Abstract Tetropium fuscum (Fabricius) (Coleoptera: Cerambycidae), a phloem-feeding and wood-boring beetle introduced from Eurasia, attacks spruce in eastern Canada alongside its native congener Tetropium cinnamopterum Kirby. We reared phloem- and wood-feeding insects (and their predators) from bolts of red and Norway spruce (Picea rubens and Picea abies) in Nova Scotia, comparing insect communities between bolts with added eggs of T. fuscum or T. cinnamopterum and bolts without added Tetropium (controls). We tested for impacts of each Tetropium on insect community structure (Simpson’s diversity, richness, and evenness). We also asked whether, consistent with Darwin’s Naturalization Hypothesis, Tetropium spp. would have greater impacts on emergence of its closer relatives (which might be most likely to compete and/or share natural enemies). Addition of Tetropium eggs (either species) to bolts lowered insect diversity in both host trees. Both richness and evenness components of diversity were always lower in +Tetropium treatments, although different components reached statistical significance in different Tetropium species × host combinations. Addition of Tetropium spp. significantly reduced emergence of some species: Evodinus monticola (Randall) (Coleoptera: Cerambycidae) was reduced by T. fuscum on both hosts and by T. cinnamopterum on Norway spruce; Hylobius congener Dalla Torre, Schenkling, and Marshall was reduced by T. fuscum on red spruce; and Xylophagus sp. (Diptera: Xylophagidae) was reduced by T. cinnamopterum on Norway spruce. However, there was no relationship between Tetropium’s impact on a community member and their phylogenetic relatedness, and the overall impacts of Tetropium presence were not very different between T. fuscum and T. cinnamopterum. Accidental introductions of exotic species to marine, freshwater, and terrestrial habitats have become more frequent over the last two centuries, especially near international ports (Mack et al. 2000, Kolar and Lodge 2001, Mooney and Cleland 2001, Bax et al. 2003, Colautti et al. 2006, Haack 2006). With steadily increasing global trade (Bradley et al. 2012, Brockerhoff et al. 2006, Hulme 2009), introductions will remain a major concern for the foreseeable future. It is, therefore, of critical importance to understand the ecology behind the establishment and impact of introduced species. When individuals of an exotic species are first introduced, they may or may not establish in the new habitat (Williamson and Fitter 1996). Following establishment, they may spread rapidly or slowly (Arim et al. 2006), interacting with native communities on which they have varying degrees of positive or negative impacts (Ricciardi and Cohen 2007). Some introduced species outcompete or otherwise suppress native species, spreading rapidly and changing overall community structure in their new range (Porter and Savignano 1990, Gotelli and Arnett 2000, Sanders et al. 2003, Hejda et al. 2009). Such species are usually referred to as “invasive”. Others have more modest effects (Diekmann et al. 2016), and are perhaps best seen as simple additions to local biotas. Invasive insect pests of forests have attracted considerable attention because of the economic value lost in damaged timber and because a few species, like the emerald ash borer (Agrilus planipennis Fairmaire [Coleoptera: Buprestidae]), have been utterly catastrophic (Herms and McCullough 2014). However, there is considerable variation in establishment success and ecological consequences of exotic insects, and other forest exotics may have less dramatic effects in their new habitats (Tobin 2015). The ability to predict which exotic species might become invasive and do damage in their invaded habitats is of considerable interest to scientists and policy makers (Ricciardi and Cohen 2007). It has been suggested that exotics with close relatives in their new range will spread more slowly and have lower population densities (Darwin 1859, Cavender-Bares et al. 2009, Dearborn et al. 2016) because they will compete with those close relatives (which will be ecologically similar) and will be attacked by their enemies (Darwin 1859, Schaefer et al. 2011). This logic suggests a contrast between species such as emerald ash borer (attacking a North American host that does not support native competitors in the same genus) and other introduced species that may arrive to find themselves co-attacking with closely related competitors as well as finding native natural enemies preadapted to attack them. Tetropium fuscum (Fabricius) (commonly referred to as the “brown spruce longhorn beetle”) is a phloem-feeding and wood-boring cerambycid beetle native to Eurasia (Juutinen 1955) that was unintentionally introduced to Halifax, Nova Scotia circa 1990 (Smith and Hurley 2000). Its establishment has not been documented beyond its province of introduction (Canadian Food Inspection Agency 2015) despite occasional trap catches in New Brunswick. In Nova Scotia, T. fuscum is sympatric with a congener, Tetropium cinnamopterum Kirby, which has a very similar life history (Drooz 1985, Rhainds et al. 2010). However, there are two differences that suggest T. fuscum could become an invasive threat. First, it appears to colonize weakened but still seemingly healthy red spruce (Picea rubens Sargent) and Norway spruce (Picea abies (L.) Karsten) (Smith and Hurley 2000, Flaherty et al. 2011), whereas T. cinnamopterum is reported to colonize only severely weakened or stressed spruce (Furniss and Carolin 1980, Flaherty et al. 2013a). Second, T. fuscum adults can emerge up to 2 wk before T. cinnamopterum (Juutinen 1955, Flaherty et al 2013b), potentially giving their larvae a developmental advantage in the phloem. In addition to its effect on host trees, exotic T. fuscum could impact the community of native insects feeding in spruce—whether through competition for phloem resources, intraguild predation, or apparent competition. Previous studies, however, have not fully resolved the possibility of such impacts. Dearborn et al. (2016) tested for the effects of T. fuscum on T. cinnamopterum and the rest of the native insect community, using contrasts between trees inside and outside the zone of T. fuscum establishment. They found lower densities of native Tetropium where the exotic species is present, suggesting negative interactions between the two, and argued that such interactions could be slowing T. fuscum’s spread. However, Dearborn et al. were not able to detect effects on other community members, and their design inevitably confounded the presence of T. fuscum with other spatial differences. Furthermore, they were not able to compare the relative effects of the exotic and native Tetropium on other community members. We used experimental additions of T. fuscum and T. cinnamopterum eggs to test for effects of those species on phloem-feeding and wood-boring insects, and their predators, within T. fuscum’s exotic range. We also expanded on Dearborn et al.’s (2016) work by examining these interactions in both the novel and most common host, red spruce (Picea rubens, native to Atlantic Canada), and in its ancestral host, Norway spruce (Picea abies, frequently planted in North America). We compared the diversity of the focal community between bolts (of each spruce species) with Tetropium infestation induced via addition of eggs and corresponding control bolts. Using the same sets of bolts, we also tested for species-level impacts of Tetropium spp. on each of the other community members. Finally, we asked whether those species-level impacts might be correlated with phylogenetic distance of the impacted species from Tetropium, as would be expected if interactions are strongest between close relatives. Methods Experimental Design In early May 2014, we felled 10 apparently healthy red spruce and 10 apparently healthy Norway spruce trees (24–26 cm diameter at breast height) at the Acadia Research Forest (45°99.876′N, 66°39.335′W) near Fredericton, New Brunswick, Canada. T. cinnamopterum occurs naturally at this site, but it is outside the current exotic range of T. fuscum. From each tree, we cut 10 bolts ~36 cm long (which is long enough to sustain galleries of most wood-inhabiting species). We coated bolt ends in paraffin wax to preserve moisture and stored the bolts in cold storage rooms (−2°C) until later use. On 9 June 2014, we placed bolts in 10 experimental blocks at each of 3 sites in Nova Scotia, Canada: Westchester Valley (45°36.557′N 63°43.608′W), Shubenacadie (45°10.079′N 63°34.274′W), and Sandy Lake (44°44.162′N 63°40.585′W). Both native and introduced Tetropium are present, and infest our host species, at these sites, although we did not need natural colonization in our experiment. Some natural colonization did occur, although this was almost certainly after bolts were deployed because neither species commonly attacks healthy trees. Both Tetropium were naturally active at this time in 2014, although in some years they have a phenological offset with T. fuscum active up to about 2 wk earlier. At Sandy Lake and Westchester, each block consisted of one red spruce and one Norway spruce bolt, without Tetropium eggs. In Shubenacadie, we added four additional bolts (two of each tree species) to each block. These bolts had either T. fuscum or T. cinnamopterum eggs introduced on them (and we call them “+T. fuscum” and “+T. cinnamopterum” bolts, respectively). To obtain these eggs, we had reared adult T. fuscum and T. cinnamopterum from bolts cut from infested red spruce trees in Nova Scotia and incubated at 20–22°C in containment facilities at the Canadian Forest Service—Atlantic Forestry Centre, Fredericton (CFS-AFC). We mated pairs of either T. fuscum or T. cinnamopterum in Petri dishes and collected eggs on black construction paper as described by Flaherty et al. (2013b). We placed 20 eggs on each experimental bolt by attaching pieces of construction paper containing one to five eggs each. We slit the bark with a scalpel, so that the paper would directly contact the bolt’s phloem, and secured the paper in the slit with pins. Eggs were distributed over three-fourth of each bolt’s circumference, and the other one-fourth of the bolt made contact with soil. After 2 wk, we removed the paper and quantified egg hatch. There were no significant differences in egg hatch (which was approximately 70%) between Tetropium species or tree species (F3,30 = 0.03, analysis of variance [ANOVA] P = 0.99). We used egg-treatment bolts at only one site because we had a limited supply of eggs, and we chose Shubenacadie for these treatments because it was the most likely to have natural populations of both Tetropium species. We placed bolts on flat ground in red spruce-dominated stands. At Shubenacadie, where there were six bolts per block, we positioned them in a circle ~10 cm apart at their closest points. At the other two sites, there were just two bolts per block, which we placed similarly (with four of the six circle positions left empty). Tetropium readily colonize bolts presented like this, and indeed three of our control bolts yielded Tetropium adults (we removed these bolts from the dataset because they were no longer appropriate controls). On 8 and 9 October 2014, we piled the bolts at each site and covered them with heavy mosquito mesh to protect them from woodpeckers and other avian predators. In late November (24–28) 2014, we moved the bolts into storage at −2°C at CFS-AFC for a simulated overwintering period. Beginning in mid-January 2015, we incubated the bolts at 20–22°C, each in a rearing cage, within containment facilities with day/night photoperiod lights (16:8 [L:D] h) to mimic summer conditions. Insect Collection We checked caged bolts for emerging insects every 7 d, sweeping bolts with brushes to dislodge insects from crevices. After preliminary sorting, we preserved insects in 70% ethanol for later identification (with the exception of Tetropium spp., which we identified immediately). We identified most emerged insects to species (Table 1), using insect keys (Bright 1976) and a reference collection of wood-inhabiting insects at CFS-AFC: Evodinus monticola (Randall) (Coleoptera: Cerambycidae), Hylobius congener Dalla Torre et al., Pissodes nemorensis (Germar), Polygraphus rufipennis (Kirby), and Xylosandrus germanus (Blandford) (Coleoptera: Curculionidae), and Urocerus albicornis (Fabricius) (Hymenoptera: Siricidae). A few we identified only to genus [Dendroctonus, prob. rufipennis (Kirby), Dryocoetes, combining affaber (Mannerheim) and autographus (Ratzeburg) (Coleoptera: Curculionidae), Thanasimus sp. (Coleoptera: Cleridae), and Xylophagus sp. (Diptera: Xylophagidae)], or to family (Coleoptera: Histeridae and Staphylinidae). All E. monticola emerged from the bolts as larvae, but were identifiable as Lepturinae; previous incubations of such larvae in our laboratories have resulted in eclosion of E. monticola adults. We disregarded small detritus-feeding flies and parasitoids. We also disregarded the smallest scolytines as they proved very difficult to collect and quantify in our cages. However, even for bolts in which they were very numerous, their combined biomass was only ~0.1% of the next-smallest species, making it unlikely that they play a large functional role in the community. We monitored emergence from our bolts for 15 wk, ending 2 wk after the last Tetropium spp. had emerged and the majority of wood-boring insects had also stopped emerging. It is, of course, possible that some insects failed to emerge from our bolts because they require more than 1 yr (simulated) to develop and emerge. However, extensive previous rearings in our laboratories suggest that such insects would be a very small fraction of the total community. Table 1. Total emergence of the collected insect taxa from red and Norway spruce from control (n = 56), +T. cinnamopterum (n = 14), and +T. fuscum (n = 20) treatment bolts Order: Family Species Habitat and habits Reference Control +T. cinnamopterum +T. fuscum Red spruce Norway spruce Red spruce Norway spruce Red spruce Norway spruce Coleoptera: Cerambycidae T. fuscum 0 0 0 0 13 13 T. cinnamopterum 0 0 32 7 0 0 E. monticola Adults are flower-feeders. Larvae feed in the phloem and emerge to pupate in the soil. Vance et al. 2003 37 107 0 3 0 5 Coleoptera: Cleridae Thanasimus sp. Predators of bark beetles. Eggs are laid in bark crevices. Larvae inhabit the phloem and feed on eggs, larvae and pupae of bark beetles. Pupation occurs in chambers under the bark. Dippel et al. 1997 0 1 0 0 0 0 Coleoptera:Curculionidae D. rufipennis Eggs are laid in the phloem on which larvae feed. Overwinter as late instar larvae, pupae or adults. Wood et al. 1982 5 0 0 0 0 0 Dryocoetes affaber or autographus Eggs are laid in the phloem on which larvae feed. Overwinter as late instar larvae, pupae or adults. Wood et al. 1982 8410 5747 3518 2057 5287 3106 P. rufipennis Eggs are laid in the phloem on which larvae feed. Overwinter as late instar larvae, pupae or adults. Wood et al. 1982 1316 643 128 165 149 211 X. germanus Invasive ambrosia beetle from Asia. Adults tunnel into the wood and cultivate ambrosia fungi on which larvae feed. Pupation and mating occurs in galleries. Oliver and Mannion 2001 12 201 0 0 0 0 H. congener Adults feed on bark of spruce seedlings. Larvae feed on the inner bark of pine and spruce logs or stumps. Levesque and Levesque 1994 41 209 4 32 1 21 P. nemorensis Breed in logging slash and trees killed by bark beetles. Larvae feed on inner bark cambium. Pupation occurs in cocoons in the wood. Anonymous 1989 204 206 3 32 12 51 Coleoptera: Staphylinidae Family: Staphylinidae Adults and larvae are non-specific predators. Inhabit organic matter. Bohac 1999 3 1 0 0 1 3 Coleoptera: Histeridae Family: Histeridae Subcortical and predatory in habit. Marshall 2006 17 17 5 3 1 9 Diptera: Xylophagidae Xylophagus sp. Larvae develop as predators under the bark. Marshall 2006 5 46 0 0 0 1 Hymenoptera: Siricidae U. albicornis Eggs are laid in the wood. Larvae feed in the heartwood. Chrystal 1928 10 7 0 0 0 0 Order: Family Species Habitat and habits Reference Control +T. cinnamopterum +T. fuscum Red spruce Norway spruce Red spruce Norway spruce Red spruce Norway spruce Coleoptera: Cerambycidae T. fuscum 0 0 0 0 13 13 T. cinnamopterum 0 0 32 7 0 0 E. monticola Adults are flower-feeders. Larvae feed in the phloem and emerge to pupate in the soil. Vance et al. 2003 37 107 0 3 0 5 Coleoptera: Cleridae Thanasimus sp. Predators of bark beetles. Eggs are laid in bark crevices. Larvae inhabit the phloem and feed on eggs, larvae and pupae of bark beetles. Pupation occurs in chambers under the bark. Dippel et al. 1997 0 1 0 0 0 0 Coleoptera:Curculionidae D. rufipennis Eggs are laid in the phloem on which larvae feed. Overwinter as late instar larvae, pupae or adults. Wood et al. 1982 5 0 0 0 0 0 Dryocoetes affaber or autographus Eggs are laid in the phloem on which larvae feed. Overwinter as late instar larvae, pupae or adults. Wood et al. 1982 8410 5747 3518 2057 5287 3106 P. rufipennis Eggs are laid in the phloem on which larvae feed. Overwinter as late instar larvae, pupae or adults. Wood et al. 1982 1316 643 128 165 149 211 X. germanus Invasive ambrosia beetle from Asia. Adults tunnel into the wood and cultivate ambrosia fungi on which larvae feed. Pupation and mating occurs in galleries. Oliver and Mannion 2001 12 201 0 0 0 0 H. congener Adults feed on bark of spruce seedlings. Larvae feed on the inner bark of pine and spruce logs or stumps. Levesque and Levesque 1994 41 209 4 32 1 21 P. nemorensis Breed in logging slash and trees killed by bark beetles. Larvae feed on inner bark cambium. Pupation occurs in cocoons in the wood. Anonymous 1989 204 206 3 32 12 51 Coleoptera: Staphylinidae Family: Staphylinidae Adults and larvae are non-specific predators. Inhabit organic matter. Bohac 1999 3 1 0 0 1 3 Coleoptera: Histeridae Family: Histeridae Subcortical and predatory in habit. Marshall 2006 17 17 5 3 1 9 Diptera: Xylophagidae Xylophagus sp. Larvae develop as predators under the bark. Marshall 2006 5 46 0 0 0 1 Hymenoptera: Siricidae U. albicornis Eggs are laid in the wood. Larvae feed in the heartwood. Chrystal 1928 10 7 0 0 0 0 Species in parentheses had total emergence <10 individuals. View Large Diversity Analysis We pooled data across sites, as preliminary analyses revealed no effect of site on the numbers of insects emerging from control bolts (data not shown). We calculated Simpson diversity, richness, and evenness for each bolt, excluding Tetropium spp. because we were looking for responses of the remaining community to Tetropium. We used two-way ANOVAs to test the dependence of each variable on tree species and egg treatment. We tested first for interactions between the two main effects (tree species and egg treatment), using type III sums of squares. As all interactions were nonsignificant, we removed them and re-ran the ANOVAs (using type II sums of squares) with only main effects. We used Tukey’s post-hoc analyses to assess treatment effects within each tree species. Phylogenetic Distance Analysis We calculated the impact of each Tetropium species, on every other species in our focal community, as the percent difference in per-bolt emergence between control and +T. fuscum or +T. cinnamopterum egg-treatment bolts. For example, if the average control bolt yielded two individuals of species X, and the average +T. fuscum bolt yielded one individual of species X, then the impact is 50%. The largest possible impact is 100% (complete suppression). A negative impact means that emergence was actually higher in +Tetropium bolts (negative impacts can be stronger than −100%). We calculated impact separately in red and Norway spruce. For each focal species in each host tree, we also tested for statistical significance of this impact estimate with one-way ANOVA followed by Tukey’s honestly significant difference comparing emergence between control and +T. fuscum or +T. cinnamopterum bolts. We used literature phylogenies (Gaunt et al. 2002, Hedges et al. 2009, Parfrey et al. 2011, Ronquist et al. 2012, Vinther et al. 2012) to estimate the topology for the phylogenetic tree including each collected species (Fig. 1). We left members of the Curculionidae as a polytomy (a node subtending more than two lineages) because phylogenetic distances from curculionids to Tetropium do not depend on the topology within that family. We used Time Tree (timetree.org), which collates divergence-date information from the literature, to estimate the phylogenetic distance from each species to T. fuscum (Supp Appendix 1 [online only]). Finally, we regressed Tetropium impact against phylogenetic distance to the affected species (including all impact estimates, regardless of their individual significance). We ran four such regressions: one each for T. fuscum and T. cinnamopterum in red, and one each in Norway, spruce. As our insect species had highly variable emergence numbers, we also ran weighted regressions (by sample size or its square root). None of the weighted regressions differed in interpretation from the unweighted ones, and we do not report them here. We also calculated regressions including and excluding three species represented by fewer than 10 total individuals; this had no effect on interpretation of our analyses. We also repeated these regressions excluding the four predatory species. Fig. 1. View largeDownload slide Phylogenetic tree (from literature phylogenies) for the focal species. Time axis (vertical) not to scale. Fig. 1. View largeDownload slide Phylogenetic tree (from literature phylogenies) for the focal species. Time axis (vertical) not to scale. Results Insect Emergence From Red and Norway Spruce Bolts We collected a total of 32,118 individual insects of our focal species (including Tetropium spp.; Table 1). The first insects emerged less than a week after simulated overwintering. The first Tetropium emerged after 2 wk, and the last after 13 wk, at which point few other insects were emerging. Of our 14 focal species or morphospecies (Table 1), three were represented by fewer than 10 individuals. Average T. fuscum emergence from +T. fuscum bolts was ~1 adult beetle/bolt, and average T. cinnamopterum emergence from +T. cinnamopterum bolts was ~3 beetles/bolt. Diversity Both tree species and Tetropium egg treatment influenced Simpson diversity of wood-associated insects, including both its richness and evenness components (Table 2). Diversity was generally lower in red spruce than in Norway spruce (Fig. 2, compare left and right top panels). The experimental addition of Tetropium spp. reduced diversity of the remaining community: +T. fuscum bolts had significantly lower diversity than control bolts for both red (P = 0.006) and Norway spruce (P = 0.0076), while +T. cinnamopterum bolts had significantly lower diversity than controls for Norway spruce (P = 0.015) and the trend for red spruce was in the same direction (P = 0.10). Overall, these declines in diversity appeared to include both richness and evenness components (Fig. 2, middle and lower panels), although these component-wise effects were not always statistically significant. Richness was significantly reduced by both egg treatments in red spruce (+T. fuscum P < 0.0001, +T. cinnamopterum P = 0.0083) but in Norway spruce, the similar trends were not quite significant (+T. fuscum P = 0.10, +T. cinnamopterum P = 0.057). Evenness was significantly reduced by both egg treatments in Norway spruce (+T. fuscum P = 0.011, +T. cinnamopterum P = 0.023), while in red spruce the effect was significant for the +T. fuscum treatment (P = 0.014), but not for the +T. cinnamopterum treatment (P = 0.17). Table 2. Effects on Simpson diversity, richness, and evenness of emerging insects of Tetropium egg treatment (+T. fuscum, +T. cinnamopterum, or control) and host species (red or Norway spruce) Metric Effect SS df F Value P Value Simpson diversity Tree species 0.29 1 12.0 0.00083 Egg treatment 0.66 2 14.0 <0.0001 Residuals 2.03 86 Richness Tree species 57.7 1 42.9 <0.0001 Egg treatment 41.7 2 15.5 <0.0001 Residuals 116 86 Evenness Tree species 0.25 1 6.31 0.014 Egg treatment 0.98 2 12.3 <0.0001 Residuals 3.43 86 Metric Effect SS df F Value P Value Simpson diversity Tree species 0.29 1 12.0 0.00083 Egg treatment 0.66 2 14.0 <0.0001 Residuals 2.03 86 Richness Tree species 57.7 1 42.9 <0.0001 Egg treatment 41.7 2 15.5 <0.0001 Residuals 116 86 Evenness Tree species 0.25 1 6.31 0.014 Egg treatment 0.98 2 12.3 <0.0001 Residuals 3.43 86 Analysis is two-way ANOVA after pooling of nonsignificant interactions. View Large Fig. 2. View largeDownload slide Effects of T. cinnamopterum (T. cinn) and T. fuscum (T. fusc) on Simpson diversity, richness, and evenness in red and Norway spruce. Average emergence values are indicated by asterisks (*), and significant differences are indicated by letter differences. There was no significant difference in richness between control, T. cinnamopterum and T. fuscum in Norway spruce. The boxes represent the first (lower) and third (higher) quartiles, and the heavy line within each box represents the median. The highest and lowest lines represent the 90th percentiles. Fig. 2. View largeDownload slide Effects of T. cinnamopterum (T. cinn) and T. fuscum (T. fusc) on Simpson diversity, richness, and evenness in red and Norway spruce. Average emergence values are indicated by asterisks (*), and significant differences are indicated by letter differences. There was no significant difference in richness between control, T. cinnamopterum and T. fuscum in Norway spruce. The boxes represent the first (lower) and third (higher) quartiles, and the heavy line within each box represents the median. The highest and lowest lines represent the 90th percentiles. Phylogenetic Distance and Impact Only a few individual species showed significant suppression by Tetropium egg treatment, and for most of these, we saw effects only in one or two Tetropium × host species treatments (Table 3). The cerambycid Evodinus monticola emerged in smaller numbers in all four Tetropium treatments (vs egg-free controls), although the difference was not significant for +T. cinnamopterum on red spruce. Hylobius congener emergence was significantly reduced by +T. fuscum treatment in red spruce, and Xylophagus sp. emergence was significantly reduced for both +Tetropium treatments in Norway spruce, but not in red spruce. There was no relationship between the impact of Tetropium and phylogenetic distance to the affected species for any of the Tetropium × host species combinations (Fig. 3; regression statistics in Table 4). Regressions without the four predators reached identical conclusions (all P > 0.24). Table 3. Post-hoc P values (Tukey’s HSD) comparing species emergence between control bolts and either +T. fuscum (+TF) or +T. cinnamopterum (+TC) bolts Order: Family Species Norway spruce Red spruce CTRL−+TF CTRL−+TC CTRL−+TF CTRL−+TC Coleoptera: Cerambycidae T. fuscum <0.0001 1.000 <0.0001 <0.0001 T. cinnamopterum 1.000 <0.0001 1.000 E. monticola 0.008 0.021 0.036 0.075 Coleoptera: Cleridae Thanasimus sp. 0.812 0.854 NA NA Coleoptera: Curculionidae D. rufipennis NA NA 0.784 0.930 Dryocoetes affaber or autographus 0.358 0.559 0.289 0.481 P. rufipennis 0.999 0.985 0.298 0.465 X. germanus 0.493 0.585 0.458 0.549 H. congener 0.135 0.681 0.050 0.328 P. nemorensis 0.804 0.758 0.173 0.187 Coleoptera: Staphylinidae Family: Staphylinidae 0.091 0.970 0.993 0.748 Coleoptera: Histeridae Family: Histeridae 0.670 0.947 0.415 0.992 Diptera: Xylophagidae Xylophagus sp. 0.001 0.0038 0.562 0.643 Hymenoptera: Siricidae U. albicornis 0.698 0.762 0.742 0.795 Order: Family Species Norway spruce Red spruce CTRL−+TF CTRL−+TC CTRL−+TF CTRL−+TC Coleoptera: Cerambycidae T. fuscum <0.0001 1.000 <0.0001 <0.0001 T. cinnamopterum 1.000 <0.0001 1.000 E. monticola 0.008 0.021 0.036 0.075 Coleoptera: Cleridae Thanasimus sp. 0.812 0.854 NA NA Coleoptera: Curculionidae D. rufipennis NA NA 0.784 0.930 Dryocoetes affaber or autographus 0.358 0.559 0.289 0.481 P. rufipennis 0.999 0.985 0.298 0.465 X. germanus 0.493 0.585 0.458 0.549 H. congener 0.135 0.681 0.050 0.328 P. nemorensis 0.804 0.758 0.173 0.187 Coleoptera: Staphylinidae Family: Staphylinidae 0.091 0.970 0.993 0.748 Coleoptera: Histeridae Family: Histeridae 0.670 0.947 0.415 0.992 Diptera: Xylophagidae Xylophagus sp. 0.001 0.0038 0.562 0.643 Hymenoptera: Siricidae U. albicornis 0.698 0.762 0.742 0.795 Boldface indicates P < 0.05 (without correction for multiple testing). View Large Fig. 3. View largeDownload slide Comparing Tetropium impact on native insect species that range in evolutionary time of divergence from either +TC (T. cinnamopterum) in red (A) and Norway spruce (C) or +TF (T. fuscum) in red (B) and Norway spruce (D). Both +TC and +TF treatments are compared with control bolts. Open symbols indicate species for which an impact calculation includes fewer than 10 individuals. Arrow in (C) represents Staphylinidae, with an impact of −800% (based on only four individuals). Fig. 3. View largeDownload slide Comparing Tetropium impact on native insect species that range in evolutionary time of divergence from either +TC (T. cinnamopterum) in red (A) and Norway spruce (C) or +TF (T. fuscum) in red (B) and Norway spruce (D). Both +TC and +TF treatments are compared with control bolts. Open symbols indicate species for which an impact calculation includes fewer than 10 individuals. Arrow in (C) represents Staphylinidae, with an impact of −800% (based on only four individuals). Table 4. Effects of phylogenetic distance on Tetropium’s impact on other wood-associated species (unweighted regression slopes, separately by host tree species) Tetropium species Host spruce Slope SE P Value T. fuscum Red −0.009 0.20 0.97 Norway −0.37 1.02 0.3 T. cinnamopterum Red −0.38 0.48 0.45 Norway 0.10 0.21 0.64 Tetropium species Host spruce Slope SE P Value T. fuscum Red −0.009 0.20 0.97 Norway −0.37 1.02 0.3 T. cinnamopterum Red −0.38 0.48 0.45 Norway 0.10 0.21 0.64 Data visualization in Fig. 3. View Large Discussion Impacts on Diversity The exotic beetle T. fuscum had significant impacts on the community structure of phloem- and wood-inhabiting insects in Nova Scotia. Addition of T. fuscum eggs significantly decreased Simpson diversity in both host trees. In red spruce, this effect had both richness and evenness components, while in Norway spruce, evenness was reduced but we could not detect an effect on richness. However, the addition of T. cinnamopterum eggs had very similar effects (Fig. 2). This similarity in impact is not surprising because the two species are closely related and share a similar life history. T. fuscum can emerge as much as 2 wk before the native T. cinnamopterum (Juutinen 1955, Rhainds et al. 2010, Flaherty et al. 2013b), though, which could plausibly give it a developmental head start and favor greater impact through either competition or intraguild predation. While there are hints at such a pattern in our diversity data, our experiment was not designed for a powerful test of this hypothesis. Our results contrast with recent work by Dearborn et al. (2016), who were unable to detect any significant impact of Tetropium invasion on Simpson diversity or species richness of phloem- and wood-inhabiting insects. However, the two studies differed in several important ways. First, Dearborn et al. (2016) compared insect communities in naturally infested, standing red spruce between areas in Nova Scotia where T. fuscum is established and areas in New Brunswick where it is absent, whereas we used manipulative experiments to allow colonization of forest-floor bolts, at the same site, with or without T. fuscum and T. cinnamopterum. Second, our study had a much larger sample size (32,000+ reared insects, vs Dearborn et al.’s 223). Third, bolt condition was better controlled in our study (in the study by Dearborn et al., replication was achieved across different trees). Finally, Dearborn et al. tracked a different focal community, including parasitoids of Tetropium and with only Urocerus albicornis in common with our study among phloem-feeders and wood-borers (Dearborn et al. 2016). Dearborn et al. (2016) did report a significant displacement of the native T. cinnamopterum by T. fuscum. Because we had very few natural colonizations by Tetropium spp., our experiment could not detect such intrageneric effects. Taken together, Dearborn et al.’s (2016) results and our own strongly suggest important effects of Tetropium attack on insect communities—but effects that are not very different between exotic and native Tetropium species. The similarity of T. fuscum and T. cinnamopterum effects on insect communities does not, however, mean that T. fuscum’s establishment is of negligible concern. T. fuscum is able to attack trees in healthier condition (Flaherty et al. 2011) and thus its effects on host-tree populations may be more severe. In addition, if T. fuscum’s attack begins earlier in the decline of a stressed tree, then its impact on insect communities may be increased. However, our experiment controlled tree (bolt) condition, and so we could not test for such priority effects. Impact and Phylogenetic Relatedness The hypothesis that ecological interactions will often be strongest between close relatives is deeply seated in our literature, going back to Darwin (1859) and his Naturalization Hypothesis. More recently, it has underlain decades of research in community ecology, and was central to the development of “phylogenetic community ecology” as a subdiscipline (Vamosi et al. 2009). In an invasive species context, it has often been suggested that exotics with close relatives in their new range will spread more slowly and have lower population densities (e.g., Darwin 1859, Cavender-Bares et al. 2009, Schaefer et al. 2011), presumably because they compete with, and share natural enemies with, those close relatives. We were not able to test this hypothesis directly because we could not manipulate the natural community and measure response of the exotic species. Instead, we tested a corollary: that the corresponding impact of the exotic on native species would be strongest for close relatives. Our data do not support this hypothesis. We found significant impacts of Tetropium (both the native and the exotic) on populations of several community members (Table 3). The most consistent and among the strongest impacts were on the cerambycid Evodinus monticola, which was the closest relative of Tetropium spp. in our focal community. Evodinus, like Tetropium, feeds in phloem (Table 1). However, despite these strong impacts on E. monticola, there was no overall relationship between impact and phylogenetic distance (Fig. 3). Indeed, two very distant relatives (Hylobius and Xylophagus) were strongly suppressed in at least one Tetropium × host tree combination, whereas others were apparently unaffected. This should not come as a surprise: although relatedness may be a predictor of ecological similarity, it is rarely a perfect one. In fact, there is some obvious dissimilarity in our community (Table 1): the clerid, histerid, and staphylinid beetles, and the fly Xylophagus, are predators, whereas the remaining taxa feed on host tissue. Inclusion of the predators is not driving our (lack of) pattern, as their omission does not change the result; but it does demonstrate two things. First, guild membership does not map cleanly onto phylogeny: it is not the case that all phloem-feeders are closer relatives, with the predators more distant. Second, in our data guild membership does not predict interaction strength any better than phylogenetic relatedness, as the predator Xylophagus showed strong suppression along with some but not all phloem-feeders. The prediction of invasive-species impacts will turn on detailed knowledge of the autecology of invaders and natives, and is unlikely to be effectively shortcut by simple metrics of relatedness or by crude classifications of species into guilds. The Establishment and Spread of T. fuscum The ecology of T. fuscum in its exotic range is interesting for several reasons, including its very slow expansion (~130 km in ~25 yr from its introduction at the port of Halifax, Nova Scotia; Canadian Food Inspection Agency 2015). Several hypotheses have been offered to account for T. fuscum’s slow expansion, including the possibility of competition (or intraguild predation) from the abundant and diverse community of phloem- and wood-associated insects found in stressed and dying red spruce. Although our experiments measured the impact of Tetropium spp. on other community members rather than the reverse, our results suggest that unless interactions are extremely asymmetric, most members of the native community are likely to exert rather little control over T. fuscum performance or population density. Other hypotheses to explain T. fuscum’s slow spread, thus, appear to merit more attention, including the apparent existence of range-edge Allee effects (Rhainds et al. 2015), interactions with the native congener T. cinnamopterum (Dearborn et al. 2016), attack by native parasitoids shared with T. cinnamopterum (Flaherty et al. 2013a), and possible interbreeding with T. cinnamopterum. Some invasions are fast, and some are slow; understanding the mechanisms behind this should be a major target of invasive-species research. Supplementary Data Supplementary data are available at Environmental Entomology online. Acknowledgments We thank Jon Sweeney, Andrew Morrison, Emily Owens, Benoit Morin, Kate Van Rooyen, John McMullen, Andrew Lewis, Glen Forbes, Cory Hughes, Wayne McKinnon, Sue He, Zach Fitch, Joel Bates, Holly Blaquiere, Zach Sylvain, Garrett Broderson, Joris Wiersinga, Clare Forbes, Keegan Moore, Lauren Stead, Chrissy Cusack, Thomas Morin, Reginald Webster, Vince Webster, and Chantelle Alderson, all of the Atlantic Forestry Centre, Canadian Forest Service, for extensive support in laboratory and field. Ken Dearborn provided advice on experiments and species identifications, and Mallory MacDonnell helped in the field. Volunteers Sarah Johnstone, Carolyn Chee, Ethan Brewster, Connor Flynn, Jennier Oulette, Oriska Williams, Hali Mavor, Brett O’Donnell-Stairs, and Anthony Sulpizio helped sort insect samples. Graham Forbes, Jasen Golding, Véronique Martel, and several anonymous reviewers commented on the manuscript. 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