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Keywords:

  • management;
  • control;
  • southern pine beetle;
  • western pine beetle;
  • mountain pine beetle;
  • Dendroctonus

Abstract

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 MATERIALS AND METHODS
  5. 3 RESULTS AND DISCUSSION
  6. 4 CONCLUSION
  7. ACKNOWLEDGEMENTS
  8. REFERENCES

BACKGROUND

Acoustic signals play a critical role in mate choice, species recognition, communication, territoriality, predator escape and prey selection. Bark beetles, which are significant disturbance agents of forests, produce a variety of acoustic signals.

RESULTS

A bioacoustic approach to reducing bark beetle reproduction within wood tissues was explored. Playback of modified biological sounds reduced beetle reproductive output, tunneling distance and adult survival.

CONCLUSION

The targeted use of biologically relevant sounds disrupts insect behaviors and could be a species-specific, environmentally friendly method of insect management. © 2013 Society of Chemical Industry

1 INTRODUCTION

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 MATERIALS AND METHODS
  5. 3 RESULTS AND DISCUSSION
  6. 4 CONCLUSION
  7. ACKNOWLEDGEMENTS
  8. REFERENCES

Bark beetles (Coleoptera: Curculionidae) are important natural disturbance agents in forests.[1-4] They occasionally reach outbreak levels, killing millions of hectares of forests and disrupting timber and other industries. Scientists and forest managers have sought solutions to bark beetle outbreaks, including forest thinning, pheromone disruption and pesticide applications.[3-5] At the tree scale, application of pesticides or pheromones has some success in protecting trees from bark beetle attack.[6, 7] The authors have tested an alternative method of control, using acoustic playbacks to disrupt the communication and performance of bark beetles within tree tissues.

Bark beetles use acoustic signals for a wide range of behavior, including mate recognition and communication,[8] territoriality,[9] species recognition,[10] predator escape[11] and possibly host selection.[12] Methods of sound production by bark beetles include stridulation and friction with substrates.[8, 10] In spite of the remarkable bioacoustic abilities of bark beetles, this aspect of their biology has received little attention.[13]

Acoustic devices are commonly used to detect pests in trees and wood materials;[14] however, the use of sounds (or vibrations) to protect plants from insects has only been used in a few systems.[15-17] The authors have explored the use of an acoustic technique for controlling bark beetle activity and reproduction. The way in which bark beetle sounds are manipulated for input into tree materials, the effects of these sounds on bark beetles within tree tissues and the potential use of acoustic methods to reduce beetle populations and protect trees are described.

2 MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 MATERIALS AND METHODS
  5. 3 RESULTS AND DISCUSSION
  6. 4 CONCLUSION
  7. ACKNOWLEDGEMENTS
  8. REFERENCES

2.1 Beetle populations

Sections of beetle-infested ponderosa pine (Pinus ponderosae P. & C. Lawson) were collected in the Coconino National Forest, Arizona, United States. Tree sections (0.5 m length) were placed in climate-controlled containers, and emerging beetles were identified to species and sex. Only the southern pine beetle, Dendroctonus frontalis Zimmermann, adults that were vigorous and healthy and had all appendages were used for recordings and bioassays. Western pine beetles, D. brevicomis LeConte, which were also collected in Arizona, and mountain pine beetles, D. ponderosae Hopkins, collected near Missoula, Montana, were used for acoustic recordings.

2.2 Experimental assay

Using an apparatus called a phloem sandwich, the authors observed D. frontalis pairs to determine the effects of sound on beetle tunneling, mating, oviposition and survival. Phloem pieces (30 × 30 cm) used in the sandwiches were collected from a healthy ponderosa pine. To make the phloem sandwich, a piece of phloem was placed between two sterile 30 × 30 cm sheets of clear plexiglass and sealed with Parafilm. Four 3 mm diameter holes were drilled into the top plexiglass sheet. One beetle pair was placed within each hole, with females introduced 1 day before males. Beetles that did not enter the phloem sandwich were replaced within 3 h. Each phloem sandwich contained four beetle pairs.

Prior to beetle introduction, a 3 cm diameter hole was also drilled in the center of the bottom piece of plexiglass, where the speaker (Pyramid TWD10 1 3/8 inch 150 W tweeter) was placed. Sound treatments were started 24 h after males were introduced. Each sandwich was subjected to one of three treatments: modified beetle sounds, radio sounds or no sound (i.e. control). The modified beetle sounds, described below, contained the stress and interrupted calls[18] from each of the three species. The radio treatment was a live feed of KZGL 103.7 FM Flagstaff. The radio treatment made it possible to determine whether sound, regardless of its biological relevance, affected beetles. The control had a speaker, but no sound was played. Playback amplitude was calibrated to a measured average level of 70 dB from a distance of 1 m from the transducer prior to coupling to the phloem sandwich.

Oviposition tunnel length, number of eggs and beetle conditions were recorded daily for 7 days. Twenty beetle pairs in five phloem sandwiches were tested for each treatment. Effects of sound treatments on tunnel lengths and number of offspring were tested using an ANOVA (JMP Pro 9). The Freeman–Halton extension of Fisher's exact test was used to determine whether mortality differed across treatments.

2.3 Sound recordings and processing

Acoustic call sequences (or sound impulse trains[19]) from three bark beetle species, D. frontalis, D. brevicomis and D. ponderosae, were recorded from separate phloem sandwiches using a Knowles Acoustics FG-3329 miniature condenser microphone placed 2 mm from the entry hole. More specifically, the male attraction call[18] (given when the male enters a female's tunnel) and rivalry call (when two males are in a tunnel) from each species were recorded and used in the ‘beetle sound’ treatment. The Knowles transducer is described by its manufacturer as having a flat upper frequency response extending to 10 kHz. In reality it has a robust ultrasonic response up to at least 100 kHz and has been used by another manufacturer (Avisoft) in microphone systems used for recording the ultrasonic sounds of bats. The microphone was routed to an Analog Devices 620 Instrumentation Op Amp and recorded at 16 bits, 44.1 kHz sample rate using a Sonic Devices 702 digital audio recorder. Beetle sounds from the three bark beetle species were combined (using Audiomulch 2.1.1) (Fig. 1) with synthetically generated sounds via a conventional summing amplifier and a balanced amplitude modulation circuit (Fig. 2).[20] This synthetically generated element, in combination with beetle sounds, provided a constantly shifting background and a variety of auditory behaviors that created unpredictable sounds and patterns (called the ‘beetle sounds’ treatment in Fig. 3; referred to as the modified sound treatment in the following text) similar to those of the radio treatment.

image

Figure 1. Systems level view of the auditory elements using Audiomulch (3.1.1) in playback experiments.

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image

Figure 2. Individual biologically relevant sounds (i.e. stress and attraction calls) from D. frontalis, D. brevicomis and D. ponderosae were played back as looping digital audio samples from the audio manipulation program Audiomulch (see Fig. 1). These sounds were also combined with a variety of digitally signal-processed versions (time-domain reordering, frequency and amplitude modulation) and remixed in continuously unpredictable ways within the same audio manipulation program. The resultant audio output signal from Audiomulch was then combined with synthetic sounds generated from a set of non-linear chaotic audio oscillators through an analog balanced amplitude modulation circuit. Beetles in phloem sandwiches were then exposed to the resultant combination of sounds (for the ‘beetle sound’ treatment): the original, unmodified, biologically relevant sound samples; the digitally signal-processed, biologically relevant sound samples; the output signal from the balanced amplitude modulation circuit, combining the signal from Audiomulch and the synthetic sounds; the original synthetic, non-linear, chaotic oscillator sounds.

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image

Figure 3. Egg production and tunneling by Dendroctonus frontalis pairs in phloem sandwiches exposed to modified beetle sounds, sound from radio or no sound for 7 days. Bars with different letters indicate significant differences between treatment means at P < 0.01.

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3 RESULTS AND DISCUSSION

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 MATERIALS AND METHODS
  5. 3 RESULTS AND DISCUSSION
  6. 4 CONCLUSION
  7. ACKNOWLEDGEMENTS
  8. REFERENCES

Female and male D. frontalis readily entered the phloem sandwiches. Approximately 81% of females entered the phloem sandwiches, and 85% of males entered. Beetle pairs in the no-sound (control) or radio treatments tunneled significantly farther (F2,35 = 115.8, P < 0.001) and deposited significantly more eggs (F2,35 = 27.0, P < 0.001) than beetle pairs in the modified sound treatment (Fig. 3). In the modified sound treatment, beetles tunneled only 0.4 cm per day, versus 2.1 cm per day in the other treatments. Additionally, over all seven days, only one egg was deposited from the 15 pairs in the modified sound treatment, compared with 117 eggs from ten pairs in the radio treatment and 204 eggs from 13 pairs in the no-sound treatment. Tunneling and egg laying rates in the no-sound and radio treatments were similar to those found in nature for D. frontalis.[21]

Beetle pairs in the no-sound or radio treatments exhibited typical behaviors: constructing tunnels, mating and depositing eggs. Beetles in the modified sound treatment exhibited flight responses such as wing extension and production of exit tunnels, failed to perform tunnel maintenance, mated infrequently and laid few eggs. Only beetles in the modified sound treatment died during the 7 day study (P = 0.051): one male and two females died. The two dead females were killed by their male partners.

As the modified sound treatments resulted in failed reproduction and tunneling by bark beetles, this method has potential for management applications. Further study is required to determine why the modified sounds negatively affected beetle pairs. One possibility is that avoidance behaviors were triggered by the sounds of competing beetle species. In Arizona, these three species, D. frontalis, D. brevicomis and D. ponderosae, have existed in ponderosa pine stands for thousands of years, often in the same tree.[22] Alternatively, the modified beetle stress calls, either intra- or interspecific, may have elicited distress behaviors, as occurs in other insects.[23] A third possibility is that the sounds may have elicited mistimed changes in chemical signals, which interrupted normal mating behavior; for example, in related bark beetle species, male acoustic calls trigger the release of the female's anti-aggregative pheromone.[24] The authors are continuing to study which aspects of the modified sounds produce the observed effects, or whether an aggregate of beetle sounds and artificial manipulations is needed for a negative effect on bark beetles to be achieved.

The tools described here could be used for the protection of individual trees or wood structures. The use of a tactile transducer (such as an exciter produced by HiWave Technologies PLC) could provide an efficient method of sound input into wood materials. The application of this acoustic technology for large forest stands is not practical, given the need to place devices on each tree. Technologies to distribute sounds over large areas or to each potential host tree would be needed to use this tool at the landscape level.

4 CONCLUSION

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 MATERIALS AND METHODS
  5. 3 RESULTS AND DISCUSSION
  6. 4 CONCLUSION
  7. ACKNOWLEDGEMENTS
  8. REFERENCES

The present findings suggest that targeted use of biologically derived acoustic signals can disrupt insect behaviors that are important to reproductive success and population growth. Additionally, the use of acoustics could be a species-specific, environmentally friendly method of insect management without any potentially lethal side effects to humans.[15] Studies are needed to determine the effects of acoustic signals on natural enemies and other inhabitants of tree tissues. The given modified sound treatment significantly reduced reproduction, survival and activity of beetles living within tree tissues. Acoustic technologies, as described here, could be used for individual tree protection, but future research is needed to test whether sound profiles can deter bark beetles from entering healthy trees, and whether they can affect natural bark beetle populations.

ACKNOWLEDGEMENTS

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 MATERIALS AND METHODS
  5. 3 RESULTS AND DISCUSSION
  6. 4 CONCLUSION
  7. ACKNOWLEDGEMENTS
  8. REFERENCES

The authors thank JP Crutchfield, C Currie, R Harrill, R Jeanne, K Klepzig, K London, J Yack and two anonymous reviewers for constructive discussions and comments. They also thank TS Davis, C Foelker, M Henry, E Jensen and K Yturralde for assistance with materials. This project was supported by the NAU Intramural Grant Program: Technology & Research Initiative Fund (to RWH). A full patent (PCT/US2011/063838) on the acoustic device was submitted in December 2011, and an international patent (WO2012/078814 A2) in December 2012.

REFERENCES

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 MATERIALS AND METHODS
  5. 3 RESULTS AND DISCUSSION
  6. 4 CONCLUSION
  7. ACKNOWLEDGEMENTS
  8. REFERENCES
  • 1
    Kurz WA, Dymond CC, Stinson G, Rampley GJ, Neilson ET, Carroll AL et al., Mountain pine beetle and forest carbon feedback to climate change. Nature 452:987990 (2008).
  • 2
    Griffin JM, Turner MG and Simard M, Nitrogen cycling following mountain pine beetle disturbance in lodgepole pine forests of Greater Yellowstone. For Ecol Manag 261:10771089 (2011).
  • 3
    Raffa KF, Aukema BH, Bentz BJ, Carroll, AL, Hicke JA, Turner MG et al., Anthropogenic amplification: the dynamics of bark beetle eruptions. BioScience 58:501517 (2008).
  • 4
    Wermelinger B, Ecology and management of the spruce bark beetle Ips typographus – a review of recent research. For Ecol Manag 202:6782 (2004).
  • 5
    Goyer R, Wagner M and Schowalter T, Current and proposed technologies for bark beetle management. J For 96:2933 (1998).
  • 6
    Grosman DM, Clarke SR and Upton WW, Efficacy of two systemic insecticides injected into loblolly pine for protection against southern pine bark beetles (Coleoptera: Curculionidae). J Econ Entomol 102:10621069 (2009).
  • 7
    Schlyter F, Semiochemical diversity in practice: antiattractant semiochemicals reduce bark beetle attacks on standing trees – a first meta-analysis. Psyche: J Entomol 2012: Article ID 268621.
  • 8
    Rudinsky JA and Michael RR, Sound production in Scolytidae: stridulation by female Dendroctonus beetles. J Insect Physiol 19:689705 (1973).
  • 9
    Rudinsky JA, Ryker LC, Michael RR, Libbey LM and Morgan ME, Sound production in Scolytidae: female sonic stimulus of male pheromone release in two Dendroctonus beetles. J Insect Physiol 22(12):167168 (1976).
  • 10
    Barr BA, Sound production in Scolytidae (Coleoptera) with emphasis on the genus Ips. Can Entomol 101:636672 (1969).
  • 11
    Lewis EE and Cane JH, Stridulation as a primary anti-predator defence of a beetle. Anim Behav 40:10031004 (1990).
  • 12
    Haack RA, Blank RW, Fink FT and Mattson WJ, Ultrasonic acoustical emissions from sapwood of eastern white pine, northern red oak, red maple, and paper birch: implications for bark- and wood-feeding insects. Fla Entomol 71(4):427440 (1988).
  • 13
    Renwick JAA and Vite JP, Systems of chemical communication in Dendroctonus. Contr Boyce Thompson Inst Pl Res 24:283292 (1970).
  • 14
    Mankin RW and Moore A, Acoustic detection of Oryctes rhinoceros (Coleoptera: Scarabaeidae: Dynastinae) and Nasutitermes luzonicus (Isoptera: Termitidae) in palm trees in urban Guam. J Econ Entomol 103:11351143 (2010).
  • 15
    Eriksson A, Anfora G, Lucchi A, Lanzo F, Virant-Doberlet M, et al. (2012) Exploitation of Insect Vibrational Signals Reveals a New Method of Pest Management. PLoS ONE 7(3): e32954. doi:10.1371/journal.pone.003295
  • 16
    Polajnar J and Čokl A, The effect of noise on sexual behaviour of the southern green stink bug Nezara viridula. Bull Insectol 61:181182 (2008).
  • 17
    Mazzoni V, Presern J, Lucchi A and Virant-Doberlet M, Reproductive strategy of the Nearctic leafhopper Scaphoideus titanus Ball (Hemiptera: Cicadellidae). Bull Entomol Res 99:401 (2009).
  • 18
    Ryker LC, Acoustic studies of Dendroctonus bark beetles. Fla Entomol 71(4):447461 (1988).
  • 19
    Mankin RW, Smith MT, Tropp JM, Atkinson EB and Jong DY, Detection of Anoplophora glabripennis (Coleoptera: Cerambycidae) larvae in different host trees and tissues by automated analyses of sound-impulse frequency and temporal patterns. J Econ Entomol 101(3):838849 (2008).
  • 20
    Hofstetter RW, McGuire R and Dunn DD, Use of acoustics to disrupt and deter wood-infesting insects and other invertebrates from and within trees and wood products. US Patent US2011/63838 (priority date 7 December 2010) and WIPO Patent Application WO/2012/078814 (publication date 14 June 2012).
  • 21
    Coulson RN and Klepzig KD, Southern Pine Beetle II. Southern Research Station General Technical Report SRS-140USDA. Southern Research Station, USDA Forest Service, Asheville, NC, 512 pp. (2011).
  • 22
    Davis TS and Hofstetter RW, The effects of gallery density and ratio on the fitness and fecundity of two sympatric bark beetles. Environ Entomol 38(3):639650 (2009).
  • 23
    Inta R, Evans TA and Lai JCS, Effect of vibratory soldier alarm signals on the foraging behavior of subterranean termites (Isoptera: Rhinotermitidae). J Econ Entomol 102:121126 (2009).
  • 24
    Rudinsky JA, Masking of the aggregation pheromone in Dendroctonus pseudotsugae Hopkins. Science 166:884885 (1969).