By Donald M. Grosman
email@example.com ~ Texas Forest Service ~ P.O. Box 310 Lufkin, TX 75902-0310
Adapted from a dissertation thesis entitled: Southern Pine Beetle, Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae): Quantitative Analysis of Chiral Semiochemicals. 1996. Department of Entomology, Virginia Tech, Blacksburg, VA, USA.
Online format prepared by Quintin C. McClellan ~ Department of Entomology ~ Virginia Tech~ Blacksburg, VA ~ USA
Semiochemical Communication System
Chemical Structure, Blends and Concentration in Species Specificity
Mechanism of Host Tree Colonization by SPB
Switching of Attack
Behavioral Chemicals and the Management of Bark Beetles
The southern pine beetle (SPB), Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae), is considered to be the most important cause of damage and mortality to pine trees in the southeastern United States (Drooz 1985). Over the last several decades, entomologists have striven to unlock the secrets that allow this native beetle to rise up in epidemic proportions that lead to such vast tree mortality. It is now well known that bark beetles possess elaborate semiochemical communication systems which they use to orientate to host material to feed, mate, and reproduce. Many detailed reviews have been provided in this area (Birch 1978, 1984; Borden 1974, 1977, 1982, 1984, 1985, 1989; Brand et al. 1979; Byers 1989; Geizler and Gara 1978; Geizler et al. 1980; Renwick and Vité 1970, 1980; Rudinsky and Ryker 1977; Ryker 1984; Smith et al. 1993; Vité and Francke 1976; Wood 1970, 1973, 1982; Wood and Bedard 1977). The chemical ecology of SPB involves a complex host of beetle- and host-produced compounds. Scientists are continually revealing the once hidden nature of these compounds and their role in insect ecology, but far more important, their significance in manipulating insect behavior. The broader aspects of SPB chemical ecology and implications for bark beetle management are addressed.
Semiochemicals are natural compounds produced and released by individuals of a species which elicit a behavioral response in members of the same or different species (Nordlund 1981). Semiochemicals which are used in intraspecific communication are referred to as pheromones. Behavioral responses to pheromones include searching for mates by one sex (e.g., sex pheromones), aggregation of both sexes at a host plant (e.g., attractant or aggregation pheromones), and dispersal of both sexes away from a specific area (e.g., inhibitor or antiaggregation pheromones). Semiochemicals used in interspecific communication are referred to as kairomones when the species receiving the chemical message benefits and allomones when the emitter of the chemical message benefits at the expense of the receiver. There is considerable overlap with regards to the functions of a compound, i.e., the same compound may serve both intra- and interspecific functions. For example, frontalin serves as an pheromone to SPB and a kairomone to its natural enemy, Thanasimus dubius (Fabricius) (Vité and Williamson 1970).
A series of studies conducted at the Boyce Thompson Institute for Plant Research provided the foundation by which the semiochemical system of SPB was first described (Coster 1970; Coster and Gara 1968; Gara 1967; Gara and Coster 1968; Renwick 1970; Renwick and Vité 1969, 1970; Vité and Crozier 1968; Vité and Renwick 1968) and later revised (Vité and Francke 1976). Recently, Smith et al. (1993) presented an extensive historical review of research on the semiochemical communication system of SPB and other members of the southern pine bark beetle guild. Although several host- and beetle-associated chemicals have been found to be produced and/or utilized by SPB as part of its communication system, behavioral responses of this beetle have only been determined for a few of these compounds.
The activity of a semiochemical is dependent on many factors including its size, shape, functional groups, degree of saturation and chirality (Tumlinson and Teal 1987). Small molecules are used when a fast response is required (e.g., alarm pheromones), while large compounds, which tend to be less volatile, are used when long, extended exposure is required (e.g., sex, aggregation, and antiaggregation pheromones). Although the structure of pheromones differs greatly between insect orders and families, generally compounds are of similar structural types within genera as seen with terpene pheromones of Ips and Dendroctonus bark beetles. The position, number, and geometry of double bonds and functional groups are also important with regard to the activity of compounds. Payne et al. (1988), evaluating the antennal olfactory and behavioral response of SPB to different frontalin analogs, showed that response to frontalin was significantly greater than to any of the analogs. Chirality, in turn, imparts a greater degree of specificity to a species' pheromone system. Silverstein (1979) described nine possible categories of behavioral response to enantiomers or diastereomers. At least two of these categories have evolved as part of the SPB semiochemical-based system. For example, SPB produce both enantiomers of frontalin, but is significantly more attracted to ()-frontalin than to the (+)-antipode (Payne et al. 1982). On the other hand, Vité et al. (1985) showed that (+)-endo-brevicomin significantly enhanced attraction of SPB to frontalure, whereas ()-endo-brevicomin inhibited response. Thus, one enantiomer may be active and the other inactive or each enantiomer may elicit different responses. Seybold (1993) provided an extensive review on the roles of chirality in olfactory-directed behavior.
Just after the discovery of the first pheromone, bombykol, from the silkworm moth, Bombyx mori (L.)., it was generally thought that each insect species produced and responded to a single pheromone (Karlson and Butenandt 1959). However, Ips paraconfusus was later found to produce and respond to a blend of three pheromones (e.g., (S)-()-ipsenol, (S)-(+)-ipsdienol, and (S)-()-cis-verbenol) (Silverstein et al. 1966). It has since been discovered that most insects produce multicomponent blends of pheromones and that the single component system is the exception rather than the rule. The blend of pheromones is important because some or all components may act as synergists; individually they elicit little or no attractiveness, but together they are highly attractive. The pheromone blend of I. paraconfusus is one example. Another example is the SPB attractant blend of frontalin, trans-verbenol, turpentine (containing a-Pinene and other monoterpenes), verbenone, and (+)-endo-brevicomin. Individual components of a blend may also function in concert to maximize steps in a behavioral sequence as has been found in several Lepidoptera species (Baker and Carde 1979, Linn et al. 1984, Teal et al. 1986). Blends and component ratios within blends play important roles in maintaining or increasing reproductive isolation of closely related species or reducing competition in sympatric species. A species may release a component which is inactive to conspecifics, but inhibitory to related species (Tumlinson and Teal 1987). On the other hand, a component, essential to reproductive behavior in the releasing species, may also be inhibitory to members of related species. Finally, two species may produce different component ratios of the same chemicals.
A summary of known or speculated biosynthetic pathways and responses to some of the most studied semiochemicals are discussed below in relation to their respective roles within an actively expanding infestation.
Upon landing on a tree, "pioneer" females bite into the bark. If the host is found to be suitable, the females begin releasing the primary aggregation pheromone, frontalin, and the synergist trans-verbenol (Fig. 1). At the same time, females release small quantities of Verbenone and endo-Brevicomin, both serving as synergists to enhance the attractiveness of frontalin. These compounds, in combination with host volatiles, primarily a-Pinene, stimulate mass aggregation of conspecifics (predominantly males) to the host (Renwick and Vité 1969, Rudinsky 1973) and are described in greater detail below.
During mass attack, arriving males land on the host, locate the entrance hole of single females and begin to release frontalin, endo-brevicomin, and verbenone in low concentrations (Fig. 2). The resulting aggregation, along with the introduction of symbiotic fungi, enables SPB to successfully attack a host tree and produce brood which emerge to attack other trees.
As the population of attacking beetles increases, the concentration of verbenone and endo-brevicomin released by males also increases. At some unknown threshold, these compounds begin to inhibit beetle response to the aggregation pheromones and cause arriving beetles to switch their attack to neighboring trees (Payne et al. 1978, Rudinsky 1973, Rudinsky et al. 1974, Vité and Renwick 1971) (Fig. 3). It has been suggested that the switching of mass attack from one host tree to a neighboring tree may be the result of both the cessation of release of attractive compounds (frontalin and a-Pinene) and the increased concentration of inhibitor pheromones (verbenone and endo-brevicomin) released from the tree as was found for Ips typographus (L.) (Schlyter et al. 1987, 1989).
The history of methods used to manipulate or control SPB are varied and imaginative (Billings 1980). Some of the earliest tactics included rapid conversion of infested material into lumber (e.g., salvage) and burning the slabs (Hopkins 1909, 1911); immersing unbarked logs in water; and exposing unsalvageable infested trees to solar heating (e.g. cut-and-leave) (St. George and Beal 1929). Some of these methods, i.e. salvage and cut-and-leave, are still used today. Other treatments, more recently evaluated, include the use of pesticides, the application of mechanical and silvicultural controls, and the use of behavioral chemicals. The use of behavioral chemicals is summarized below.
There is extensive literature regarding the use of semiochemicals in the management of insect pests (Beroza 1970, 1976; Birch 1974; Borden 1989, 1993; Mitchell 1981; Wood 1982,). Borden (1989) described five principal means by which semiochemicals can influence the population dynamics of bark beetles: mediation of aggregation and mass attack on new hosts; cessation of aggregation and shifting of attack to an unexploited region of the host or to new hosts; induction of aggregation by species that compete for the same host resource; inhibition of aggregation and attack by species that compete for the same resource; and mediation of host finding by commensal and entomophagous insects. The author listed six fundamental strategies for potential pest management of scolytids, including:
Bark beetles of the genera Dendroctonus, Ips, and Scolytus are the most destructive pests of forests in the Northern Hemisphere. Damage from these insects causes losses of billions of cubic feet of timber valued at millions of dollars each year (Drooz 1985; Furniss and Carolin 1977). Tactics currently used to control bark beetles, such as salvage, cut-and-leave, or chemical control are not always successful and/or are of environmental concern.
The use of semiochemicals as management tools show considerable promise in reducing damage and mortality by bark beetles. Some of these compounds have already been successfully used to monitor population trends or as a mass trapping and/or disruption tactic (Borden 1993). The exploitation of semiochemicals as management tools requires a thorough understanding of the mechanisms involved in the production and release of and response to these chemicals by the target species. In addition, it is important to have an understanding of the effects of semiochemicals applied on the target species and associated organisms. Lanier et al. (1972) was one of the first to suggest that the indiscriminate use of semiochemicals could theoretically lead to resistance. Such a phenomenon has been studied with regards to use of pheromones in mating disruption of the pink bollworm moth, Pectinophora gossypilla (Saunders) (Haynes et al. 1984, Haynes and Baker 1988). Just as there is the potential for the development of semiochemical resistance in the target insect, there is also the potential for the development of response "resistance" in natural enemies as many of these insects use host pheromones as kairomones.
Baker, T.C. and Carde, R.T. 1979. Analysis of pheromone-mediated behavior in male Grapholitha molesta, the oriental fruit moth (Lepidoptera: Tortricidae). Environ. Entomol. 8: 956-968.
Berisford, C.W., Brady, U.E., Fitzpatrick, G.E., Franklin, C.K., Hastings, F.L., Jones, A.S., Lashomb, J.H., Mizell, R.F., III, Neel, W.W. and Radenovich, I.R. 1981. Efficacy studies: Prevention. pp. 3-8, in F.L. Hastings, and J.A. Coster (eds.). Field and Laboratory Evaluations of Insecticides for Southern Pine Beetle Control. USDA Forest Service, Gen. Tech. Rep. DE-21.
Berosa, M. (ed.). 1970. Chemicals Controlling Insect Behavior. Acedemic Press. New York.
Berosa, M. (ed.). 1976. Pest Management with Insect Sex Attractants and Other Behavior Controlling Chemicals. Am. Chem. Soc. Symp. Series 23, Am.Chem. Soc., Washington, D.C.
Billings, R.F. 1980. Direct Control. pp. 179-192, in R.C. Thatcher, J.L. Searcy, J.E. Coster, and G.D. Hertel (eds.). The Southern Pine Beetle. USDA Forest Service, Tech. Bull. 1631.
Billings, R.F. 1985. Southern pine beetles and associated insects: effects of rapidly-released host volatiles on response to aggregation pheromones. Z. ang. Entomol. 99: 483-491.
Billings, R.F. 1988. Forcasting southern pine beetle infestation trends with pheromone traps. pp. 295-306, in T.L. Payne and H. Saarenmaa (eds.). IUFRO Symposium: Integrated Control of Scolytid Bark Beetles., Vancouver, B.C. Canada, Va. Polytech. Instit. and State Univ., VA.
Billings, R.F., Berisford, C.W., Salom, S.M., and Payne, T.L. 1995. Application of semiochemicals in the management of southern pine beetle infestations: current status of research. pp. 30-38, in S.M. Salom and K.R. Hobson (eds.). Application of Semiochemicals for Management of Bark Beetle Infestations-Proceedings of an Informal Conference. December 12-16, 1994, Dallas, TX. USDA, Forest Service, Intermountain Res. Stat., Gen. Tech. Rep. No. 318.
Birch. M.C. (ed.). 1974. Pheromones. North-Holland Publ. Co., New York. 495 p.
Birch, M.C. 1978. Chemical communication in pine bark beetles. Amer. Scientist. 66: 409-419.
Birch, M.C. 1984. Aggregation in bark beetles. pp. 331-353, in W.J. Bell and R.T. Carde (eds.). Chemical Ecology of Insects. Chapman and Hall, New York.
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. 1980. Pheromonal attraction and allomonal interruption of Ips pini in California by the two enantiomers of ipsdienol. J. Chem. Ecol. 6: 703-717.
Borden, J.H. 1967. Factor influencing the response of Ips confusus (Coleoptera: Scolytidae) to male attractant. Can. Entomol. 99: 1164-1193.
Borden, J.H. 1974. Aggregation pheromones in the Scolytidae. pp. 135-160, in M. Birch (ed.). Pheromones. North-Holland Publ. Co., New York.
Borden, J.H. 1977. Behavioral responses of Coleoptera to pheromones, allomones, and kairomones. pp. 169-198, in H.H. Shorey and J.J. McKelvey Jr. (eds.). Chemical Control of Insect Behavior: Theory and Application. John Wiley and Sons, New York.
Borden, J.H. 1982. Aggregation pheromones. pp. 74-139, in J.B. Mitton and K.B. Sturgeon (eds). Bark Beetles in North American Conifers. University of Texas Press, Austin.
Borden, J.H. 1984. Semiochemical-mediated aggregation and dispersion in the Coleoptera. pp. 123-149, in T. Lewis (ed.). Insect Communication. Acedemic Press, New York.
Borden, J.H. 1985. Aggregation pheromones. pp. 257-289, in G.A. Kerkut and L.I. Gilbert (eds.). Comprehensive Insect Physiology, Biochemistry and Pharmacology: Behavior (Vol. 9). Pergamon Press, New York, N.Y.
Borden, J.H. 1989. Semiochemicals and bark beetle populations: Expoitation of natural phenomena by pest management stategies. Holarct. Ecol. 12: 501-510.
Borden, J.H. 1993. Strategies and tactics for the use of semiochemicals against forest insect pests in North America. pp. 265-279, in R.D. Lumsden and J.L. Vaughn (eds.). Pest Management: Biologically Based Technologies. ACS Conf. Proc., Amer. Chem. Soc., Washington, D.C.
Brand, J.M., Bracke, J.W., Britton, L.N., Markovetz, A.J. and Barras, S.J. 1976. Bark beetle pheromones: production of verbenone by a mycangial fungus of Dendroctonus frontalis. J. Chem. Ecol. 2: 195-199.
Brand, J.M., Bracke, J.W., Markovetz, A.J., Wood, D.L. and Browne, L.E. 1975. Production of verbenol pheromone by a bacterium isolated from bark beetles. Nature (London). 254: 136-137.
Brand, J.M., Young, J.C., and Silverstein, R.M. 1979. Insect pheromones: a critical review of recent advances in their chemistry, biology, and application. Chem. Org. Naturst. 37: 1-190.
Byers, J.A. 1989. Chemical ecology of bark beetles. Experientia. 45: 271-283.
Camors, F.B., Jr. and Payne, T.L. 1973. Sequence of arrival of entomophagous insects to trees infested with the southern pine beetle. Environ. Entomol. 2: 267-270.
Coster, J.A. 1970. Certain aspects of pheromone release and aggregation behavior in the southern pin beetle (Coleoptera: Scolytidae). Ph.D. Dissertation. Texas A&M University.
Coster, J.A. and Gara, R.I. 1968. Studies on the attack behavior of the southern pine beetle. II. Response to attractive host material. Contrib. Boyce Thompson Instit. 24: 69-75.
Coster, J.E. and Vité, J.P. 1972. Effects of feeding and mating on pheromone release in the southern pine beetle. Ann. Entomol. Soc. Am. 65: 263-266.
Dixon, W.N. and Payne, T.L. 1980. Attraction of entomophagous and associate insects of the southern pine beetle to beetle- and host tree-produced volatiles. J. Ga. Entomol. Soc. 15: 378-389.
Drooz, A.T. (ed.). 1985. Insects of Eastern Forests. USDA Forest Service, Misc. Pub. No. 1426. 608 pp.
Furniss, R.L. and Carolin, V.M. 1977. Western Forest Insects. USDA Forest Service, Misc. Pub. No. 1339. 654 p.
Gara, R.I. 1967. Studies on the attack behavior of the southern pine beetle. I. The spreading and collapse of outbreaks. Contrib. Boyce Thomp Instit. 23: 349-354.
Gara, R.I. and Coster, J.A. 1968. Studies on the attack behavior of the southern pine beetle. III. Sequence of tree infestation within stands. Contrib. Boyce Thompson Instit. 24: 77-86.
Geizler, D.R. and Gara, R.I. 1978. Mountain pine beetle attack dynamics in lodgepole pine. pp. 182-187, in A.A. Berryman, G.D. Amman, and R.W. Stark (eds.). Theory and Practice of Mountain Pine Beetle Management in Lodgepole Pine Stands. Univ. of Idaho and USDA Forest Service, Moscow, ID andWashington, D.C.
Geizler, D.R., Gallucci, V.F. and Gara, R.I. 1980. Modelling the dynamics of mountain pine beetle aggregation in a lodgepole pine stand. Oecologia. 46: 244-253.
Hayes, J.L., Strom, B.L., Roton, L.M. and Ingram, L.L., Jr. 1994. Repellent properties of the host compound 4-allylanisole to the southern pine beetle. J. Chem. Ecol. 20: 1595-1615.
Haynes, K.F. and Baker, T.C. 1988. Potential for evaluation of resistance to pheromones: worldwide and local variation in communication system of pink bollworm moth, Pectinophora gossypiella. J. Chem. Ecol. 14: 1547-1560.
Haynes, K.F., Gaston, L.K., Pope, M.M. and Baker, T.C. 1984. Potential for the evolution of resistance to pheromones: interindividual and interpopulational variation in chemical communication system of pink bollworm moth. J. Chem. Ecol. 10: 1551-1565.
Hopkins, A.D. 1909. Practical information on the Scolytid beetles of North American forests. I. Bark beetles of the genus Dendroctonus. USDA, Bur. Entomol. Bull. 83. 169 p.
Hopkins, A.D. 1911. The dying of pine in the southern states: Cause, extent, and remedy. USDA, Farm. Bull. 476. 14 p.
Hughes, P.R. 1973. Dendroctonus: production of pheromones and related compounds in response to host monoterpenes. Z. ang. Entomol. 73: 294-312.
Hughes, P.R. 1975. Pheromones of Dendroctonus: origin of a-Pinene oxidation products present in emergent adults. J. Insect Physiol. 21: 687-691.
Hunt, D.W.A., Borden, J.H., Lindgren, B.S., and Gries, G. 1989. The role of autoxidation of a-Pinene in the production of pheromones of Dendroctonus ponderosae (Coleoptera: Scolytidae). Can. J. For. Res. 19: 1275-1283.
Johnson, P. and Coster, J.E. 1978. Probability of attack by southern pine beetle in relation to distance from an attractive host tree. For. Sci. 24: 574-580.
Karlson, P. and Butenandt, A. 1959. Pheromones (ectohormones) in insects. Ann. Rev. Entomol. 4: 39-58.
Kinzer, G.W., Fentiman, A.F., Page, T.F., Foltz, R.L., Vité, J.P. and Pitman, G.B. 1969. Bark beetle attractants: Identification, synthesis and field bioassay of a new compound isolated from Dendroctonus. Nature (London). 221: 477-478.
Lanier, G.N., Birch, M.C., Schmitz, R.F. and Furniss, M.M. 1972. Pheromones of Ips pini.(Coleoptera: Scolytidae): variation in response among three populations. Can. Entomol. 104: 1917-1923.
Linn, C.E., Bjostad, L.B., Du, J.W., and Roelofs, W.L. 1984. Redundancy in a chemical signal: behavioral responses of male Trichoplusia ni to a 6-component sex pheromone blend. J. Chem. Ecol. 10: 1635-1658.
McCarty, F.A., Billings, P., Richerson, J.V., Payne, T.L. and Edson, L.J. 1980. Response of the southern pine beetle to behavioral chemicals in the laboratory. J. Georgia Entomol. Soc. 15: 307-317.
Mitchell, E.R. (ed.). 1981. Management of Insect Pests with Semiochemicals: Concepts and Practice. Plenum Press, New York.
Mirov, N.T. 1961. Composition of gum turpentines of pines. USDA Forest Service, Tech. Bull. 1239. 156 pp.
Moore, R.N., Golumbric, C. and Fisher, G.S. 1956. Autoxidation of a-Pinene. J. Amer Chem. Soc. 78: 1173-1176.
Nordlund, D.A. 1981. Semiochemicals: a review of the terminology. pp. 13-28, in D.A. Nordlund, R.L. Jones , and W.J. Lewis (eds.). Semiochemicals: Their Role in Pest Control. John Wiley & Sons, New York.
Payne, T.L. 1979. Pheromone and host odor perception in bark beetles. pp. 27-57, in T. Narahashi (ed.). Neurotoxicology of Insecticides and Pheromones. Plenum Publ. Corp.
Payne, T.L. 1980. Life history and habits. pp. 7-28, in R.C. Thatcher, J.L. Searcy, J.E. Coster, and G.D. Hertel (eds.). The Southern Pine Beetle. USDA Forest Service, Tech. Bull. 1631.
Payne, T.L., Andryszak, N.A., Weiser, H., Dixon, E.A., Ibrahim, N. and Coers, L. 1988. Antennal olfactory and behavioral response of the southern pine beetle, Dendroctonus frontalis, to analogs of its aggregation pheromone frontalin. J. Chem. Ecol. 14: 1217-1225.
Payne, T.L. and Billings, R.F. 1988. Effect of pheromone and pheromone plus tree cutting on suppression of southern pine beetle infestations. pp. 267-274, in T.L.Payne and H. Saaenmaa (eds.). IUFRO Symposium: Integrated Control of Scolytid Bark Beetles., Vancouver, B.C., Canada, VA Polytech. Instit. and State Univ., Blacksburg, VA.
Payne, T.L. and Billings, R.F. 1989. Evaluation of (S)-verbenone applications for suppressing southern pine beetle (Coleoptera: Scolytidae) infestations. J. Econ. Entomol. 82: 1702-1708.
Payne, T.L., Billings, R.F., Berisford, C.W., Salom, S.M., Grosman, D.M., Dalusky, M.J. and Upton, W.W. 1992. Disruption of Dendroctonus frontalis (Coleoptera: Scolytidae) infestations with an inhibitor pheromone. J. Appl.. Entomol. 114: 341-347.
Payne, T.L., Coster, J.E., Richerson, J.V., Edson, L.J. and Hart, E.R. 1978. Field response of the southern pine beetle to behavioral chemicals. Environ. Entomol. 7(4): 578-582.
Payne, T.L. and Dickens, J.C. 1976. Adaptation to determine receptor system specificity in insect olfactory communication. J. Insect Physiol. 22: 1569-1572.
Payne, T.L. and Richerson, J.V. 1985. Pheromone-mediated competitive replacement between two bark beetle populations: influence on infestation suppression. Z. ang. Entomol. 99: 131-138.
Payne, T.L. and Richerson, J.V. 1979. Management implications of inhibitors for Dendroctonus frontalis (Col., Scolytidae). Bull. Soc. Entomol. Suisse. 52: 323-331.
Payne, T.L., Richerson, J.V., Dickens, J.C., West, J.R., Mori, K., Berisford, C.W., Hedden, R.L., Vité, J.P. and Blum, M.S. 1982. Southern pine beetle: olfactory receptor and behavior discrimination of enantiomers of the attractant pheromone frontalin. J. Chem. Ecol. 8: 873-881.
Prema, B.R. and Bhattacharyya, P.K. 1962. Microbial transformation of terpenes II. transformation of a-Pinene. Appl. Microbiol. 10: 524-528.
Renwick, J.A.A. 1967. Identification of two oxygenated terpenes from the bark beetles Dendroctonus frontalis and Dendroctonus brevicomis. Contrib. Boyce Thompson Instit. 23: 355-360.
Renwick, J.A.A. 1970. Chemical aspects of bark beetle aggregation. Contrib. Boyce Thompson Instit. 24: 337-341.
Renwick, J.A.A. and Vité, J.P. 1969. Bark beetle attractants: mechanisms of colonization by Dendroctonus frontalis. Nature. 224: 1222-1223.
Renwick, J.A.A. and Vité, J.P. 1970. Systems of chemical communication in Dendroctonus. Contrib. Boyce Thompson Instit. 24: 283-292.
Renwick, J.A.A. and Vité, J.P. 1980. Biology of Pheromones. pp. 1-28, in R. Wegler (ed.). Chemie der Pflanzenschutz- und Schadlingsbekampfungsmittel. Springer-Verlag, Berlin Heidelberg.
Renwick, J.A.A., Hughes, P.R. and Ty, T.D. 1973. Oxidation productions of pinene in the bark beetle Dendroctonus frontalis. J. Insect Physiol. 19: 1735-1740.
Richerson, J.V., McCarty, F.A. and Payne, T.L. 1980. Disruption of southern pine beetle infestations with frontalure. Environ. Entomol. 9: 90-93.
Richerson, J.V. and Payne, T.L. 1979. Effects of bark beetle inhibitors on landing and attack behavior of the southern pine beetle and beetle associates. Environ. Entomol. 8: 360-364.
Rudinsky, J.A. 1973. Multiple functions of the southern pine beetle pheromone verbenone. Environ. Entomol. 2: 511-514.
Rudinsky, J.A., Morgan, M.E., Libbey, L.M. and Putnam, T.B. 1974. Antiaggregative rivalry pheromone of the mountain pine beetle, and a new arrestant of the southern pine beetle. Environ. Entomol. 3: 90-97.
Rudinsky, J.A. and Ryker, L.C. 1977. Olfactory and auditory signals mediating behavioral patterns of bark beetles. Colloques Internationaux du C.N.R.S. Comportement des Insectes et Milieu Trophique. 265: 195-209.
Ryker, L.C. 1984. Acoustic and chemical signals in the life cycle of a beetle. Sci. Amer. 250: 112-115, 118-123.
Ryker, L.C. and Yandell, K.L. 1983. Effect of verbenone on aggregation of Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae) to synthetic attractant. Z. ang. Entomol. 96: 452-459.
Salom, S.M., Billings, R.F., Upton, W.W., Dalusky, M.J., Grosman, D.M., Payne, T.L., Berisford, C.W. and Shaver, T.N. 1992. Effect of verbenone enantiomers and racemic endo-brevicomin on response of Dendroctonus frontalis (Coleoptera: Scolytidae) to attractant-baited traps. Can. J. For. Res. 22: 925-931.
Salom, S.M., Birgersson, G., Payne, T.L. and Berisford, C.W. 1991. Electroantennagram responses of the southern pine beetle parasitoid Dinotiscus dendroctoni (Ashmead) (Hymenoptera: Pteromalidae) to potential semiochemicals. J. Chem. Ecol. 17: 2527-2538.
St. George, R.A. and Beal, J.A. 1929. The southern pine beetle: a serious enemy of pines in the South. USDA Farm. Bull. 1568. 18 pp.
Schlyter, F., Birgersson, G. and Leufven, A. 1989. Inhibition of attraction to aggregation pheromone by verbenone and ipsenol: density regulation mechanisms in bark beetle Ips typographus. J. Chem. Ecol. 15: 2263-2277.
Schlyter, F., Byers, J.A. and Lofqvist, J. 1987. Attraction to pheromone sources of different quantity, quality, and spacing: density-regulation mechanisms in bark beetle Ips typographus. J. Chem. Ecol. 13: 1503-1523.
Seybold, S.J. 1993. Role of chirality in olfactory-directed behavior: aggregation of pine engravor beetles in the genus Ips (Coleoptera: Scolytidae). J. Chem. Ecol. 19: 1809-1831.
Silverstein, R.M. 1979. Enantiomeric composition and bioactivity of chiral semiochemicals in insects. pp. 133-146, in F.J. Ritter (ed.). Chemical Ecology: Odour Communication in Animals. Elsevier/North-HollandBiomedical Press.
Silverstein, R.M. Rodin, J.O. and Wood, D.L. 1966. Sex attractants in frass produced by male Ips confusus [now I. paraconfusus] in ponderosa pine. Science. 154: 509-510.
Smith, M.T., Salom, S.M. and Payne, T.L. 1993. The southern bark beetle guild: an historical review of the research on the semiochemical-based communication system of the five principle species. VA. Agric. Exp. Stn., Bull. 93-4. Blacksburg, VA. 106 pp.
Svihra, P., Paine, T.D. and Birch, M.C. 1980. Interspecific olfactory communications in the southern pine beetles. Naturwissen 67: 518.
Swain, K.M. and Remion, M.C. 1980. Direct control of the southern pine beetle. USDA Forest Service, Agric. Handbook. 575. 15 pp.
Teal, P.E.A., Tumlinson, J.H. and Heath, R.R. 1986. Chemical and behavioral analyses of volatile sex pheromone components released by Heliothis virescens (F.) females (Lepidoptera: Noctuidae). J. Chem. Ecol. 12: 107-126.
Tumlinson, J.H. and Teal, P.E.A. 1987. Relationship of structure and function to biochemistry in insect pheromone systems. pp. 3-26. in G.D. Prestwich and G.J. Blomquist (eds.). Pheromone Biochemistry. Acedemic Press, Orlando, FL.
Vité, J.P. 1970. Pest management systems using synthetic pheromones. Contrib. Boyce Thompson Instit. 24: 343-350.
Vité, J.P., Billings, R.F., Ware, C.W. and Mori, K. 1985. Southern pine beetle: enhancement or inhibition of aggregation response mediated by enantiomers of endo-brevicomin. Naturwissen. 72: 99-100.
Vité, J.P. and Crozier, R.G. 1968. Studies on the attack behavior of the southern pine beetle. IV. Influence of the host condition on aggregation pattern. Contrib. Boyce Thompson Instit. 24: 87-93.
Vité, J.P. and Francke, W. 1976. The aggregation pheromones of bark beetles: Progress and problems. Naturwissen. 63: 550-555.
Vité, J.P. and Renwick, J.A.A. 1968. Insect and host factors in the aggregation of the southern pine beetle. Contrib. Boyce Thompson Instit. 24: 61-63.
Vité, J.P. and Renwick, J.A.A. 1971. Inhibition of Dendroctonus frontalis response to frontalin by isomers of brevicomin. Naturwissen. 8: 418-419.
Vité, J.P. and Williamson, D.L. 1970. Thanasimus dubius: Prey perception. J. Insect Physiol. 16: 233-239.
Williamson, D.L. 1971. Olfactory discerment of prey by Medetera bistriata (Diptera: Dolichopodidae). Ann. Entomol. Soc. Am. 64: 585-589.
Wood, D.L. 1970. Pheromones of bark beetles. pp. 301-316, in D.L. Wood, R.M. Silverstein, and M. Nakajima (eds.). Control of Insect Behavior by Natural Products. Acedemic Press, New York.
Wood, D.L. 1973. The selection and colonization of ponderosa pine by bark beetles. pp. 101-117, in H.F. van Emdem (ed.). Insect-Plant Relationships. Blackwell Sci. Publ., London.
Wood, D.L. 1982. The role of pheromones, kairomones and allomones in the host selection and colonization behavior of bark beetles. Ann. Rev. Entomol. 27: 411-446.
Wood, D.L. and Bedard, W.D. 1977. The role of pheromones in the population dynamics of the western pine beetle. Proc. XV Int'l. Congr. Entomol., Washington, D.C., pp. 643-652.