BioControl (2012) 57:263–276 DOI 10.1007/s10526-011-9392-4 Risks of biological control for conservation purposes Daniel Simberloff Received: 21 January 2011 / Accepted: 30 June 2011 / Published online: 24 July 2011 Ó International Organization for Biological Control (IOBC) 2011 Abstract Striking successes in classical biological and that for biological control, the risk that a species, control in agriculture and rangelands engender great once introduced, will spread beyond its intended range, interest in using this technology for wildlands conser- and the consequences of such spread, are not routinely vation and environmental purposes. However, well treated by risk assessors. This phenomenon deserves known unintended consequences of several biological far more attention. Global changes—especially cli- control projects have led to concern that possible mate change—can lead to modified ranges and effica- environmental benefits do not warrant inherent risks. cies of introduced biological control agents and their Four risks demand attention: (1) direct attack on non- targets. Although many examples show that climatic targets; (2) indirect effects on non-targets; (3) dispersal niches are often not conserved, an important first of a biocontrol agent to a new area, either autono- routine step would be to combine climatic envelopes mously or with deliberate or inadvertent human with general circulation models for predicted future assistance; (4) changed relationships between a control climates. Finally, actions based on a risk assessment agent and a native species, particularly as generated by are always implemented in a framework of predicted global climate change. Procedures for assessing risk of costs and benefits, which are inevitably asymmetric, so direct attack on non-targets by phytophagous biolog- it is critically important that all stakeholders, including ical control agents have steadily improved and an conservationists, participate in the decision-making expanded centrifugal phylogenetic approach appears process. to provide adequate insight. Direct non-target impacts by entomophages are more difficult to predict. Myriad Keywords Climate change Á Dispersal Á Ecosystem possible indirect effects, some subtle but nonetheless impact Á Indirect effect Á Non-target host Á important, present a far greater challenge, and tech- Risk assessment niques of assessing such risks are in their earliest infancy and not as closely regulated. Despite promi- nent examples in both the general invasion literature Introduction Handling Editor: Roy van Driesche The impetus for the growth of classical biological control to deal with introduced species arose from & D. Simberloff ( ) famous successful campaigns in the United States Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USA in the late 19th and early 20th centuries aimed at e-mail: [email protected] eliminating pests of agriculture or ranching. For 123 264 D. Simberloff instance, cottony cushion scale (Icerya purchasi) was These two projects were old ones, the snail, the controlled on citrus in California by the Australian mongoose, and four of the five other ‘‘worst’’ vedalia ladybeetle, Rodolia cardinalis (Caltagirone and invaders (all but the myna) are generalized predators, Doutt 1989), and Chrysolina beetles from Australia and they are not insects. A common response among suppressed Klamath weed (Hypericum perforatus), modern practitioners of biological control is that such which was poisoning cattle and sheep in California projects would not be undertaken today, as the (Huffaker and Kennett 1959). Striking successes such dangers of such non-target impacts are well recog- as these, in which seemingly intractable, expensive nized by professional entomologists, and generalized problems were solved in perpetuity and with minor feeders are shunned (e.g., Murphy and Evans 2009). cost, were subsequently matched by other successful Nevertheless, some more recent instances of insects projects, some of which achieved international rec- introduced for biological control have had troubling ognition—for example, control of pest Opuntia cactus non-target impacts. The case of the weevil Rhinocyl- species in Australia by the South American cactus lus conicus is particularly well known (van Driesche moth Cactoblastis cactorum (Dodd 1940). It is et al. 2008). First introduced from France to North primarily this record of successful projects in the America in 1968 by Agriculture Canada to control service of agriculture and ranching that earned the invasive musk thistle (Carduus nutans), then widely technology a reputation as a ‘‘green’’ alternative to distributed in the United States by federal and state chemical pesticides, particularly as the various non- agencies, this seed predator attacks at least 22 native target impacts of the latter were heralded by Rachel species of Cirsium in North America, including some Carson in Silent Spring (1962) and by many in the species of conservation concern that have been environmental movement triggered by that book. shown to be seed-limited (Louda et al. 1997, 2003; However, there were early biocontrol debacles as Pemberton 2000), among 88 native species and 29 well. The small Indian mongoose (Herpestes auro- subspecies and varieties (NatureServe 2010). It is punctatus), introduced in 1872 primarily for rat control even the primary cause of endangerment of the from the vicinity of Calcutta to Jamaica, then carried federally listed Suisun thistle Cirsium hydrophilum from Jamaica to other islands in the West Indies var. hydrophilum (United States Department of the (occasionally to control snakes as well as rats) and to Interior 1997). The project leaders responsible for Hawaii, and independently from Asia to a number of the initial testing, from Agriculture Canada and other islands around the world, has combined with the Commonwealth Institute of Biological Control, introduced rats and cats to cause several extinctions of recognized the possibility of important non-target endemic mammal and bird species and subspecies and impacts (Zwo¨lfer and Harris 1971, 1984) but con- threatens a number of other taxa (Hays and Conant ducted tests on only one native species of Cirsium 2007). Beginning in 1955, the rosy wolf snail, plus five European species introduced to North Euglandina rosea was introduced widely, first from America and concluded, incorrectly, that the facts Florida to Hawaii, then to various island groups that the weevil chose to oviposit and feed on the primarily in the Pacific, to control the previously target musk thistle, that larval mortality was rela- introduced giant African snail Lissachatina fulica. tively high on the few Cirsium tested, and that adults Euglandina rosea has globally extinguished over 50 that do mature on these Cirsium were smaller than island endemic snail species, such as species of Partula those maturing on Carduus nutans meant that impact in French Polynesia and Achatinella in Hawaii on non-target species would be minimal (Zwo¨lfer and (Civeyrel and Simberloff 1998; Cowie 2002, 2011). Harris 1984). Both the mongoose and the rosy wolf snail are regarded Another increasingly well-known example is that by the World Conservation Union (IUCN) as among of the multicolored Asian lady beetle Harmonia the 100 worst global invaders (Lowe et al. 2001), as are axyridis, a generalist predator of soft-bodied insects. at least five other species introduced for biological First introduced as a biocontrol agent to North control: the flatworm Platydemus manokwari, the cane America in 1916, it was frequently released in large toad (Rhinella marinus), the western mosquitofish numbers in the United States and Canada in the (Gambusia affinis), the Indian myna (Acridotheres 1980s (Koch et al. 2006; Koch and Galvan 2008). tristis), and the stoat (Mustela erminea). It was widely established in North America by 2000, 123 Risks of biological control for conservation purposes 265 although controversy surrounds the source(s) of the In fact, at least four types of risks are apparent: (1) established population (Koch and Galvan 2008). direct attack on non-targets; (2) indirect effects on The beetle was quickly recognized as having non-targets; (3) dispersal of the biocontrol agent to a non-target impacts on native insects, including both new area; (4) changed relationships between a control native coccinellids and phytophagous insects, and agent and a native species, including change gener- also harmed fruit production and became a household ated by global climate change. pest (Koch and Galvan 2008). It has recently spread to South America and northwest Europe, and its introduction for biological control is now widely Direct effects on non-targets regarded as a mistake (Roy and Wajnberg 2008). Although biocontrol began as a technique for pest Variants of the centrifugal phylogeny method control in agriculture and rangelands, it has increas- (Wapshere 1974) have become the modus operandi ingly been used for ecological or conservation pur- for biological control of plants. As a safeguard, poses, in some instances generating great benefits. For Wapshere suggested adding several economically instance, in Florida, the South American alligatorweed important plants to the list, and nowadays often other (Alternanthera phyloxeroides) has been well con- plants are added based on phytochemical or morpho- trolled by the alligatorweed flea beetle, Agasicles logical similarity or other reasonable concerns. The hygrophila, plus a moth and