Detection programs for non-native species of bark and woodboring beetles require trap lure blends that can detect multiple species at the same time, thereby minimizing program costs (Fan et al. 2019, Hanks and Millar 2013, Poland and Rassati 2019, Rice et al. 2020). Lure combinations with the cerambycid pheromones 2,3-hexanediols and 3,2-hydroxyketones are successful in the detection of numerous species of cerambycids in eastern North America, particularly those that inhabit hardwood forests (Hanks and Millar 2013, 2016). Additionally, complex lure blends can provide opportunities for determining biodiversity of the woodboring guild (Dodds et al. 2015, Wickham et al. 2021).

In the southeastern United States, traps baited with ethanol + α-pinene are attractive to multiple species of longhorn beetles (Coleoptera: Cerambycidae) that inhabit pine forests (Miller 2006, 2020; Miller et al. 2015). The addition of the Ips bark beetle pheromones ipsenol and ipsdienol to traps baited with ethanol + α-pinene significantly enhances the abundance and diversity of cerambycid species captured in traps (Miller et al. 2011, 2013b, 2015). Ipsenol is used as a pheromone by Ips grandicollis (Eichhoff), whereas Ips avulsus (Eichhoff) and Ips calligraphus (Germar) use ipsdienol (Allison et al. 2012). Lanierone and cis-verbenol are two additional pheromones used by I. avulsus and I. calligraphus, respectively, in the southeastern United States (Allison et al. 2012; Miller et al. 2003, 2005). The goal of this study was to assess the benefit of adding lanierone and/or cis-verbenol to traps baited with the pine beetle lure blend of ethanol + α-pinene + ipsenol + ipsdienol. The primary focus of the study was on cerambycids; a secondary focus was on the responses of bark and ambrosia beetles, and associated predators.

Materials and Methods

A trapping study was conducted 7 May–17 June 2021 to determine the effects of lanierone and cis-verbenol (racemic) on catches of forest beetles in traps baited with the pine beetle lure blend (ethanol + α-pinene + ipsenol + ipsdienol). Ethanol and α-pinene [75%(–)] lures with release rates of 0.5 g/d and 1–6 g/d, respectively, were obtained from Scotts Canada (Victoria, BC, Canada). Synergy Semiochemicals Inc. (Burnaby, BC, Canada) supplied lures of ipsenol (racemic), ipsdienol (racemic), and lanierone, each with release rates of 0.1-0.2 mg/d, and cis-verbenol [87%(–)] released at 1–3 mg/d. All release rates were determined at 23°C by the respective manufacturer.

Six replicate blocks of four 10-unit black multiple-funnel traps (Synergy Semiochemicals) per block were set in a mature upland pine and hardwood forest at the Scull Shoals Experimental Forest (Greene Co.) in north Georgia, USA (33.7731°N, 83.2396°W). The primary tree species were Pinus taeda L., P. echinata Miller, Quercus alba L, Q. falcata Michaux, Liquidambar styraciflua L., and Carya tomentosa Sargent. The holes at the bottom of each funnel within a trap were enlarged from 5 to 12 cm to allow lures to be hung within funnels (Miller et al. 2013a). Traps were hung on twine tied between trees and >2 m from any tree and spaced approximately 10 m apart within and between blocks. Approximately 200 ml of an aqueous solution of propylene glycol (Winter-Eez RV & Marine Antifreeze, Southwin Ltd., Greensboro, NC) was placed in each collection cup to kill and preserve captured beetles (Miller and Duerr 2008). A piece (2.5 × 5.0 cm) of VaporTape II (Hercon Environmental Corp., Emigsville, PA) was attached under the canopy of each trap to prevent nest building by paper wasps.

All traps were baited with the pine beetle lure blend of ethanol + α-pinene + ipsenol + ipsdienol (P). In a randomized complete block design, one of the following four treatments was allocated to each of the four traps within each block: (1) P alone; (2) P + lanierone (L); (3) P + cis-verbenol (cV); and (4) P + L + cV. Voucher specimens were deposited in the University of Georgia Collection of Arthropods (UGCA), Athens, GA, USA.

SYSTAT (ver. 13) and SigmaStat (ver. 3.01) statistical packages (SYSTAT Software Inc., Point Richmond, CA) were used to analyze trap catch data for species with total counts ≥ 30. As needed, data were transformed by ln(Y + 1) to obtain normality and homoscedasticity, verified by the Shapiro-Wilk and equal variance tests, respectively. Data were analyzed by a mixed-model analysis of variance (ANOVA) with treatment as the fixed factor, followed by the Holm-Sidak multiple-comparison test for species affected by the treatments (α = 0.05). The Holm-Sidak test controls the overall experiment-wise error rate at 0.05 (Glantz 2005). For species affected by treatments, data were further analyzed by a mixed-model ANOVA using the following model factors: (1) L; (2) cV; and (3) L × cV.

Results

Cerambycidae. A total of 3,031 longhorn beetles were captured in the study, representing six cerambycid species (Table 1). Catches of cerambycids in traps baited with the pine beetle lure blend were not affected by lanierone and/or cis-verbenol for all six species: Acanthocinus nodosus (F.), Acanthocinus obsoletus (LeConte), Astylopsis arcuata (LeConte), Monochamus titillator (F.), Neoclytus acuminatus (F.), and Xylotrechus sagittatus (Germar) (Coleoptera: Cerambycidae) (Table 2).

Table 1 Numbers of beetles (Coleoptera) captured in multiple-funnel traps baited with ethanol + α-pinene + ipsenol + ipsdienol (P), with or without lanierone (L) and/or cis-verbenol (cV).

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Table 1 Continued.

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Table 2 Mean ± SE number per trap, and F and P values (ANOVA) for beetle species not affected by lure treatments.

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Curculionidae. The ambrosia beetle Cnestus mutilatus (Blandford), the bark beetles Dendroctonus terebrans LeConte and Hylastes porculus Erichson, and the weevils Hylobius pales (Herbst), Pachylobius picivorus (Germar), and Stenoscelis brevis (Boheman) were unaffected by the lure treatments (Table 2). In contrast, four species of bark beetles were affected by lure treatments. Lanierone lures affected trap catches of I. avulsus and I. grandicollis (Table 3). Traps baited with lanierone (with or without cis-verbenol) caught more I. avulsus than those baited with pine beetle lure blend alone or the blend + cis-verbenol (Fig. 1A). Catches of I. grandicollis were greater in traps baited with the pine beetle lure blend + lanierone than in traps baited with the pine beetle lure blend alone (Fig. 1B). Catches of I. calligraphus were affected by all three factors, whereas catches of H. tenuis were affected by cis-verbenol and the interaction between cis-verbenol and lanierone (Table 3). Catches of I. calligraphus were highest in traps baited with the pine lure blend + cis-verbenol and lowest in traps baited with the pine beetle lure blend (with or without lanierone) (Fig. 1C). Lanierone significantly reduced catches of I. calligraphus in traps baited with the pine lure blend + cis-verbenol (Fig. 1C). Traps baited with the pine beetle lure blend + cis-verbenol caught more H. tenuis than traps baited solely with the pine beetle lure blend (Fig. 1D).

Table 3 ANOVA results for effects of lanierone (L), cis-verbenol (cV), and the interaction of L × cV on catches of beetles in traps baited with ethanol + α-pinene + ipsenol + ipsdienol.

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Predators. Catches of the predatory species Temnoscheila virescens (F.) (Coleoptera: Trogossitidae) and Thanasimus dubius (F.) (Coleoptera: Cleridae) were unaffected by lure treatments (Table 2). Although catches of Enoclerus nigripes (Say) (Coleoptera: Cleridae) were affected by the interaction between lanierone and cis-verbenol (Table 3), catches in traps baited with the pine beetle lure blend alone were not different from those in traps co-baited with lanierone and/or cis-verbenol (Fig. 1E). Catches of Platysoma spp. (Coleoptera: Histeridae) were affected by cis-verbenol (Table 3) with catches in traps baited with the pine beetle lure blend + cis-verbenol + lanierone greater than those in traps baited solely with the pine beetle lure blend (Fig. 1F). The lanierone trap treatment affected catches of Lasconotus spp. (Coleoptera: Zopheridae) (Table 3), with catches in traps baited with the pine beetle lure blend + lanierone (with or without cis-verbenol) greater than those in traps baited solely with the pine beetle lure blend (Fig. 1G). Aulonium spp. (Coleoptera: Zopheridae) were caught in all traps except those baited solely with the pine lure blend (Fig. 1H).

Discussion

The addition of lanierone and/or cis-verbenol had no effect on catches of all six species of cerambycids captured in traps baited with the pine beetle lure blend of ethanol + α-pinene + ipsenol + ipsdienol (Table 2). Similarly, there were no treatment effects on catches of reproduction and snout weevils, several species of bark and ambrosia beetles (Curculionidae), and some species of associated predators (Cleridae, Tenebrionidae, and Trogossitidae) (Table 2). The major exception to this pattern were the responses of Ips bark beetles, especially I. avulsus (Fig. 1A–C). Unless managers are targeting Ips species specifically, there is no obvious benefit in adding lanierone and/or cis-verbenol to the pine beetle lure blend for detecting bark and woodboring beetles, and associated predators. The abundance of I. avulsus in traps baited with lanierone would slow processing of collections focused on detections of other taxa.

Results in this study may provide some additional insights into the chemical ecology of Ips avulsus, I. calligraphus, and I. grandicollis, which breed in various species of southern pines, often in the same tree (Allison et al. 2012). In 2009, Allison et al. (2012) found that catches of I. calligraphus in Georgia and Louisiana were highest in traps baited with ipsdienol + cis-verbenol, both pheromones of I. calligraphus, whereas catches were reduced with the addition of ipsenol, which is not a pheromone for I. calligraphus but is for I. grandicollis; lanierone was not tested. Similarly, I found that catches of I. calligraphus in traps baited with the pine beetle lure blend of ethanol + α-pinene + ipsenol + ipsdienol were significantly enhanced by the addition of cis-verbenol; an effect interrupted with the addition of lanierone (Fig. 1C). Miller et al. (2005) found that lanierone (pheromone for I. avulsus) reduced catches of I. calligraphus in traps baited with ipsdienol + cis-verbenol in Florida, Georgia, and Louisiana. These behaviors could minimize host competition interactions of I. calligraphus with I. grandicollis and/or I. avulsus.

Similar to previous results in Florida, Georgia, Louisiana, and North Carolina (Miller et al. 2005), I found no effect of cis-verbenol on catches of I. grandicollis in traps baited with the pine beetle lure blend (Fig. 1B). In contrast, trap catches of I. grandicollis increased with the addition of lanierone (Fig. 1B). Similarly in a phenology study of Ips spp. in Georgia, Brownell (2014) found that catches of I. grandicollis in traps baited with ipsenol + ipsdienol + lanierone were twice those in traps baited with its pheromone ipsenol and the host volatile α-pinene. These data suggest the possibility of a positive association between I. grandicollis and I. avulsus, the latter using lanierone as a pheromone (Miller et al. 2003, 2005). Ipsenol is the pheromone for I. grandicollis and attracts I. avulsus, which does not use ipsenol as a pheromone (Miller et al. 2003, 2005). The relationship between these two species in host use and allocation deserves further study and clarification.

The magnitude of the effects of lanierone on catches of I. avulsus in this study was surprising. There was a 44-fold increase in catches of I. avulsus in traps baited with the pine lure blend + lanierone compared with those in traps baited with the pine lure blend alone and a 69-fold increase in traps baited with the pine lure blend + lanierone + cis-verbenol compared with those in traps baited with the pine lure blend + cis-verbenol (Fig. 1A). Miller et al. (2005) noted only a two- to fourfold increase in catches of I. avulsus in traps baited with ipsenol + ipsdienol by the addition of lanierone, which is more than an order of magnitude less than the present study. The pine beetle lure blend does contain ethanol and α-pinene, a combination that reduces attraction of I. avulsus to traps baited with ipsenol + ipsdienol (Miller 2020, Miller and Crowe 2018, Miller et al. 2011). It may be that lanierone overrides the interruptive effect of host compounds by providing a species-specific indicator of host availability and mating opportunity for I. avulsus.

Species of Platysoma (Histeridae), Lasconotus, and Aulonium (Zopheridae) are thought to be predators of bark beetles (Dixon and Payne 1979, 1980; Goyer et al. 1980; Linit and Stephen 1983; Rohlfs and Hyche 1984; Steed and Wagner 2008; Stephen and Dahlsten 1976) and respond positively to pheromones produced by Ips spp. (Allison et al. 2013). The flight activity of Platysoma spp coincides with that of Ips spp in Louisiana (Shepherd and Goyer 2003). In a cage study with bolts of Pinus taeda L., Shepherd and Goyer (2005) found that brood mortality of I. calligraphus and I. grandicollis was significantly higher with the addition of Platysoma parallelum (Say) (Coleoptera: Histeridae) to the cages. In California, early-instar larvae of Lasconotus subcostulatus Kraus (Coleoptera: Zopheridae) feed on fungi under the bark of pine trees but switch to feeding on larvae of Ips paraconfusus (LeConte) as late-instar larvae (Hackwell 1973). In Israel, adult Aulonium ruficorne Olivier (Coleoptera: Zopheridae) feed on the eggs and larvae of the bark beetles Orthotomicus erosus (Wollaston) and Pityogenes calcaratus Eichhoff (Coleoptera: Curculionidae) (Podoler et al. 1990).

In this study, Lasconotus spp were most abundant in traps baited with lanierone (Fig. 1G), mirroring the response profile of I. avulsus (Fig. 1A). In contrast, the response profile of Platysoma spp was highest in traps baited with both compounds (Fig. 1F), suggesting generalist predation of Ips spp. Responses by Aulonium spp in our study also appear to be linked with those of lanierone and cis-verbenol as none were caught in traps without these compounds (Fig. 1H). The diversity of predators associated with bark and woodboring beetles underscores the need to understand their ecologies, particularly with the advent of non-native species of bark and woodboring beetles and climate change. This may be particularly important for trapping programs targeting pest species of bark beetles. Large captures of predators in such trapping programs may undermine the ability of predators to control populations of pest bark beetles.