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JEN 128(9/10) doi: 10.1111/j.1439-0418.2004.00899.633–638 Attractive responses by Monochamus galloprovincialis (Col.,Cerambycidae) to host and bark beetle semiochemicals J. A. Pajares1, F. Ibeas1, J. J. Dı´ez1 and D. Gallego2 1Departamento de Produccio´n Vegetal y Recursos Forestales, ETSIIAA, Universidad de Valladolid, Palencia; 2Departamento de Zoologı´a y Antropologı´a Fı´sica, Universidad de Murcia, Murcia, Spain Ms. received: April 27, 2004; accepted: July 30, 2004 Abstract: The pine sawyer Monochamus galloprovincialis is the European vector of the recently introduced pine woodnematode. This nematode is the causal organism of pine wilt disease, a serious tree killer in East Asia. Efficacious baitsand traps to monitor and control this beetle are now required. The effect of bark beetle (Ips spp.) pheromonecomponents, released individually (ipsenol) or in blends (ipsenol, ipsdienol, cis-verbenol and methyl-butenol), togetherwith host volatiles (turpentine or a-pinene and ethanol) on M. galloprovincialis trap catches has been studied in Spain.
A kairomonal response by male and female of M. galloprovincialis to Ips semiochemicals was found. Beetles were moreattracted to host blends supplemented with bark beetle pheromones than to host volatiles alone. Ipsenol alone wasattractive to pine sawyers, and was synergistic with a-pinene and ethanol. The full blend of the four Ips semiochemicalsand the host compounds was highly attractive. Multiple-funnel traps were as effective as black cross-vane traps incapturing this insect when the escape of trapped beetles was prevented. Trapping of non-target bark beetle predatorswas also evaluated. The trogossitid Temnochila coerulea and clerid Thanasimus formicarius were kairomonally attractedto and killed in traps baited with bark beetle pheromones. These results suggest that effective monitoring ofM. galloprovincialis would be possible by baiting any of these traps with host volatiles and Ips semiochemicals, butreduction of the lure components and trap modification to minimize impact on predators should be considered.
Key words: cis-verbenol, a-pinene, ipsdienol, ipsenol, methyl-butenol, traps lished report, 1997, in McIntosh et al., 2001) or as highas 30% in log yards in Alberta (Safranyik and Raske, Bark and wood boring longhorn beetles form a large 1970). In Europe, timber degradation by Monochamus group of species usually colonizing woody plants that sutor (Linnaeus), Monochamus sartor (Fabricius) and are severely stressed, often near to death, by fire, drought Tetropium castaneun (Linnaeus) affected 120 000 m3 of or by the action of other organisms. Many adults feed on pine and 225 000 m3 of spruce in Romania during the nectar or pollen of flowers while others feed on bark in 1990s (Evans et al., 2004). Apart from this damage, the the crown of trees. Eggs are usually deposited in bark roles of the species in the genus Monochamus Dejean as crevices or in niches chewed within the bark. Larvae vectors of the pine wood nematode, Bursaphelenchus bore under the bark, feeding in the phloem tissues, later xylophilus (Steiner et Buhrer) Nickle, the causal agent of mining into the sapwood, and in some cases into the pine wilt disease, are of enormous relevance. Healthy heartwood, to complete their development and to finally trees are inoculated with nematodes during adult pupate in characteristic pupal cells (Bense, 1995). Most maturation feeding on the shoots (Mamiya and Enda, forest cerambycids are considered secondary pests of 1972) and transmission to susceptible dying or dead trees that could be included in the stressed or dead host trees occurs during female oviposition. Disease expres- species categories (sensu Hanks, 1999), representing sion and extensive tree mortality has been associated good biological indicators of forest biodiversity. How- with the presence of highly susceptible tree species, ever, a few species are capable attacking and killing suitable vector species and mean daily summer temper- living, healthy trees or those with defences that have atures above 20°C (Rutherford et al., 1990). Pest risk been weakened (Hanks et al., 1995; Hanks, 1999; Smith assessments concluded that the nematode would survive and Humble, 2000; Macleod et al., 2002).
in Europe, although tree mortality would likely be The most economically important damage produced restricted to the warmer southern countries (Evans by longhorned beetles is timber degradation caused by et al., 1996). Recent discovery of the pine wood larva boring in the sapwood and heartwood. For nematode causing death of Pinus pinaster trees in example, estimated degrade losses caused by ceramby- Portugal (Mota et al., 1999) has created great concern cid larvae in Canada have been set at $43 million in Europe. Monochamus galloprovincialis (Olivier) has annually in British Columbia (Phero Tech Inc. unpub- been confirmed as the vector of B. xylophilus in Portugal were as effective as cross-vane traps in trapping (Sousa et al., 2001), thus increasing the demand for M. scutellatus and M. obtusus (Morewood et al., 2002).
effective methods to monitor and control this beetle.
In this paper we report results of field experiments Many woodborers infesting dying conifers are aimed to: (i) determine if M. galloprovincialis would known to be attracted by host odours (Phillips et al., also present a kairomonal response to Ips spp. phero- 1988) and commercial baits are currently based on host mone components that could be used for control monoterpenes (a-pinene) and ethanol. Billings and purposes, (ii) compare the efficacy of black-panel (1984) and Billings (1985) demonstrated in cross-vane traps vs. multiple-funnel traps in capturing North America a kairomonal response by Monochamus M. galloprovincialis and (iii) determine if non-target titillator (Fabricius) to blends of bark beetle phero- bark beetle predators would be also attracted and mones, synergized by host turpentine. Allison et al.
(2001, 2003) suggest that this behaviour may benefithost-seeking woodborers by mitigating the cost of hostlocation and placing larval cerambycids in the proxim- ity of bark beetle larvae which may serve as prey items.
Recent studies have found kairomonal responses by Four experiments were carried out at two different sites in four other Monochamus species in Canada [M. clamator north-west and south-east Spain. Experiments 1 and 2 were (LeConte), M. scutellatus (Say), M. notatus Casey and set up at a planted P. pinaster forest with trees approximately M. obtusus Drury] to bark beetle pheromone blends 60 years old in Sierra de la Culebra, Zamora, and were consisting of ipsenol, ipsdienol, 3-methyl-2-cyclohexen- conducted from 26 June to 8 August and 8 August to6 October 2003 respectively. They compared 12-unit mul- 1-one and frontalin (Allison et al., 2001). Further tiple-funnel traps (Lindgren, 1983; Phero Tech Inc. Delta, research on the individual bioactivity of bark beetle BC, Canada) to cross-vane traps made by the authors with semiochemicals showed that ipsenol and ipsdienol, two interlocked black PVC panels, 80 cm high, 30 cm wide, aggregation pheromones of Ips DeGeer spp., were held at right angles by an iron frame and connected to a highly synergistic to a-pinene and ethanol in the 33-cm diameter white plastic funnel ending in a 500 ml attraction of M. clamator and M. scutellatus, whereas collecting bottle. Both traps were tested baited with host pheromone compounds emitted by Dendroctonus volatile stimuli either alone or supplemented by a blend of Ips spp. semiochemicals (table 1). Traps were hung by a rope to Several trap designs have been tested for capturing branches of trees and suspended 3–4 m above ground. The large woodborers. It has been shown that traps with four treatments for experiments 1 and 2 were: host volatilesin (i) cross-vane traps or (ii) multiple funnel traps, host black silhouettes are significantly more effective volatiles plus Ips spp. pheromone blend in (iii) cross-vane or (iv) multiple-funnel traps. Host volatiles consisted of Pinus M. scutellatus, than traps with clear vanes (de Groot spp. turpentine plus ethanol in experiment 1 and of a-pinene and Nott, 2001). In another experiment, black-panel and ethanol in experiment 2. The pheromone blend was cross-vane traps were more effective than dry multiple- composed of ipsdienol, cis-verbenol and 2-methyl-3-butenol funnel traps for capturing several North American in experiment 1 and of ipsdienol, ipsenol and 2-methyl- Monochamus species (McIntosh et al., 2001). Of the three suggested potential limitations of multiple-funnel Experiments 3 and 4 were conducted from 20 June to traps for trapping Monochamus beetles [(i) escape by 10 August and 10 August to 26 September 2003, in a Pinus captured insects from the collecting cup, (ii) insects halepensis natural forest at Sierra Espun˜a, Murcia. They falling outside the funnel column and (iii) poor visual tested the response of M. galloprovincialis to differentcombinations of host volatiles and Ips pheromone com- orientation to a narrow silhouette], the former proved pounds deployed in 12-unit multiple-funnel traps suspended to be important. Thus, when multiple-funnel traps between trees with the top funnel 1.8 m above ground.
were provided with water-filled collecting cups they Table 1. Compounds tested as attractants for Monochamus galloprovincialis in field experiments a Phero Tech Inc. Delta, BC, Canada; Esencias Catala´ S.L., Gandı´a, Valencia, Spain; Panreac Quı´mica S.A., Montcada i Reixac,Barcelona, Spain; Unio´n Resinera Espan˜ola S. A., Madrid, Spain.
b Release devices for ipsdienol, ipsenol, cis-verbenol and 2-methyl-3-butenol were from Phero Tech Inc.
Release devices for a-pinene, ethanol and turpentine were 50 ml plastic vials with perforated caps. All compounds were released sepa-rately.
c Release rates for ipsdienol, ipsenol, cis-verbenol and 2-methyl-3-butenol were determined at 25°C by Phero Tech Inc.; release rates fora-pinene, ethanol and turpentine were gravimetrically calculated at Universidad de Valladolid at 27–30°C.
d Turpentine distilled from Pinus spp. resin. Major compounds were determined at INIA, Madrid, Spain, as: a-pinene (65.1%), b-pinene(20.8%), limonene (1.9%), longifolene (1.6%), camphene (1.1%).
Ó 2004 Blackwell Verlag, Berlin, JEN 128(9/10) doi: 10.1111/j.1439-0418.2004.00899.633–638 Attractive responses by Monochamus galloprovincialis Experiment 3 tested the effect of supplementing host volatiles with ipsenol and ipsdienol. Treatments were: turpentine plusethanol (i) alone; (ii) plus ipsenol; (iii) plus ipsenol and In experiments 1 and 2, catches of both sexes of ipsdienol and (iv) plus ipsdienol, cis-verbenol and 2-methyl- M. galloprovincialis were significantly greater in traps 3-butenol. Experiment 4 tried to determine if there was baited with host volatiles plus the three-component synergism between ipsenol and host volatiles and compare it blend of Ips spp. pheromones than in traps baited with with a full blend of host and Ips compounds. Traps were host volatiles alone (fig. 1). Host volatiles alone (either baited with (i) a-pinene plus ethanol; (ii) ipsenol; (iii) a-pinene turpentine plus ethanol in experiment 1 or a-pinene plus ethanol and ipsenol and (iv) a-pinene plus ethanol, plus ethanol in experiment 2) resulted in low trap ipsenol, ipsdienol, cis-verbenol and 2-methyl-3-butenol.
catches at the release rates tested. No differences were All experiments were deployed in seven randomized com- observed in the trap catches of cross-vane traps and plete blocks. Distance between traps was at least 100 m andnearest blocks were 700 m apart. Collecting cups were multiple-funnel traps baited with either host volatiles provided with a small piece of DDVP insecticide (Econex alone or host volatiles plus bark beetle semiochemicals S. L., Murcia, Spain) to avoid escape of the trapped beetles.
in either experiment 1 or 2. This suggests that both Captured M. galloprovincialis were collected every 10–14 days types of traps are equally effective in capturing and stored frozen until identified and sexed (Vives, 2000).
M. galloprovincialis, providing the insects cannot Adults of bark beetle predators Thanasimus formicarius escape from the collecting receptacle.
(Linnaeus) and Temnochila coerulea (Olivier) were also In experiment 3, multiple funnel traps baited with collected to assess trapping of these natural enemies.
Pinus spp. turpentine plus ethanol trapped very few Data for each sex or species (predators) were transformed individuals of M. galloprovincialis (fig. 2). Addition of by log10(x + 1) to meet assumptions of normality and ipsenol to the host blend greatly increased catches of homocedasticity, and subjected to anova (GLM) for rand-omized complete blocks with the SAS System software ( males and females of this beetle. Traps baited with host volatiles, ipsenol and ipsdienol did not catch any more Institute Inc., 1999–2000). Mean values were compared byTukey’s multiple comparisons test at a ¼ 0.05.
beetles than traps baited with host volatiles plus ipsenolalone. Similarly, the addition of the three-componentpheromone blend tested in experiment 1, ipsdienol, cis-verbenol and methyl-butenol, to traps baited with host volatiles alone, had the same effect on M. galloprovin- cialis trap catches as the addition of ipsenol alone.
Experiment 4 tested the synergistic effect between host volatiles and ipsenol. As before, traps baited with host Experiment 1
Experiment 3
Experiment 2
Experiment 4
Fig. 1. Catches of Monochamus galloprovincialis inSierra de la Culebra, Zamora, Spain to cross-vane Fig. 2. Catches of Monochamus galloprovincialis in (CRV) or to multiple-funnel (MF) traps baited with Sierra Espun˜a, Murcia, Spain to multiple-funnel traps host volatile blend alone or supplemented with Ips spp.
baited with host volatile blend alone or with Ips spp.
pheromone blend. Components are Tu, turpentine; aP, semiochemicals. Components are Tu, turpentine; aP, a-pinene; Et, ethanol; Id, ipsdienol; Is, ipsenol; cV, cis- a-pinene; Et, ethanol; Id, ipsdienol; Is, ipsenol; cV, cis- verbenol; Mb, 2-methyl-3-butenol. For each sex, bars verbenol; Mb, 2-methyl-3-butenol. For each sex, bars followed by the same letter are not significantly different.
followed by the same letter are not significantly different.
Tukey’s test, P > 0.05. anova statistics are: experiment Tukey’s test, P > 0.05. anova statistics are: experiment 1: males F ¼ 3.02, d.f. ¼ 9, P ¼ 0.0221, n ¼ 7; females 3: males F ¼ 9.19, d.f. ¼ 9, P < 0.0001, n ¼ 7; F ¼ 4.18, d.f. ¼ 9, P ¼ 0.0048, n ¼ 7; experiment 2: males F ¼ 7.58, d.f. ¼ 9, P ¼ 0.0001, n ¼ 7; females experiment 4: males F ¼ 21.45, d.f. ¼ 9, P < 0.0001, F ¼ 9.99, d.f. ¼ 9, P < 0.0001, n ¼ 7 n ¼ 7; females F ¼ 19.81, d.f. ¼ 9, P < 0.0001, n ¼ 7 Ó 2004 Blackwell Verlag, Berlin, JEN 128(9/10) doi: 10.1111/j.1439-0418.2004.00899.633–638 la Culebra, Zamora (exp. 1and 2) and in Sierra Espun˜a, Tu, turpentine; aP, a-pinene; Et, ethanol; Is, ipsenol; Id, ipsdienol; cV, cis-verbenol; Mb, 2-methyl-3-butenol. For each experiment and species, means followed by the same letter are not significantlydifferent. Tukey’s test, P > 0.05. anova statistics are: T. coerulea: experiment 1, F ¼ 9.46, d.f. ¼ 9,P < 0.0001, n ¼ 7; experiment 2, F ¼ 5.00, d.f. ¼ 9, P ¼ 0.0018, n ¼ 7; experiment 3, F ¼ 2.01,d.f. ¼ 9, P ¼ 0.0987, n ¼ 7; experiment 4, F ¼ 3.47, d.f. ¼ 9, P ¼ 0.0119, n ¼ 7; T. formicarius:experiment 1, F ¼ 15.47, d.f. ¼ 9, P < 0.0001, n ¼ 7; experiment 2, F ¼ 2.18, d.f. ¼ 9,P ¼ 0.0766, n ¼ 7.
stimuli (a-pinene and ethanol) alone did not captured 2003). In all experiments, addition of blends of Ips spp.
many beetles (fig. 2). Traps baited with ipsenol alone pheromone components greatly increased attraction to captured six times more beetles than those baited with host volatiles. Ipsenol, the sole pheromone component the host blend alone. A synergistic effect was observed tested individually, was attractive to both sexes of when both baits were released together. Catches of both M. galloprovincialis, corroborating the previous finding male and female M. galloprovincialis obtained by host by Allison et al. (2003) that this compound is a stimuli plus ipsenol were two times higher than those kairomone for M. scutellatus and M. clamator. Even resulting from the sum of catches obtained by the host ipsenol alone was more attractive to M. galloprovin- stimuli alone and ipsenol alone. Addition of the full cialis than a-pinene plus ethanol, and a synergistic effect blend of Ips spp. components, ipsdienol, ipsenol, cis- was found when the three compounds were released verbenol and methyl-butenol, to a-pinene and ethanol together (experiment 4; fig. 2). Notably, a very high significantly raised the catches (3.6 times) of both sexes number of beetles were captured with the full blend of compared with those in traps releasing a-pinene, a-pinene, ethanol, ipsenol, ipsdienol, cis-verbenol and methyl-butenol (experiment 4; fig. 2). The significance Two major bark beetle predators, Temnochila coeru- of this result is enhanced by the fact that M. gallopro- lea (Trogossitidae) and Thanasimus formicarius (Cleri- vincialis populations in the trapping area were estima- dae), were also captured (table 2). Temnochila coerulea ted to be of moderate to low level, based on the existing trap catches were high during the first half of the breeding material. The practical application of a six- summer in both sites (experiments 1 and 3) but catches component lure is unclear. Although very effective in dropped notably during the second half. A clear attracting M. galloprovincialis, it may be too complex kairomonal response of this species to bark beetle and costly for use in operational monitoring or mass semiochemicals was found in experiment 1 (site 1, early trapping programmes. However, it may be possible to summer) but in the other tests no significant differ- improve this bait by reducing the number of compo- ences occurred between baits releasing the host blend nents without lowering its effectiveness.
alone or supplemented with bark beetle compounds, Host monoterpenes and ethanol are known to although mean values were always higher in the attract several woodborers infesting stressed or mori- later case. Fewer T. formicarius were trapped than bund conifer trees. In Japan, the vector of the pine wilt T. coerulea in site 1; however this predator was also disease Monochamus alternatus Hope, was attracted to attracted to bark beetle blends. No effect of trap type on a blend of 10 monterpenes (Ikeda et al., 1980, 1981).
trap catches was observed for either of these predators.
The North American pine sawyers Monochamus caro-linensis (Olivier) and M. titillator were captured inhigher numbers in traps baited with turpentine plusethanol than in those baited with turpentine alone (Fatzinger, 1985). In another study, trap catches of Our results extend to M. galloprovincialis the kairomo- M. carolinensis were unaffected by the addition of nal response to bark beetle pheromones found for other ethanol to turpentine, while attraction of M. titillator was Monochamus species in North America (Billings and enhanced (Phillips et al., 1988). Che´nier and Philoge`ne Cameron, 1984; Billings, 1985; Allison et al., 2001, (1989) found that a-pinene was more attractive to Ó 2004 Blackwell Verlag, Berlin, JEN 128(9/10) doi: 10.1111/j.1439-0418.2004.00899.633–638 Attractive responses by Monochamus galloprovincialis M. scutellatus than a blend of other minor turpentine black silhouette to the insects but trapping surface of components (b-pinene, 3-carene, limonene, myrcene cross-vane traps was 32% greater (5717 cm2 vs.
and camphene) and stated that a-pinene and ethanol 7540 cm2). Morewood et al. (2002) studied the reasons acted synergistically, although this result was not clear- of the lower efficacy of multiple-funnel traps with dry cut. In our experiments, host volatile baits, whether collection cups compared with cross-vane traps when turpentine plus ethanol or a-pinene plus ethanol, had capturing Monochamus spp. (McIntosh et al., 2001).
very little effect on M. galloprovincialis trap catches.
They observed that the poorer performance of the Release rates were quite high and comparable with multiple-funnel traps was the result of the escape of the North American studies that did observe an effect insects from the dry cups and not to the falling outside (Allison et al., 2001, 2003). It is possible that the low of the funnel column. In our experiments, beetles were catches observed in this study may be the result of the prevented from escaping by killing them with a small low population levels in the study area. In any case, a block of insecticide. Thus, the light, easy-to-use, synergism was observed between a-pinene and ethanol standard multiple-funnel trap seems effective enough and ipsenol (experiment 4; fig. 2). Consequently, host for operational trapping of M. galloprovincialis, but volatiles should be considered an integral component of escape of captured insects must be somehow avoided effective baits for mass-trapping M. galloprovincialis.
(insecticide, water filling, etc.). However this require- The possibility that only a-pinene is required to enhance ment would lead to the elimination of non-target the response deserves further testing.
insects, particularly bark beetle predators. Kairomo- All the four bark beetle components in the most nal responses of bark beetle natural enemies to bark attractive bait are emitted in the pheromonal signals beetle semiochemicals and host volatiles are well from European Ipini species infesting pines [e.g. Ips known (e.g. Dahlsten, 1982; Gre´goire et al., 1992; Ross sexdentatus (Boerner), Ips acuminatus (Gyllenhall), Ips and Daterman, 1995; Dahlsten et al., 2003; Schroeder, mannsfeldii (Watchl) and Ips (Orthotomicus) erosus 2003). In this study high numbers of T. coerulea and (Wollaston) (Kohnle et al., 1988, 1993)]. These are T. formicarius were attracted and subsequently killed generally secondary species breeding in stressed, fallen in traps baited with these stimuli. Thus, if these stimuli or dying trees, but some may become primary attackers were used for trapping M. galloprovincialis, bark beetle and kill healthy trees when favourable conditions predators would also be removed along with the target (drought, windthrown trees, forest fires) allow popula- species. This may have negative effects on bark beetle tions to reach outbreak levels. Dispersal flights of these population dynamics. Minimizing the capture of species widely overlap spatially and temporally with predators is then required and some simple modifica- that of M. galloprovincialis during the summer, so it tions of trap design have already been tested (Ross and would be advantageous for the pine sawyers to respond kairomonally to the pheromonal signals released by between these species could allow using a screen filter these secondary bark beetles. On the contrary, primary of appropriate size within the collection cup, retaining bark beetles obligatorily attack standing, living trees, Monochamus beetles and leaving predators to escape although they do not always succeed in killing them. In through the open drainage hole in the bottom.
that sense, signals from these primary attackers would Results presented here shows the potential of be less reliable indicators of suitable host material for attractive baits containing host volatiles and Ips woodborers and this may explain the lack of response semiochemicals (experiment 4) deployed in multiple- by North American Monochamus to Dendroctonus spp.
funnel traps for operational monitoring and trapping pheromones (Allison et al., 2003). In North America, of M. galloprovincialis. However, improvement of the ipsenol significantly enhanced attraction of both sexes lure (i.e. reduction of components) and trap modifica- of M. clamator and of M. scutellatus males to host tion should be studied before a trap-out programme response of M. clamator to the host blend. However,only the response of M. scutellatus females was significantly higher to traps baited with both ipsenoland ipsdienol than to each individually added to the We thank J.M. Sierra, A. Martı´n, G. Pe´rez (Centro de host blend (Allison et al., 2003). In our case, ipsenol Sanidad Forestal de Calabazanos, Junta de Castilla y Leo´n) was attractive to M. galloprovincialis, either released and J.D. Cabezas (Parque Regional de Sierra Espun˜a, alone (experiment 4; fig. 2) or when combined with the Murcia) for access to field sites, G. Sa´nchez (DGCN, host blend (experiments 3 and 4; fig. 2). Addition of Madrid) for assistance, and C. Garcı´a-Vallejo (CIFOR-INIA; Madrid) for turpentine analysis. Financial support ipsdienol to the host plus ipsenol bait did not increase was provided by Direccio´n General de la Naturaleza, response (experiment 3; fig. 2). The other two compo- Ministerio de Medio Ambiente, Madrid.
nents of the highly attractive bait, cis-verbenol andmethyl-butenol, were only tested in blends so it isdifficult to know their role in attraction. Specific tests to ascertain the individual role of these components are Allison, J. D.; Borden, J. H.; McIntosh, R. L.; Grott, P.; Gries, R., 2001: Kairomonal responses by four Monoch- Multiple-funnel traps were as effective as cross-vane amus species (Coleoptera: Cerambycidae) to bark beetle traps for trapping M. galloprovincialis in experiments 1 pheromones. J. Chem. Ecol. 27, 633–646.
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