMENTALIMPACTS OF CLASSICAL BIOLOGICAL CONTROL1 Francis G. Howarth J. Linsley Gressitt Center for Research in Entomology, Bernice Pauahi Bishop Museum, P.O. Box 19000-A, Honolulu, Hawaii 96817 KEYWORDS: extinctions, endangeredspecies, genetically engineeredorganisms, nontarget organisms,alien species PERSPECTIVES AND OVERVIEW Biologicalcontrol, the use of living organismsto control pest populations, dates from ancient times (117, 127). However,100 years have passed since AlbertKoebele intentionally introduced the Australianvedalia lady beetle via NewZealand (6, 86) into Californiaorange groves in 1889,where it spectacu- larly controlled the cottony-cushionscale. This milestonemarks the start of modernclassical biological control--the importationand release of an organ- ism outside its natural range for the purposeof controlling a pest species. Classicalbiological control has also includedcertain other introductionsthat by Texas A&M University - College Station on 03/21/06. For personal use only. enhancebeneficial organisms,e.g. pollinators (8, 118, 127), scavengers(8, Annu. Rev. Entomol. 1991.36:485-509. Downloaded from arjournals.annualreviews.org 11, 118), and competitors(11, 82). Undertakinga reviewof the environmentalimpacts of this control method is timelyas the secondcentury of classical biologicalcontrol begins and as the rapid developmentof biotechnologycreates the specter of newrisks fromthe purposefulrelease into the environmentof an increasingnumber of artificially engineeredorganisms (98, 120). Furthermore,mounting criticism of chemi- IThis paper is dedicated to the late Wayne C. Gagn6 whose wit and committment to insect conservation provided many insights to this review. 485 0066-4170/91/0101-0485 $02.00 Annual Reviews www.annualreviews.org/aronline 486 HOWARTH cals in pest control, including increasing public fear and the banning of pesticides, and developmentof resistance to pesticides have inspired renewed enthusiasmfor classical biological control introductions. The manysuccesses in biological control and the available data on the history of introductions have been well reviewed (6, 11, 23, 70, 117, 129). The introduction of biological control agents has often been declared to be environmentally safe and risk free (4, 7, 17, 23, 28, 59, 72, 82, 126). However, adequate data to defend this assertion on safety have not been systematically gathered. In 1899, David Sharp (114) wrote to L. O. Howard concerning Koebele’s program of importing biological control agents into Hawaii: It is importantthat a permanentrecord shall be securedof whatMr. Koebele has done in mattersthat mayaffect the fauna,and we shall be muchobliged if youwill drawup a statementas full as youcan on these points. Mr.Koebele is actually makinga huge biologicalexperiment, and the particularsshould be fully recorded,though it mustbe very longbefore the resultscan be at all accuratelyestimated. Unfortunately, Sharp’s advice has not been heeded, as few workers have studied the effects of purposefully introduced species on nontarget organisms or other aspects of the environment(75, 76). The limited information on the environmentalimpacts of biological control is scattered within the control and ecological literature or remains unpublished or, worse, ungathered. Often, different names have been used for the same organism, making comparisons betweenthe control and ecological literature difficult. Recordsof biological control importations and releases for manyregions are also scanty (5). Koebele and manyother early workers recorded only those species that they thought were successful (118), and for manyregions no records exist for the vast majority of introductions that were tried (5, 118). Therefore, absence evidence of negative environmental impacts is not evidence of absence of these impacts. by Texas A&M University - College Station on 03/21/06. For personal use only. Documentationof significant environmental impacts is accumulating, and Annu. Rev. Entomol. 1991.36:485-509. Downloaded from arjournals.annualreviews.org awarenessof the problemis increasing (30, 57, 61, 75, 94, 96, 97,125, 129). Muchof the evidence of environmental damagehas been gathered serendipi- tously during unrelated field studies (e.g., 54, 90, 106). Several recent workshops and symposia on biological control have included sessions on environmental impacts (e.g. 66, 135, 76, 134). Biological control introductions are part of the muchlarger problemof the invasion of newareas by alien species, whichare recognized as a major factor in species extinctions (63, 79). This formof biological pollution is one of the most critical problemsfacing managersof natural areas and nature reserves and has been the subject of important recent reviews (29, 49, 77, 79, 83). The Annual Reviews www.annualreviews.org/aronline IMPACTS OF BIOLOGICALCONTROL 487 main premise of classical biological control is based on the fact that alien organisms disrupt established populations. This review calls attention to the wide variety of concerns and problems inherent in purposeful introductions. If the outcomes of purposeful in- troductions, including those of classical biological control and genetically engineered organisms, are to becomepredictable, we must ask the right questions and gather appropriate data to answer them (88, 94). A review environmental conflicts resulting from past purposeful introductions should provide clues useful in foreseeing the environmentalrisks of future actions. This knowledgeshould also allow greater skill in preventing or mitigating environmental problems. Although this review mainly concerns insects and other arthropods, microorganisms, molluscs, and vertebrates are included because these groups have also been introduced by entomologists acting under the aegis of biological control. Impacts on both the humanand natural environments are covered. Natural environments also have significant eco- nomic, cultural, aesthetic, scientific, and other humanvalues. In reviewing the negative aspects of classical biological control, I do not intend to slight its positive aspects. Past and current workers have used the best methods and theories available in attempting to improvehuman welfare, in manyinstances with spectacular success (6). BENEFICIAL ASPECTS OF BIOLOGICAL CONTROL The manybenefits to the environment of classical biological control have been well documented(e.g. 6, 11, 13, 23, 47, 47a, 64, 70, 100, 109, 117, 129, 134). Most classical biological control programs have been aimed at pests in agroecosystemsand disease vectors with significant successes mea- sured in long-term economicand public health benefits (e.g. 6, 11, 13, 23, 47, 100, 129). Biological control of pests usually has been safer to public health than has chemical control (7, 94, 95, 97). Manyearlier programstargeted alien weedsand pests that also incidentally by Texas A&M University - College Station on 03/21/06. For personal use only. had invaded native habitats. Undoubtedly,the control of manyof these aliens Annu. Rev. Entomol. 1991.36:485-509. Downloaded from arjournals.annualreviews.org [e.g. rabbits and cactus in Australia (49, 70), the shrub Lantanain Hawaii (37), and scale insects and cactus in South Africa (44, 109, 140)] benefitted native species. A dilemmapresented by alien invasions into nature reserves is that any control attempt will have some negative impacts. However, an uncontrolled alien species may endanger more native species than would intrusive but successful efforts to control it (57, 62, 109), Biological control has special promise in somecases because it can target the pest and achieve control without many of the adverse impacts of mechanical or chemical methods(109). The level of control sometimesachieved makesit economical- ly appealing in inaccessible terrains or over large tracts. Annual Reviews www.annualreviews.org/aronline 488 HOWARTH NEGATIVE IMPACTS OF CLASSICAL BIOLOGICAL CONTROL Negative environmental impacts of biological control introductions have not been well documented in the literature (61, 104, 107, 125). The major environmentalrisks have been perceived as only those that affect the success of the control program(7, 43), and most studies of the risks and negative impacts have considered only the humanenvironment [i.e. whether or not the pest was controlled, or whether the agent damagedcrop plants, beneficial organisms, or humanhealth (5, 7, l 1, 75, 76, 96, 97)]. In fact, biological control agents affect the environmentin a variety of ways. Theyhave failed to control the pest, enhancedthe targeted pest, synergistically interacted with other organismsto enhancepest problems, affected public health, and attack- ed nontarget organisms. In short, some have becomepests themselves. EndangeredSpecies and Extinctions In no other aspect is classical biological control strategy morein conflict with environmental protection than as the cause of species extinctions. Most extinction studies have been done in hindsight after biologists realize that a species has disappeared. A widely accepted tenet amongecologists holds that biological control agents cannot cause extinctions (7, 22, 109, 127). Yet extinctions of both target and nontarget species have been well documented, and local extirpation of pests by biological control agents maybe a common phenomenon(88, 89, 96). LEVUANAMOTH The control of the coconut moth, Levuana iridescens, on