Acoustic cues and mating behavior of Dendroctonus ... · PDF fileAcoustic cues and mating behavior of Dendroctonus (Coleoptera:Curculionidae:Scolytinae) species 1Dan R. West Email:

Acoustic cues and mating behavior of Dendroctonus (Coleoptera:Curculionidae:Scolytinae) species

1Dan R. West

Email: [email protected] or [email protected]

Abstract

Acoustic production in the bark beetle genus Dendroctonus (Coleoptera: Curculionidae:

Scolytinae) is thought to be used in the communication within and between species competing

for mates, nutrient and habitat acquisition, and initiation of long range pheromone release.

Differences in acoustic properties between three species within the Dendroctonus genus provide

evidence of species specificity (Rudinsky, 1974). Morphological structures used in sound

production of D. valens were first described by Hopkins in 1909. The Scanning Electron

Micrograph (SEM) allowed detailed image resolution to depict the elytral file on the posterior tip

of the hardened forewing in concert with a file on the 7th or 8th abdominal sternite of both male

(Rudinsky, 1974) and female Dendroctonus beetles (Rudinsky, 1973). The stridulation made by

the male morphological features is believed to be utilized in close range mate attraction and

acceptance acoustics, acoustical stress signals, and aggressive rivalry behavior with acoustics

(Ryker, 1988). Female acoustic studies of Dendroctonus species have described the sound

production as chirps or clicking which differ in properties from males believed to be produced by

the elytral and abdominal files (Rudinsky, 1973). The female chirps or clicks are hypothesized

to be used in communicating territory to adjacent females in gallery selection and spacing

(Rudinsky, 1973). Mate selection behavior by female Dendroctonus species was highly

correlated to acoustic production by males versus artificially altered males lacking stridulation

capability (Ryker, 1976). Intra-species male to male aggression was identified by the acoustic

production intensity and duration in prospective female mate niches (McGhehey, 1968;

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West, 2009 Dendroctonus Sound Production: Review

Rudinsky, 1974; Rudinsky, 1976; Ryker, 1988). Further, the aggressive rivalry stridulation

between males during territorial battles for prospective females is followed by chirping, believed

to be used in mate attraction (Rudinsky, 1974). Aggression behavior between males has been

documented through several bodies of work and synthesized within this review. Pheromone

release triggered from acoustic production was shown within species while chemostimuli

produced acoustic stridulation in bioassay experiments of the Dendroctonus genus (Rudinsky,

1974). Hypotheses surrounding reproductively isolated populations of Dendroctonus ponderosae

(mountain pine beetle) based on the acoustic properties produced by individuals from three hosts

(Pinus ponderosae, Pinus contorta, Pinus monticola) showed no difference in mate attraction

signals (Yandell, 1984). The inter-species and intra-species acoustic production and behavior

regarding territory, mate attraction, and stress signals of several Dendroctonus bark beetles is

synthesized in this review.

Introduction

Acoustic production in insects has been well documented in many families of insects,

such as Acrididae, Tettigoniidae, Plecoptera, Cerambycidae, Elateridae, Lucanidae, Passalidae,

Cicadidae, Corixidae, and Gryllidae to name a few families within the orders Hemiptera,

Orthoptera, Plecoptera, and Coleoptera. Ewing (1989) described the sound production as

categorical mechanisms falling within vibration, percussion, stridulation, click mechanisms or air

expulsion.Vibrations are generally conducted through unspecialized body parts, such as

abdominal rotation or wing pulses in mosquitoes (Culicidae) (Claridge, 2006). Percussion

acoustics are characterized as drumming of the substrate or body parts and known in Isoptera

(termites), Plecoptera (stoneflies), and Tetigoniidae (bushcrickets) for example (Claridge, 2006).

By contracting and relaxing special muscles within insect bodies moving modified areas of the

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cuticle. Click mechanisms are displayed for example in Hemiptera, and Lepidoptera (Claridge,

2006). The expulsion of air through tracheal spiracles or mouthparts is a less common sound

producing mechanism, and is seen in some Lepidoptera, most notably the Sphingidae (Claridge,

2006). Bark beetles of the genus Dendroctonus possess specialized structures used to produce

sound through friction or rasping, which is known as stridulation.

The Dendroctonus genus has been extensively studied in North America due to their

economic importance and ability to cause widespread mortality through major forest ecotypes

resulting in substantial loss to timber producing species. The Dendroctonus genus has been

described as the greatest biological threat to the major economic forest species. The acoustic

production of Dendroctonus species has been sporadically studied since the late 1960’s. Hopkins

(1909) described members of this genus in great detail and depicted the posterior elytral file and

7th abdominal tergite stridulating scraper in D. valens. The communicative properties of acoustic

production were explored in the Douglas fir beetle (Dendroctonus pseudotsugae) by Rudinsky in

1968 at Oregon State University with follow-up work in additional species of Dendroctonus

throughout his career. In the early 1970’s, publications on the observation of acoustic production

by both female and male Dendroctonus beetles by rubbing their abdominal scraping processes or

files (plectrum) and elytral files (pars stridens) together induced pheromone production and mate

acceptance (Michael and Rudinsky, 1972, Rudinsky and Michael, 1973).

Hypotheses regarding possible population isolation within species from multiple hosts

were tested through short range acoustical communication via morphology of the pars stridens

and plectrum of Dendroctonus ponderosae (mountain pine beetle). Work in 1984 showed D.

ponderosae reared in 3 host pine species (ponderosae pine, P. ponderosa; lodgepole pine, P.

contorta; white pine, P. monticola) did not support population divergence based on host

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selection (Yandell, 1984). The findings of Yandell (1984) give evidence to no distinguishable

separation with regards to acoustic production within the D. ponderosae. However, species

specificity was determined in six male Dendroctonus through morphology and acoustic

properties (Michael and Rudinsky, 1972) with follow-up work depicting oscillograms from six

Dendroctonus species stridulation properties reported on by Ryker in 1988.

Mate acceptance through acoustic communication and chemostimulus were identified by

Libbey at al. (1974) in Dendroctonus brevicomis (western pine beetle). Further work in the

western pine beetle followed (Ryker,1988) providing detailed oscillograms of chirp frequency

and intensity in the presence of rival males, courtship behavior of females and chemostimulus

attraction of males to frass containing female pheromone. The observed aggressive mating

behaviors of Dendroctonus ponderosae (mountain pine beetle) were described (Ryker and

Rudinsky, 1976) which followed up the brief behavioral findings of McGhehey (1968) which

described the itrasex male aggressive territorial behavior of the same species. McGhehey

reported on the territorial behavior of an individual mountain pine beetle male to an individual

virgin female gallery in reference to additional rivalry males.

The economic importance of Douglas-fir as a timber species prompted further research in

infesting Dendroctonus pseudotsugae (Douglas-fir beetle) and the subtleties of acoustic and

pheromone interplay (Rudinsky, 1968, 1969, Rudinsky and Ryker, 1976, Ryker, 1984). The

detailed research of acoustic production in Dendroctonus species allowed for the discovery of

pheromone release triggers in Dendroctonus pseudotsugae (Rudinsky, 1968). In addition,

acoustic studies provided an understanding in pheromone release between sexes of an individual

species, an understanding in passive and aggressive communication between and within species

of Dendroctonus, and communication between the gallery territory of egg laying females to

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prevent over-colonization and resource competition of brood. A review of the acoustic

production, territorial behavior, mate acceptance through acoustic production, and pheromone-

acoustic interaction in Dendroctonus species follows.

Acoustic production-morphology

Hopkins (1909) described the male 7th abdominal tergite stridulating scraper in

Dendroctonus valens. The posterior (rear) undersides approximating the apex of both elytra

possess a file or series of ridges used to rub against the tergal scraper or plectrum, forming

acoustic vibrations (Figure 1a and 1b). Chapman (1955) first described the acoustic “chirping” of

male Dendroctonus psuedotsugae. Lyon (1958) described the stridulation apparatus (abdominal

scraper and elytral file) in additional Dendroctonus species. Michael and Rudinsky (1972)

described and measured the stridualtory apparatus in six male Dendroctonus species (Douglas fir

beetle, D. pseudotsuga; mountain pine beetle, D. ponderosae; red turpentine beetle, D. valens;

western pine beetle, D. brevicomis; southern pine beetle, D. frontalis; spruce beetle, D.

rufipennis) for the purpose of examining species specificity in the morphology of acoustic

production. The species were chosen based on inter-species pheromone characteristics and their

individual attraction to host volatiles. None of the species selected by the authors share a

preference for single host volatiles and a likeness in pheromone composition. Significant

differences in overall elytral file length, distance between individual teeth on the top half

(cephalic) and bottom half (caudal), and number of teeth on the file were described (Michael and

Rudinsky, 1972). Dendroctonus ponderosae (the mountain pine beetle) and D. pseudotsugae

(Doug-fir beetle) had no significant difference in elytra file length and total single elytron length,

however the number of teeth and distance between those teeth were significant (Table 1).

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Scan the Hopkins document for images.


Prior to 1973 it was generally accepted that only Dendroctonus males stridulate, or

produce acoustics. Rudinsky and Michael (1973) report on the stridulation apparatus of four

Dendroctonus females (D. valens, D. rufipennis, D. ponderosae, and D. psuedotsugae) capable

of producing acoustic vibrations (Table 2). Two additional female Dendroctonus species (D.

brevicomis D. frontalis) were described to lack elytral files believed to be necessary for acoustic

production. The acoustic production of female Dendroctonus is characterized as chirps or clicks

in comparison to the much longer in duration male stridulation. By manipulating and filling the

sternal files of D. brevicomis, which do not possess an elytral file but still produce sound via

a strenal file, Rudinsky and Michael (1973) were able to demonstrate that females indeed use the

same apparatus as the males to produce the stridulating click or chirp.

Territorial behavior and mate acceptance

Dendroctonus species are monogynous with ultimately one male and one female to a

constructed gallery. The territorial behavior of male D. ponderosae to virgin females and

additional rivalry males was determined by McGhehey (1968) to result in aggressive behavior

between the competing males. Virgin female mountain pine beetles were established in

laboratory lodgepole pine rearing slabs and remained isolated for one day. On the second day, a

virgin male was introduced in the gallery and again on the third day an additional male was

placed near the gallery entrance and observations were conducted. McGhehey noted the

intruding male immediately began to stridulate while searching and locating the gallery entrance.

Upon entering the gallery, the male continued to periodically stridulate until noticed by the initial

male. Aggressive stridulation began from the first male as if to warn the intruder of the occupied

gallery. A face to face attack ensued with continued stridulation. Violent stridulation behavior

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was noted upon initial contact between the males accompanied by pushing the intruder. The

second arriving or intruder male was pushed out of the gallery after approximately 2 minutes of

attack. The intruding male having been persuaded away by the initial male left the gallery

vicinity, however if he was forced to return near the same gallery entrance he would again

attempt to gain entry. This activity would continue until the gallery entrance was packed with

frass.

Further investigation by Rudinsky and Michael (1974) revealed male stridulation during

mate attraction and courtship as well as aggressive behavior between competing males.

Observations were conducted with D. frontalis showing rivalry stridulation production and

behavior in competing males with similar results in limited trials of D. brevicomis and D.

rufipennis. Males oriented and entered galleries initiated by females and stridulated continuously

for several minutes. After the initial continuous stridulation, pauses began for 30 seconds with

longer pauses of two to three minutes occurring as time elapsed. During the longer pauses,

female stridulation was recorded allowing the work of Rudinsky and Michael (1973) in female

Dendroctonus to compliment the suspicion that the acoustic female production serves the

purpose of mate attraction and gallery spacing in site acquisition. Similar to the findings of

McGhehey in D. ponderosae, males of the D. frontalis initially occupying a female constructed

gallery began continuously stridulating in the event of an additional male arrival (Rudinsky and

Michael, 1974). Further findings from Rudinsky and Michael (1974) show initial males backed

the secondary intruding males out of the gallery by pushing with fast movements of the abdomen

and hind legs. When extricated from the gallery, the initial male would turn and face the

intruding male and begin pushing away with a face to face orientation while continuously,

strongly stridulating which the authors called “rivalry chirps”. The initial male would then turn

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and re-enter the gallery while producing rivalry chirps for up to 40 seconds. Rivalry chirps

transitioned into mate attractant chirps after 1 to 1 ½ minutes if no further perturbation occurred.

If two males were manually confined to an attractive female gallery or confined to glass tubes

without female stimulation, violent attacks occurred resulting in dismemberment and death.

Attractant chirps were easily distinguished from rivalry chirps and significantly different from

stress chirps evoked by manually applying pressure to the beetles. The data suggest a warning or

notification purpose of the stridulation called rivalry chirps between males vying for the

opportunity of courtship and acceptance in a prospective female.

Ryker and Rudinsky (1976) examined D. ponderosae stridulation in more detail by

asking if males exhibit rivalry acoustics as in previously reported D. frontalis. This report also

questioned whether the female chirp of D. ponderosae occurs in conjunction with mating

behavior. Male mountain pine beetles produced an interrupted chirp while confronting rival

males as well as the initial entry of a female constructed gallery. Simple, multi-impulse chirps

were produced by females in response to male stridulation at the gallery entrance. The

interrupted male chirp triggers an aggression toward an unmated female thought to be used in

testing the fitness of the female (Ryker and Rudinsky, 1976). A transition to uninterrupted male

stridulation occurred prior to mating. Female acoustic production ceased during courtship.

Surgically altered males lacking the ability to stridulate were met nine out of twelve trials with

biting, pushing aggressive females that produced continuous chirps while ejecting the males

from the gallery entrance. Since mating success by silenced males was 25% compared to 100%

with stridulating capable males, the interrupted male chirp is thought to function as a premating

or mate acceptance behavior in this species.

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Ryker (1988) reported oscillogram recordings from D. pseudotsugae, D. ponderosae, D.

brevicomis, D. valens, and D. frontalis. Gallery initiating females produce territorial chirps or

clicks to communicate spacing in all five species. Males of the five reported Dendroctonus

species produce aggressive chirps when fighting rather than those acoustics produced during

mate acceptance and courtship. This suggests an acoustic importance in reproductive success

between males. The attractant chirp is produced by four (D. pseudotsugae, D. brevicomis, D.

valens, and D. frontalis) of the five species of the Dendroctonus explored by Ryker (1988). The

attractant chirp of the D. pseudotsugae and D. brevicomis was shown to have initiated the

pheromone release attracting females and males when in low concentrations and signaling to

arriving beetles when in high concentration the host is nearing capacity (Rudinsky et al. 1976b).

Rudinsky et al. (1976b) further concluded the anti-aggregation pheromone released by both male

and female D. pseudotsugae is triggered by the acoustic stimulation of the opposite sex. The

literature shows that without the close range acoustic production in Dendroctonus species,

aggressive behavior is exhibited and pheromone release is not achieved.

Acoustic production - pheromone interaction

Rudinsky (1968) discovered the release of an anti-aggregation pheromone in D.

pseudotsugae initiated by chirping males within or over attractive female constructed galleries.

The term pheromone refers to the conglomeration of chemicals produced and released as a

communicative signal which in Dendroctonus species serves to aggregate or disperse incoming

cohorts. Further work by Rudinsky and Michael (1972) resulted in the recordings of male

attractant Douglas-fir beetle chirps in the presence of low-concentration, female pheromone

laden frass. The female response clicks are more frequent upon the male digging into the gallery

entry which triggers him to release an anti-aggregation pheromone methylcyclohexenone (MCH)

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(Rudinsky, 1976). MCH in low concentration acts as an attractant pheromone, however when

concentration of the MCH are great, the pheromone plume acts as an anti-aggregating signal

reducing the likelihood of overpopulation in any given selected Douglas fir. The male attractant

chirp, or intermittent chirp, signals the female to actively release MCH and causes her to

stridulate loudly (Rudinsky and Michael, 1973). The discovery of MCH as a concentrated anti-

aggregation pheromone in D. psedotsugae led to further investigative chemical work in D.

ponderosae as identifying endo-brevicomin and verbenone as potential anti-aggregation control

methods (Ryker and Yandell, 1983, Borden et al. 1987). As of 2009, verbenone alone as a

control method is still under debate as to its efficacy in epidemic mountain pine beetle

populations. However, not discussed in detail here, when verbenone is coupled with nonhost

angiosperm volatiles used on ponderosa pine to reduce attack of western pine beetle the results

show some reduced affect on infestation (Fettig et al., 2008, 2009).

When two male D. pseudotsugae are placed in a single vial, both individuals would chirp

and attack each other with pheromone release, however if two females were placed in a single

vial, no pheromone release was detected (Rudinsky et al. 1973b). When both male and female

were placed together a large quantity of MCH was produced. Females were separated and

subjected to a recording of male acoustic stimulation upon which MCH was released. This result

gives evidence that both sexes of D. pseudotsugae produce the anti-aggregating pheromone

MCH. Male D. ponderosae also stridulate in response to female produced pheromone frass or

synthetic produced trans-verbenone (Michael and Rudinsky, 1972). Ryker (1988) noted the

female D. brevicomis (western pine beetle), produces acoustic clicks at approximately 8 clicks

per minute when alone and not accompanied by a male in the gallery. If she is disturbed by either

another female or a gallery entering male, the production of a female multi-impulse chirp is

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initiated at approximately twice per second (Ryker, 1988). The males of this species produce an

interrupted chirp when attracted to female pheromone laden frass and when courting the female

(Ryker, 1988).

Conclusions

Acoustic production in Dendroctonus species has been shown to play an important

component in the overall suite of communication between and within species. Acoustic cues are

thought to be a close range intra and interspecies communication mechanism triggering the

pheromone release used in long range communication. Morphological differences in acoustic

production capabilities have been determined between species and between male and females of

a particular species within this genus indicating species and gender acoustic specificity. Males of

the genus Dendroctonus do not tolerate the presence of additional males in a female gallery with

warning stridulation and battles for gallery occupation between males. In polygynous bark

beetles, such as members of the Ips genus, it has been demonstrated that males colonize the host

and females produce the acoustic stridulation which is the opposite of monogynous

Dendroctonous beetles. Acoustic communication between sexes of D. ponderosae was

established as a mate acceptance mechanism (Ryker, 1976). Male and female stress chirps have

been characterized as well as female agreement chirps, simple female clicks and chirps, male

attractant chirps, male courtship chirps, male rivalry or aggressive chirps, and simple male

chirps. The acoustic properties of stridulating are known to communicate varying behaviors in

concert with pheromone release comlimenting the suite of Dendroctonus communication.

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References

Chapman, J.A. 1955. Sex determination by stridulation sounds in the Douglas fir beetle, Dendroctonus pseudotsugae. Bi-monthly progress report. Div. Forest Biology., Ottawa 11:2

Claridge, M. 2006. Chapter 1: Insects sounds and communication – An introduction. In Insect Sounds and Communication: Physiology, Behavior, Ecology and Evolution. Drosopoulos, S., Claridge, M.F. (eds.) CRC Press, Boca Raton, FL. p 532

Ewing, A.W. 1989. Arthropod Bioacoustics: Neurobiology and behaviour. Edinburgh University Press, Edinburgh. p 260

Fettig, C.J., Dabney, C.P., McKelvey, S.R., Huber, D.P.W. 2008. Nonhost angiosperm volatiles and verbenone protect individual ponderosa pines from attack by western pine beetle and red turpentine beetle (Coleoptera : Curculioniclae, Scolytinae). Western Journal of Applied Forestry 23: 40-45

Fettig, C. J., McKelvey, S. R., Dabney, C. P., Borys, R. R., Huber, D. P. W. 2009. Response of Dendroctonus brevicomis to different release rates of nonhost angiosperm volatiles and verbenone in trapping and tree protection studies. Journal of Applied Entomology 133: 143-154

Hopkins, A.D. 1909. Contributions toward a monograph of the Scolytid Beetles. I. The genus Dendroctonus. Technical Series No. 17 Part 1. US Govt. Printing Office, Washington DC.

Lyon, R.L. 1958. A useful secondary sex character in Dendroctonus bark beetles. Canadian Entomologist 60: 582-584

McGhehey, J.H. 1968. Territorial behavior of bark-beetle males. Canadian Entomologist 100: 1153

Michael, R.R., Rudinsky J.A. 1972. Sound production in Scolytidae: Specificity in male Dendroctonus beetles. Journal of Insect Physiology 18: 2189-2201

Rudinsky, J.A., 1968. Pheromone-mask by the female Dendroctonus pseudotsugae Hopkins, an attractant regulator. Pan-Pacific Entomologist 44: 284-250

Rudinsky, J.A., 1969. Masking of the aggregation pheromone in Dendroctonus pseudotsugae Hopkins. Science 166: 884-885

Rudinsky, J.A., Michael, R.R. 1972. Sound production in Scolytidae: chemostimulus of sonic signal by the Douglas-fir beetle. Science 175: 1386-1390

Rudinsky, J.A., Michael, R.R. 1973. Sound production in Scolytidae: Stridulation by female Dendroctonus beetles. Journal of Insect Physiology 19: 689-705

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Rudinsky, J.A., Michael, R.R. 1974. Sound production in Scolytidae: ‘Rivalry’ behavior of male Dendroctonus beetles. Journal of Insect Physiology 20: 1219-1230

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

Rudinsky, J.A., Ryker, L.C., Michael, R.R., Libbey, L.M., Morgan, M.E., 1976b. Sound production in Scolytidae: Female sonic stimulus of male pheromone release in two Dendroctonus beetles. Journal of Insect Physiology 22: 1675-1681

Rudinsky, J.A., Ryker, L.C. 1976. Sound production in Scolytidae: Rivalry and premating stridulation of male Douglas-fir beetles. Journal of Insect Physiology 20: 1219-1230

Ryker, L.C., Rudinsky, J.A. 1976. Sound production in Scolytidae: Aggressive and mating behavior of the mountain pine beetle. Annals of the Entomological Society of America 69: 677-680

Ryker, L.C. 1988. Acoustic studies of Dendroctonus bark beetles. Florida Entomologist 71: 447-461

Ryker, L.C., Yandell, K.L. 1983. Effect of verbenone on aggregation of Dendroctonus ponderosae Hopkins (Coleoptera:Scolytidae) to synthetic attractant. Zeitschrift fur Angewandte Entomologie-Journal of Applied Entomology 96: 452-459

Yandell, K.L. 1984. Sound production of Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae): a comparison of populations from three host pines in Oregon. Zeitschrift fur Angewandte Entomologie 97: 180-187

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Figures and Tables

Table 1. Measured elytral files and length of elytron from male Dendroctonus species. Reproduced from Michael and Rudinsky, 1972.

Table 2. Measured elytral files and measured length of elytron from female Dendroctonus species. Reproduced from Rudinsky and Michael, 1973.

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Figure 1a. Stridulating scraper (plectrum) in D. valens. Reproduced from Hopkins, 1909.

Figure 1b. Elytral file (pars stridens) in D. valens. Reproduced from Hopkins, 1909.

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Figure 2. Stridulating apparatus of female Dendroctonus sp. Reproduced from Rudinsky and Michael, 1973.

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Figure 3a,b. The acoustic properties of Dendroctonus pseudotsugae (a) and Dendroctonus ponderosae (b). Reproduced from Ryker 1988

Figur 3a.

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Figure 3b.

Contact:

1Dan R. West Colorado State University Dept. Bioagricultural Sciences and Pest Management C109 Plant Sciences Fort Collins, CO. 80523

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Acoustic cues and mating behavior of Dendroctonus ... · PDF fileAcoustic cues and mating behavior of Dendroctonus (Coleoptera:Curculionidae:Scolytinae) species 1Dan R. West Email: