BIOLOGICAL CONTROL-PARASITOIDS AND PREDATORS Prey Suitability and Phenology of Leucopis spp. (Diptera: Chamaemyiidae) Associated With Hemlock Woolly Adelgid (Hemiptera: Adelgidae) in the Pacific Northwest 1 1,2 1,3,4 SARAH M. GRUBIN, DARRELL W. ROSS, AND KIMBERLY F. WALLIN Environ. Entomol. 40(6): 1410Ð1416 (2011); DOI: http://dx.doi.org/10.1603/EN11127 ABSTRACT Leucopis spp. (Diptera: Chamaemyiidae) from the PaciÞc Northwest previously were identiÞed as potential biological control agents for the hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae), in the eastern United States. We collected Leucopis spp. larvae from A. tsugae infested western hemlocks in Oregon and Washington and reared them on an unidentiÞed Pineus spp., Pineus strobi (Hartig), Adelges cooleyi (Gillette), Adelges piceae (Ratzeburg), and A. tsugae in three no-choice tests. Leucopis spp. survival on A. tsugae was signiÞcantly higher than on A. piceae during the 2010 progrediens generation test and signiÞcantly higher than on P. strobi and A. cooleyi during the 2010 sistens generation test. However, across all three tests, some larvae completed development to adult on all four of the alternative adelgid species. Larvae that survived to the adult stage were identiÞed as Leucopis argenticollis Zetterstedt and Leucopis piniperda Malloch. These results suggest that populations of L. argenticollis and L. piniperda in the PaciÞc Northwest may not be speciÞc to A. tsugae. We also studied the phenology of Leucopis spp. on fourteen A. tsugae infested western hemlock trees in Oregon and Washington over a period of 14 mo. Leucopis spp. larvae were collected year-round, but highest densities coincided with the presence of progrediens and sistens eggs and adults of A. tsugae. There was a positive correlation between Leucopis spp. and A. tsugae abundance. KEY WORDS Adelges tsugae, biological control, Leucopis argenticollis, Leucopis piniperda, prey suitability The hemlock woolly adelgid, Adelges tsugae Annand ban and horticultural settings, their use in forests is (Hemiptera: Adelgidae), accidentally was introduced limited by accessibility, potential nontarget effects, into eastern North America from a location in south- and other ecological and economic concerns (Cowles ern Japan (Havill et al. 2006). It was Þrst discovered 2009, Dilling et al. 2009, Ford et al. 2010). Conse- near Richmond, VA in 1951 (Stoetzel 2002), but did quently, a classical biological control program was not cause signiÞcant mortality of eastern hemlocks initiated in 1992 with the intent of providing long- until the 1980s (McClure 1987, Souto et al. 1996). It has term, region-wide suppression of A. tsugae populations been spreading throughout the eastern United States (McClure 2001, Cheah et al. 2004). Because parasi- at a mean rate of 12.5 km/yr and appears to be limited toids of adelgids are uncommon, if they exist at all, only by cold temperatures (Shields and Cheah 2005, biological control efforts have focused primarily on Evans and Gregoire 2006, Morin et al. 2009). It is now predators (Wilson 1938, Montgomery and Lyon 1996, found from northern Georgia to southern Maine Yu et al. 2000, Zilahi-Balogh et al. 2002) and, to a (Anonymous 2009) causing high levels of mortality to smaller extent, entomopathogens (Reid et al. 2009). eastern and Carolina hemlocks, Tsuga canadensis (L.) This program has led to the release of three coleop- Carrie´re and Tsuga caroliniana Engelmann, respec- teran predator species, Sasajiscymnus tsugae (Sasaji tively (Orwig and Foster 1998, Eschtruth et al. 2006, and McClure) (Coccinellidae) from Japan, Scymnus Faulkenberry et al. 2009). sinuanodulus Yu and Yao (Coccinellidae) from China, Although insecticide applications are effective for and Laricobius nigrinus Fender (Derodontidae) from suppressing A. tsugae populations, particularly in ur- western North America (Cheah et al. 2004, Mausel et al. 2010). However, none of these predators have yet provided the desired suppression of A. tsugae popu- 1 Department of Forest Ecosystems and Society, Oregon State Uni- versity, 321 Richardson Hall, Corvallis, OR 97331Ð5752. lations, and efforts have continued to identify other 2 Corresponding author, e-mail: [email protected]. predator species in Asia and western North America 3 The Rubenstein School of Environment and Natural Resources, as good candidates for release in the eastern United The University of Vermont, 81 Carrigan Dr., Burlington, VT 05405Ð States (Yu et al. 2000, Zilahi-Balogh et al. 2007, Kohler 0088. 4 USDA Forest Service, Northern Research Station, South Burling- et al. 2008, Yu and Montgomery 2008, Gatton et al. ton, VT 05403. 2009). 0046-225X/11/1410Ð1416$04.00/0 ᭧ 2011 Entomological Society of America December 2011 GRUBIN ET AL.: PREY SUITABILITY AND PHENOLOGY OF Leucopis spp. 1411 In the PaciÞc Northwest, Kohler et al. (2008) iden- ined under a dissecting microscope, and Leucopis spp. tiÞed 55 species of predators representing 14 families eggs and larvae were removed. The immature Leucopis associated with A. tsugae on western hemlock, Tsuga spp. were used immediately for testing because there heterophylla (Raf.) Sargent, of which L. nigrinus was were no rearing methods or artiÞcial diet known for the most abundant, followed by two species of these insects, although rearing procedures have been Chamaemyiidae (Diptera), Leucopis argenticollis developed for aphidophagous Leucopis spp. (Gaimari Zetterstedt and Leucopis piniperda Malloch (as Leu- and Turner 1996). copis atrifacies Aldrich) (S. Gaimari, personal com- In addition to A. tsugae eggs, collected from the munication). Both L. argenticollis and L. piniperda are same sites as the Leucopis spp., four alternative species known adelgid specialists (McAlpine and Tanasijts- of prey were used in host suitability tests based on hunk 1972, Tanasijtshuk 2002), but this was the Þrst taxonomic or ecological similarity to A. tsugae as well record of either species associated with A. tsugae as seasonal and geographic availability (Kuhlmann et (Kohler et al. 2008). Leucopis argenticollis is a Holar- al. 2005). All selected test prey were species of Adel- ctic species that was previously found in colonies of gidae, representing both genera in the family. All test several Pineus species in Russia, India, Canada, and the prey were Þeld collected in the egg stage and held at United States (McAlpine and Tanasijtshunk 1972). 3ЊC until used in the feeding trials. The four alternative Leucopis piniperda is found throughout Canada and prey were an unidentiÞed Pineus spp. collected from the United States in association with several Adelges branches on young lodgepole pine, Pinus contorta Dougl. and Pineus spp. (Greathead 1995, Tanasijtshuk 2002). ex. Loud., located in the Deschutes National Forest near After the introduction of Adelges piceae (Ratzeburg) Bend, OR; P. strobi collected from an ornamental plant- into North America, L. argenticiollis was found asso- ing of white pine, Pinus monticola Dougl. ex D. Don, in ciated with A. piceae in eastern Canada (McAlpine and Wilsonville, OR; A. piceae collected from Fraser Þr, Abies Tanasijtshunk 1972). fraseri (Pursh), in a Christmas tree plantation in Lane The potential value of chamaemyiids as biological County, OR; and Adelges cooleyi (Gillette) collected control agents for adelgids has been recognized since from an ornamental Douglas-Þr, Pseudotsuga menziesii at least the 1930s. After the accidental introduction of (Mirb.) Franco, located on the Oregon State University Pineus pini (Macquart) into Australia, Wilson studied campus in Corvallis, OR. the natural enemies of P. pini and Pineus strobi Hartig Three no-choice feeding tests were conducted; one in England (Wilson 1938). He identiÞed Neoleucopis during the 2009 A. tsugae sistens generation, and two obscura (Haliday) as the most efÞcient predator of in 2010, coinciding with the A. tsugae progediens and these species and suggested that it should be intro- sistens generations. The number of Leucopis spp. im- duced into Australia for biological control of P. pini. matures fed each alternative prey depended upon the Subsequently, a number of chamaemyiid species have number that could be found during each A. tsugae been considered for biological control of Pineus and generation, and ranged from 16 to 36 (Table 1). Dur- Adelges species throughout the world with varying ing the 2009 sistens generation, test prey were A. degrees of success (Rawlings 1958, Zu´ n˜ iga 1985, Cul- tsugae and the unidentiÞed Pineus spp.; during the liney et al. 1988, Zondag and Nuttall 1989, Mills 1990, 2010 progrediens generation, test prey were A. tsugae, Greathead 1995, Zilahi-Balogh et al. 2002). P. strobi, A. cooleyi, and A. piceae; and during the 2010 Other than a few collection records, there is little sistens generation, test prey were A. tsugae, P. strobi, published information about the biology and ecology and A. cooleyi. of L. argenticollis and L. piniperda. Because these spe- Individual Leucopis spp. eggs or larvae of any devel- cies are common and abundant associates of A. tsugae opmental stage were randomly assigned to each test prey in the PaciÞc Northwest, populations from this region as they were collected. Feeding test containers were may be sources of additional introductions for the 50-mm-diameter petri dishes with 2.5-cm holes drilled in biological control program in the eastern United the lid and covered with Þne mesh screen. Two layers of States. Our objectives were to 1) compare the suit- Þlter paper