Biol Invasions (2017) 19:3141–3159 DOI 10.1007/s10530-017-1514-1 FOREST INVASION Ecology of forest insect invasions E. G. Brockerhoff . A. M. Liebhold Received: 13 March 2017 / Accepted: 14 July 2017 / Published online: 20 July 2017 Ó Springer International Publishing AG 2017 Abstract Forests in virtually all regions of the world trade. The dominant invasion ‘pathways’ are live plant are being affected by invasions of non-native insects. imports, shipment of solid wood packaging material, We conducted an in-depth review of the traits of ‘‘hitchhiking’’ on inanimate objects, and intentional successful invasive forest insects and the ecological introductions of biological control agents. Invading processes involved in insect invasions across the insects exhibit a variety of life histories and include universal invasion phases (transport and arrival, herbivores, detritivores, predators and parasitoids. establishment, spread and impacts). Most forest insect Herbivores are considered the most damaging and invasions are accidental consequences of international include wood-borers, sap-feeders, foliage-feeders and seed eaters. Most non-native herbivorous forest insects apparently cause little noticeable damage but some species have profoundly altered the composition and ecological functioning of forests. In some cases, Guest Editors: Andrew Liebhold, Eckehard Brockerhoff and non-native herbivorous insects have virtually elimi- Martin Nun˜ez / Special issue on Biological Invasions in Forests nated their hosts, resulting in major changes in forest prepared by a task force of the International Union of Forest composition and ecosystem processes. Invasive preda- Research Organizations (IUFRO). tors (e.g., wasps and ants) can have major effects on forest communities. Some parasitoids have caused the Electronic supplementary material The online version of this article (doi:10.1007/s10530-017-1514-1) contains supple- decline of native hosts. Key ecological factors during mentary material, which is available to authorized users. the successive invasion phases are illustrated. Escape from natural enemies explains some of the extreme & E. G. Brockerhoff ( ) impacts of forest herbivores but in other cases, severe Scion (New Zealand Forest Research Institute), PO Box 29237, Riccarton, Christchurch 8440, New impacts result from a lack of host defenses due to a Zealand lack of evolutionary exposure. Many aspects of forest e-mail: [email protected] insect invasions remain poorly understood including URL: http://www.b3nz.org indirect impacts via apparent competition and facili- E. G. Brockerhoff tation of other invaders, which are often cryptic and Better Border Biosecurity Collaboration, Lincoln, New not well studied. Zealand Keywords Biogeographic patterns Á Biotic A. M. Liebhold US Forest Service Northern Research Station, resistance Á Establishment Á Impacts Á Invasibility Á Morgantown, WV, USA Invasion pathways Á Invasiveness Á Spread Á Transport 123 3142 E. G. Brockerhoff, A. M. Liebhold Introduction 450 400 Insects are by far the world’s most species rich group USA Europe New Zealand 350 of organisms with approximately 1 million described 300 species (Brusca and Brusca 2003). It is estimated that 250 there are perhaps another seven million species that 200 remain undescribed (Groombridge and Jenkins 2002) 150 and that insects represent more than 50% of all species 100 on earth. Insects play important roles in food web 50 interactions (as herbivores, saprophages, predators 0 and parasites), ecosystem processes (such as pollina- 1810 1820 1830 1840 1850 1860 1870 1880 1890 1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 2010 Cumulative number Cumulative of species detections tion, energy flow, biogeochemical cycling, ecological < 1801 Year succession), and eco-evolutionary processes (e.g., Price et al. 2011). Given their species richness and Fig. 1 Cumulative number of detections (i.e., new establish- wide involvement in ecosystem processes, it is not ments) of non-native forest insect species over time in the USA, Europe, and New Zealand. Data shown are for non-native surprising that insects are also prominent as invasive insects ‘feeding on forest trees’ in the USA and New Zealand) or species both in terms of their number and their impacts ‘feeding on woody plants’ (Europe). Data for the USA (showing (e.g., Kenis et al. 2009; Roques et al. 2009; Brocker- detections until 2010) are based on Aukema et al. (2010) and hoff et al. 2010). Similar observations have been made Yamanaka et al. (2015); data for Europe are according to Roques et al. (2016) and Alain Roques (pers. comm.); for New for invasive insects specific to forests. In the USA Zealand data see Suppl. Mat. 1 alone, ca. 455 non-native insect species feeding on trees were recorded, with about 2.5 new species detections per year (Aukema et al. 2010) (Fig. 1). In such as hemlock woolly adelgid causing an increase of Europe, more than 200 non-native insects inhabiting trees and shrubs other than hemlock, including some woodlands and forests are known (Roques et al. 2009) invasive non-native species (Small et al. 2005), (ii) and approximately 400 species feeding on woody temporary or ongoing decline of forest fauna (e.g., plants (Roques et al. 2016). Brooks 2001), and (iii) changes in forest ecosystem The most widely reported ecological impacts of processes and the provision of ecosystem services invasive forest insects are those by herbivores dam- (Stadler et al. 2005; Boyd et al. 2013). The economic aging or killing trees. A well-documented example impacts of invasive tree-feeding forest insects can be concerns the hemlock woolly adelgid, Adelges tsugae, very substantial with annual costs in the USA of ca. a sap-feeder that was accidentally moved from Japan $2.2 billion in local and federal government expendi- to N. America (Virginia) probably in 1911, first tures, $1.5 billion in lost residential property values, detected there in the 1950s and has since spread across and $150 million in forest landowners’ timber loss most of the range of eastern hemlock, Tsuga canaden- (Aukema et al. 2011). sis, in the eastern USA (Havill and Montgomery Non-native saprophytic insects, as well as preda- 2008). It kills hemlock trees and this has led to a tors, parasitoids and parasites, are also numerous in regional decline in the dominance of hemlock and forests around the world, but these are generally less reversal of successional trends in eastern N. American well studied. Exceptions to this trend include invasive forests (Small et al. 2005; Morin and Liebhold 2015). ants and wasps which have impacts on other fauna that The impacts of emerald ash borer, Agrilus planipen- are well documented (e.g., Gillespie and Reimer 1993; nis, following its invasions of eastern N. America and Beggs 2001; O’Dowd et al. 2003). In New Zealand, western Russia, are even more spectacular, as it is the invasive European wasp Vespula vulgaris is causing massive mortality of ash trees, Fraxinus spp., extremely abundant in Nothofagus forests where it and eliminating the majority of its host trees in the preys on a wide range of invertebrates and may totally invaded areas of N. America (Straw et al. 2013; Herms extirpate some species locally (Beggs 2001). In and McCullough 2014; Morin et al. 2017). A range of addition, V. vulgaris consumes large quantities of indirect impacts of herbivores have been reported, honeydew and it thereby competes with native inver- including (i) changes in plant species composition tebrates and birds for this important food source 123 Ecology of forest insect invasions 3143 (Beggs 2001). In some cases, invasive predators can Ecology of transport and arrival have indirect effects on forest plant communities such as those following the invasion of Christmas Island by World trends of increasing international trade and the yellow crazy ant, Anoplolepis gracilipes (O’Dowd globalization during the last two centuries have led to et al. 2003). Invasive pollinators may reduce the rate of unprecedented movement of species around the world. pollination of native plants; for example, the intro- While most insect invasions are accidental, some duced bumblebee Bombus terrestris ‘robs’ nectar from species, such as certain pollinators and biological New Zealand’s kowhai trees by biting holes into its control agents, have been introduced intentionally. As flowers without actually pollinating them (Donovan the mechanisms of transport and arrival differ consid- 1980). erably between accidental invasions and intentional Although there are thousands of invasive insects, introductions, we will consider these separately. these represent only a very small fraction of the world’s insect species. These species have succeeded Accidental introduction pathways in overcoming multiple barriers along the successive universal phases of invasions that are transport and Contrary to other taxa such as mammals, birds and arrival, establishment in an invaded area, spread and plants, intentional introductions are not the main cause impact (Liebhold and Tobin 2008; Blackburn et al. of non-native insect invasions. Most non-native insect 2011). Invasive species are thought to possess certain species have been accidentally transported with traits that predispose themtobecomingsuccessful imported goods or unintentionally carried by passen- invaders. This has received much attention in plants; gers. However, information on the pathways respon- for example, invasive plants tend to be larger and sible for insect