How Risky Is Biological Control? Comment JH. Frank Ecology, Vol. 79, No. 5. (Jul., 1998), pp. 1829-1834. Stable URL hitp:/flinks.jstor-org/sicisici=0012-9698% 28 199807%2979%3A5% 3C 1829%3 AHRIBCC%3E2.0,CO%3B2-A Ecology is currently published by The Ecological Society of America. Your use of the ISTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at hup:/www,jstororglabout/terms.hml. ISTOR’s Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at hupulwww.jstor.orgijournalsiesa,hum, ch copy of any part of'a JSTOR transmission must contain the same copyright notice that appears on the sereen or printed page of such transmission, ISTOR is an independent not-for-profit organization dedicated to creating and preserving a digital archive of scholarly journals. For more information regarding JSTOR, please contact support @ jstor.org. hupulwww jstor.org/ Tue Mar 14 17:49:01 2006July 1998 Acknowledgments This work was supported by the Australian Research Coun: cit and the Naturl Sctences and Engincering Research Can cil of Canada, Literare ited Caley, M. 2. and D. Sehluter, 1997. The relationshipbetween Toeal and regional diversity. Ecology 78°70-80. Cornell, H. V. 19850. Local and regional richness of eynipine izill wasps on California oaks. Ecology 66:1247-1260, TORS. Species assemblages of eynipine gall wasps ‘are not saturated. American Naturalist 126:565-569, \Westoby, M, 1985, Two main relationships among the com- nents of species richness, Proceedings ofthe Ecological Society of Australia 14:103-107 1993. Biodiversity in Australia compared with other ‘continents, Pages 170-177 in RE. Ricklefs and D. Schl tex, editors. Species diversity in ecologieal communities: Iistorical and geographical perspectives. University of Chi- cago Press, Chicago, Illinois, USA. 10998. The relationship between Local and regior ‘iversity: comment. Eeology 79:1825-1827 eo, 2%) 808 pp 929-1894 HOW RISKY IS BIOLOGICAL CONTROL? COMMENT JH, Frank! ‘The authors of a paper “How risky is biological control?" (Simberloff and Stiling 1996) wrote about the risk of dispersal of biological control agents to areas that were not intended to be occupied, and to nontarget species. They claim that intzoduction of biological cor trol agents is risky, and that such agents should be judged "guilty until proven innocent.” I think the legal ‘metaphor chosen by Simberloff and Stiling is inappr priate, and I prefer to compare biological control to surgery rather than to law. First, as in biological con- trol, surgery is one of several alternative courses of action to address a specific problem. There ate risks Manuscript received 23 December 1996; revised 20 Oe- tober 1997: accepted { November 1997, "nfomology and Nematology Department, University of Florida, Gainesville, Florida 32611-0630, USA. COMMENTS: 1829 associated with surgery and with alternatives to sur- ‘gery, and these must be compared. Second, as in bi ‘logical contro, surgery has advanced in the past 130 years. It is no more appropriate to criticize moder biological control for disastrous introductions of the distant past (e.g, of the Indian mongoose, Herpestes ‘auropunctatus) than to erticize modern surgery for deaths through lack of antiseptic methods used in the pst, but many have learned from such errors agree with Simberloff and Sting that risk/benefit analysis is an important preliminary to biological con- trol introductions. As an example of an introduction of biological control agents against nonindigenous pest insects, SimberlofT and Stiling cited actions of the Uni- versity of Florida's mole cricket research program. I this comment I provide a risk/benefit analysis of intro- ‘duetions made by this program, Because T have been involved in the program for 12 years I am familiar with data (published only recently hence Iess readily avail- able to Simberloff and Stiling) relevant to the questions posed by Simberloff and Stiling. They ask: “What is the likelihood that these [introduced] control agents would spread and, if they did, what is the probable cffect on [a] native species [of mole cricket, Gryllo- talpa major}”? 1 ask, additionally, what are the likely ‘environmental and economic effects of alternatives 10 introducing these biological control agents? My goal inthis comment is twofold, Firs, I show how ecologists knowledgeable of a biological control system can con- ‘duet necessary risk/benefit analyses. Second, I show that in the specific case of mole cricket biological con- trol the risks to G. major are teivial, but that the cost (Go agriculture and horticulture) of not undertaking the program is very high and the harm from currently used ‘chemical pesticides to nontarget organisms is wide- spread. A broad perspective of biological control From January 1971 10 late 1991 (a period of not quite 21 years), 271 immigrant insect species were newly reported as established in Florida (Frank and McCoy 1992), Few of these uninvited species have been stud ied. Among the immigrants were a few species, on average detected at about one per year, that either were known to be important pests elsewhere, or made theit presence conspicuous as major pests (Frank and Me- Coy 1992). When these pests affected agriculture in the broadest sense, or infested buildings, or caused an- noyance by biting, they became targets of control by repeated application of existing broad-spectrum pes- ticides. The natural tend is therefore for increasing use of pesticides, which is beneficial for commerce and creates jobs, but is costly to purchasers and detrimental to the environment. These invasive species may thus have far greater effects on ecosystems, both directly1830 and indirectly by prompting use of chemicals, than do the few specialized biological control agents that were {imported and established during this period (Frank and ‘MeCoy 1993) to reduce pest populations. ‘Sometimes exotic pests proved very costly to control by chemicals or proved nol very susceptible to existing chemicals, and these were the first 10 be evaluated for possible biological control. In other words, it is ge erally the failure of chemical conteol that instigates @ biological control campaign. This reflects economic pressure rather than environmental benefit, but it is {economic pressure that most often generates research funds for biological control, Biological control cam paigns are also occasionally initiated against immigrant pests of native plants with no assigned commercial val- tue, with no motive other than to protect the environ- ‘ment (e.g., Frank and Thomas 1994), but funding for such campaigns is abysmally difficult to obtain. ‘Simberloff and Stiling advocate that biological con- ‘ol agents should be tested against nontarget organisms before release. They suggest that even if a biological control agent does not now attack a nontarget organism, it may Tater evolve to do so. I think that biological control agents should be tested against nontarget or ‘ganisms that are closely related to the target pest Lalso think that environmental and economic costs of inac- tion and of alternative actions should be weighed. In the example of the introduction of three biological control agents against Scapteriscus mole crickets in Florida, no testing against the rare Gryllosalpa major was performed because of allopatry and distant rela- tionship of G. major to Scapteriscus. Native congeners of the biological control agents had failed to attack the invading Scapreriscus mole crickets in an inadvertent field experiment of =80 yr, suggesting that a rapid host shift by the biological control agents would not occur Large economic losses caused by Scapteriscus mole crickets, and harm done by chemical pesticides to non- target organisms, ruled against a long-term test for & host shift before release. Subsequent data have thus far vindicated the risk that was taken and have shown bet fits from the releases, No risk/benefit analysis was “written before release because none was then required (only a statement of host specificity was required), but requirements for documentation are now more stringent in permit applications. Phylogeny and biogeography of mole crickets ‘The pest mole crickets in the southern USA are three South American species of Scapteriscus which arrived in ships' ballast ~ 1900. These belong tothe tribe Seay leriscini, whereas native mole crickets belong to the ‘genera Neocurtilla and Grollotalpa of the tribe Gry lotalpini (Otte 1994) and differ in behavior, habitat, physiology, and natural enemies. The invading Seap- COMMENTS: cology, Vol. 79, No.5 teriscus species have colonized sandy and otherwise friable soils of the coastal plain in the subtropical and mild temperate climatic zones of the southern USA plus, recently, the southern Arizona-California border (Frank 1994), (Of the two native mole erickets considered by Sim- berloff and Stiling, Neocurtilla hexadactyla, occurs in heavy soils in the eastern USA northward to the Great Lakes. It never was a target of biological control, and is not rare (Frank 1994). I use this species, because it is native in the areas where the biological conteol agents were released and because the mole cricket program thas data about it, as a model for the tribe Gryllotalpini Simberloff and Stiling express concern about Gryllo- falpa major, which occurs in heavy soils in prairie remnants in Arkansas, Kansas, Missouri, and Okla- hhoma and is rare because of habitat loss (Vaughn etal 1993). It was proposed in 1990 as a candidate for fed cral listing as a threatened species (not as an endan- gered species, as stated by Simberloff and Stling), but ‘was removed from candidacy in 1992 because it is not as rare as had been suspected (Vaughn et al. 1993) Specificity of native natural enemies The native Neocurtilla hexadactyla has its own spe- 90 yr inadvertent ficld experiment have, afterall, failed to show the possibility of one of the steps: host-switching by native natural enemies belonging to the genera Larra, Ormia, and Steinernema to invasive Scapteriscus species, despite the abundant food supply represented by these pest mole crickets. ‘The rarity of G. major provides a safeguard. If, some- how, one of the imported biological control agents a rives in the habitat of G. major, the frequency of en- ‘counter with this mole cricket would be low and this ‘would hinder a host shi. The risks of alternatives to biological control Simberloff and Stiling question the risks of intro- ducing the three above-mentioned biological control agents. The other side of the balance sheet isthe benefit that biological conteol of Scapreriscus mole erickets cean achieve. At stake, in Florida alone (much more is at risk in other southern states) are ~10° ha of bahia- grass (Paspalum notatum) pastures, ~5 X 10° ha of bahiagrass and bermudagrass (Cynodon spp.) turf (in- cluding ~1200 golf courses), other pasture and turf grasses, and ~45 000 ha of the most susceptible veg- tables (tomato, bell pepper, egg plant, cabbage, and cucurbits). Bahiagrass pastures are the mainstay of beef and dairy-cattle production in Florida and are damaged by Scapteriscus mole crickets 10 the point that pastures ‘may be entirely destroyed, The only alternatives to the biological control agents thatthe mole ericket progran hnas introduced are (1) no action, and (2) afew chemical pesticides that can be used where cattle graze. Frequent use of those pesticides is 100 costly for most cattle ranchers because of the low prices for beef, and in the past they have used the cheap but persistent and en Vironmentally harmful pesticide chlordane (Frank 1994), In 1986, damage and costs of control to turf grasses by Scapteriscus mole crickets in Florida were estimated as >$44 million annually, with an additional $33 mil- lion in Alabama, Georgia, and South Carolina; losses in other states (North Carolina, Louisiana, Mississippi, and Texas) were not estimated (R. D. Hudson, unpub- lished presentation). As a result of the damage they cause in the southeast, Scapteriscus mole crickets are the most important pests on golf courses in the country (Shaw 1993). The standard method of treatment in Flor fda as in other southern states is the use of broad- spectrum chemical pesticides (e.g, carbaryl, ethoprop, and fonofos). Playing fields and home lawns are ex: tremely important sites of use of chemical pesticidesJuly 1998 in Florida, with expenditures on control of Scapteriscus unrelated to economic returns and very high because ‘of Florida's large human population, expectation of year-round use of turf, and mild climate, Roadside rights-of-way are often damaged by mole crickets, and Department of Transportation personnel want alterna- tives to chemical pesticides. The reality of massive kills ‘of birds after ingesting diazinon-poisoned mole eric cts on golf courses ended in 1988 (the year that the mole cricket program released its third biological co! tol agent in Florida), and only the specter seems 10 remain (Rainwater et al, 1995), Yet, an equal reality is that harm to nontarget invertebrates has hardly Less- ‘ened. Chemical insecticides such as ethoprop, carbaryl, and fonofos at labelled dosages are lethal to earth- ‘worms, and other chemical pesticides that are com- monly used against mole crickets suppress populations ‘of nontarget arthropods such as spiders, carabids, and staphylinids that can serve as generalist predators of mole crickets Potter 1994 and references therein). Pop- ulations of many hundreds of nontarget invertebrate species are harmed on golf courses and lawns and play- ing flelds in the southern USA by treatment with chem- ical pesticides against Scapteriscus mole crickets, Un- fortunately, nobody has assessed the value of such in- vertebrates Now, vegetable fields in Florida are usualy fumigated with a methyl bromide/chloropierin mixture to control soil-dwelling pests including mole crickets (eg., Noling and Becker 1994). This chemical mixture is a potent biocide which kills vitally all soil organisms. ‘The picture, though economists have documented lit- tle of it, is one of tremendous annual Tosses due to Seapteriscus mole crickets, with chemical pesticides Still the overwhelming recourse for preventive use by farmers, ranchers, and turf managers. Biopesticides like Steinernema seapterisci (and also S. riobravis, a less specialized nematode from the southwestern USA) ‘currently make up a tiny percentage of total use. Clas- sical biological control agents (Lavra bicolor, Ormia depleta, and Steinernema scapterisci are reducing pop- ulations of Seapreriscus borellii and S. vicinus (Park- man et al. 1996; H. Prank unpublished data for 1995— 1996) and are therefore reducing the need to apply pesticides. However, their contribution is little appre- Ciated, because nobody outside the mole cricket pr ‘gram even monitors their presence, much less their effects on mole crickets, Tens of millions of dollars worth of chemical pesticides are applied annually to soils in Florida (and much more in other southern states) to kill Seapteriscus mole crickets, and such ap- plications yield only temporary control. The chemicals do not kill Scapreriscus mole crickets only, and it is likely that most soil-dwelling invertebrates are Killed by chemical pesticides over hundreds of thousands of ‘COMMENTS: 13 hectares annually. Annual sales of chemicals for con- trol of Scapteriscus mole erickets are an important source of revenue for chemical companies which, nat- urally, do not support the development of biological control alternatives. Scapteriscus mole cricket populations vary in time and space and therefore so does the damage they cause and the cost of chemicals used against them. Incom- plete economic data exist for mole crickets in turf, not in pastures or vegetables. Such data do not address the ‘question of the damage done by chemical pesticides to nontarget invertebrates, "The surgery performed by introduction of biological control agents against Scapreriscus mole crickets is jus tified environmentally and economically. It has not caused collateral damage and appears unlikely to be able to do so. Acknowledgments [thank 3. L Capinera, M. A. Hoy. L. P. Lounibos. 8. D. Porter 1. Walker and reviewers foreiticism of manuscript drafs This is Florida Ageicultural Experiment Station journal series no, R0S519, Literature clted Bathon, H. 1996, Impact of entomopathogenie nematodes ‘on non-target hosts, Biocontrol Science and Technology 6 31-434 Castner. L, 1984, Suitability of Scapreriscus mole crickets 1s hosts of Larra bicolor (Hymenoptera: Sphecidae). En tomophaga 29:323-329, Jers, R-U, and H. M. T Hokkanen. 1996. Insect biocon- trol with won-endemic nematodes (Steinernema and Het ‘rorhabalits spp. conclusions and recommendations of & Combined OECD and COST workshop on scientific and regulatory policy issues. Biocontol Science and Technol- by 6.208.302. Frank, J. H. 1994, Inoculative biological contral of mote ‘rickets, Pages 457-475 in A. R. Leslie, editor, Handbook ff integrated pest management for turf and ornamentals, Lewis, Boca Raton, Florida, USA. Frank, J. Hand E. D. MeCoy. 1992. The immigration of insets to Florida, with a tabulation of records published since 1970, Florida Entomologist 35:1-28. Frank, J. H., and B,D. McCoy. 1993. The inroduction of insects into Florida, Florida Entomologist 761-53. Frank, JH, and M,C. Thomas, 1994, Metamaxins callzona {(Cheviolas) (Coleoptera Curculionidae). an immigrant pest, destroys bromeliads in Florida, Canadian Entomolo Eis 126-673-682. Frank, J H., JP Parkman, and FD. Bennett. 1998. Larne bicolor (Hymenoptera: Sphecidae), a biological contrat agent of Scapreriscus mole crickets (Orthoptea: Gryllo- Ualpidae) established in-northem Florida, Horida nto mologist 78:619-623, Frank, 1 H., TJ. Walker, and J. P. Parkman. 1996. The Introduction establishment and spread of Ormia depletain Florida, Biological Contol 6:368-377834 ‘COMMENTS Ecology, Vol. 79, No. 5 Menke, A. $. 1992, Mole cricket hunters of the genus Larra Eon 7%) 108: AMIS in the New World (Hymenoptera: Sphecidae: Lavtinac) Journal of Hymenoptera Research 1175-234 Nguyen. K. B, and G. C. Smart 1991. Pathogenicity of Sicinernema seapterisc! to Selected invertebrates. Journal fof Nematology 28:7-11 Nguyen. KB. and G. C. Smart. 1992. Sieinernema neo: ‘urulls sp" (Rhabditida: Steinernematidae) and a key 10 the species ofthe genus Steinernema, Journal of Nematol oy 24:463-477, NNoling, J. W, and J. O. Hecker. 1994, The challenge of ‘research and extension to define and implement alternatives to methyl bromide, Journal of Nematology, Supplement 26(48):573-586, ue, D._ 1994. Family Grytlotapidae subfamily Gryllowl nae. Pages 98-100 in Orthopteran species le |. Crickets (Grylioides). A systematic catalog. The Orhoptersts So fet) and The Academy of Natural Sciences of Philadel phia, Philadelphia, Pennsylvania, USA Parkman, J.P and G. C. Smart. 1996, Case study: Inco- ‘ction of Steinemema seapterieci im Florida, Biocontrol Science and Technology 6:413-419, Parkman, JP, J.H. Frank, TJ. Walker, and D. J. Schuster 1996, Classical biological control of Seapteriscus pp. (OF- thoptera: Gryllotalpidae) in Florida. Envieonmental Ento- mology 25:1415-1420. Parkman, J.P. W. G. Hudson, J. H. Prank, K. B. Nguyen, ‘and G.'C. Smart. 1993. Establishment and persistence of Sieinermema scuperisel (Rhabiitida: Steinernematide) i {eld populations of Seapterisus mole erickets (Orthop Grytlotalpida)- Journal of Entomological Science 28 190, Potter, D. A. 1998, Etfects of pesticides on Bene ‘vertebrates in turf. Pages 59-70 in A, Re Leslie, editor Handbook of integrated pest management for turt and ot namentals. Lewis, Boca Raton, Florida, USA. Pruct,,C.. and F D. Bennet. 1991. Behavior of two species of Larra in Santa Crue, Bolivia. Sphecos 24: 15-16 Rainwater, TR, V. A. Leopold, M. J. Hoopes, and R. 1 ‘Kendall. 1995. Avian exposure to organophosphorus and carbamate pesticides on a coastal South Caroling goll ourse. Environmental Toxicology and) Chemistry 14 2158-2161 Ricci, M., I. Glazer, J. F Campbell, and R. Gaugler. 1996. ‘Comparison of bioassays to measure virulence of different centomopathogenic nematodes. Biocontiol Science and “Technology 6:235-253, Robert, DJ. Amoroso, and R. R. Hoy. 1992. The evolu- Tionary Convergence of hearing ina parasitoid My and its host. Science 2581135-1137, Shaw, M, 1993, Practical strategies for mole ericket man- ‘agement, Golf Course Management (May 1993)-43-47, Simberloff, D. and P. Sting. 1996. How risky is biological ‘control? Ecology 77:1965-1974 Stock, 5. P. 1995. Natural populations of entomopathogenic nematodes in the pampean region of Argentina, Nemato 2143-148, 3, C.C, S. M. Glenn, and 1. H. Butler. 1993. Char- “American Midland Naturalist 130:364-371 T.J.,and DE. Figg. 1990. Song and acoustie barrow ‘ofthe prairie mole cricket, Grylorapa major (Orthoptera Geyllidae). Journal of the Kansas Entomological Society (63:237-282 ‘Walker, TJ. P Parkman, J. H. Frank, and D. 3. Schuster 1096. Seasonality of Onniadepleta and limits co it spread. Biological Conteol 6:378-383, HOW RISKY IS BIOLOGICAL CONTROL? REPLY Daniel Simberloff’ and Peter Stiling* Ifa surgical rather than a legal metaphor is appro- priate for biological control (Frank 1998), we cannot agree that, because biological contro, like surgery, has Tearmed from errors inthe past, all current practices are beyond criticism. For example, the recent introduction ‘of the flatworm Platydemus manokwari to several is- lands in the Pacific and Indian Oceans (e.g, Muniappan 1987) to control the giant African snail (Achatina fu- ica) is widely seon as potentially as damaging to non larget native species as that of the small Indian mon- ‘Boose (Herpestes auropunctatus) that Frank concedes was disastrous. This project seems not to have been informed by the well publicized global extinctions of native snails caused by earlier introductions to control the giant Aftican snail (Hopper and Smith 1992); the ‘wide introduction of a generalized predator is the an- tithesis of surgical. Of course much of modem biolog- ical control, particularly of plants, is practiced with ‘more concer than in the past about potential impacts ‘on nontarget species. However, potential risks, costs, ‘and benefits are still not carefully analyzed in many projects. Our paper (Simberloff and Stiling 1996) sought to demonstrate this problem and to point out that such analyses will not be easy. Frank's attempts along these lines are certainly a beginning, but many ‘weaknesses remain, For risk, he argues that, since native congeners of {introduced biocontrol agents have failed to attack Seap- teriscus mole crickets in 80 yeats, there is litle reason to believe that the introduced species themselves would attack native hosts. We are unaware of any basis for this reasoning. Granted that the probability of a rapid hhost-shift by any host-specific species is probably low, ‘we know of no literature that suggests that, if species A hhas not shifted hosts in time interval X, congeneric species B is unlikely to shift hosts in time interval ¥. Certainly there is need for much research on this point. It is known that rapid host shifts do oceur (see, ©-8. Manuscript received 2 January 1998: accepted 6 January’ 1998, "Department of Ecology and Evolutionary Biology, Uni: versity of Tennessee, Knowille, Tennessee 37996 USA. "Department of Biology, University of South Florida, Tam: pi, Florids 33620 USA,