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How risky is biological control? Comment.

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 introduction of biological control 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 inappropriate, and I prefer to compare biological control to surgery rather than to law. First, as in biological control, surgery is one of several alternative courses of action to address a specific problem. There are risks associated with surgery and with alternatives to surgery, and these must be compared. Second, as in biological control, surgery has advanced in the past 130 years. It is no more appropriate to criticize modern biological control for disastrous introductions of the distant past (e.g., of the Indian mongoose, Herpestes auropunctatus) than to criticize modern surgery for deaths through lack of antiseptic methods used in the past, but many have learned from such errors.

I agree with Simberloff and Stiling that risk/benefit analysis is an important preliminary to biological control introductions. As an example of an introduction of biological control agents against nonindigenous pest insects, Simberloff and Stiling cited actions of the University of Florida's mole cricket research program. In this comment I provide a risk/benefit analysis of introductions made by this program. Because I have been involved in the program for 12 years I am familiar with data (published only recently hence less readily available 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 effect on [a] native species [of mole cricket, Gryllotalpa major]"? I ask, additionally, what are the likely environmental and economic effects of alternatives to introducing these biological control agents? My goal in this comment is twofold. First, I show how ecologists knowledgeable of a biological control system can conduct necessary risk/benefit analyses. Second, I show that in the specific case of mole cricket biological control the risks to G. major are trivial, but that the cost (to agriculture and horticulture) of not undertaking the program is very high and the harm from currently used chemical pesticides to nontarget organisms is widespread.

A broad perspective of biological control

From January 1971 to 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 studied. 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 their presence conspicuous as major pests (Frank and McCoy 1992). When these pests affected agriculture in the broadest sense, or infested buildings, or caused annoyance by biting, they became targets of control by repeated application of existing broad-spectrum pesticides. The natural trend 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 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 McCoy 1993) to reduce pest populations.

Sometimes exotic pests proved very costly to control by chemicals or proved not very susceptible to existing chemicals, and these were the first to be evaluated for possible biological control. In other words, it is generally the failure of chemical control that instigates a 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 campaigns are also occasionally initiated against immigrant pests of native plants with no assigned commercial value, with no motive other than to protect the environment (e.g., Frank and Thomas 1994), but funding for such campaigns is abysmally difficult to obtain.

Simberloff and Stiling advocate that biological control 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 later evolve to do so. I think that biological control agents should be tested against nontarget organisms that are closely related to the target pest. I also think that environmental and economic costs of inaction 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 Gryllotalpa major was performed because of allopatry and distant relationship of G. major to Scapteriscus. Native congeners of the biological control agents had failed to attack the invading Scapteriscus mole crickets in an inadvertent field experiment of [greater than or equal to]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 nontarget organisms, ruled against a long-term test for a host shift before release. Subsequent data have thus far vindicated the risk that was taken and have shown benefits 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 [approximately]1900. These belong to the tribe Scapteriscini, whereas native mole crickets belong to the genera Neocurtilla and Gryllotalpa of the tribe Gryllotalpini (Otte 1994) and differ in behavior, habitat, physiology, and natural enemies. The invading Scapteriscus 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 crickets considered by Simberloff 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 control agents were released and because the mole cricket program has data about it, as a model for the tribe Gryllotalpini. Simberloff and Stiling express concern about Gryllotalpa major, which occurs in heavy soils in prairie remnants in Arkansas, Kansas, Missouri, and Oklahoma and is rare because of habitat loss (Vaughn et al. 1993). It was proposed in 1990 as a candidate for federal listing as a threatened species (not as an endangered species, as stated by Simberloff and Stiling), 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 specialized natural enemies including the wasp Larra analis (Sphecidae) and the nematode Steinernema neocurtillae (Steinernematidae). Six native species of flies of the genus Ormia (Tachinidae) are parasitoids of various insects (some Orthoptera, some unknown), but none of their hosts is a mole cricket.

Simberloff and Stiling, reasonably, express no concern about N. hexadactyla, which has somehow expanded its range to South America and has even been considered a pest there (I presume that its native North American natural enemies did not accompany it to South America). They express concern for Gryllotalpa major, which is far more closely related to N. hexadactyla than to Scapteriscus. No specialized natural enemies of G. major are known.

Introduced biological control agents and the risks they pose

The targets of the mole cricket program are the three Scapteriscus species, which differ considerably from one another in behavior and susceptibility to the introduced biological control agents (Frank 1994). Just as N. hexadactyla has its own specialized native natural enemies in the USA, so Scapteriscus spp. have specialized natural enemies in South America. Those that the mole cricket program has imported, released, and established in Florida against Scapteriscus are Larra bicolor, Ormia depleta, and Steinernema scapterisci (Frank 1994).

Larra spp. are diurnal digger wasps for which the only recorded hosts are mole crickets (Menke 1992). The only Larra species imported from South America and established in Florida is Larra bicolor, first from a stock originating from Belem, Para, Brazil (via Puerto Rico), and later from a stock from Santa Cruz, Bolivia (Frank et al. 1995). The Brazilian stock of L. bicolor, apparently for climatic reasons, failed to become established in central and north Florida, despite releases there. The Bolivian stock became established at 29 [degrees] N, its only place of release. This Larra species is a specialist on Scapteriscus mole crickets and is normally repelled by the defensive behavior of Neocurtilla hexadactyla (Castner 1984). Under laboratory conditions, when N. hexadactyla and a female L. bicolor are confined together in a glass vial, the attacking female L. bicolor sometimes succeeds in laying an egg on N. hexadactyla, but the resultant Larra larva dies, apparently due to physiological defenses of this nonhost mole cricket (Pruett and Bennett 1991). Evidence of specialization also comes from early attempts at introduction of L. bicolor into Hawaii in the 1920s against a nonindigenous Gryllotalpa species; the wasp failed to become established (Frank et al. 1995). The biological control practitioners at that early date failed to understand that L. bicolor specializes on Scapteriscus mole crickets, and that Scapteriscus is not closely related to Gryllotalpa. These observations suggest that a host shift by L. bicolor to mole crickets of the tribe Gryllotalpini is a remote possibility.

Ormia spp. females are nocturnal, larviparous, phonotactic flies that locate hosts (from some distance) by tracking the courtship song of male hosts (e.g., Robert et al. 1992). The stock of Ormia depleta imported into Florida is from Piracicaba, Sao Paulo, Brazil. Releases were made in all regions of Florida (and in Alabama, Georgia, and North Carolina), and the fly has occupied all areas south of [approximately]28 [degrees] N, but has not achieved a permanent presence northward (Frank et al. 1996, Walker et al. 1996). Evidence for its specificity to Scapteriscus borellii and S. vicinus is given by Frank et al. (1996). The songs of its Scapteriscus hosts are continuous trills, whereas that of G. major is a set of brief chirps, resembling that of the nonhost N. hexadactyla (Walker and Figg 1990). Since its introduction, O. depleta has not adapted to attack N. hexadactyla (we have found no infected specimens), which is not rare and is now sympatric with Scapteriscus in the coastal plains. The available data suggest a host shift to Gryllotalpa or Neocurtilla is unlikely.

Steinernema spp. are entomopathogenic nematodes with considerable interspecific differences in specialization to hosts. In the early 1980s some 2000 mole crickets trapped at various locations in Florida were held for emergence of entomopathogenic nematodes. Some Neocurtilla hexadactyla produced a steinernematid nematode described later as Steinernema neocurtillae, which has not yet been found in any other mole cricket (Nguyen and Smart 1992). Trapping of Scapteriscus mole crickets in Uruguay, however, yielded a steinernematid nematode subsequently described as Steinernema scapterisci which proved to be highly pathogenic to Scapteriscus borellii and S. vicinus, but not to S. abbreviatus even under ideal laboratory conditions (Nguyen and Smart 1991). Establishment was obtained in small plots in Florida pastures in 1985. These plots were monitored weekly for five years by trapping mole crickets, holding the mole crickets individually in vials, and identifying nematodes that emerged from all dead and dying mole crickets. Some 200 N. hexadactyla were trapped, along with many more Scapteriscus spp., but only Scapteriscus spp. were infected by S. scapterisci (Parkman et al. 1993). There is thus no evidence that S. scapterisci attacks Neocurtilla hexadactyla even when the latter exists commingled with an infected Scapteriscus population in Florida. That N. hexadactyla has its own entomopathogenic nematode, Steinernema neocurtillae, which has not been found in Scapteriscus, suggests that these two nematode species are coevolved with their hosts and that transfer to mole cricket hosts of other tribes is very improbable.

The main use of steinernematid nematodes has not been as classical biological control agents (as above), but as biopesticides, to be applied at very high density ([approximately]200 000/[m.sup.2]) to soils in expectation of immediate kill of target pests whose defenses are overwhelmed by huge numbers of the nematodes. Biossays of several nematode species (e.g., Ricci et al. 1996) show poor performance of S. scapterisci in standardized tests against larvae of wax moth (Galleria mellonella), indicating that it would not be an effective biopesticide for general use. However, S. scapterisci makes a good biopesticide for use against Scapteriscus borellii and S. vicinus, achieving kill of these insects comparable to that achieved by chemicals. This nematode is produced and marketed for that purpose alone in the coastal plains of the southern USA. A recent intensive review of the use of steinernematid and heterorhabditid nematodes as biopesticides demonstrated them to be relatively safe to nontarget organisms (Bathon 1996, Ehlers and Hokkanen 1996, Parkman and Smart 1996, and others in the same volume).

Climate and allopatry reduce risks

These three introduced biological control agents originated from the tropical (Larra bicolor, Ormia depleta), and mild temperate regions (Steinernema scapterisci) of South America. These organisms were released in Florida without knowledge of the northernmost latitude they might occupy in the continental USA, because it cannot be predicted accurately. The hope was that they might occupy the entire range of North America that is now occupied by invasive Scapteriscus mole crickets: the milder climates of the coastal plains from North Carolina to Florida and west to Texas (not including the prairie states). Reality shows that the Belem strain of Larra bicolor has been unable to survive north of southern Florida, and the Santa Cruz strain occurs only at 29 [degrees] N in northern Florida. I expect that L. bicolor's range will expand southward, but I am no longer optimistic that it will expand northward because of its tropical origin. The Piracicaba strain of Ormia depleta has not been able to establish a permanent presence even as far north as 29 [degrees] N. Of the three biological control agents that the mole cricket program has established in Florida, Steinernema scapterisci is the most likely to be able to tolerate the winter temperatures of the states in which G. major exists, because this species occurs naturally at 35 [degrees] S in Scapteriscus borellii in the pampas of Argentina (Stock 1995). However, the imported stock came from Uruguay and has not yet been shown to survive the winters north of [approximately]31.5 [degrees] N (southern Georgia) although it has been tested and marketed as a biopesticide in South Carolina (C. Gorsuch, unpublished data). Simberloff and Stiling express concern that one or more of these three biological control agents might attack G. major in Arkansas, Kansas, Missouri, or Oklahoma (33 [degrees] 40.5 [degrees] N). Current evidence of climatic limitations of the imported stock of biological control agents suggests that such a range expansion is unlikely.

The range of G. major is distant from that of any of the Scapteriscus invaders in the USA. For propagules of any of these biological control agents to cross hundreds of kilometers of territory unoccupied by mole crickets other than N. hexadactyla (which proves not to be a suitable host for any of them) and then instantaneously (death is at most weeks away) to adapt to a scarce nonhost (Gryllotalpa major) that is much more closely related to N. hexadactyla than to the Scapteriscus hosts is so remote as to be untenable.

Evolution of natural enemies, and rarity of G. major

If the imported biological control agents are to evolve to kill G. major, then the possible steps are: (1) evolve to kill and reproduce in N. hexadactyla, (2) adapt to colder climates, (3) expand range using N. hexadactyla as hosts until sympatry with G. major is achieved, and (4) evolve to kill yet another host, G. major. An alternative scenario is that (1) one of the Scapteriscus species (most likely S. borellii) expands its range to become sympatric with G. major, (2) that one of the biological control agents adapts to colder climates and follows this host, and (3) that this biological control agent evolves to kill G. major. I cannot state categorically that these steps will never happen, nor can I state that some hummingbird will never evolve to insectivory, but I think the risks are extremely low. The results of a (now) [greater than]90 yr inadvertent field experiment have, after all, 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, somehow, one of the imported biological control agents arrives in the habitat of G. major, the frequency of encounter with this mole cricket would be low and this would hinder a host shift.

The risks of alternatives to biological control

Simberloff and Stiling question the risks of introducing the three above-mentioned biological control agents. The other side of the balance sheet is the benefit that biological control of Scapteriscus mole crickets can achieve. At stake, in Florida alone (much more is at risk in other southern states) are [approximately][10.sup.6] ha of bahiagrass (Paspalum notatum) pastures, [approximately]5 x [10.sup.5] ha of bahiagrass and bermudagrass (Cynodon spp.) turf (including [approximately]1200 golf courses), other pasture and turf grasses, and [approximately]45 000 ha of the most susceptible vegetables (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 to the point that pastures may be entirely destroyed. The only alternatives to the biological control agents that the mole cricket program has introduced are (1) no action, and (2) a few chemical pesticides that can be used where cattle graze. Frequent use of those pesticides is too costly for most cattle ranchers because of the low prices for beef, and in the past they have used the cheap but persistent and environmentally harmful pesticide chlordane (Frank 1994).

In 1986, damage and costs of control to turf grasses by Scapteriscus mole crickets in Florida were estimated as [greater than]$44 million annually, with an additional $33 million in Alabama, Georgia, and South Carolina; losses in other states (North Carolina, Louisiana, Mississippi, and Texas) were not estimated (R. D. Hudson, unpublished 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 Florida as in other southern states is the use of broadspectrum chemical pesticides (e.g., carbaryl, ethoprop, and fonofos). Playing fields and home lawns are extremely important sites of use of chemical pesticides 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 alternatives to chemical pesticides. The reality of massive kills of birds after ingesting diazinon-poisoned mole crickets on golf courses ended in 1988 (the year that the mole cricket program released its third biological control agent in Florida), and only the specter seems to remain (Rainwater et al. 1995). Yet, an equal reality is that harm to nontarget invertebrates has hardly lessened. Chemical insecticides such as ethoprop, carbaryl, and fonofos at labelled dosages are lethal to earthworms, and other chemical pesticides that are commonly 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). Populations of many hundreds of nontarget invertebrate species are harmed on golf courses and lawns and playing fields in the southern USA by treatment with chemical pesticides against Scapteriscus mole crickets. Unfortunately, nobody has assessed the value of such invertebrates.

Now, vegetable fields in Florida are usually fumigated with a methyl bromide/chloropicrin mixture to control soil-dwelling pests including mole crickets (e.g., Noling and Becker 1994). This chemical mixture is a potent biocide which kills virtually all soil organisms.

The picture, though economists have documented little of it, is one of tremendous annual losses due to Scapteriscus mole crickets, with chemical pesticides still the overwhelming recourse for preventive use by farmers, ranchers, and turf managers. Biopesticides like Steinernema scapterisci (and also S. riobravis, a less specialized nematode from the southwestern USA) currently make up a tiny percentage of total use. Classical biological control agents (Larra bicolor, Ormia depleta, and Steinernema scapterisci) are reducing populations of Scapteriscus borellii and S. vicinus (Parkman et al. 1996; H. Frank unpublished data for 1995-1996) and are therefore reducing the need to apply pesticides. However, their contribution is little appreciated, because nobody outside the mole cricket program 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 Scapteriscus mole crickets, and such applications yield only temporary control. The chemicals do not kill Scapteriscus mole crickets only, and it is likely that most soil-dwelling invertebrates are killed by chemical pesticides over hundreds of thousands of hectares annually. Annual sales of chemicals for control of Scapteriscus mole crickets are an important source of revenue for chemical companies which, naturally, 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. Incomplete 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 Scapteriscus mole crickets is justified environmentally and economically. It has not caused collateral damage and appears unlikely to be able to do so.


I thank J. L. Capinera, M. A. Hoy, L. P. Lounibos, S. D. Porter, T. J. Walker, and reviewers for criticism of manuscript drafts. This is Florida Agricultural Experiment Station journal series no. R-05519.

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Title Annotation:response to D. Simberloff and P. Stiling, Ecology, vol. 77, p. 1965, 1996
Author:Frank, J.H.
Date:Jul 1, 1998
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