Chemical ecology of bark beetles (Scolytidae)

Byers, J.A. Chemical Ecology of Bark Beetles. Experientia 45:271-283.

Continued...

Attack density regulation and termination of aggregation/attack mediated by semiochemicals. In response to the pheromone from the pioneer beetles resident in the tree, flying beetles orient to the tree, some joining established galleries while others begin excavations in the bark. The release of pheromone from these many new attacks increases perhaps as a logistic function such that the resinous defenses of the tree are overwhelmed⁴⁵^,⁶⁸^, ¹⁰⁸^,¹⁵². Once the tree has been rendered effectively defenseless, the functional cooperation among beetles ends and competition for the two-dimensional phloem becomes progressively more severe as the aggregation and attack continues²^,¹⁴^,³⁴.

This intense competition has provided strong selection pressures for the evolution of individuals adept at avoiding or reducing the degree of competitive interactions with conspecifics and with individuals of competing species³⁴^,³⁸. As mentioned previously, I. paraconfusus males can determine the likelihood of competition based on the strength of the pheromone signal. They avoid orientating to the highest release sources while females prefer these areas of the tree³³. At the peak of the female landing period on a felled tree, the male landing rate actually declined indicating that males may have been attracted (as shown in long-range orientation through a grid of traps) but did not land and then chose to fly elsewhere³³. These behaviors would serve to spread the colonization area in Ips³³^,¹²⁰^, ¹²¹ and P. chalcographus⁴⁴ as well as by a more simple "spill-over" or imprecision in orientation to pheromone. This latter mechanism may also account primarily for the switch of attack focus to surrounding trees by D. frontalis and other pest species³^,⁵²^,¹¹⁹.

Bark beetles appear to have behavioral mechanisms which space the attacks and gallery systems in order to reduce competition to tolerable levels. The mechanisms by which beetles choose whether to attack near previously attacked sites and at what distance are poorly known. Spacing of attacks has been shown in D. ponderosae¹²⁴^,¹¹⁸, D. frontalis⁸⁸, D. pseudotsugae⁶⁷, T. piniperda⁹⁶ and I. typographus³⁴. A computer method of comparing simulated attack densities at various minimal spacings between nearest neighbors to the natural attack patterns has been developed³⁴. It showed that I. typographus attacks would have the observed average nearest neighbor distances if the beetles initiated entrance holes at least a minimum allowed distance (MAD) of 2.5 cm from other holes. This distance was apparently the same regardless of the natural attack density and thus appears to be an inherent biological distance characteristic of the species³⁴.

The possible mechanisms that account for these spaced attack distributions and the MAD are (1) olfactory communication³⁴, (2) stridulation/acoustic communication⁶⁷^,¹¹²^-1¹⁶, (3) selection of bark structures⁵⁷^,¹¹⁸, and (4) visual inspection of attack sites or beetles, or various combinations of these. Olfactory communication between Ips males has been discussed above and could also function even more strongly at close-range. In D. pseudotsugae, an arriving male stridulates at the female's entrance hole and stimulates her to release MCH¹¹³^,¹¹⁵. The male also releases MCH⁸³^,¹⁰⁶ which has an inhibitory effect at long-range and apparently also at close- range¹¹²^-1¹⁵. Verbenone, trans-verbenol and (+)-ipsdienol have been shown to inhibit attraction of D. brevicomis to pheromone components at long- range¹³^,³⁰ and (-)-trans- verbenol at close-range³². Female stridulation alone has been implicated in the spacing of D. brevicomis¹¹³. Bark structure does influence the selection of attack site⁵⁷^,¹¹⁸ as well as the density of attacks, but it may have little affect on the spacing patterns or MAD.

Termination of aggregation and attack may be the result of saturation of the available bark areas as constrained by the spacing mechanism (MAD)³⁴. After the sexes pair, the production of pheromone declines as shown experimentally in I. paraconfusus²⁸ and by observations of gut volatile contents in tree-colonizing I. typographus¹⁷ and D. brevicomis⁴⁵. Thus, a spacing mechanism and cessation of attractant release after mating could explain the mechanism of termination of the aggregation. However, in T. piniperda termination may also be influenced by verbenone emanating from infested logs with only a small portion from the beetles themselves⁴³^,⁸⁰. Similar studies with I. typographus have shown that verbenone from microbial activity in infested trees may play a major role in termination of the aggregation⁶^,¹⁵^,⁸ ¹^,⁸²^,¹¹⁹.

In Fig. 5, semiochemical mechanisms which mediate the aggregation, attack density and termination of aggregation are presented for four species of bark beetle.

Fig. 5. Theoretical mechanisms for regulation of aggregation and attack density (intraspecific competition) and termination of aggregation in four species of bark beetles. A. Ips paraconfusus colonization of ponderosa pine. The male beetle arrives first (1) and constructs a nuptial chamber in the phloem layer. His release of ipsenol (Ie), ipsdienol (Id) and cis-verbenol (cV) [2], attracts both sexes [3]^126-128,150, but at higher concentrations near the source, males are inhibited in close-range orientation and thus land in adjacent areas of lower male attack density [4](Byers 1983)³³. This process is repeated and serves to evenly spread the colonization and regulate attack density [5](Byers 1983)³³. After males are joined by several females, their production of the pheromone components, Ie and Id, declines rapidly [6](Byers 1981)²⁸ and the tree becomes unattractive to beetles [7]. However, it appears that an additional mechanism (verbenone, V, from microbes in the tree?) is needed to both regulate density and terminate attack initiation during the later stages of colonization [8]. V has been shown to inhibit attraction to natural pheromone(Byers and Wood 1980)³⁹.

B. Ips typographus colonization of Norway spruce. The male arrives first [1] and releases 2-methyl-3-buten-2-ol (MB) and cis-verbenol (cV) [2] which attracts both sexes from a distance [3]⁸, but as males approach high concentrations of pheromone they become less precise than females in close-range orientation and so land in adjacent areas [4]^120,121. These sex-specific behaviors function to spread the attack and limit attack density in a way similar to I. paraconfusus. Males of I. typographus also reduce their release of pheromone components after "mating" [5]¹⁷ but in addition they release small quantities of ipsenol (Ie) and ipsdienol (Id)^15,17, which inhibit response of both sexes probably only at close range [6]^6,119. These compounds could function to both regulate attack density and terminate aggregation (along with a decline in attractants). However, verbenone (V) from microorganisms in the bark beetle galleries [7] could be the more general inhibitor responsible for termination of aggregation [8]^6,81,82,119.

C. Dendroctonus brevicomis colonization of ponderosa pine. The female beetle arrives first [1] and bores into the trunk and after feeding produces exo-brevicomin (eB) [2]¹²⁹, which primarily attracts males [3]^35,37. Males, upon locating a female gallery, soon release frontalin (F) [4]⁷⁴, which synergizes with eB to elicit a mass aggregation [5]^11,12. However, at the same time females and males produce trans- verbenol (tV)³² and males produce verbenone (V) and (+)-ipsdienol (Id)^30,45. At close range these compounds apparently inhibit the attraction of beetles to eB and F (tV appears to primarily affect females while Id and V affect both sexes, which would regulate the attack density^13,30,32. After several days the production and release of eB and F diminishes to levels that are unattractive at long range⁴⁵. The few females attracted during this latter period may be inhibited from attacking by the still significant, although reduced levels of tV [7]⁴⁵. The few males would not find any unpaired females and so would continue searching elsewhere. Verbenone may also increase in release rate as the tree decays and so inhibit beetles [8], although measurements have not been done.

D. Tomicus piniperda colonization of Scots pine. Both sexes arrive simultaneously in mass on the first April day above 13^o C in response to host monoterpenes, terpinolene, (± )-alpha-pinene and (+)-3-carene, released from resinous wounds incurred during winter storms [1]^47,80. Females and males pair up under bark flakes and the females tunnel into the bark followed immediately behind by the male. Trees that have fallen earlier in the winter and are beginning to decay probably release ethanol which in relatively small amounts may enhance the attraction to monoterpenes [2]⁷⁶ but at higher amounts is inhibitory⁷⁶. Both sexes contain verbenone (V) in the largest amounts shortly after entering the tree and amounts decline thereafter [3]⁸⁰ while V released from the tree continues to increase [4]⁴³ possibly due to microbial activity in the tissues surrounding the galleries. Ethanol may increase in release rate due to fermentative processes (unproven) while monoterpene release gradually decreases⁴³. V released in traps at rates comparable to rates released from infested sections of a tree was able to inhibit attraction of both sexes to the attractive monoterpenes also released at natural rates⁴³. V may serve both to space attacks (when released from individuals) and to terminate the aggregation (when released generally by microbial decay).

Interspecific interactions mediated by semiochemicals. Semiochemicals function in interactions between bark beetles in primarily two ways: (1) as allomones for interspecific communication of resource use in order to avoid competition and (2) as kairomones for use in locating weakened hosts colonized by another species. In California and other regions of the western United States, four pest bark beetles compete more or less for ponderosa pine (Fig. 6).

Fig. 6. Inhibition of the attraction response to conspecific pheromone by allomones produced by four sympatric bark beetles, Dendroctonus brevicomis, D. ponderosae, Ips paraconfusus, and I. pini which appear to function in reducing interspecific competition for ponderosa pine in California. Response inhibition by the pheromones trans-verbenol, verbenone, and (+)- ipsdienol may also reduce intraspecific competition in D. brevicomis. The asterisks indicate pheromone attractants and black squares indicate pheromone inhibitors of attraction.

Verbenone released by male D. brevicomis, in addition to its intraspecific effects, appears to inhibit the response of its competitor, I. paraconfusus, to pheromone³⁹. Verbenone has also been found in I. pini males from Idaho that had fed in red pine logs, but no behavioral role was ascribed⁷⁹. However, I suggest here that the observed inhibition of attraction of I. paraconfusus to its pheromone by logs infested with I. pini¹⁹ appears due in part to verbenone, a major volatile component in I. pini⁷⁹^,¹⁴². Earlier it was reported that only (-)-ipsdienol from I. pini was responsible for inhibition of I. paraconfusus⁸⁴. Thus, the inhibitory effect of verbenone on I. paraconfusus may have resulted from selection pressures to reduce interspecific competition from both D. brevicomis and I. pini (Fig. 6). Similarly, the inhibitory effects of verbenone on D. brevicomis could be the result of selection pressures from both intra- and interspecific competition (from I. pini). Multiple selection pressures could also account for the inhibitory effects of trans-verbenol on D. brevicomis³² (Fig. 6) which is produced in significant amounts by D. brevicomis³², by I. pini⁷⁹^,¹⁴² and by D. ponderosae¹⁰⁷. The (+)-ipsdienol produced by male I. paraconfusus¹²⁶ and by male D. brevicomis in the early stages of colonization⁴⁵ may function both to reduce intraspecific competition in both species³⁰^,³³ and to reduce interspecific competition from I. pini in both species (Fig. 6)²⁰^,³⁰.

A similar situation of competitive interactions exists for four sympatric bark beetles of southern pines (Fig. 7).

Fig. 7. Inhibition of the attraction response to conspecific pheromone by allomones produced by four sympatric bark beetles, Dendroctonus frontalis, Ips grandicollis, I. calligraphus, and I. avulsus which appear to function in reducing interspecific competition for southern pines in the southeastern United States^21,136. Verbenone also acts as a pheromone in D. frontalis that reduces response to aggregation pheromone. The asterisks indicate pheromone attractant and the black square a pheromone inhibitor.

I. calligraphus produces (-)-ipsdienol as one of the attractive components¹⁴²^,¹⁴⁴ and this also acts as an allomone to inhibit I. grandicollis attraction to its pheromone²¹^,¹⁴³. Allomonal volatiles from I. avulsus are inhibitory to I. calligraphus²¹. Verbenone, produced by D. frontalis1⁰⁶^,¹⁰⁹ acts as a pheromone that inhibits attraction as well as an allomone that inhibits attraction of I. grandicollis²¹. The use of allomones appears to reduce competitive interactions among the southern pine beetles just as they do in the western pine beetles.

The bark beetles attacking pines in the southern United States are different from their western counterparts¹⁸^,¹⁹^, ³⁹, however, in that they are cross-attractive to each others pheromones (Fig. 8)²¹^,¹³⁶.

Fig. 8. Cross attraction of four sympatric bark beetles colonizing pines in the southeastern United States^21,136. Thick lined arrows indicate strong attraction (65%-100% of conspecific attraction), thin lines indicate weaker attraction (5-12%) and dashed lines little attraction (2-5%).

The reason for the strongest interspecific attraction, I. avulsus attraction to pheromone of I. calligraphus, is probably that I. avulsus locates weakened hosts already infested by I. calligraphus and that the potential competition is tolerable since both species utilize somewhat different levels of the tree (Fig. 7)⁹⁸^,¹³⁶.

Therefore, the above discussion indicates that olfactory systems evolve as a result of the relative benefits of multiple factors including avoidance of intra- and interspecific competition. Coevolution would favor the sharing of semiochemicals so that specific compounds could serve in communication both intra- and interspecifically. There would also be a selection pressure for use of biosynthetic pathways that produce the semiochemicals from host precursors, as long as the precursors were consistently available. Thus (+)-ipsdienol, from myrcene, and trans-verbenol (and possibly verbenone), from alpha-pinene, may have become pheromone components and allomones for a growing list of species. However, another hypothesis is that verbenone was already consistently present in decaying hosts due to microbial activity²⁵^,²⁶^,⁴³^,⁸², and then was subsequently used over evolutionary time by bark beetles as pheromones and allomones³⁸.

The predators, parasites and other associated insects interacting with bark beetles comprise a complex guild of species. During the course of aggregation of D. brevicomis on ponderosa pine, over 100 species of insects were collected¹³⁴. Associated insects of bark beetles locate the breeding habitat either by landing at random, or using kairomones from the beetle (often their pheromones)⁷^,¹²^,¹ ⁴⁰^,¹⁴⁶^,¹⁴⁷ or other kairomones from the dying tree⁷⁶ or possibly other associated insects. The primary requirements of a kairomone are that it be a reliable indicator of host condition or presence and that the host (or fermentative process) can not dispense with its use. Thus, pheromone components of bark beetles are the most likely volatiles to be utilized as kairomones by predators and parasitoids since the adaptive advantages for the emitter outweigh the disadvantages as a kairomone, and so no net selection pressure for changing to other compounds will occur.

The chemical ecology of adult and larval interactions under the bark (e.g. they appear to avoid intersecting galleries³⁸), callow adult movements, emergence, and overwintering (Fig. 1, d-h) are practically unknown. Gregoire et al.⁶⁶ indicated that larval D. micans maintained a feeding aggregation in response to cis-verbenol. Fungal interactions with bark beetles in regard to host tree resistance⁶⁸^,¹⁰⁸^,¹²⁵, nutrition of larvae¹⁰ and host unsuitability²⁵^,²⁶^, ⁴³^,⁸¹ are not well understood. Sexual recognition and species recognition are due in part to stridulation⁹ but probably more so by specific cuticular chemicals¹⁰⁵ - a subject not yet investigated in bark beetles.

The field of chemical ecology of bark beetles encompasses much more than can be covered here, but it is hoped that one can appreciate that bark beetles and their associates are among the best of model systems for the study of chemical ecology.

1 Alcock, J., Natural selection and communication among bark beetles. Fla. Entomol. 65 (1981) 17-32.

2 Anderbrant, O., Schlyter, F., and Birgersson, G., Intraspecific competition affecting parents and offspring in the bark beetle Ips typographus. Oikos 45 (1985) 89-98.

3 Anderbrant, O., Schlyter, F., and L�fqvist, J., Dynamics of tree attack in the bark beetle Ips typographus under semi-epidemic conditions, in: Integrated Control of Scolytid Bark Beetles. in press. Eds T.L. Payne and H. Saarenmaa, Virginia Tech. Press, Blacksburg 1989.

4 Atkins, M.D., Lipid loss with flight in the Douglas-fir beetle. Can. Entomol. 101 (1969) 164-165.

5 Baker, T.C. Pheromone-modulated movements of flying moths, in: Mechanisms in Insect Olfaction, pp. 39-47. Eds T.L. Payne, M.C. Birch and C.E.J. Kennedy. Clarendon Press, Oxford 1986.

6 Bakke, A., Inhibition of the response in Ips typographus to the aggregation pheromone; field evaluation of verbenone and ipsenol. Z. Angew. Entomol. 92 (1981) 172-177.

7 Bakke, A., and Kvamme, T., Kairomone response in Thanasimus predators to pheromone components of Ips typographus. J. Chem. Ecol. 7 (1981) 305-312.

8 Bakke, A., Fr�yen, P., and Skatteb�l, L., Field response to a new pheromonal compound isolated from Ips typographus. Naturwissenschaften 64 (1977) 98.

9 Barr, B.A., Sound production in Scolytidae (Coleoptera) with emphasis on the genus Ips. Can. Entomol. 101 (1969) 636-672.

10 Barras, S.J., Reduction of progeny and development in the southern pine beetle following removal of symbiotic fungi. Can. Entomol. 105 (1973) 1295-1299.

11 Bedard, W. D., Silverstein, R. M., and Wood, D. L., Bark beetle pheromones. Science 167 (1970) 1638-1639.

12 Bedard, W.D., Tilden, P.E., Wood, D.L., Silverstein, R.M., Brownlee, R.G., and Rodin, J.O., Western pine beetle: Field response to its sex pheromone and a synergistic host terpene, myrcene. Science 164 (1969) 1284-1285.

13 Bedard, W.D., Tilden, P.E., Lindahl, K.Q.Jr., Wood, D.L., and Rauch, P.A., Effects of verbenone and trans-verbenol on the response of Dendroctonus brevicomis to natural and synthetic attractant in the field. J. Chem. Ecol. 6 (1980) 997-1013.

14 Berryman, A.A., Dynamics of bark beetle populations: Towards a general productivity model. Environ. Entomol. 3 (1974) 579-585.

15 Birgersson, G., and Bergstr�m., Volatiles released from individual spruce bark beetle entrance holes: quantitative variations during the first week of attack. J. Chem. Ecol. in press (1989).

16 Birgersson, G., Schlyter, F., Bergstr�m, G., and L�fqvist, J., Individual variation in aggregation pheromone content of the bark beetle Ips typographus. J. Chem. Ecol. 14 (1988) 1735-1759.

17 Birgersson, G., Schlyter, F., L�fqvist, J., and Bergstr�m. G., Quantitative variation of pheromone components in the spruce bark beetle Ips typographus from different attack phases. J. Chem. Ecol. 99 (1984) 1164- 1193.

18 Birch, M.C., Aggregation in bark beetles. in: W.J. Bell and R.T. Card� (eds.) Chemical ecology of insects. (1984) 331-353. Sinauer Associates. Sunderland, Mass.

19 Birch, M.C., and Wood, D.L., Mutual inhibition of the attractant pheromone response by two species of Ips (Coleoptera: Scolytidae). J. Chem. Ecol. 1 (1975) 101-113.

20 Birch, M.C., Light, D.M., Wood, D.L., Browne, L.E., Silverstein, R.M., Bergot, B.J., Ohloff, G., West, J.R., and Young, J.C., Pheromonal attraction and allomonal interruption of Ips pini in California by the two enantiomers of ipsdienol. J. Chem. Ecol. 6 (1980) 703-717.

21 Birch, M.C., Svihra, P., Paine, T.D., and Miller, J.C., Influence of chemically mediated behavior on host tree colonization by four cohabiting species of bark beetles. J. Chem. Ecol. 6 (1980) 395-414.

22 Borden, J.H., Aggregation pheromones, in: Bark Beetles in North American Conifers: A System for the Study of Evolutionary Biology, pp. 74-139. Eds J.B. Mitton and K.B. Sturgeon. Univ. Texas Press, Austin 1982.

23 Borden, J.H., Hunt, D.W.A., Miller, D.R., and Slessor, K.N., Orientation in forest Coleoptera: An uncertain outcome of responses by individual beetles to variable stimuli. in, T.L. Payne, M.C. Birch, and C.E.J. Kennedy (eds.). Mechanisms in Insect Olfaction. Clarendon Press, Oxford. (1986) 97-109.

24 Borden, J.H., Chong, L., McLean, J.A., Slessor, K.N., and Mori, K., Gnathotrichus sulcatus: synergistic response to enantiomers of the aggregation pheromone sulcatol. Science 192 (1976) 894-896.

25 Brand, J.M., and Barras, S.J., The major volatile constituents of a basidiomycete associated with the southern pine beetle. Lloydia. 40 (1977) 398-400.

26 Brand, J.M., Bracke, J.W., Britton, L.N., Markovetz, A.J., and Barras, J.S., Bark beetle pheromones: Production of verbenone by a mycangial fungus of Dendroctonus frontalis. J. Chem. Ecol. 2 (1976) 195-199.

27 Browne, L.E., Wood, D.L., Bedard, W.D., Silverstein, R.M., and West, J.R., Quantitative estimates of the Western pine beetle attractive pheromone components, exo-brevicomin, frontalin, and myrcene in nature. J. Chem. Ecol. 5 (1979) 397-414.

28 Byers, J.A., Effect of mating on terminating aggregation during host colonization in the bark beetle, Ips paraconfusus. J. Chem. Ecol. 7 (1981) 1135-1147.

29 Byers, J.A., Pheromone biosynthesis in the bark beetle, Ips paraconfusus, during feeding or exposure to vapours of host plant precursors. Insect Biochem. 11 (1981) 563-569.

30 Byers, J.A., Male-specific conversion of the host plant compound, myrcene, to the pheromone, (+)-ipsdienol, in the bark beetle, Dendroctonus brevicomis. J. Chem. Ecol. 8 (1982) 363-371.

31 Byers, J.A., Influence of sex, maturity and host substances on pheromones in the guts of the bark beetles, Dendroctonus brevicomis and Ips paraconfusus. J. Insect Physiol. 29 (1983) 5-13.

32 Byers, J.A., Bark beetle conversion of a plant compound to a sex-specific inhibitor of pheromone attraction. Science 220 (1983) 624-626.

33 Byers, J.A., Sex-specific responses to aggregation pheromone: Regulation of colonization density by the bark beetle Ips paraconfusus. J. Chem. Ecol. 9 (1983) 129-142.

34 Byers, J.A., Nearest neighbor analysis and simulation of distribution patterns indicates an attack spacing mechanism in the bark beetle, Ips typographus (Coleoptera: Scolytidae). Environ. Entomol. 13 (1984) 1191-1200.

35 Byers, J.A., Interactions of pheromone component odor plumes of western pine beetle. J. Chem. Ecol. 13 (1987) 2143-2157.

36 Byers, J.A., Upwind flight orientation to pheromone in western pine beetle tested with rotating windvane traps. J. Chem. Ecol. 14 (1988) 189-198.

37 Byers, J.A., Novel diffusion-dilution method for release of semiochemicals: Testing pheromone component ratios on western pine beetle. J. Chem. Ecol. 14 (1988) 199-212.

38 Byers, J.A., Behavioral mechanisms involved in reducing competition in bark beetles. Holarct. Ecol. (1989) in press.

39 Byers, J.A., and Wood, D.L., Interspecific inhibition of the response of the bark beetles, Dendroctonus brevicomis and Ips paraconfusus. J. Chem. Ecol. 6 (1980) 149-164.

40 Byers, J.A., and Wood, D.L., Interspecific effects of pheromones on the attraction of the bark beetles, Dendroctonus brevicomis and Ips paraconfusus in the laboratory. J. Chem. Ecol. 7 (1981) 9-18.

41 Byers, J.A., and Wood, D.L., Antibiotic-induced inhibition of pheromone synthesis in a bark beetle. Science 213 (1981) 763-764.

42 Byers, J.A., Anderbrant, O., and L�fqvist, J., Effective attraction radius: A method for comparing species attractants and determining densities of flying insects. J. Chem. Ecol. (1988) in press.

43 Byers, J.A., Lanne, B.S., and L�fqvist, J., Host-tree unsuitability recognized by pine shoot beetles in flight. Experientia (submitted).

44 Byers, J.A., Birgersson, G., L�fqvist, J., and Bergstr�m, G., Synergistic pheromones and monoterpenes enable aggregation and host recognition by a bark beetle, Pityogenes chalcographus. Naturwissenschaften 75 (1988) 153- 155.

45 Byers, J.A., Wood, D.L., Craig, J., and Hendry, L.B., Attractive and inhibitory pheromones produced in the bark beetle, Dendroctonus brevicomis, during host colonization: Regulation of inter- and intraspecific competition. J. Chem. Ecol. 10 (1984) 861-877.

46 Byers, J.A., Birgersson, G., Appelgren, M., L�fqvist, J., and Bergstr�m, G., Isolation of insect pheromone synergists from complex host-plant odors by gas chromatographic fractionation and subtractive-combination bioassay. J. Chem. Ecol. (submitted).

47 Byers, J.A., Lanne,2type c:\wp\wpfiles\macro.txt
B.S., Schlyter, F., L�fqvist, J., and Bergstr�m, G., Olfactory recognition of host-tree susceptibility by pine shoot beetles. Naturwissenschaften 72 (1985) 324-326.

48 Byrne, K.J., Swiger, A.A., Silverstein, R.M., Borden, J.H., and Stokkink, E., Sulcatol: population aggregation pheromone in Gnathotrichus sulcatus (Coleoptera: Scolytidae). J. Insect Physiol. 20 (1974) 1895-1900.

49 Cade, S.C., Hrutfiord, B.F., and Gara, R.I., Identification of a primary attractant for Gnathotrichus sulcatus isolated from western hemlock logs. J. Econ. Entomol. 3 (1970) 1014-1015.

50 Card�, R.T., and Baker, T.C. Sexual communication with pheromones, in: Chemical Ecology of Insects. pp. 355-383. Eds W.J. Bell and R.T. Card�. Sinauer Associates, Sunderland, Mass 1984.

51 Choudhury, J.H., and Kennedy, J.S., Light versus pheromone-bearing wind in the control of flight direction by bark beetles, Scolytus multistriatus. Physiol. Entomol. 5 (1980) 207-214.

52 Coulson, R.N., Population dynamics of bark beetles. Ann. Rev. Entomol 24 (1979) 417- 447.

53 Dickens, J. C., Behavioural and electrophysiological responses of the bark beetle Ips typographus to potential pheromone components. Physiol. Entomol. 6 (1981) 251-261.

54 Dickens, J.C., Specificity in perception of pheromones and host odours in Coleoptera. in: Mechanisms in insect olfaction, (eds.) T.L. Payne, M.C. Birch and C.E.J. Kennedy. Clarendon Press, Oxford. (1986) 253-261.

55 Dickens, J.C., Payne, T.L., Ryker, L.C., and Rudinsky, J.A., Multiple acceptors for pheromonal enantiomers on single olfactory cells in the Douglas-fir beetle, Dendroctonus pseudotsugae Hopk. (Coleoptera: Scolytidae) J. Chem. Ecol. 11 (1985) 1359-1370.

56 Doskotch, R.W., Chatterji, S.K., and Peacock, J.W., Elm bark derived feeding stimulants for the smaller European elm bark beetle. Science 167 (1970) 380-382.

57 Elkinton, J.S., and Wood, D.L., Feeding and boring behavior of the bark beetle Ips paraconfusus (Coleoptera: Scolytidae) on the bark of a host and non-host tree species. Can. Entomol. 112 (1980) 797-809.

58 Elkinton, J.S., Wood, D.L., and Browne, L.E., Feeding and boring behavior of the bark beetle, Ips paraconfusus, in extracts of ponderosa pine phloem. J. Chem. Ecol. 7 (1981) 209-220.

59 Francke, W., and Vit�, J.P., Oxygenated terpenes in pheromone systems of bark beetles. Z. Angew. Entomol. 96 (1983) 146-156.

60 Francke, W., Sauerwein, P., Vit�, J.P., and Klimetzek, D., The pheromone bouquet of Ips amitinus. Naturwissenschaften 67 (1980) 147-148.

61 Francke, W., Heemann, V., Gerken, B., Renwick, J.A.A., and Vit�, J.P., 2-ethyl-1-6-dioxaspiro[4.4]nonane, principal aggregation pheromone of Pityogenes chalcographus (L.). Naturwissenschaften 64 (1977) 590-591.

62 Furniss, M.M., Baker, B.H., and Hostetler, B.B., Aggregation of spruce beetles (Coleoptera) to seudenol and repression of attraction by methylcyclohexenone in Alaska. Can. Entomol. 108 (1976) 1297-1302.

63 Gilbert, B.L., Baker, J.E., and Norris, D.M., Juglone (5-hydroxy-1, 4-napthoquinone) from Carya ovata, a deterrent to feeding by Scolytus multistriatus. J. Insect Physiol. 13 (1967) 1453-1459.

64 Goeden, R.D., and Norris, D.M., Attraction of Scolytus quadrispinosus (Coleoptera: Scolytidae) to Carya spp. for oviposition. Ann. Entomol. Soc. Am. 57 (1964) 141-146.

65 Graham, K., Release by flight exercise of a chemotropic response from photopositive domination in a scolytid beetle. Nature 184 (1959) 283-284.

66 Gregoire, J.C, Broekman, J.C., and Tondeur, A., Chemical communication between the larvae of Dendroctonus micans Kug. (Coleoptera, Scolytidae). Med. Chem. Agis. Comp. Insectes 7 (1982) 253-257.

67 Hedden, R.L., and Gara, R.I., Spatial attack pattern of a western Washington Douglas-fir beetle population. For. Sci. 22 (1976) 100-102.

68 Hodges, J.D., Elam, W.W., Watson, W.R., and Nebeker, T.E., Oleoresin characteristics and susceptibility of four southern pines to southern pine beetle (Coleoptera: Scolytidae) attacks. Can. Entomol. 111 (1979) 889-896.

69 Hughes, P.R., Myrcene: a precursor of pheromones in Ips beetles. J. Insect Physiol. 20 (1974) 1271-1275.

70 Hunt, D.W.A., Borden, J.H., Pierce, H.D., Jr., Slessor, K.N., King, G.G.S., and Csyzewska, E.K., Sex-specific production of ipsdienol and myrcenol by Dendroctonus ponderosae (Coleoptera: Scolytidae) exposed to myrcene vapors. J. Chem. Ecol. 12 (1986) 1579-1586.

71 Hynum, B.G., and Berryman, A.A., Dendroctonus ponderosae (Coleoptera: Scolytidae): pre-aggregation landing and gallery initiation on lodgepole pine. Can. Entomol. 112 (1980) 185-191.

72 Kennedy, J.S., Some current issues in orientation to odour sources, in: Mechanisms in Insect Olfaction. pp. 11-25. Eds T.L Payne, M.C. Birch and C.E.J. Kennedy. Clarendon Press, Oxford 1986.

73 Kinzer, G.W., Fentiman, A.F., Jr., Page, T.F., Foltz, R.L., Vit�, J.P., and Pitman, G.B., Bark beetle attractants: identification, synthesis and field bioassay of a new compound isolated from Dendroctonus. Nature 211 (1969) 475-476.

74 Kirkendall, L.R., The evolution of mating systems in bark and ambrosia beetles (Coleoptera: Scolytidae and Platypodidae). Zool. J. Linn. Soc. 77 (1983) 293- 352.

75 Klimetzek, D., and Francke, W., Relationship between the enantiomeric composition of o-pinene in host trees and the production of verbenols in Ips species. Experientia 36 (1980) 1343-1345.

76 Klimetzek, D., K�hler, J., Vit�, J.P., and Kohnle, U., Dosage response to ethanol mediates host selection by 'secondary' bark beetles. Naturwissenschaften 73 (1986) 270-272.

77 Krebs, C.J., Ecology. (1972) 3-4, Harper and Row, New York. 694 p.

78 Lanier, G. N., Integration of visual stimuli, host odorants, and pheromones by bark beetles and weevils in locating and colonizing host trees, in: Herbivorous Insects: Host-Seeking Behavior and Mechanisms. pp. 161-171. Ed S. Ahmad. Academic Press, New York 1983.

79 Lanier, G.N., Classon, A., Stewart, T., Piston, J.J., and Silverstein, R.M., Ips pini: the basis for interpopulational differences in pheromone biology. J. Chem. Ecol. 6 (1980) 677-687.

80 Lanne, B.S., Schlyter, F., Byers, J.A., L�fqvist, J., Leufv�n, A., Bergstr�m, G. , Van Der Pers, J.N.C., Unelius, R., Baeckstr�m, P., and Norin, T., Differences in attraction to semiochemicals present in sympatric pine shoot beetles, Tomicus minor and T. piniperda. J. Chem. Ecol. 13 (1987) 1045-1067.

81 Leufv�n, A., and Birgersson, G., Quantitative variation of different monoterpenes around galleries of Ips typographus (Coleoptera: Scolytidae) attacking Norway spruce. Can. J. Bot. 65 (1987) 1038-1044.

82 Leufv�n, A., Bergstr�m, G., and Falsen, E., Interconversion of verbenols and verbenone by identified yeasts isolated from the spruce bark beetle Ips typographus. J. Chem. Ecol. 10 (1984) 1349-1361.

83 Libbey, L.M., Morgan, M.E., Putnam, T.B., and Rudinsky, J.A., Isomer of antiaggregative pheromone identified from male Douglas-fir beetle: 3-methylcyclohexen-1-one. J. Insect Physiol. 22 (1976) 871-873.

84 Light, D.M., and Birch, M.C., Inhibition of the attractive pheromone response in Ips paraconfusus by (R)-(-)-ipsdienol. Naturwissenschaften 66 (1979) 159.

85 Light, D.M., and Birch, M.C., Bark beetle enantiomeric chemoreception: Greater sensitivity to allomone than pheromone. Naturwissenschaften 69 (1982) 243-245.

86 Lorio, P.L. Jr., and Hodges, J.D., Oleoresin exudation pressure and relative water content of inner bark as indicators of moisture stress in loblolly pines. For. Sci. 14 (1968) 392-398.

87 MacConnell, J.G., Borden, J.H., Silverstein, R.M., and Stokkink, E., Isolation and tentative identification of lineatin, a pheromone from the frass of Trypodendron lineatum (Coleoptera: Scolytidae). J. Chem. Ecol. 3 (1977) 549-561.

88 Mayyasi, A.M., Coulson, R.N., Foltz, J.L., Hain, F.P., and Martin, W.C., Functional description of within-tree larval and progeny adult populations of Dendroctonus frontalis (Coleoptera: Scolytidae). Can. Entomol. 108 (1976) 363-372.

89 Miller, J.M., and Keen, F.P., Biology and control of the western pine beetle. U.S. Dept. Agric. Misc. Publ. No. 800.

90 Moeck, H.A., Ethanol as the primary attractant for the ambrosia beetle Trypodendron lineatum (Coleoptera: Scolytidae). Can. Entomol. 102 (1970) 985-995.

91 Moeck, H.A., Field test for the primary attraction of the spruce beetle. Environ. Can. For. Serv. Bi-mon. Res. Notes 34 (1978) 8.

92 Moeck, H.A., Wood, D.L., and Lindahl, K.Q.Jr., Host selection behavior of bark beetles (Coleoptera: Scolytidae) attacking Pinus ponderosa, with special emphasis on the western pine beetle, Dendroctonus brevicomis. J. Chem. Ecol. 7 (1981) 49-83.

93 Murlis, J., The structure of odour plumes, in: Mechanisms in Insect Olfaction. pp. 27- 38. Eds T.L. Payne, M.C. Birch and C.E.J. Kennedy. Clarendon Press, Oxford 1986.

94 Mustaparta, H., Angst, M.E., and Lanier, G.N., Receptor discrimination of enantiomers of the aggregation pheromone ipsdienol, in two species of Ips. J. Chem. Ecol. 6 (1980) 689-701.

95 Mustaparta, H., Tommer�s, B.�., Baeckstr�m, P., Bakke, J.M., and Ohloff, G., Ipsdienol-specific receptor cells in bark beetles: Structure-activity relationships of deuterium-labelled ipsdienol. J. Comp. Physiol. 154 (1984) 591-595.

96 Nilssen, A.C., Spatial attack pattern of the bark beetle Tomicus piniperda L. (Col., Scolytidae). Norw. J. Entomol. 25 (1978) 171-175.

97 Norris, D.M., Role of repellents and deterrents in feeding of Scolytus multistriatus. in: Host Plant Resistance to Pests, pp. 215-230. Ed P.A. Hedin. Am. Chem. Symp. Ser. No. 63, 1977.

98 Paine, T.D., Birch, M.C., and Svihra, P., Niche breadth and resource partitioning by 4 sympatric species of bark beetles. Oecologia 48 (1981) 1-6.

99 Payne, T.L., Pheromone and host odor perception in bark beetles, in: Neurotoxicology of Insecticides and Pheromones, pp. 27-57. Ed T. Narahashi. Plenum Pub. Co., New York 1979.

100 Payne, T.L., and Dickens, J.C. Adaptation to determine receptor system specificity in insect olfactory communication. J. Insect Physiol. 22 (1976) 1569-1572.

101 Payne, T.L., Klimetzek, D., Kohnle, U., and Mori, K., Electro-physiological and field responses of Trypodendron-spp to enantiomers of lineatin. Z. Angew. Entomol. 95 (1983) 272-276.

102 Payne, T.L., Richerson, J.V., Dickens, J.C., West, J.R., Mori, K., Berisford, C. W., Hedden, R.L., Vit�, J.P., and Blum, M.S., Southern pine beetle: Olfactory receptor and behavior discrimination of enantiomers of the attractant pheromone frontalin. J. Chem. Ecol. 8 (1982) 873-881.

103 Peacock. J.W., Lincoln, C.L., Simeone, J.B., and Silverstein, R.M., Attraction of Scolytus multistriatus (Coleoptera: Scolytidae) to a virgin-female-produced pheromone in the field. Ann. Entomol. Soc. Am. 64 (1971) 1143-1149.

104 Pearce, G.T., Gore, W.E., Silverstein, R.M., Peacock, J.W., Cuthbert, R.A., Lanier, G.N., and Simeone, J.B., Chemical attractants for the smaller European elm bark beetle, Scolytus multistriatus (Coleoptera: Scolytidae). J. Chem. Ecol. 1 (1975)
115-124.

105 Peschke, K., Cuticular hydrocarbons regulate mate recognition, male aggression, and female choice of the rove beetle, Aleochara curtula. J. Chem. Ecol. 13 (1987) 1993-2008.

106 Pitman, G.B., and Vit�, J.P., Biosynthesis of methylcyclohexenone by male Douglas-fir beetle. Environ. Entomol. 3 (1974) 886-887.

107 Pitman, G.B., Vit�, J.P., Kinzer, G.W., and Fentiman, A.F., Jr., Bark beetle attractants: trans-verbenol isolated from Dendroctonus. Nature 218 (1968) 168-169.

108 Raffa, K.F., and Berryman, A.A.,. Physiological aspects of lodgepole pine wound responses to a fungal symbiont of the mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Scolytidae). Can. Entomol. 115 (1983) 723-734.

109 Renwick, J.A.A., and Vit�, J.P., Systems of chemical communication in Dendroctonus. Contrib. Boyce Thompson Inst. 24 (1970) 283-292.

110 Renwick, J.A.A., Hughes, P.R., and Krull, I.S., Selective production of cis- and trans-verbenol from (-)- and (+)-a-pinene by a bark beetle. Science 191 (1976) 199-201.

111 Renwick, J.A.A., and Dickens, J.C., Control of pheromone production in the bark beetle, Ips cembrae. Physiol. Entomol. 4 (1979) 377-381.

112 Rudinsky, J.A., Multiple functions of the Douglas-fir beetle pheromone, 3-methyl-2-cyclohexen-1-one. Environ. Entomol. 2 (1973) 579-585.

113 Rudinsky, J.A., and Michael, R.R., Sound production in Scolytidae: Stridulation by female Dendroctonus beetles. J. Insect Physiol. 19 (1973) 689-705.

114 Rudinsky, J.A., and Ryker, L.C., Sound production in Scolytidae: rivalry and premating stridulation of male Douglas-fir beetle. J. Insect Physiol. 22 (1976) 997- 1003.

115 Rudinsky, J.A., Morgan, M.E., Libbey, L.M., and Michael, R.R., Sound production in Scolytidae: 3-methyl-2-cyclohexen-1-one released by the female Douglas-fir beetle in response to male sonic signal. Environ. Entomol. 2 (1973) 505-509.

116 Rudinsky, J.A., Morgan, M.E., Libbey, L.M., and Putnam, T.B., Additional components of the Douglas-fir beetle (Col., Scolytidae) aggregative pheromone and their possible utility in pest control. Z. Angew. Entomol. 76 (1974) 65-77.

117 Ryker, L.C., Acoustic and chemical signals in the life cycle of a beetle. Sci. Am. 250 (1984) 112-115,118-123,154

118 Safranyik, L., and Vithayasai, C., Some characteristics of the spatial arrangement of attacks by the mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Scolytidae), on lodgepole pine. Can. Entomol. 103 (1971) 1607-1625.

119 Schlyter, F., Birgersson, G., and Leufv�n, A., Inhibition of attraction to aggregation pheromone by verbenone, ipsenol and ipsdienol: Density regulation mechanisms in the bark beetle Ips typographus. J. Chem. Ecol. in press (1989).

120 Schlyter, F., Byers, J.A., and L�fqvist, J.A., Attraction to pheromone sources of different quantity, quality and spacing: Density-regulation mechanisms in the bark beetle Ips typographus. J. Chem. Ecol. 13 (1987) 1503-1523.

121 Schlyter, F., L�fqvist, J., and Byers, J.A., Behavioural sequence in the attraction of the bark beetle Ips typographus to pheromone sources. Physiol. Entomol. 12 (1987) 185-196.

122 Schlyter, F., Birgersson, G., Byers, J.A., L�fqvist, J., and Bergstr�m, G., Response of spruce bark beetle, Ips typographus, to aggregation pheromone candidates. J. Chem. Ecol. 13 (1987) 701-716.

123 Schurig, V., and Weber, R., Use of glass and fused-silica open tubular columns for the separation of structural, configurational and optical isomers by selective complexation gas chromatography. J. Chromatog. 289 (1984) 321-332.

124 Shepherd, R.F., Distribution of attacks by Dendroctonus ponderosae Hopk. on Pinus contorta Dougl. var. latifolia Engelm. Can. Entomol. 97 (1965) 207-215.

125 Shrimpton, D.M., Resistance of lodgepole pine to mountain pine beetle infestation (1978) 64-76. in, Theory and practice of mountain pine beetle management in lodgepole pine forests. Forest, Wildlife and Range Exp. Sta. Univ. Idaho,Moscow, Idaho 224 pp. 126 Silverstein, R.M., Rodin, J.O., and Wood, D.L., Sex attractants in frass produced by male Ips confusus in ponderosa pine. Science 154 (1966) 509-510.

127 Silverstein, R.M., Rodin, J.O., and Wood, D.L., Methodology for isolation and identification of insect pheromones with reference to studies on California five-spined Ips. J. Econ. Entomol. 60 (1967) 944-949.

128 Silverstein, R.M., Rodin, J.O., Wood, D.L., and Browne, L.E., Identification of two new terpene alcohols from frass produced by Ips confusus in ponderosa pine. Tetrahedron 22 (1966) 1929-1936.

129 Silverstein, R.M., Brownlee, R.G., Bellas, T.E., Wood, D.L., and Browne, L.E., Brevicomin: Principal sex attractant in the frass of the female western pine beetle. Science 159 (1968) 889-891.

130 Slessor, K.N., King, G.G.S., Miller, D.R., Winston, M.L., and Cutforth, T.L., Determination of chirality of alcohol or latent alcohol semiochemicals in individual insects. J. Chem. Ecol. 11 (1985) 1659-1667.

131 Smith, R.H., The fumigant toxicity of three pine resins to Dendroctonus brevicomis and D. jeffrei. J. Econ. Entomol. 54 (1961) 365-369.

132 Smith, R.H.,. Variation in the monoterpenes of Pinus ponderosa Laws. Science 143 (1964) 1337-1338.

133 Smith. R.H., Local and regional variation in the monoterpenes of ponderosa pine xylem resin. USDA For. Ser. Res. Pap. PSW-56 (1969) 1-10.

134 Stephen, F.M., and Dahlsten, D.L., The arrival sequence of the arthropod complex following attack by Dendroctonus brevicomis (Coleoptera: Scolytidae) in ponderosa pine. Can. Entomol. 108 (1976) 283-304.

135 Sturgeon, K.B., Monoterpene variation in ponderosa pine xylem resin related to western pine beetle predation. Evolution 33 (1979) 803-814.

136 Svihra, P., Paine, T.D., and Birch, M.C., Interspecific olfactory communications in southern pine beetles. Naturwissenschaften 67 (1980) 518.

137 Tommer�s, B.�., Mustaparta, H., and Gregoire, J.C., Receptor cells in Ips typographus and Dendroctonus micans specific to pheromones of the reciprocal genus. J. Chem. Ecol. 10 (1984) 759-769.

138 Vanderwel, D., and Oehlschlager, A.C., Biosynthesis of pheromones and endocrine regulation of pheromone production in Coleoptera, in: Pheromone Biochemistry. pp. 175-215. Eds G.D. Prestwich and G.J. Blomquist. Academic Press, New York 1987.

139 Vit�, J.P., and Gara, R.I., Volatile attractants from ponderosa pine attacked by bark beetles (Coleoptera: Scolytidae). Contrib. Boyce Thompson Inst. 21 (1962) 251-273.

140 Vit�, J.P., and Williamson, D.L., Thanasimus dubius: prey perception. J. Insect Physiol. 16 (1970) 233-239.

141 Vit�, J.P., and Wood, D.L., A study on the applicability of the measurement of oleoresin exudation pressure in determining susceptibility of second growth ponderosa pine to bark beetle infestation. Contrib. Boyce Thompson Inst. 21 (1961) 67-78.

142 Vit�, J.P., Bakke, A., and Renwick, J.A.A., Pheromones in Ips (Coleoptera: Scolytidae): Occurrence and production. Can. Entomol. 104 (1972) 1967-1975.

143 Vit�, J.P., Hedden, R., and Mori, K., Ips grandicollis: field response to the optically pure pheromone. Naturwissenschaften 63 (1976) 43-44.

144 Vit�, J.P., Ohloff, C., and Billings, R.F., Pheromone chirality and integrity of aggregation response in southern species of the bark beetle, Ips sp. Nature 272 (1978) 817-818.

145 Vit�, J.P., Pitman, G.B., Fentiman, A.F.Jr., and Kinzer, G.W., 3-Methyl-2-cyclohexen-1-ol isolated from Dendroctonus. Naturwissenschaften 59 (1972) 469.

146 Wood, D.L., Selection and colonization of ponderosa pine by bark beetles, in: Insect Plant Relationships. pp. 101-117. Ed H.F. van Emden. Blackwell Sci. Pub., London 1972.

147 Wood, D.L., The role of pheromones, kairomones, and allomones in the host selection and colonization behavior of bark beetles. Ann. Rev. Entomol. 27 (1982) 411-446.

148 Wood, D.L., Akers, R.P., Owen, D.R., and Parmeter, J.R., Jr., The behaviour of bark beetles colonizing ponderosa pine, in: Insects and the Plant Surface. pp. 91- 104. Eds Juniper and Southwood. Arnold Publ., London 1986.

149 Wood, D.L., Browne, L.E., Silverstein, R.M., and Rodin, J.O., Sex pheromones of bark beetles - I. Mass production, bioassay, source, and isolation of the sex pheromone of Ips confusus (LeC.). J. Insect Physiol. 12 (1966) 523-536.

150 Wood, D.L., Stark, R.W., Silverstein, R.M., and Rodin, J.O., Unique synergistic effects produced by the principal sex attractant compounds of Ips confusus (LeConte)(Coleoptera: Scolytidae). Nature
215 (1967) 206.

151 Wood, D.L., Browne, L.E., Ewing, B., Lindahl, K., Bedard, W.D., Tilden,P.E., Mori, K., Pitman, G.B., and Hughes, P.R., Western pine beetle: specificity among enantiomers of male and female components of an attractant pheromone. Science 192 (1976) 896-898.

152 Wood, S.L., The bark and ambrosia beetles of North and Central America (Coleoptera: Scolytidae), a taxonomic monograph. Great basin naturalist memoirs, Brigham Young Univ., Provo, Utah. (1982) 1359 p.