Historical Accumulation of Nonindigenous Forest Pests in the Continental United States

Articles Historical Accumulation of Nonindigenous Forest Pests in the Continental United States Nonindigenous forest insects and pathogens affect a range of ecosystems, industries, and property owners in the United States. Evaluating temporal patterns in the accumulation of these nonindigenous forest pests can inform regulatory and policy decisions. We compiled a comprehensive species list to assess the accumulation rates of nonindigenous forest insects and pathogens established in the United States. More than 450 nonindigenous insects and at least 16 pathogens have colonized forest and urban trees since European settlement. Approximately 2.5 established nonindigenous forest insects per year were detected in the United States between 1860 and 2006. At least 14% of these insects and all 16 pathogens have caused notable damage to trees. Although sap feeders and foliage feeders dominated the comprehensive list, phloem- and wood-boring insects and foliage feeders were often more damaging than expected. Detections of insects that feed on phloem or wood have increased markedly in recent years. Keywords: invasive pests, forest insects, forest pathogens, feeding guild, detection rates N onindigenous insects and pathogens pose a significant threat to the productivity and diversity of forest ecosystems in the United States (Liebhold et al. 1995, Wilcove et al. 1998, Simberloff 2000, Allen and Humble 2002). Awareness of the ecological and economic impacts associated with introduced insects and pathogens (hereafter, pests) has increased in recent years, in part because of highly damaging pests such as the Asian longhorned beetle (Anoplophora glabripennis [Motschulsky]), emerald ash borer (Agrilus planipennis Fairmaire), and sudden oak death (Phytophthora ramorum Werres, De Cock & Man in’t Veld) (Nowak et al. 2001, Rizzo and Garbelotto 2003, Cappaert et al. 2005). Unintentional introductions of nonindigenous species are typically by-products of economic activity. Phytophagous (plant-feeding) insects and plant pathogens may be transported inadvertently with their hosts when nursery stock, produce, or related commodities are shipped. Additional introductions occur when species hitchhike on commodities that may or may not include their host plants (Levine and D’Antonio 2003, Work et al. 2005, McCullough et al. 2006, Westphal et al. 2008). Fortunately, only a fraction of species that arrive in a new environment become established, and an even smaller proportion become invasive pests (Williamson and Fitter 1996). Along with other countries, the United States has implemented regulations designed to reduce the rate of introductions of nonindigenous plant-feeding insects and plant pathogens, beginning with the Plant Quarantine Act (1912). Subsequent regulatory efforts arose from the Organic Act (1944), the International Plant Protection Convention (1952), the Federal Plant Pest Act (1957), the National Environmental Policy Act (1970), and the Plant Protection Act (2000). Within the United States, federal or state quarantines, inspections, and other regulatory efforts are often imposed to limit the transport of established invasive insects and plant pathogens into new regions. Temporal patterns of introductions As a result of rapidly increasing global trade and travel, one might expect a concurrent trend of rising rates of nonindigenous species establishment (Levine and D’Antonio 2003). Indeed, patterns of acceleration in cumulative numbers of establishments have been documented in a variety of taxonomic groups (Wonham and Pachepsky 2006), but such temporal trends have never been demonstrated for forest pests. We investigated whether the rate of accumulation of nonindigenous forest pests in the continental United States has (a) accelerated with increases in international trade and travel during recent decades, (b) remained steady, or (c) decreased as a result of more stringent regulatory measures. Nonindigenous organisms have been introduced both intentionally and accidentally since Europeans first arrived in North America in the 1500s (Levine and D’Antonio 2003, Westphal et al. 2008). More than 400 insect species native to Europe feed on trees, shrubs, or other woody vegetation in North America (Matern et al. 2002, Mattson et al. 2007, BioScience 60: 886–897. ISSN 0006-3568, electronic ISSN 1525-3244. © 2010 by American Institute of Biological Sciences. All rights reserved. Request permission to photocopy or reproduce article content at the University of California Press’s Rights and Permissions Web site at www.ucpressjournals.com/ reprintinfo.asp. doi:10.1525/bio.2010.60.11.5 886 BioScience • December 2010 / Vol. 60 No. 11 www.biosciencemag.org Juliann E. Aukema, Deborah G. M c Cullough, Betsy Von Holle, Andrew M. Liebhold, Kerry Britton, and Susan J. Frankel Articles List of established insect pests We assembled a list of nonindigenous insects known to colonize forest trees with at least one recorded location of establishment in the continental United States (available at www.biosciencemag.org http://knb.ecoinformatics.org/knb/metacat/nuding.7.6/knb). We based our list on published lists and reports (Mattson et al. 1994, 2007, Haack 2006, Langor et al. 2009) and communications with experts. Species included in our list had to feed on at least one tree species found in native forests or common in urban forest settings (e.g., Eucalyptus). We excluded species that have gradually expanded their ranges continuously as a result of migration or climate change, and indigenous invaders (i.e., species native to the United States but introduced into previously uncolonized US regions). We excluded insects and pathogens that colonize primarily agricultural commodities, shrubs, herbaceous plants, and dead or processed wood, as well as predatory, parasitic, and aquatic insects, detritivores, pollinators, and those insects that feed on trees only occasionally. For each insect species on our list, we recorded taxonomy (order, family, genus, species), year or approximate year the species was detected or identified in the United States (when known), feeding guild, and primary host species (when available). For the family Curculionidae, we distinguished between the subfamily Scolytinae, which includes bark and ambrosia beetles, and other curculionids (weevils) for some analyses because of differences among these groups in behavior, survey efforts, and potential impacts. Insects in the order Hemiptera were grouped by suborder for some analyses, when we wished to distinguish among Prosorrhyncha (true bugs), Clypeorrhyncha (leafhoppers, froghoppers), and Sternorrhyncha (aphids, adelgids, scales, whiteflies). When the date of detection for a given species was approximate, we used the following guidelines for analysis: approximately 1950 5 1950; earlier than 1950 5 1949; 1950s 5 1955; 1800s 5 1850. When more than one date was reported, we used the earliest date for analysis (e.g., 1950 and 1956 5 (...truncated)