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Comparative Cold Tolerance and Climate Matching Of Biological Control 58 (2011) 96–102 Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Comparative cold tolerance and climate matching of coastal and inland Laricobius nigrinus (Coleoptera: Derodontidae), a biological control agent of hemlock woolly adelgid ⇑ D.L. Mausel , R.G. Van Driesche, J.S. Elkinton University of Massachusetts, Department of Plant, Soil and Insect Science, 102 Fernald Hall, Amherst, MA 01003, United States article info abstract Article history: Laricobius nigrinus (Coleoptera: Derodontidae) was first collected near the coastal city of Victoria, British Received 1 June 2010 Columbia, Canada for release as a biological control agent to suppress tree-killing densities of hemlock Accepted 8 April 2011 woolly adelgid, Adelges tsugae (Hemiptera: Adelgidae), in the eastern United States. Beetles established Available online 20 April 2011 in warm areas of the invaded range of A. tsugae, but had a low probability of establishment in cold areas. With the goal of locating beetles with greater cold-tolerance, we collected hundreds of adults in the Keywords: northern Rocky Mountains. To support planned releases of these inland L. nigrinus, the cold tolerance Tsuga canadensis of field-collected coastal (Seattle, WA) and inland (Coeur d’Alene and Moscow, ID) adults and climate Adelges tsugae match index scores (CLIMEX v.2) of these collection areas and parts of the eastern United States were Laricobius nigrinus Classical biological control compared. We found that individuals of inland L. nigrinus were more cold tolerant than those of coastal Intraspecific variation L. nigrinus, based on higher survival in a winter field cage study in Massachusetts and a lower superco- Cold tolerance oling point in a laboratory assay. Inland L. nigrinus also had higher survival than coastal L. nigrinus after Climate matching an 18 h exposure to sub-zero temperatures in another laboratory assay. Areas of the eastern United States infested with A. tsugae and receiving L. nigrinus releases matched the climate of Seattle and Coeur d’Alene reasonably well, but Coeur d’Alene had higher index values over a considerably larger area than Seattle. Accordingly, inland L. nigrinus appears preferable for release in the colder portions of A. tsugae’s invaded range in the eastern United States. Published by Elsevier Inc. 1. Introduction impact on A. tsugae populations (Mausel et al., 2008). This ‘‘coastal’’ L. nigrinus, however, had a low probability of establishment in Adelges tsugae Annand (Hemiptera: Adelgidae), native to Asia colder areas, either in more northerly locations or at high eleva- and western North America, was accidentally introduced to east- tions, likely due to winter low temperatures (Mausel et al., 2010) ern North America from Japan (Havill et al., 2006) and is recog- that exceeded the cold tolerance limits of the beetle (Humble nized as the most important pest of eastern hemlock, Tsuga and Mavin, 2005). canadensis (L.) Carrière, and Carolina hemlock, Tsuga caroliniana If available, release of a L. nigrinus ‘‘biotype’’ with greater cold Engelmann (Anonymous, 2005). Laricobius nigrinus Fender (Cole- tolerance could improve both establishment probability and im- optera: Derodontidae), a predator released against A. tsugae in pact on A. tsugae because L. nigrinus is most active during the cold the eastern United States, is native to the northwestern United seasons (Zilahi-Balogh et al., 2003a,b) and release areas in the east- States and western Canada (Fender, 1945). The original releases ern United States are colder than the Puget Trough (Humble and in the eastern United States were made with beetles collected from Mavin, 2005). L. nigrinus has been recorded from the Rocky Moun- the Puget Trough area (e.g., Victoria, British Columbia and Seattle, tains (e.g., Coeur d’Alene and Moscow, Idaho in this study) of the Washington), which has a mild maritime climate. After their re- northwestern United States and Canada (Fender, 1945; Lawrence, lease, beetles from Victoria established in the mid- and southern 1989; Bright, 1991), an area with a continental climate. In this ‘‘in- Appalachian Mountains (Lamb et al., 2006; Mausel et al., 2010), land’’ area, winters are colder and snowier than in the coastal areas where they proved to be well synchronized and demonstrated an from which the original L. nigrinus beetles were collected for re- lease. Additionally, inland summers are warmer and precipitation occurs year-round, while on the coast summers are cooler and ⇑ Corresponding author. Fax: +1 413 545 5858. drier (Humble and Mavin, 2005). The similarity of seasonal tem- E-mail address: [email protected] (D.L. Mausel). perature and precipitation patterns between collection and release 1049-9644/$ - see front matter Published by Elsevier Inc. doi:10.1016/j.biocontrol.2011.04.004 D.L. Mausel et al. / Biological Control 58 (2011) 96–102 97 sites (i.e., climate matching) is fundamental to natural enemy D. Don, infested with Pineus similis (Gillette) (Hemiptera: Adelgi- introductions, and mismatched natural enemies can fail to estab- dae) at the University of Idaho Arboretum, Moscow, Latah Co., ID lish or spread throughout a pest’s invaded range (Hopper et al., (46.7 N, 117.0 W; elevation 805 m). Beetles were shipped over- 1993). night on excelsior in escape-proof containers to the University of Another principle of classical biological control is to collect Massachusetts, Amherst, and were placed in environmental cham- large numbers of a natural enemy over a wide variety of environ- bers at 5 °C day and 2 °C night, 75% relative humidity (RH), season- ments in its native range to capture population variation in traits ally adjusted photoperiod, where they were fed locally collected that may influence effectiveness (Hopper et al., 1993). Coastal A. tsugae ad libitum before use in experiments. and inland L. nigrinus are disjunct, being isolated by a lack of suit- Adult beetles from both Coeur d’Alene and Moscow, ID (col- able host plants for adelgids in the arid Columbia Plateau area lected from different adelgid species) were confirmed morpholog- (Burns and Honkala, 1990), which divides the Cascade Mountains ically to be L. nigrinus by both Zilahi-Balogh (Canadian Food from the Rocky Mountains. Small but consistent differences in Inspection Agency) and Vandenberg (US Department of Agricul- COI gene sequences between coastal and inland L. nigrinus (0.5% se- ture, Agriculture Research Service). Furthermore, DNA sequences quence divergence) suggest that these beetles represent distinct from the mitochondrial COI gene from Coeur d’Alene and Moscow populations but that they are the same species (Havill, Personal beetles were indistinguishable from each other but were distin- Communication). Despite a lack of extensive data on the actual guishable from coastal beetles (Havill, Personal Communication). boundaries of L. nigrinus populations in a genetic context, re- The adelgid on western white pine was identified as P. similis by stricted gene flow between coastal and inland sources implies a comparing its COI sequence with other specimens determined by potential for long-term genetic differentiation in important life- morphology (Havill, Personal Communication). history features such as host-range and cold tolerance. Laricobius spp. are considered adelgid specialists (Lawrence and Hlavac, 2.2. Experiments 1979) and host-range testing of inland L. nigrinus suggests low risk to non-target organisms (Mausel et al., unpublished data) as deter- 2.2.1. Survival in field cages mined previously for coastal L. nigrinus (Zilahi-Balogh et al., 2002). To test for differences in survival of coastal (Seattle) and inland The existence of intraspecific variation in beetle cold tolerance has (Coeur d’Alene and Moscow) L. nigrinus adults under harsh winter been demonstrated previously in the Scolytidae (Bentz and Mul- conditions, we conducted a field cage study from 20 December lins, 1999; Lombardero et al., 2000; Khåi et al., 2007). 2007 to 17 January 2008 in Leverett, MA (42.4 N, 72.5 W) using That such natural enemy variation matters is shown in a 10 year eastern hemlock at a site with 183 m elevation and an eastern as- field experiment in New Zealand, in which release of Microctonus pect with 20% slope. Ten A. tsugae-infested eastern hemlock trees, hyperodae Loan (Hymenoptera: Braconidae) sourced from east of separated by 20 m along a transect, were selected for use, with the Andes outperformed releases sourced from west of the Andes treatments arranged in a randomized complete block design in a successful biological control program against the South Amer- (n = 10). Cages were bags made of sewn polyester fabric ican weevil Listronotus bonariensis (Kuschel) (Coleoptera: Curculi- (0.25 mm mesh size), 0.6 m wide, and 0.9 m long (National Filter onidae) (Phillips et al., 2008). Knowledge of L. nigrinus variation Media Corp., Wallingford, CT). Three branches (>2 m height) with in cold tolerance could be used to design an efficient collection high adelgid densities (i.e., nearly every needle base having an and release program. Here we report results of studies on the rel- adelgid) were tagged per tree, and each caged branch was ran- ative degree of cold tolerance of coastal and inland populations of domly assigned to a beetle treatment (Seattle, Coeur d’Alene, or L. nigrinus. Adult survival during winter was compared in field Moscow). Ten adult beetles were placed inside each cage. The cage cages on hemlock branches in western Massachusetts. In the labo- was pulled over the branch, and tightly closed with a cable tie ratory, the supercooling point of adults and the survival of adults around the bag and stem. One temperature logger (iButton, Maxim after an 18 h exposure to sub-zero temperatures (i.e., 1.5 °C above Integrated Products Inc., Sunnyvale, CA) was deployed per tree in a the mean supercooling point of coastal L. nigrinus) were compared. cage and data were recorded at 1-h intervals.
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