Tetropium fuscum (Coleoptera: Cerambycidae) is a Eurasian longhorn beetle and forest pest that first became invasive to Nova Scotia, Canada around 1990. In the time since its introduction, T. fuscum has spread only about 150 km from its point of introduction. In its invasive range, T. fuscum co-exists with its congener Tetropium cinnamopterum. Although they are ecologically similar species, T. fuscum tends to infest healthier trees and has a smaller host range than T. cinnamopterum. If they successfully interbreed, this could lead to hybrid individuals that are more problematic than either parent species. On the other hand, if T. fuscum can make mating errors in the field, but is not producing hybrid offspring, then this waste of mating resources could help explain the slow spread of T. fuscum in North America. We conducted no-choice and choice mating experiments between T. fuscum and T. cinnamopterum males and females and determined that both T. fuscum and T. cinnamopterum males make mate-choice errors with heterospecific females in a laboratory setting. Our results suggest that mating errors may play a role in the slow spread of T. fuscum in North America.

Congener, hybridisation, invasion biology, mating behaviour

Invasive species are a threat to global biodiversity (Rhymer and Simberloff 1996; Vitousek et al. 1997) and those that successfully establish exploit resources, such as food and shelter, thereby decreasing resources available to native species. They can also act as natural enemies (predators or parasites) for the native species they encounter. Furthermore, depletion of food sources, predation or removal of an important predator by an invasive species can have catastrophic ripple effects in an ecosystem. The rate of invasion by introduced species has been steadily rising due to climate change, habitat modification, international trade (Findley and O’Rourke 2007) and globalisation in transport of unprocessed wood products (Haack 2006), allowing for accidental introductions (Allendorf et al. 2001; Sax et al. 2007; Kelly and Sullivan 2010). Invasive species are now ubiquitous (Seebens et al. 2016) and cause significant ecological and economic impacts around the globe (Vitousek et al. 1996; Pimentel et al. 2000, 2005). Nearly half of the endangered species in the USA are threatened because of competition with and predation by invasive species (Stein and Flack 1996).

Several factors determine whether an introduced species will establish itself and become invasive in a novel habitat (Ehrlich 1986; Williamson and Griffiths 1996). Understanding factors that drive invasiveness could allow us to predict and prevent potential invaders and manage those already present (Pyšek and Richardson 2010). Traits that are predictors of invasiveness across taxa include high dispersal ability (Moyle 1986; O’Connor et al. 1986; Kolar and Lodge 2001), high reproductive rates (Gallagher et al. 2014; Mathakutha et al. 2019), high competitive ability (O’Connor et al. 1986; Newsome and Noble 1986; Moyle 1986), high propagule production (O’Connor et al. 1986; Kolar and Lodge 2001), association with humans (Kolar and Lodge 2001; García-Berthou 2007; Mathakutha et al. 2019), fast growth (Newsome and Noble 1986; Kolar and Lodge 2001), ability to tolerate and adapt to a broad range of conditions (Ehrlich 1986; Moyle 1986), large body size (Ehrlich 1986; Kolar and Lodge 2001; García-Berthou 2007) and a generalist diet (Ehrlich 1986). However, the specific combination of species traits that would allow a species to invade one habitat may not extend to the same species in another habitat or a different species in that same habitat (Lodge 1991) and we still lack a fully predictive understanding of invasions and the multiple factors that can determine invasiveness.

Many species are accidentally introduced but do not establish or experience population growth sufficient to gain pest status (Williamson and Griffiths 1996). Species that successfully establish, but then undergo limited spread, such as the phloem-feeding longhorn beetle, Tetropium fuscum Fabricius (Coleoptera: Cerambycidae), are poorly understood and offer an interesting window on traits and ecological factors that determine invasiveness. We examine some factors that may be negatively impacting reproductive rate in T. fuscum and, thus, impeding its ability to invade North America.

Tetropium fuscum experienced initial success in establishment and population growth upon its introduction to North America (in or before 1990), but by 2010, it had spread only ~ 80 km from its point of entry in Halifax, Nova Scotia (Canada) (Rhainds et al. 2011). To date, it has only been identified in one small area in the south-eastern part of the neighbouring Province of New Brunswick (CFIA 2017), an additional 70 km from its point of introduction. T. fuscum is native to western Europe and northern Eurasia (Juutinen 1955), including areas with climates very similar to the invasive range in Nova Scotia. It was first discovered in mature red spruce trees in Point Pleasant Park, Halifax, NS, in 1999 (Smith and Hurley 2000), but collections in the Nova Scotia Museum of Natural History indicate that it had been present since at least 1990, having been misidentified as its native counterpart T. cinnamopterum Kirby (Sweeney et al. 2004). In its native range, T. fuscum attacks predominately stressed or moribund Norway spruce (Picea abies (Linnaeus) Karsten) (Juutinen 1955), but in Nova Scotia, it has been observed attacking apparently healthy red spruce (Picea rubens Sargent), white spruce (Picea glauca Moench (Voss)), black spruce (Picea mariana (Miller) Britton, Sterns and Poggenburg) and Norway spruce (Smith and Humble 2000).

Tetropium fuscum is unusual in that the introduced population neither died out, nor saw rapid and successful expansion in North America. T. fuscum has established a stable population in the Halifax area, but its expansion into other parts of North America has been extremely slow (Rhainds et al. 2011). T. fuscum’s co-existence with the native congener T. cinnamopterum in the invaded range and their ecological similarities could result in Allee effects that contribute to its slow spread in North America. The two species share many similarities including phenology and preferred host plants. Tetropium fuscum and T. cinnamopterum both emerge in the spring, beginning in May and their flight period lasts until late August (Juutinen 1955). Although T. fuscum emerges on average 2 weeks earlier than T. cinnamopterum, their flight periods overlap significantly (Rhainds et al. 2011). Tetropium fuscum is limited to trees in the genus Picea (spruces), while T. cinnamopterum’s somewhat broader host range includes Picea spp. amongst other conifers (Furniss and Carolin 1980), providing plenty of opportunity for interspecific encounters. Notably, the species share the highly conserved male-produced pheromone component S-fuscumol, which synergises attraction of males and females of both species when combined with host (spruce) volatiles (Silk et al. 2007; Rhainds et al. 2010; Sweeney et al. 2010). Thus, pheromone blends emitted by males of one species may attract females of both species, particularly if the male is emitting from a host tree – and this sets the stage for possible mate choice errors. Mate choice also involves more local signalling; however, T. fuscum and T. cinnamopterum males both respond to cuticular hydrocarbons on the surface of females (Silk et al. 2011).

We hypothesised that Tetropium fuscum males, where the two species co-occur, make mate choice errors by sometimes mating with T. cinnamopterum females rather than with T. fuscum females. Such errors might be expected to be particularly common near T. fuscum’s range edge. Invasive species populations are often the densest at the epicentre of invasion and become more sparsely distributed closer to the range edge (Udvardy and Papp 1969; Sagarin and Gaines 2002; Sagarin et al. 2006; Mlynarek et al. 2017). Thus, near the edge of their invasive range, T. fuscum males are likely to encounter primarily T. cinnamopterum females. If such matings produce fewer or no viable, fertile offspring, then wasted mating resources would hinder population growth of T. fuscum. Copulation by Tetropium spp. can take several hours to complete and these beetles only live for 1–4 weeks on average (Juutinen 1955). Thus, the time it takes to locate and copulate with even one female is a non-negligible proportion of the entire lifespan of a Tetropium male; repeated mating errors would be even more costly. We tested whether mate choice errors occur for T. fuscum and T. cinnamopterum males in the laboratory, using: 1) choice experiments reflecting mate encounters expected at the centre of the invaded range where both species are common and 2) no-choice experiments reflecting mate encounters expected at range edges where T. fuscum will more frequently encounter T. cinnamopterum.

We saw evidence of interspecific mating by both Tetropium fuscum and T. cinnamopterum males in the no-choice experiment. For both species, males attempted and succeeded significantly less with heterospecific females than with conspecific females. However, rates of heterospecific attempts and successes were both considerable. While both T. fuscum and T. cinnamopterum males took longer to attempt mating with a heterospecific female than a conspecific one, they still mated quite rapidly with heterospecific females. The same was true for time until successful mating. We often observed males touching females with their antennae prior to attempting to copulate, consistent with reports that Tetropium spp. males respond to female cuticular hydrocarbons (Silk et al. 2011), but inconsistent (because heterospecific matings still occurred) with a model in which a cuticular-hydrocarbon “match” is required for mating. Silk et al. (2011) also observed low percentages of heterospecific mating in both T. fuscum and T. cinnamopterum with dead females and suggested this may be due to the presence of a common cuticular hydrocarbon, 11-methylheptacosane, on the elytra of females of both species – although the overall mix of hydrocarbons differs between the species. T. fuscum males attempted and succeeded with heterospecific females more frequently than did T. cinnamopterum males, but we do not know whether this reflects lesser ability to recognise heterospecific partners or looser specificity in accepting them.

Tetropium beetles make mating errors even when they have ample opportunity to avoid them. Under choice conditions, one of twelve T. fuscum males mated heterospecifically. While we did not observe any heterospecific matings by T. cinnamopterum males in the choice experiment, our sample size was small and we cannot reject an underlying rate as high as 19%. In these choice trials, both T. fuscum and T. cinnamopterum males made first mating attempts in the same mean amount of time regardless of whether that attempt was on a heterospecific or conspecific female. We considered that perhaps males would simply mate with the first female they bumped into in the Petri dish, but in fact, first-touch female species did not adhere to any significant pattern, while both species of males preferentially made their first mating attempt on conspecific females. This indicates that males have the ability to “choose” conspecific females over heterospecific females – but they do not always do so.

Both T. fuscum and T. cinnamopterum males spent as much time in copula with heterospecific females as they did with conspecific females. This suggests that Tetropium males determine the suitability of a mate (imperfectly), based on the precopulatory act of touching the cuticular hydrocarbons of the female. If the barrier to copulation were something pericopulatory, like a genital lock-and-key mechanism, we would expect to see prematurely terminated copulation in heterospecific pairs. It also suggests that beetles will pay full time and resource costs of heterospecific matings, rather than breaking them off and moving on to other mating opportunities.

Our matings were all conducted in Petri dish arenas and, like any laboratory experiment, may not fully capture insect behaviour in nature. Lab experiments are commonly used to investigate arthropod mating behaviour for a wide range of arthropods including beetles (Nilsson et al 2002; Kumano et al. 2010; Rutledge and Keena 2012), moths (Jiménez-Pérez and Wang 2003; Bento et al. 2006), bed bugs (Reinhardt et al. 2009), predatory bugs (Bonte et al. 2012) and wolf spiders (Vaccaro et al. 2010). Lab experiments are particularly important for invasive species, where field manipulations may be logistically and/or ethically problematic. Experiments under field conditions, perhaps with captive beetles released near the centre of the invasive range where such releases do not threaten to accelerate the invasion, would be worth pursuing.

While mating errors occurred under both choice and no-choice conditions, they were much more frequent in our no-choice experiments. In no-choice situations, T. fuscum males were more reluctant to attempt mating and less likely to successfully copulate with heterospecific females than with conspecific females; but given enough time, many of them did. This suggests that T. fuscum males may become less choosy the longer they go without locating a mate, a situation that may be most common at range edges. In Nova Scotia, the population density of T. fuscum is highest at the range centre and decreases outwards (Heustis et al. 2017; Anderson, unpublished data). At the edges of T. fuscum’s invasive range, then, males are more likely to encounter T. cinnamopterum females than T. fuscum females. If such hybrid matings do not produce fertile offspring, this could reinforce the edge of their range preventing the population from spreading further (Rhainds et al. 2015). Such Allee effects can limit spatial spread of a species even after establishment of a stable population (Keitt et al. 2001).

Of course, it is also possible that heterospecific matings do produce viable and fertile offspring. If so, the encounter between the two Tetropium species could pose a different set of challenges to forest managers. Hybrid offspring may exhibit traits intermediate to their parents (Roe et al. 2014; Patterson et al. 2017), hybrid breakdown (McQuillan et al. 2018; Pâques 2019) or hybrid vigour (Shao et al. 2019; Kumar et al. 2020). Tetropium fuscum attacks more vigorous trees than T. cinnamopterum (Smith and Humble 2000), although T. cinnamopterum can attack a broader range of conifers in North America than T. fuscum can (Furniss and Carolin 1980). Hybrid Tetropium might display both traits and, thus, be more threatening to North American forests than either parental species. There are similar concerns in other invasive insects. For instance, the winter moth Operophtera brumata Linnaeus is invasive to north-eastern North America and co-exists with its native congener Operophtera bruceata Hulst (Elkinton et al. 2010; Simmons et al. 2014). As in Tetropium, sex pheromones are highly conserved across the genus and the sex pheromone blend of O. brumata females attracts both O. brumata and O. bruceata males (Khrimian et al. 2010). Unsurprisingly, O. bruceata and O. brumata are known to hybridise (Elkinton et al. 2010) and, in this case, the hybrids are fertile (Havill et al. 2017). In winter moth, hybridisation between the invasive and native congeners may be aiding the spread by alleviating the Allee effects often seen in small founder populations of invasive species (Elkinton et al. 2014). Furthermore, the intermediate traits exhibited by hybrids could confer an invasive and evolutionary advantage to the hybrid offspring (Havill et al. 2017). All this suggests that it will be important to determine whether mating errors in Tetropium produce offspring and, if so, if those offspring are fertile and display hybrid vigour. But do they? Although very few morphologically intermediate Tetropium specimens have been identified in eastern Canada, morphology is not always a reliable predictor of introgression (Rhymer et al. 1994). We are currently surveying wild populations to determine whether hybrid beetles occur where the two Tetropium species are sympatric.

Allee effects, arising from mate-choice errors, are not the only mechanism that could be behind the slow range expansion of T. fuscum. Pinned edges of a species’ geographical range can result from many things. Dispersal limitation can often slow an invasion, especially for species that are unlikely to be transported by humans. Restrictions on the movement of untreated lumber and firewood (Canadian Food Inspection Agency 2019) may have slowed the Tetropium invasion, but are unlikely to be responsible for its near cessation. More interestingly, Darwin’s naturalisation hypothesis suggests that, when a species invades an area where a close relative is already established, it will be less likely to successfully establish due to higher competition for resources (Darwin 1859; Jiang et al. 2010; but see Ricciardi and Mottiar 2006; Park and Potter 2013; Sol et al. 2021) and such competition can pin range edges (Heller and Gates 1971; Bull and Possingham 1995; Case and Taper 2000). Tetropium fuscum may be in direct competition for resources with T. cinnamopterum, at least in Picea spp. Indeed, in Nova Scotia, T. fuscum has largely displaced the native T. cinnamopterum in the invaded zone (Dearborn et al. 2016). Furthermore, the two species are exploited by some of the same species of parasitoids, particularly in stressed spruce trees (Flaherty et al. 2011). It is perhaps most likely that a combination of factors is responsible for the apparently pinned range edge of T. fuscum, including competition with the native species and shared natural enemies as well as mating errors. Testing this hypothesis directly in wild populations will, unfortunately, be difficult.

Tetropium fuscum is not spreading as rapidly and destructively as other invasive forest pests, such as emerald ash borer (Agrilus planipennis Fairmaire). Emerald ash borer was first detected in North America in 2002, making its invasion about as old as T. fuscum’s, but it has already killed hundreds of millions of ash (Fraxinus spp.) trees in the USA alone (Herms and McCullough 2014), costs tens of billions of dollars for mitigation (Kovacs et al. 2010) and is now spreading in eastern Canada. However, our results do not mean that we should ignore the potential for future T. fuscum spread. Many invasive species experience a “lag phase” in which their population size and range do not increase rapidly at the beginning of the invasion (Mack 1981) while the population evolves to be better adapted to the novel environment or until environmental changes allow the species to spread (Crooks and Soulé 1999). It is important to continue the monitoring of T. fuscum populations in North America, so that we are not caught off guard should a sudden increase in population size or emergence of introgressed individuals become problematic.

We have demonstrated that T. fuscum and T. cinnamopterum males make mate-choice errors in the lab and we present a logical case that this may also happen in the field, especially near the edges of the invasion zone. This may well play an important role in impeding the North American spread of T. fuscum. If so, there are implications beyond T. fuscum’s invasion in particular. While some invasive species establish without any close relatives sharing their new habitat, many others, like Tetropium, invade alongside native congeners. Adding mate-choice errors to the list of reasons this can matter advances our understanding of why some introductions spread catastrophically, while others fade quietly away.

We thank Kate Van Rooyen, Cory Hughes, Vince Webster, Chantelle Kostanowicz, Allyson Heustis and John Dedes for assistance in the field, as well as Mischa Giasson for both field and laboratory assistance. We are grateful to several anonymous reviewers for comments on the manuscript. This project was supported by NSERC Discovery Grants to Stephen B. Heard and Deepa S. Pureswaran and Canadian Forest Service research funds to Deepa S. Pureswaran and Jon Sweeney.