In conifer-infesting bark beetles (Coleoptera: Curculionidae: Scolytinae), it is common for dispersing, host-seeking individuals to respond to odours produced by host trees either when these compounds are alone or present with beetle pheromone components (Miller and Borden Reference Miller and Borden2000; Pureswaran and Borden Reference Pureswaran and Borden2005; Hofstetter et al. Reference Hofstetter, Gaylord, Martinson and Wagner2012). These odours include various monoterpenes present in the host’s defensive resin that are released copiously following a breach of the tree’s inner bark or sapwood (Ruel et al. Reference Ruel, Ayres and Lorio1998; Tisdale et al. Reference Tisdale, Nebeker and Hodges2003; Seybold et al. Reference Seybold, Huber, Lee, Graves and Bohlmann2006). Mechanical injury (e.g., windthrow, lightning strike, harvesting operations) and insect attacks can result in release of large quantities of host volatiles (Coulson et al. Reference Coulson, Flamm, Pulley, Payne, Rykiel and Wagner1986; Strömvall and Petersson Reference Strömvall and Petersson1991; Pureswaran and Sullivan Reference Pureswaran and Sullivan2012). Presumably, these odours are attractive because they signal the location of trees of a suitable taxon that have been damaged and potentially weakened, rendering them more susceptible to colonisation (Schroeder and Lindelow Reference Schroeder and Lindelow1989; Tunset et al. Reference Tunset, Nilssen and Andersen1993; Pureswaran and Borden Reference Pureswaran and Borden2005). Evidence also suggests that concentrations of airborne resin volatiles may provide information on susceptibility and suitability of an individual host tree (Byers et al. Reference Byers, Lanne, Löfqvist, Schlyter and Bergström1985; Liu et al. Reference Liu, Wang, Xu and Sun2011; Burke and Carroll Reference Burke and Carroll2016). High levels could signify a strong defensive response and resin production in quantities that might prove lethal to invading bark beetles (Erbilgin and Raffa Reference Erbilgin and Raffa2000; Raffa et al. Reference Raffa, Aukema, Erbilgin, Klepzig and Wallin2005; Byers Reference Byers2012). Hence, relatively nonaggressive bark beetles that are less tolerant of resin defences may be attracted to low concentrations of host monoterpenes but repelled by high concentrations (Miller and Borden Reference Miller and Borden2000; Erbilgin et al. Reference Erbilgin, Powell and Raffa2003), resulting in a peaked, biphasic dose response to these compounds (Erbilgin et al. Reference Erbilgin, Powell and Raffa2003; Raffa et al. Reference Raffa, Aukema, Erbilgin, Klepzig and Wallin2005).

The bark beetle Ips avulsus (Eichhoff) is native to the southeastern United States of America and can be a consequential killer of pines (Pinaceae) when population numbers are high (Nebeker Reference Nebeker, Coulson and Klepzig2011). Pioneering males initiate galleries in the trees’ phloem and release a two-component pheromone (ipsdienol and lanierone) that attracts mates as well as other males that initiate attacks (Vité et al. Reference Vité, Bakke and Renwick1972; Birgersson et al. Reference Birgersson, Dalusky, Espelie and Berisford2012). Sufficient attacks can deplete resin defences of living hosts and render them suitable for colonisation. Ips avulsus is considered a bark beetle of intermediate aggressiveness, typically attacking weakened, wind-thrown, broken, or other trees with compromised defences, and this species only occasionally colonises healthy trees (Coulson et al. Reference Coulson, Flamm, Pulley, Payne, Rykiel and Wagner1986; Flamm et al. Reference Flamm, Pulley and Coulson1993). Evidence for a role of host monoterpenes in the chemical ecology of I. avulsus is limited. High (1–6 g/day) release of turpentine (the monoterpene-dominated distillate of pine resin) or the primary monoterpene of I. avulsus hosts, alpha-pinene (Mirov Reference Mirov1961; Bookwalter et al. Reference Bookwalter, Riggins, Dean, Mastro, Schimleck, Sullivan and Gandhi2019), either alone or with ethanol, reduces response of I. avulsus to traps baited with Ips pheromone components (Billings Reference Billings1985; Miller et al. Reference Miller, Asaro, Crowe and Duerr2011; Miller Reference Miller2020). There is no evidence of attractiveness of host odours, including alpha-pinene, to I. avulsus, either alone or with pheromones (Vité et al. Reference Vité, Gara and von Scheller1964; Birch et al. Reference Birch, Svihra, Paine and Miller1980; Svihra Reference Svihra1982; Billings Reference Billings1985; Smith et al. Reference Smith, Payne and Birch1990; Miller et al. Reference Miller, Asaro, Crowe and Duerr2011).

In the above-mentioned tests indicating that alpha-pinene reduces attraction of I. avulsus, the pheromone and alpha-pinene were released from the same point in space (a trap). However, in nature, host odours and bark beetle pheromones may differ in their points of origin, and it is possible that, under these circumstances, the semiochemicals may interact differently and produce altered behavioural responses by the beetles. When its release point is displaced, alpha-pinene might provide an attractive cue for presence of host material while not signalling host unsuitability and mortality risk at the pheromone source. As such, one might expect enhanced, rather than reduced, catches of I. avulsus by pheromone lures when displaced, high-release devices of alpha-pinene are present. The following study tested this hypothesis.

Three lines of five 12-unit multiple funnel traps (Lindgren Reference Lindgren1983) were established within mature pine forest (predominantly Pinus taeda Linnaeus) in central Louisiana, United States of America (within 2 km of 31.447° N, 92.286° W). Traps were more than 20 m from a road, more than 5 m from the nearest pine, and 100–200 m apart within the lines. More than 1 km separated the lines. Collection cups of the traps were 1–2 m above the ground and contained several centimetres of diluted propylene glycol. Traps were uniformly baited with “bubble” type lures releasing I. avulsus pheromone components ipsdienol (racemic, 0.6–0.8 mg/day at 25 °C; > 95% purity) and lanierone (0.05 mg/day at 25 °C; > 95% purity) attached to the trap midway vertically (Synergy Semiochemicals Corp., Delta, British Columbia, Canada; release and purity data provided by manufacturer). Treatments (factor TRTMT) were (1) no additional lure, (2) a low-rate release device of alpha-pinene attached to the trap, (3) a low-rate alpha-pinene device suspended approximately 1.5 m above the ground from a plastic pole positioned 4 m from the trap, and (4) and (5) similar to treatments 2 and 3, respectively, but each with a high-rate alpha-pinene device. alpha-Pinene devices were attached to traps at the same height as the pheromone components but on the opposite side of the trap. The pole supporting the displaced alpha-pinene device was positioned randomly relative to the trap at either 0°, 72°, 144°, 216°, or 288° from north within each line. The low-rate alpha-pinene device was a completely filled (4-mL), low-density polyethylene transfer pipette with a heat-sealed tip (Samco, San Francisco, California, United States of America; 0.06 g/day release); the high-rate device was a sealed low-density polyethylene enclosure (15 cm × 18 cm; 0.069 mm barrier thickness; 200 mL alpha-pinene; a 15 × 15-cm piece of burlap inside the enclosure wicked liquid throughout the interior; 8 g/day release) constructed with an impulse sealer. The alpha-pinene was 27% (+)enantiomer and at least 98% purity (Sigma-Aldrich, Milwaukee, Wisconsin, United States of America). Release rates for alpha-pinene devices were measured gravimetrically in a fume hood at mean 23 °C. Treatments initially were assigned randomly to traps within each line. Catches were collected at 3- to 5-day intervals, at which time treatments were re-randomised among traps within lines without replacement to a previous position. Rotations and collections occurred until every treatment had been at a trap position once (75 samples). The experiment was conducted from 2 to 20 September 2010.

Data (catches of I. avulsus, cube-root transformed) were analysed as a multiple Latin-squares design, with each trap line representing a square (factor SQUARE), and, within each square, each collection date (factor DATE) representing a row and each trap (factor TRAP) representing a column. Generalised linear model factors were SQUARE, TRTMT, DATE, SQUARE * TRTMT, DATE * TRTMT, and TRAP(SQUARE). The error term for tests was SQUARE * TRTMT. Suitability of the transformation was determined through examination of residuals plots. Tukey’s tests were used for all-pairwise comparisons (α = 0.05). Statistical analysis was performed with SAS 9.4 (SAS Institute, Cary, North Carolina, United States of America).

A total of 3606 I. avulsus (identified according to Wood (Reference Wood1982)) was trapped. Catches were influenced by treatment (F = 16.7; df = 4, 8; P < 0.001; Fig. 1). Catches with the low-rate alpha-pinene device, either on or off the trap, did not differ from the control (no alpha-pinene). High-rate devices of alpha-pinene reduced catches of I. avulsus below the level of the control (approximately half) when placed on the trap but increased catches above the control (approximately double) when placed 4 m away.

Fig. 1. Mean (± standard error) responses of bark beetle Ips avulsus to multiple-funnel traps baited with devices releasing Ips avulsus aggregation pheromone (ipsdienol and lanierone) and host odour alpha-pinene (αP) at two different rates (low = 0.06 g/day; high = 8 g/day; at ∼23 °C) either from the trap itself or a point 4 m away. Means associated with same letter were not significantly different (Tukey’s test, α = 0.05). Raw means are shown; statistical analyses were performed with cube-root transformed data.

The results indicate that high-release sources of alpha-pinene may either enhance or reduce I. avulsus response to its aggregation pheromone depending on proximity of the release points of the semiochemicals. This result is consistent with that of Miller and Crowe (Reference Miller and Crowe2018) who found that I. avulsus catches were greater in a pheromone-baited trap if it was located 6 m rather than 2 m from a trap releasing ethanol and a high rate of alpha-pinene (0.5 and 1–6 g/day, respectively); however, their test did not determine whether the effects were the result of attraction or inhibition. Hence, alpha-pinene could have distinct functions for I. avulsus at different spatial scales. The attraction-enhancing effect of the high-rate alpha-pinene device in the present experiment occurred at 4 m and thus presumably would influence beetle behaviour within a space encompassing multiple potential host trees and a substantial portion of the host bole. The antagonistic effects of alpha-pinene occurred at a smaller distance (15–20 cm separated the alpha-pinene and pheromone devices on the trap). This antagonism may divert beetles from portions of the host where high concentrations of alpha-pinene indicate a vigorous and potentially lethal defensive response. Thus, for I. avulsus, alpha-pinene may function both as (a) a host patch or “host habitat” location cue (Payne Reference Payne1983), enhancing location of sites with trees potentially suitable for colonisation, and as (b) a short-range indicator of insufficient susceptibility and suitability of a particular host or a portion thereof. However, because the experiment used a pheromone lure, conclusions must be confined to the context of an ongoing beetle attack; the possible role of alpha-pinene in “pioneer” attacks requires further study. Furthermore, it is unknown how often host-seeking I. avulsus in nature might encounter airborne alpha-pinene concentrations comparable to those produced by the high-release devices.

The alternatively enhancing or reducing effects of alpha-pinene on I. avulsus responses are potentially attributable to an undiscovered biphasic dose response (i.e., with attractive or repellent effects produced by either low or high concentrations, respectively (Rudinsky Reference Rudinsky1973; Sullivan and Brownie Reference Sullivan and Brownie2021), a phenomenon often termed “multifunctionality” in the bark beetle literature) to alpha-pinene. Ips avulsus’ sibling species, Ips pini (Say), has a biphasic dose response to alpha-pinene released from traps baited with aggregation pheromone (Erbilgin et al. Reference Erbilgin, Powell and Raffa2003), as does the white pine cone beetle, Conophthorus coniperda (Schwarz) (Coleoptera: Curculionidae) (Miller et al. Reference Miller, Crowe, Asaro and Debarr2003). Average airborne concentration of a semiochemical is influenced by both the rate of release and the distance from the release point (Strand et al. Reference Strand, Lamb, Thistle, Allwine and Peterson2009; Cardé Reference Cardé2021). Because of this, a biphasic dose response may coincide with a biphasic “distance-response” (Sullivan and Mori Reference Sullivan and Mori2009; Sullivan Reference Sullivan2016). The experiment tested only two release rates of alpha-pinene (0.06 and 8 g/day), and response to traps was not altered by the low-rate device whether it was located on or off the trap. Whether an intermediate or lower rate of alpha-pinene from the trap can enhance attraction remains to be tested. Also, future research should address whether distances of host odour release greater than 4 m from the pheromone source can enhance I. avulsus attraction.

These results and interpretation provide further evidence that operational lures for Ips avulsus and perhaps other species of less aggressive bark beetles might be improved by deploying host odour devices away from pheromone-baited traps (Miller and Crowe Reference Miller and Crowe2018).