A large proportion of the insects which have invaded new regions and countries are emerging species, being found for the first time outside their native range. Being able to detect such species upon arrival at ports of entry before they establish in non-native countries is an urgent challenge. The deployment of traps baited with broad-spectrum semiochemical lures at ports-of-entry and other high-risk sites could be one such early detection tool. Rapid progress in the identification of semiochemicals for cerambycid beetles during the last 15 years has revealed that aggregation-sex pheromones and sex pheromones are often conserved at global levels for genera, tribes or subfamilies of the Cerambycidae. This possibly allows the development of generic attractants which attract multiple species simultaneously, especially when such pheromones are combined into blends. Here, we present the results of a worldwide field trial programme conducted during 2018–2021, using traps baited with a standardised 8-pheromone blend, usually complemented with plant volatiles. A total of 1308 traps were deployed at 302 sites covering simultaneously or sequentially 13 European countries, 10 Chinese provinces and some regions of the USA, Canada, Australia, Russia (Siberia) and the Caribbean (Martinique). We intended to test the following hypotheses: 1) if a species is regularly trapped in significant numbers by the blend on a continent, it increases the probability that it can be detected when it arrives in other countries/continents and 2) if the blend exerts an effective, generic attraction to multiple species, it is likely that previously unknown and unexpected species can be captured due to the high degree of conservation of pheromone structures within related taxa. A total of 78,321 longhorned beetles were trapped, representing 376 species from eight subfamilies, with 84 species captured in numbers greater than 50 individuals. Captures comprised 60 tribes, with 10 tribes including more than nine species trapped on different continents. Some invasive species were captured in both the native and invaded continents. This demonstrates the potential of multipheromone lures as effective tools for the detection of ‘unexpected’ cerambycid invaders, accidentally translocated outside their native ranges. Adding new pheromones with analogous well-conserved motifs is discussed, as well as the limitations of using such blends, especially for some cerambycid taxa which may be more attracted by the trap colour or other characteristics rather than to the chemical blend.

Cerambycidae, early detection, Holarctic, invasion, multi-pheromone blend, pheromone trapping

During the last several decades, the unprecedented development of worldwide trade has resulted in increasing translocation and establishment of non-native insects outside their native ranges, with little evidence of saturation (Seebens et al. 2017, 2021). Insect herbivores, accidentally introduced as plant contaminants, appear to be mainly responsible for this sharp increase, at least in Europe (Roques 2010; Pergl et al. 2017). Amongst these non-native herbivores, species associated with woody plants largely dominate, accounting for 76.5% of all herbivore species newly recorded in Europe from 2000 to 2014, while species of importance to agricultural plants and products are a minority (Roques et al. 2016). The increased extent of trade in ornamental plants has been suggested as a major driver of this increase (Liebhold et al. 2012; Eschen et al. 2014; Essl et al. 2015; Roques et al. 2020). Additionally, wood packaging material (e.g. pallets, crating, dunnage) transported with international cargo shipments represents another significant pathway for introduction of non-native phloem- and wood-boring insects (Aukema et al. 2010; Haack et al. 2014; Lovett et al. 2016). An average of 6.1 non-native insect species attacking woody plants became newly established in Europe per year from 2000–2019, compared to 2.4 cases per year from 1950–1970 (Roques et al. 2020). Similar trends were observed in North America (Aukema et al. 2010), New Zealand (Brockerhoff and Liebhold 2017) and at a slower rate in China (Roques et al. 2020).

Another key attribute of this recently-arrived, non-native entomofauna is the increasing presence of “emerging” species, which have not been reported previously as invaders and are not considered to be pests in their native ranges. Arrival of these species probably results from evolving changes in trade routes and imported goods, which leads to accessibility to new pools of species (Seebens et al. 2018). For example, the emerald ash borer, Agrilus planipennis Fairmaire, was not considered a significant pest until it invaded North America, where it has caused massive damage (Dang et al. 2022). The same is true for a number of other xylophagous cerambycid beetle species which have recently invaded Europe, such as the Asian mulberry longhorned beetle, Xylotrechus chinensis (Chevrolat) (Sarto i Monteys and Torras i Tutusaus 2018), the round-headed apple-tree borer, Saperda candida Fabricius (Nolte and Krieger 2008) and the Asian redneck longhorned beetle Aromia bungii (Faldermann) (Russo et al. 2020). At first, such species were typically not subject to regulatory measures or strict phytosanitary inspections at borders because their invasive potential had not been recognised. For example, only seven of the 117 non-native insect species that infest woody plants that established in Europe during the period 1995–2012 had been intercepted in such inspections (Eschen et al. 2015). In Australia, 61 of the 135 non-native species established in forests during the period 2003–2016 had never been intercepted, despite relatively intensive border controls (Nahrung and Carnegie 2021). Therefore, the development of new strategies to detect such unanticipated and unregulated species as early as possible is essential to implement rapid and effective eradication or containment measures (Nahrung et al. 2023).

Deployment of traps baited with broad-spectrum semiochemical lures at ports-of-entry (Brockerhoff et al. 2006; Rassati et al. 2014, 2015a; Hoch et al. 2020) or other high-risk sites (e.g. urban wood-waste landfills and industrial sites, Rassati et al. 2015b; Rabaglia et al. 2019) could be one such early detection tool. Given the difficulty of predicting which species may arrive and in what numbers (i.e. propagule pressure), such lures should be efficient even at low population densities and should ideally attract multiple species from different taxa (family, subfamily, tribe). Combining pheromones of several species into blends could be expected to result in such a generic attraction when antagonistic effects amongst blend components are relatively minor, for example, reduced attraction of relatively few species, such that the net effect of blending multiple components is an increase in the number of target taxa detected. The addition of plant volatiles, acting as kairomones, may further enhance the attraction. For instance, a pine specialist, Monochamus galloprovincialis (Olivier), was significantly more attracted when its pheromone, monochamol, was combined with volatiles from its pine hosts (Alvarez et al. 2016). Similarly, ethanol had a synergist effect on the capture of species related to broadleaved trees in Eurasia (Phymatodes testaceus [L.]; Sweeney et al. 2014; Fan et al. 2019) and in southern USA (Miller et al. 2017). However, the addition of plant volatiles did not affect, either positively or negatively, the captures of several other cerambycid species (Fan et al. 2019). Overall, relationships between host volatiles and cerambycids are probably more dependent on the exploited host and less on insect taxonomy. Potential for using blended lures for detection would be further enhanced if each component of the blend was attractive to multiple related species, i.e. a pheromone or kairomone shared by species within a genus or tribe as occurs in the longhorned beetle family Cerambycidae.

This large family of Coleoptera includes between 34,000 and 38,000 described species (Rossa and Goczał 2021; Tavakilian and Chevillotte 2022). Although recent molecular studies using a multigene approach revealed that the phylogeny at the upper taxonomic levels is not completely resolved and still under debate (Lee and Lee 2020; Nie et al. 2020), Tavakilian and Chevillotte (2022) recognised 13 subfamilies. The subfamily Lamiinae is by far the most diverse with more than 21,000 species, 3,002 genera and 86 tribes, followed by Cerambycinae (> 12,000 species, 1,848 genera, and 119 tribes), Lepturinae (> 1,830 species, 232 genera, 11 tribes), Prioninae (> 1,250 species, 311 genera, 26 tribes) and Spondylidinae (> 150 species, 32 genera, seven tribes); other subfamilies are smaller and much less diverse. Cerambycid larvae of many species develop as endophytic borers concealed beneath the bark of woody plants or, much less frequently, within herbaceous plants. This cryptic lifestyle, coupled with the usual long duration of the hidden larval stages, facilitates the transport of these insects around the world in logs and wooden packing materials (Eyre and Haack 2017), but also via trade in living plants if the plants have a sufficiently large diameter. For example, larvae of the citrus longhorned beetle, Anoplophora chinensis (Forster), were detected in Japanese maples, Acer palmatum Thunb., shipped to Europe (Eschen et al. 2015). Thus, a steadily increasing number of cerambycid species have become globally important as invasive forest and orchard pests (Venette and Hutchison 2021).

Recent advances in the chemical ecology of cerambycids and, particularly, the identification of volatile pheromones that act as long-range attractants, have provided new tools and opportunities for monitoring invasive woodborers. In total, pheromones or likely pheromones have been identified for more than 400 cerambycid species worldwide (Millar and Hanks 2017). Furthermore, field experiments have shown that these pheromones can be deployed in blends, with a potential generic attraction for both native and non-native species (Hanks et al. 2012; Hanks and Millar 2016; Hanks et al. 2018; Fan et al. 2019; Flaherty et al. 2019; Rassati et al. 2019). Currently, the aggregated data suggest that species in the subfamilies Cerambycinae, Lamiinae and Spondylidinae use male-produced aggregation-sex pheromones to attract both sexes, whereas species in the subfamilies Prioninae and Lepturinae use female-produced pheromones that attract only males (Hanks and Millar 2016). This research has revealed striking patterns in pheromone chemistry. Pheromone components are frequently highly conserved amongst species within genera, tribes and even at the subfamily level (Hanks and Millar 2013, 2016). For example, in the subfamily Lamiinae, hydroxyethers are used as aggregation-sex pheromones by many species native to different continents. Thus, 2-(undecyloxy)ethanol, or monochamol, is a pheromone component shared by European, North American and Asian species in the genus Monochamus, all of which vector the pine wood nematode (Bursaphelenchus xylophilus [Steiner & Buhrer]) (Pajares et al. 2010; Hanks and Millar 2016; Boone et al. 2018; Lee et al. 2018). In addition, field trials in southern China showed that four lamiine species in genera other than Monochamus were attracted to monochamol (Wickham et al. 2014). A number of other compounds are widely shared amongst species within a given subfamily in different world regions. For example, terpenoids such as fuscumol ([E]-6,10-dimethyl-5,9-undecadien-2-ol) and its acetate, are aggregation sex-pheromone components for many species in the subfamily Spondylidinae and Laminae (Mitchell et al. 2011; Hanks and Millar 2016). In contrast, many species in the subfamily Cerambycinae from different continents utilise short-chain (6–10 carbon) hydroxyketones, such as 3-hydroxyalkan-2-ones and 2-hydroxyalkan-3-ones and the corresponding syn- and anti-2,3-alkanediols as aggregation-sex pheromones (Hanks and Millar 2016). Prionic acid ([3R,5S]-3,5-dimethyldodecanoic acid) similarly appears to be shared as a sex pheromone by several genera of the subfamily Prioninae on different continents (Barbour et al. 2011; Wickham et al. 2016a). This sharing of pheromone components by species in different world regions suggests that traps baited with these compounds have a good chance of detecting non-native, phylogenetically-related invaders that are introduced to another continent. Moreover, combining several of these pheromone components in a single blend has the potential to detect a broader range of species.

During the last 10 years, the generic effectiveness of such multi-component blends has been tested on different continents, but using different pheromone combinations, either alone or in combination with kairomones, such as ethanol and α-pinene (e.g. Miller et al. 2017; Fan et al. 2019). In Illinois, USA, Hanks et al. (2012) first tested a six-component blend, which included racemic 3-hydroxyhexan-2-one, syn- and anti-2,3-hexanediols, fuscumol, fuscumol acetate, monochamol and racemic 2-methylbutan-1-ol. Ten cerambycid species were caught in significant numbers in these trials, including four species in the subfamily Cerambycinae and six in the subfamily Lamiinae. Hanks et al. (2018) then tested this 6-component blend at a larger scale in several regions of the USA, adding both prionic acid and plant volatiles to the traps. The pheromone blend attracted about twice as many species as any of the individual components and the species attracted by the blend included three subfamilies, whereas individual components attracted species within only one subfamily. The inclusion of prionic acid also resulted in the additional captures of Prionus spp. which were not trapped by the previous six-pheromone blend. In a natural reserve in Yunnan (China), Wickham et al. (2021) trapped 71 species with another generic lure comprised of six components, three of which were the same as those used in the USA (anti-2,3-hexanediol, racemic 3-hydroxyhexan-2-one and monochamol). In France, using an 8-pheromone blend consisting of the same compounds as Hanks et al. (2018) to which was added geranylacetone targeting Spondylininae (Halloran et al. 2018), Fan et al. (2019) trapped 118 species, of which 114 were native species that represented 48% of the French cerambycid fauna. Trapping more than 50% of the species in 25 of the 41 cerambycid tribes present in the country indicates a considerable generic attraction of this 8-pheromone blend, significantly higher than an earlier trial which tested a blend of four pheromones. By contrast, unbaited control traps deployed in the same French sites caught very few species. Other trials of potentially generic blends, including fewer or different compounds, were carried out in Russia (Sweeney et al. 2014), Australia (Hayes et al. 2016), Brazil (Silva et al. 2017), Poland, Italy and Canada (Flaherty et al. 2019; Rassati et al. 2019, 2021). Results from Australia differed from those reported in other continents because the tested blend attracted no more species than 3-hydroxyhexan-2-one alone (Hayes et al. 2016).

When using multi-pheromone blends, antagonistic effects might occur with either pheromone components or host plant volatiles (e.g. Hanks et al. 2018; Rassati et al. 2021). The North American species Neoclytus acuminatus acuminatus (F.), for example, was strongly attracted by syn-2,3-hexanediol, but the addition of racemic 3-hydroxyhexan-2-one to the latter pheromone interrupted attraction (Rassati et al. 2021). Addition of host plant volatiles, such as ethanol, significantly enhanced attraction of some cerambycid species (Sweeney et al. 2014; Miller et al. 2017; Hanks et al. 2018), but, with the exception of P. testaceus, had little effect on catch of cerambycid species in other studies (Fan et al. 2019). However, as long as inhibition did not completely prevent attraction, one trap with a multi-pheromone lure may still be somewhat more cost-effective than deploying multiple traps baited with individual lures. This can be assessed by a cost-benefit analysis, i.e. estimating the labour and materials costs of deploying and servicing a network of traps baited with single components, versus the costs of deploying and servicing a single trap baited with a blend of the same components.

Results of these different experiments on various continents stimulated us to propose a worldwide trapping programme using a standardised ‘generic’ 8-pheromone blend in all countries/trapping sites. The blend included the following compounds known to be widely shared amongst cerambycids of related taxa: fuscumol, fuscumol acetate, monochamol, geranylacetone, anti-2,3-hexanediol, 3-hydroxyhexan-2-one (C6-ketol), 2-methylbutan-1-ol and prionic acid. The programme relied on the following hypotheses: 1) if a species is attracted in significant numbers by the blend in a region, it increases the probability that it can be detected when it arrives at ports-of-entry in other regions and 2) if the blend exerts an effective, generic attraction to multiple species, it is likely that previously unknown and unexpected species can be captured due to the high degree of conservation of pheromone structures within related taxa, as described above. Our overarching objective was to build a global database of cerambycid species trapped by the 8-pheromone blend. To this end, field trials were conducted during 2018–2021 using operational protocols that were standardised as much as possible at all sites worldwide to cover simultaneously or sequentially 13 European countries, 10 Chinese provinces and some regions of the USA, Canada, Australia, Russia (Siberia) and the Caribbean. Over the course of the study, we also tested the possibility of adding new compounds to enlarge the pool of species trapped. Therefore, in 2020, two additional pheromones, the sex-aggregation pheromones trichoferone (a hydroxyketone pheromone of the velvet longhorned beetle, Trichoferus campestris (Faldermann) (Ray et al. 2019) and (E)-2-cis-6,7-epoxynonenal, the pheromone of the invasive species A. bungii (Xu et al. 2017), were added to the original 8-pheromone blend and tested in France and China. In addition, ethanol and α-pinene were included in most trials as synergists for some cerambycids.

A total of 78,321 longhorned beetles were trapped, representing 376 species, including 373 Cerambycidae, two Vesperidae and one Disteniidae species (Table 3). The cerambycids belonged to eight subfamilies, including 156 species of Cerambycinae, 102 species of Lamiinae, 78 species of Lepturinae, 21 species of Spondylidinae, 12 species of Prioninae, two species of Necydalinae and one species of Parandrinae (Fig. 1). Captures comprised 60 tribes, with 10 tribes including more than nine species trapped on different continents; in decreasing order the tribe Clytini (64 spp.), followed by Lepturini (44 spp.), Rhagiini (32 spp.), Acanthocinini (31 spp.), Callidiini (20 spp.), Monochamini (18 spp.), Saperdini (10 spp.) and Aseminii, Pogonocherini and Prionini (nine spp. each; Fig. 2). Generally, fewer species were trapped in the Caribbean and Australia, where only a limited number of traps had been deployed. Some of the captured species belonged to tribes other than those targeted, such as Callidiopini (Curtomerus flavus [F.] in Martinique and Bethelium sp. in Australia), Eburiini (Eburia spp. in Martinique) and Tillomorphini (Gourbeyrella madininae Chalumeau & Touroult in Martinique).