Oecologia (2000) 122:121–128 © Springer-Verlag 2000 Dean E. Pearson · Kevin S. McKelvey Leonard F. Ruggiero Non-target effects of an introduced biological control agent on deer mouse ecology Received: 04 May 1999 / Accepted: 14 August 1999 Abstract Release of exotic insects as biological control Key words Biological control · Centaurea maculosa · agents is a common approach to controlling exotic plants. Peromyscus maniculatus · Exotic plants · Urophora Though controversy has ensued regarding the deleterious direct effects of biological control agents to non-target species, few have examined the indirect effects of a Introduction “well-behaved” biological control agent on native fauna. We studied a grassland in west-central Montana infested Exotic plants have invaded vast areas of grasslands, prai- with spotted knapweed (Centaurea maculosa) to examine ries, and savannas in western North America, greatly re- the effects of knapweed invasion and two gall fly biologi- ducing the extent and, in some cases, threatening the via- cal control agents (Urophora affinis and U. quadrifasci- bility of these systems (Harris and Myers 1984; Baker ata) on the native deer mouse (Peromyscus maniculatus). 1986; Mack 1986; Harris 1988; Tyser and Key 1988; Stomach-content analysis revealed that Urophora were Lacey 1989; DeLoach 1991; Tyser 1992; Tyser and the primary food item in Peromyscus diets for most of the Worley 1992). In spite of the dramatic vegetation chang- year and made up 84–86% of the winter diet. Stomach es that follow noxious weed invasion in native grass- contents indicated that wild-caught mice consumed on lands (Myers and Berube 1983; Tyser and Key 1988; average up to 247 Urophora larvae mouse–1 day–1, while Rice et al. 1997), little is known about how these shifts feeding trials revealed that deer mice could depredate in plant community composition affect ecological inter- nearly 5 times as many larvae under laboratory condi- actions at higher trophic levels. Moreover, many systems tions. In feeding trials, deer mice selected knapweed invaded by exotic plants have been further complicated seedheads with greater numbers of galls while avoiding by the introduction of exotic insects intended as biologi- uninfested seedheads. When Urophora larvae were pres- cal control agents. In some cases, introduced insects fail ent in knapweed seedheads, deer mice selected microhab- to significantly affect the target weed while rapidly itats with moderately high (31–45% cover) and high achieving high biomass in response to the elevated den- knapweed infestation (≥46% cover). After Urophora sities of its host plant (e.g., Myers and Harris 1980). Un- emerged and larvae were unavailable to Peromyscus, der such circumstances, the insect introduced for biolog- mice reversed habitat selection to favor sites dominated ical control may begin to interact with native organisms by native-prairie with low knapweed infestation (0–15%). to effect its own influence as an exotic agent. Effects of Establishment of the biological control agent, Urophora biological control agents on non-target species can be spp., has altered deer mouse diets and habitat selection by detrimental (Howarth 1983, 1991; Simberloff 1991, effecting changes in foraging strategies. Deer mice and 1992; Simberloff and Stiling 1996a,1996b). other predators may reduce Urophora populations below Spotted knapweed (Centaurea maculosa) is among a threshold necessary to effectively control spotted knap- the most aggressively invasive and extensively estab- weed. lished of the exotic plants in western North America (Maddox 1979; Harris and Myers 1984; Lacey 1989; Sheley et al. 1998). As of 1988, spotted knapweed occu- pied nearly 3 million ha in the northwestern United D.E. Pearson (✉) · K.S. McKelvey · L.F. Ruggiero States and western Canada, resulting in the loss and deg- USDA Forest Service, Rocky Mountain Research Station, radation of large expanses of native prairies, grasslands, Forestry Sciences Laboratory, PO Box 8089, Missoula, MT 59807, USA and savannas (Lacey 1989). e-mail: dpearson/[email protected] As many as 12 species of exotic insects have been re- Fax: +1-406-5432663 leased in the West to control spotted knapweed (Sheley 122 et al. 1998). Two species of gall fly (Urophora affinis rifasciata on the food habits and habitat use of the na- and U. quadrifasciata) introduced in the early 1970s, tive deer mouse. were among the first insects released to control spotted knapweed in western North America (Harris 1980a; Story and Nowierski 1984). Urophora lay eggs in imma- Materials and methods ture knapweed seedheads from mid-June to September (Story et al. 1992). The larvae induce the plant to form a We conducted research in rough fescue (Festuca scabrella) and gall within which the larvae overwinter in the knapweed bluebunch wheatgrass (Agropyron spicatum) grassland types seedheads until pupating in May and emerging in mid (Mueggler and Stewart 1980) that were heavily invaded by spotted knapweed. Knapweed cover ranged from 0 to 95%, resulting in a June (Zwolfer 1970; Story et al. 1992). This behavior re- mosaic of knapweed and native-vegetation patches. Most of the duces seed production by creating a metabolic sink at the native portions of the study area were dominated by rough fescue critical period of seed development (Harris 1980b) and followed by Idaho fescue (F. idahoensis) and a mix of native forbs physically displaces seeds due to competition for space (see Mueggler and Stewart 1980 for descriptions and species lists for vegetation types) with bluebunch wheat grass making up a (Story 1977). lesser component. Bluebunch wheatgrass dominated other sites Urophora spp. are currently established in most areas followed by rough fescue, Idaho fescue, and native forbs. The where spotted knapweed occurs (Harris 1980b; Maddox study area ranged from 1100 to 1700 m elevation on the west as- 1982; Story and Nowierski 1984; Story et al. 1987; pect of Mount Sentinel, due east of Missoula, Montana. Average annual precipitation is 34 cm year–1 with about one-third of this Story et al. 1992) and reach high biomass where knap- occurring as rain in May and June. Average monthly temperatures weed attains high densities. For example, populations of range from –6°C in January to 19°C in July (averages 1949–1994 Urophora spp. in British Columbia have attained densi- from Missoula Johnson Bell National Weather Station). ties 12–18 times greater than those observed in their na- We snap-trapped the study area monthly from March 1997 to tive habitats in Europe (Myers and Harris 1980). In ad- February 1998. Twenty mousetraps were placed at 10-m intervals along each of three transects. Transects were chosen over grids to dition to their elevated biomass, which may serve to at- maximize captures and more effectively assess the community tract predators, Urophora are vulnerable to predation sampled (D.E. Pearson and L.F. Ruggiero, unpublished work). throughout the year because the larvae overwinter in Transects were located ≥200 m apart, parallel to each other and galls within knapweed seedheads. Additionally, adults perpendicular to the slope. We set out traps for 3–7 days (usually 5 days), generally during the first week of each month, and are susceptible to predation while mating on and ovipos- checked them once each day. Trapping effort varied between tran- iting within knapweed flowerheads. As a result, Uroph- sects to equalize sample size among months for stomach content ora spp. have acquired several native predators that at- analysis. We baited traps with approximately 1.0 g of peanut but- tack both larval and adult stages. Story et al. (1995) de- ter within the enclosed metal loop of the trap treadle using a 30-ml syringe. Transect, trap station, and date were recorded for each an- termined that deer mice (Peromyscus maniculatus), imal upon capture and animals were frozen within approximately white-tailed deer (Odocoileus virginianus), and black 1 h of collection. capped chickadees (Parus atricapillus) were the prima- We separated our data into two seasons to test the hypothesis ry predators of Urophora larvae, and that the native spi- that habitat selection by P. maniculatus differed between the peri- der, Dyctina major, preyed heavily on adult flies. Pear- od when Urophora larvae were present in knapweed seedheads (September–May) and the post-emergence period when Urophora son (1999) suggested that Peromyscus maniculatus were larvae were unavailable to P. maniculatus (June–August). Because the dominant predator of larval stages of Urophora spp. snap-trapping generated insufficient captures from June to August He showed that in February mice consumed an average 1997 for habitat analysis (24 animals), we intensively live-trapped of 212 Urophora larvae mouse–1 day–1 and that Uroph- an additional area of Mount Sentinel in August 1998. We set out seven transects of 25 Sherman live traps placed at 10-m intervals ora made up an average of 90% of the stomach contents to encompass patches of near-pristine native grasslands and sites of P. maniculatus during a period of food shortage that exhibiting a range of knapweed infestation. Traps were baited with coincided with the onset of breeding. He speculated that peanut butter and whole oats and checked once each morning for the presence of an abundant, readily accessible resource 4 days. We marked animals with #1005–1 monel ear tags (Nation- al Band and Tag Co., Newport, Ky., USA) and identified to spe- such as Urophora larvae during the historical population cies, weighed, sexed, aged, and determined reproductive status of bottleneck for P. maniculatus (Sadleir 1965; Fairbairn each individual prior to release. The live-trapping area was located 1977) could have a profound impact on their popula- on the same aspect of the mountain and approximately 200 m tions, altering the affected small-mammal communities higher in elevation than the snap trapping transects. The new site and the predators that depend on them.