Many scolytine beetle species have been expanding in new territories, travelling with wood and plants for planting, sometimes with a high impact on plant health. Here, we attempt to quantify the mobility of these species and to identify the biological drivers of mobility and impact. Mobility was estimated by counting the numbers of landmasses (contiguous pieces of land, surrounded by ocean or sea) colonised by each species. A series of potential drivers (taxonomic tribes; feeding regimes; polyphagy; reproductive strategy; host taxa; aggregation pheromones and long-range primary attractants), as well as impact on host health were recorded. A total of 163 species were identified, out of 5546 counted in the whole subfamily. The cosmopolitan taxa amongst the subfamily showed significant disharmony with regards to invasion frequency. Four tribes (Xyleborini; Ipini; Crypturgini; Hylastini) were significantly over-represented and two others (Corthylini; Hexacolini) were under-represented. Some 53% of the 163 species are inbreeding, a very significant excess as compared to the whole subfamily (29%). The inbreeders colonised more landmasses than the outbreeders. There is a significant relationship between the number of host families attacked by a species and the number of colonised landmasses. Most of the invasive species are recorded to respond to long-range host primary attractants, only one quarter respond to pheromones. All very mobile species respond to long-range primary attractants and none is known to respond to pheromones. Very mobile species are all associated with a substantial or moderate impact. The most mobile species belong to a limited number of subtribes. They are often inbreeding, polyphagous and respond to long-range primary attractants, but do not produce pheromones. However, there are many counter-examples. The outbreeding Scolytus multistriatus attacks only three host families, producing aggregation pheromones and has established in thirteen landmasses, with a high impact. Due to these many exceptions, species-based risk prediction relying on the few traits routinely analysed in literature suffers from important uncertainties.

ambrosia beetles, bark beetles, entry, establishment, fungi, geographic distribution, impact, inbreeding, landmasses, polyphagy, quarantine, risk assessment, spread, semiochemicals

Very few species are studied in depth before they become noticeable pests. Consequently, most attempts to assess the risk of potentially invasive species rely on limited information. Invasive species assessments now use multiple methodologies ranging from consensus-seeking horizon scans to climate match modelling. However, nearly all these methodologies suffer from one fundamental problem – lack of information about the interactions between a specific species and its potential new environment or hosts.

The typical solution is to take a broader taxonomic perspective and assume that the ecology of a species can be derived from the ecology of related species for which there is more knowledge or to assume that species within a genus are ecologically similar. The invasive species modelling literature is rich with examples of assessments of genera or even entire families or even guilds (see, for example, Mech et al. 2019; Barwell et al. 2020; Schulz et al. 2021).

Some of the most damaging forest pests in the world are bark and ambrosia beetles belonging to the weevil (Curculionidae) subfamily Scolytinae. Global climate change and intense silviculture enabled species, such as Dendroctonus ponderosae Hopkins and Ips typographus L., to multiply to epidemic proportions in North America and Europe, respectively (Grégoire et al. 2015; Hicke et al. 2016) with a total of 455.7 million m³ of pine killed by D. ponderosae in British Columbia between 2000 and 2015 (British Columbia Government 2019) and 148 million m³ of spruce killed by I. typographus between 1950 and 2000 in Europe (Schelhaas et al. 2003), with dramatically increasing damage during the last few years (Hlásny et al. 2021). In addition to these species which are currently spreading within their native continents only, many others have been expanding their territorial range worldwide, especially travelling with international trade. Bark and ambrosia beetles may additionally cause damage as vectors of pathogenic fungi. The redbay ambrosia beetle, Xyleborus glabratus Eichhoff, of Asian origin, was first reported in North America in 2002 (Rabaglia et al. 2006). It vectors the fungal symbiont, Raffaelea lauricola T.C. Harr., Fraedrich and Aghayeva, causing “laurel wilt”. At least 300 million Persea borbonia L. Spreng. (redbay trees) have been killed by laurel wilt in the USA (Hughes et al. 2017) and several other tree species of the Lauraceae family, including avocado (Persea americana Mill.) are also affected by the disease. Another example is the polyphagous shot hole borer, Euwallacea fornicatus Eichhoff (Stouthamer et al. 2017; Smith et al. 2019), a Scolytinae which, together with a symbiotic Fusarium sp. fungus, attacks a large number of plants, mostly in cultivated settings in its area of origin, Asia, as well as, more recently, in areas of introduction1 in North America (Rabaglia et al. 2006), Israel (Mendel et al. 2012) and South Africa (Paap et al. 2018). The North American species Dendroctonus valens LeConte was reported in China at the end of the 1990s and, by 2005, it had spread over 500,000 ha of pine forest in three provinces, killing more than 10 million Pinus tabuliformis Carr. (Yan et al. 2005). Other harmful Scolytinae species killing living trees and recently introduced into Europe include the Asian ambrosia beetle, Xylosandrus crassiusculus (Motschulsky), the black twig borer, X. compactus (Eichhoff) and the walnut twig beetle, Pityophthorus juglandis Blackman. This latter species vectors the pathogenic fungus Geosmithia morbida Kolarík, Freeland, Utley and Tisserat, causing thousand cankers disease of walnuts, Juglans spp. (EPPO 2015; Seybold et al. 2019).

The observed spread of these species and many others continues. At the same time, dozens of bark- and ambrosia beetle species have been introduced into non-native regions without any detectable impact. Most bark beetle “tramp species” are harmless.

So far, at least 163 species out of the ~ 6,000 described scolytine species (Hulcr et al. 2015) are known to have established outside of their native areas (Table 1 and Suppl. material 1). The remaining ninety-eight percent of scolytine species are, thus, still potentially able to colonise new territories and their potential impact is still mostly unknown.

Other species that have not spread to date and which are not recognised as harmful, might start expanding their range, benefiting from the trade of new commodities or from commercial movements along new routes. These beetles, alone or together with pathogens, may also colonise new hosts that may prove to be more susceptible than their native hosts or form new associations with local pathogens as suggested by Rassati et al. (2019a). For both known and unrecognised spreading species, the possibility that they can be successfully introduced into new areas and their subsequent potential economic or environmental impact are two major components of phytosanitary risk.

“Horizontal” regulations globally addressing the host plants of non-native pests are locally implemented. For example, all non-European Scolytinae-attacking conifers are targeted in the European Union by phytosanitary requirements applying to the importation of coniferous wood2 (EU 2019), but equivalent requirements do not exist for the trade of non-coniferous wood. A recent EPPO study focused on twenty-six representative Scolytinae and Platypodinae ambrosia- and bark beetle species associated with non-coniferous wood (EPPO 2020; Grousset et al. 2020). Sixteen life-history traits and other factors were qualitatively weighed with expert knowledge against invasion success. Inbreeding, polyphagy (number of host families) and the lack of aggregation pheromones were common features of species with a successful introduction history. Association with pathogenic fungi, the use of aggregation pheromones and the capacity to attack and kill new host species were identified as factors contributing to high impact. One of the important conclusions of this EPPO study was that traits related to species with a past invasion history had a strong influence on invasion risks. However, it was found that the main factors that are driving successful establishment and impact vary from species to species and are not always fully identified. One important recommendation of this study was that horizontal phytosanitary measures similar to those for conifer wood better address the risk than regulation of individual species. In another recent study, Lantschner et al. (2020) similarly reviewed 123 Scolytinae species with a history of invasion, focusing on biological characteristics (feeding regime and mating strategy), cumulative trade between world regions, size of source species pools, forest area and climatic matching between the invaded and source regions. They identified sib-mating as a major factor favouring the movement of Scolytinae species into new territories, but also found that a non-biological trait, cumulative trade between world regions, is a primary driver of scolytine invasion.

At a broader taxonomic scale, Mech et al. (2019) and Schulz et al. (2021) focused on the impact of non-native herbivorous insects established in North America. They found that the evolutionary proximity between the native and novel host plants, life history traits of the novel hosts and the presence of native close congeners with a long-term association with the novel host were better predictors of impact than were traits of the invading insects themselves.

In this study, we tried to demonstrate that even relatively closely related species can differ in their capacity to colonise new territories and in their impact. We used presence in at least two landmasses (defined below) as a criterion to select 163 “mobile” Scolytinae species and quantified further their mobility by counting the number of colonised landmasses, according to the literature. We also ranked their impact on plant health. Finally, we attempted to identify biological and ecological features (feeding regimes, inbreeding, polyphagy, aggregation pheromones, primary attractants, conifer/non-conifer hosts or both), associated with differences in mobility and impact.

The counting of colonised territories served as a proxy to estimate mobility. A dataset of Scolytinae species known to have spread beyond geographical barriers (across seas or oceans in this study) was constructed (Suppl. material 1), including any species distributed across at least one barrier (hereafter designated as “Scolytinae with an invasion history” - SIH), irrespective of its area of origin which is often difficult to delimit (see, for example, Lin et al. 2021). The list includes all the Scolytinae species from the EPPO study (EPPO 2020; Grousset et al. 2020), as well as the species introduced into North America, New Zealand and Europe, listed respectively by Haack (2001, 2006), Brockerhoff et al. (2006) and Kirkendall and Faccoli (2010). This initial set was expanded using information mostly from Wood and Bright (1992), Lantschner et al. (2020), Atkinson (2021) and from other publications (full list of references in Suppl. material 1). The dataset was completed in December 2020 and, therefore, does not include several important studies (in particular Bright 2021) published after this date.

Amongst the biological features taken into account, the association with pathogens was not considered as a predictor because, in addition to previously known species, species so far harmless on their native hosts (e.g. R. lauricola, G. morbida) become pathogenic when their vectors colonise new host trees. Besides, scolytines species considered as harmless are sometimes found associated with aggressive pathogens (Wingfield and Gibbs 1991), making pathogens a dubious predictor of impact. Climatic requirements, dispersal capacity and voltinism were also not considered, because of the wide knowledge gap regarding these potential drivers (but see EPPO 2020 and Grousset et al. 2020).

Throughout this review, several biological traits, particularly inbreeding and polyphagy, appear correlated with higher introduction potential and impact in new areas. However, as with the results obtained in EPPO (2020) and Grousset et al. (2020) for a narrower range of species, none of these traits, alone or combined, explains the success of all the SIH species and there are obvious outliers. For example, the over-represented tribes Crypturgini and Hylastini (Table 1) are outbreeders. The moderately polyphagous X. glabratus (4 host families) has a much higher impact than H. eruditus (65 host families). More generally, 59 SIH species attack hosts in only one plant family, suggesting many exceptions to the influence of polyphagy on introduction. Whilst aggregation pheromones do not appear to favour establishment, there is the exception of E. fornicatus.

To summarise, some of the identified drivers are widespread amongst SIH species, but none is shared by the whole group, making it difficult to characterise univocally the potentially successful invaders amongst the bark- and ambrosia beetles of the world. In addition, the non-biological risk factors, as identified in EPPO (2020) and Lantschner et al. (2020), also play an important role. As concluded in EPPO (2020), the main factors that are driving successful establishment and impact vary from species to species and are not always fully identified. Still, one single feature common to most of the SIH species has been implicitly identified in this study on species crossing geographical barriers: their capacity to travel by trade, either on wood commodities and wood packaging material or on plants for planting or on fruits, depending on the species. The major conclusion of the present study is, thus, that, because of the lack of drivers that could allow for robust predictions regarding the invasive potential of any scolytine species, it is safer to consider the establishment of horizontal measures for trade of commodities.

HJ and AB participated in this study as part of the HOMED project (http://homed-project.eu/), which received funding from the European Union’s Horizon 2020 Research and Innovation Programme, under grant agreement no. 771271. We are grateful to Sandy Liebhold and Miloš Knížek for useful comments on an earlier draft.