Temperature-Dependent Parameters of Stridulatory Signals in the Four-Eyed Fir Bark Beetle, Polygraphus proximus (Coleoptera: Curculionidae: Scolytinae)

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Please cite this article as: I.A. Kerchev, Temperature-Dependent Parameters of Stridulatory Signals in the FourEyed Fir Bark Beetle, Polygraphus proximus (Coleoptera: Curculionidae: Scolytinae), Journal of Asia-Pacific Entomology (2020), doi: https://doi.org/10.1016/j.aspen.2020.01.011

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Ivan A. Kerchev

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Temperature-Dependent Parameters of Stridulatory Signals in the Four-Eyed Fir

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Bark Beetle, Polygraphus proximus (Coleoptera: Curculionidae: Scolytinae).

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Institute of Monitoring of Climatic and Ecological Systems of the Siberian Branch of Russian Academy of Sciences, Tomsk, 634055, Russia e-mail: [email protected] Phone / fax: (+7-3822)491855 / (+7-3822) 491978

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Abstract

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Acoustic signals are an essential part of the multi-modal systems of conspecific

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communication among insects. The patterns of abiotic factors effects on their communication

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parameters are of great interest for prognostic purposes in current climatic instability and for

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practical application in order to manage their populations.

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The aim of this study was to reveal the dependence of the parameters of acoustic signals

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produced by bark beetle Polygraphus proximus, an aggressive alien stem pest on the

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environmental temperature. Male stridulatory signals were recorded in seven temperature

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settings (5–35 °C), and changes in their temporal parameters were evaluated under laboratory

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conditions.

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The obtained results allowed us to reveal the pattern of temperature dependence of

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signals produced by P. proximus. More than half of the insects were found to actively stridulate

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at 5 °C. Raising temperature caused an increment in chirp rate that continued to increase up to 30

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°C. Further temperature increase led to suppression of signaling in most of the tested males. The

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obtained results showed a number of patterns of temperature effect on the parameters of acoustic

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signals which might be universal for representatives of different bark beetles genera with various

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stridulatory apparatus types.

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Key words: bark beetle, temperature effect, acoustic signals, chirp 1

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Introduction

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Insects are poikilothermic animals, and much of their activity is directly dependent on

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environmental conditions (Walker, 1975; Pires and Hoy, 1992; Sanborn, 2004). Temperature

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affects the rate of biochemical processes in the insect body and the neuromuscular response,

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which strongly modulates acoustic communication (Gerhardt and Huber, 2002; Sanborn, 2005).

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This area of study is of current relevance because of the need to predict possible effects of global

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warming on important components of terrestrial and aquatic ecosystems (Pörtner and Knust,

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2007; Kearney, et al., 2009; Conrad et al., 2017). One of the important issues that influences

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temperature is determining the mechanism to correctly recognize a signal that is modified by

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exposure to various temperatures. When choosing a sexual partner, it is assumed that this

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problem can be solved by insects in two ways Conrad et al., 2017). One way is “temperature

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coupling”, where a change in the signal is accompanied by parallel changes in receiver

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preferences resulting from a change in temperature (Gerhardt, 1978). Another possibility is that

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the receiver preference stays the same, regardless of temperature. In this case, the signals that are

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less modulated by temperature would be recognized correctly, and in the case of mating signals,

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will be more attractive (von Helversen and von Helversen, 1981; Ritchie et al., 2001)

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The influence of temperature fluctuations on the parameters of acoustic signals was

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studied mostly in a few taxonomic groups that were preferred by bioacoustics specialists:

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Orthoptera and Hemiptera (Doherty, 1985; Souroukis et. al., 1991; Pires and Hoy, 1992;

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Korsunovskaya and Zhantiev, 2007; Zhemchuzhnikov and Knyazev, 2015). Narrow selectivity

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during choosing a model organism caused significant disproportion in the study of the effect of

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temperature on the insect’s acoustic communication and did not involve the largest orders, such

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as Coleoptera, Hymenoptera, and Hemiptera (Fonseca and Revez, 2002; Sanborn, 2004; Andrew

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et al., 2013; Conrad et al., 2017). The range of studied species should be expended because of

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effects of polysemy in communication activity that is observed even within congeners (Sanborn

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and Mater, 2000; Fonseca and Revez, 2002; Sueur and Sanborn 2003; Sanborn, 2006).

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Bark beetles (Scolytinae) are representatives of the family Curculionidae, which is one of

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the largest beetle families, and they are important agents in the carbon cycle in forest ecosystems

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(Weed et al., 2015). According to the latest reports, the ability of acoustic signaling in this group

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is observed in 107 species, which were mainly studied in genera such as Dendroctonus Erichson,

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Ips De Geer, and Scolytus Geoffroy (Dobai, 2017), which have significant ecological and

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economic impacts through periodical outbreaks.

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In our study, Polygraphus proximus, a Far Eastern stem pest of the trees from genus

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Abies (Baranchikov, 2010), was chosen for the experiment. Because this pest is an exceptional

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threat to the boreal forests of the northern hemisphere, it has been included on the European and

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Mediterranean Plant Protection Organization Alert list since 2014. The invasion of this species

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into the territory of Southern Siberia from the Far East led to large-scale degradation of

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aboriginal dark-coniferous forests (Krivets et al., 2015; Kononov et al., 2016). Currently, P.

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proximus is a model that is used to study the various ecological effects of forest pest invasions on

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the environment (Kerchev, 2014; Krivets et al., 2015) and the behavior of bark beetles including

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acoustic communication (Kerchev, 2019). P. proximus stridulates during different types of

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intraspecific communication by producing signals that are distinguishable based on temporal

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parameters. The first signal appears under the elyta-tergal type of stridulating, which is noted in

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three contexts; these contexts are stress, rivalry behavior, and courtship. During courtship, males

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also produce the second type of chirps, which are registered only in male−female interactions

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inside galleries. Pre-copula signals are produced by rubbing the tibia against the elytral margin

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just before copulation (Kerchev, 2019).

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The aim of this study was to reveal the dependence of acoustic signal parameters on changes in the ambient air temperature in bark beetles.

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Materials and methods

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Collection and storage of insects

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For the experiments, overwintering P. proximus imago specimens were collected together

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with fir bark from their brood trees in May 2018 in the Tomsk Region of the dark-conifer

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plantation in the Kornilovskoe forest (56°49′15″ N; 85°37′07″ W). Sexual identification was

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performed based on morphological characteristics. The males were distinguished by the presence

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of two frontal protuberances, and the females were identified by dense seta on the frons (Stark

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1952; Kerchev, 2014). Insects were placed individually in separate labelled 5-mL glass tubes 3

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containing crushed pieces of fir bark, and the tubes were closed on the top with a moistened

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cotton plug. Before the experiment, the beetles were stored in the TS-1/20 SPU incubator (JSC

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Smolensk SKTB SPU, Smolensk) at 4°C for 2 days.

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Design Recordings of male−female interactions were obtained using a microphone that was placed inside a tube (diameter, 1 cm), which represents the arena (Kerchev, 2019).

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The audio recording was performed using a Behringer condenser microphone (Willich-

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Münchheide II, Germany) (model: ECM 8000; 15–20 000 Hz), and a Zoom R16 digital recorder

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(Tokyo, Japan) with a 20 Hz–44.1 kHz frequency range and a 24-bit sampling rate. The recorded

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signals were saved in the WAV format.

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Signals were produced using an elytra-tergal stridulatory apparatus (Kerchev, 2019)

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under seven different temperature conditions, ranging from 5°C to 35°C, which were increased

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in increments of 5°C for each pair of beetles. The duration of each audio recording was 15

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minutes. This time period was chosen because it was insufficient for the beetles to intrude into

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the bark and to change the context of interaction between them.

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Before recording at each temperature, a continuous pure tone that was centered at the

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mean dominant frequency (9.8 kHz; 40 dB) was produced by the tone generator (GWIinstec

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SFG2107; Taiwan, China) and was recorded. The distance from the microphone to the resonator

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400 RT 160 (40 kHz; 74 dB) in both cases was 1.5 cm. No distortion of the time and frequency

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parameters of the test signal was detected during temperature changes.

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The temperature regime under the audio recording was changed every 24 hours. In the

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intervals between the experiments, insects were placed into tubes and stored at 5°C. To prevent

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insect damage to each other in the interval between recordings, they were placed individually in

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numbered 2-mL glass tubes that were closed with a moistened swab. Before each recording, the

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insects underwent a 2-hour adaptation period to the new temperature regime, after which they

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were released into the arena (Fig. 1).

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Terminology and measurements

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For each record, indicators such as syllable duration, inter-syllable interval, number of

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chirps per syllable, chirp rate, chirp duration, inter-chirp interval, number of tooth-strikes, and

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inter-tooth-strike interval (Fig. 2) were analyzed based on the terminology proposed in previous

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studies (Ryker and Rudinsky, 1976; Pureswaran et al., 2016; Kerchev, 2019). Individual chirps

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were identified using the band-limited energy detector in Raven Pro 1.5 (Cornell Lab of

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Ornithology; Ithaca, NY, USA) (Charif et al., 2010). A syllable and the minimum interval

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between adjacent syllables were empirically found on the sonogram for each recording at a

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distance between the chirp series that exceeded the average interval between the minimal groups

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of chirps (three intervals were used for analysis).

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Statistical analysis

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Each parameter in each record was measured at five points that were calculated using the

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RANDBETWEEN function in Microsoft Excel. The mean values that were taken for each

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recording were analyzed, and a consistency check of the parameter variations was performed

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using the Kendall coefficient of concordance (W). Signal parameters were compared using the

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Kruskal–Wallis test (H-test), and for statistically significant differences, multiple comparisons

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were performed using the FDR correction (Benjamini and Hochberg, 1995). The Spearman’s

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rank correlation coefficient (rs) was used to determine the strength of the relationship between

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signal parameters and temperature conditions. All of the statistical analyses were performed

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using Statistica 8.0 (StatSoft Inc.; Tulsa, OK, USA). In all cases, p < 0.05 was considered

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significant, p < 0.01 highly significant and p < 0.001 very highly significant.

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Results

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During the recordings at 5–30°C, at least 22 out of 37 beetles were found to produce

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signals (e.g. a set of 10-s records of stridulation by the same male at different temperatures; see

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the media file (Kerchev, 2020)). When the temperature was increased to 35°C, only eight male

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beetles continued to stridulate. Only four specimens stridulated during all seven temperature

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conditions. The control group consisting of four beetles, which was recorded at 22°C over the

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entire experimental period, consistently retained the ability to signal.

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Analysis of the signal characteristic variability in males showed a high consistency for

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such characteristics such as intertooth-strike interval, inter-chirp interval, chirp duration, and

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chirp rate (Table 1).

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The median concordance was established for the parameters of syllable duration and number of chirps per syllable (Table 1).

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For multiple comparisons, highly significant differences were established for almost all

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signal parameters under the tested settings, except for the number of chirps per syllable and the

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number of tooth-strikes per chirp.

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Among the analyzed characteristics of the P. proximus signals, a strong correlation

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between ambient temperature and chirp rate was found (Spearman rank-order correlations (rs =

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0.8; p <0.05).

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The average coefficient of the negative correlation with temperature increase was noted

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for several parameters (Fig. 3), as follows: chirp duration, inter-chirp interval, and inter-tooth-

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strike interval (rs = −0.6; p<0.05). Weak feedback with temperature was observed for the

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duration of the inter-syllable interval (rs = −0.4; p <0.05) and syllable duration (rs = −0.3; p

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<0.05) were observed. No statistically significant correlations with temperature were established

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for the number of tooth-strikes or chirps per syllable (rs = 0.02; rs = 0.04; p>0.05, respectively).

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Discussion 6

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The correlation between the temperature change and the temporal signal parameters has been established for the first time in bark beetles and for Coleopteran insects in general.

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There was no statistically significant relationship between syllable duration and the

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number of chirps per syllable, and it is likely to be more dependent on the context, as described

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previously (Kerchev, 2019). Temperature fluctuations did not yield significant changes in the

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number of tooth-strikes per chirp. In the signals that were produced by bark beetles in the genus

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Dendroctonus, this parameter was directly related to the number of ridges on the pars stridens

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(Fleming, 2013; Yturalde and Hofstetter, 2015). We previously found that the number of tooth-

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strikes may vary depending on the context of the produced signal (Kerchev, 2019).

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A strong correlation between the rate of chirps per unit of time and the increase in

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temperature was noted previously for many Orthoptera representatives (Doherty, 1985; Beckers

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and Schul, 2008) and other cold-blooded animals such as amphibians (Gayou, 1984). An

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increase in the chirp rate also caused a decrease in chirp duration, without changes in the

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amplitude of abdominal movement, which otherwise would have an influence on the number of

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tooth-strikes per chirp.

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As shown by neurophysiological studies of grasshoppers and crickets, the impulses of

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some spontaneously active neurons in the insect’s central nervous system result from phase

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rearrangements, which are able to synchronize mainly with conspecific signals. This mechanism,

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acting as an internal oscillator, makes it possible to separate intraspecific signals with a slight

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differece in rhythm from the external noise (Zhantiev and Korsunovskaya, 2014). The

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mechanisms used in mass synchronization of conspecific signals in insects that use another

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channel for communication are probably of the same neurophysiological nature (e.g. fireflies,

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Carlson et al., 1976). Thus, significant signal modulations that are noted in the temperature range

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from 5 to 30°C and the operation of their recognition mechanism to maintain the role of

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intraspecific communication, most likely work in accordance with the “temperature coupling”

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theory that was mentioned earlier. 7

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The number of insects that produced signals (n = 22) shows that the low-temperature

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setup (5°C) is not a threshold for production of acoustic signals and general activity of the adult

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species. This temperature is 10°C lower than that at which mass swarming of beetles occurs in

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the region of invasion (Kerchev, 2014). Thus, acoustic signals are the first way for bark beetles

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to communicate at the imago stage, and it probably retains priority significance until feeding on

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the tissues of a fresh host tree.

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We assume that collective stridulation of males after wintering may serve as a signal to

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the colony beneath the bark that the environmental temperature has reached values that are

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suitable for dispersal flight, or as a signal for females to emerge from the brood tree.

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A dramatically reduced number of stridulating males at 35°C also indicates that this

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temperature is above the optimum condition limits. In the field, P. proximus avoids colonizing

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sides of the tree trunk that can be exposed to the direct sunlight.

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Although none of the tested males that were released into the arena were under the

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protection of their nest or behaving as if to attack a stranger, the characteristics of their signals

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(except for syllable parameters) were similar in terms of temporal parameters to the signals of

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the rivalry or aggression context (Kerchev, 2019). Probably a necessary condition for male

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stridulation in the context of courtship is the presence of aggregation pheromones, the production

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of which was excluded by the design of the experiment.

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Application of the acoustic or vibrational signals in addition to semiochemicals to disrupt

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the mechanisms of transmission or perception of intraspecific signals is a developing area of pest

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control (Mazzoni et al., 2018). This approach, as well as methods for identifying wood boring

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pests by species-specific signals (Mankin et al., 2008), requires a better understanding of the

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signal parameters depending on variations in environmental factors, and experimental studies

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can significantly increase our knowledge of these patterns. This will ultimately lead to increased

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effectiveness of their practical application.

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Conclusions Temporal characteristics of acoustic signals that are produced by P. proximus are temperature dependent.

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Temperature affects the production of acoustic signals by P. proximus through changes in

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motility during stridulation, as evidenced by the altered signal characteristics that are dependent

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on the frequency of insect movements.

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These results made it possible to establish several patterns in the temperature dependence

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of acoustic signaling in bark beetles, which might be universal for species with different types of

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stridulation. However, for other genera, and possibly for species within the genus Polygraphus,

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tendencies and the dependence on temperature effects can be different and may require an

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individual approach to target various species.

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Acknowledgements:

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The author owes an immense gratitude to the assistant Julia A. Tsoi for conducting laboratory

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recordings. This research was supported by the Russian Science Foundation (17-74-10034).

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Zhantiev R.D., and Korsunovskaya O.S., 2014. On recognition of sound communication

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signals in bush crickets (Orthoptera, Tettigoniidae). Entomol. Rev. 94(6), 815–819.

336

https://doi.org/10.1134/S0013873814060025

337 338 339 340

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341 342

Table 1. The results of the analysis of variability of the signal parameters in Polygraphus proximus males depending on temperature. Parameter

343 344

(N)

W

H-test

(r`-values)

(Z`-values)

Inter syllable interval

283

0.14

146.14*

Syllable duration

283

0.5

46.46*

Number of chirps/ syllable

283

0.31

14.3

Chirp rate

278

0.95

176.97*

Chirp duration

277

0.80

114.98*

Inter chirp interval

276

0.89

159.20*

Tooth-strikes/ chirp

274

0.09

12.8

Intertooth-strikes interval

276

0.85

122.96*

*p<0.001, without asterisk – insignificant. In the column H-test the Z-factor values (measure of statistical effect size) are given.

345 346 347 348 349 350 351 352 353 354 355 356 357 358

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Figure legends:

359 360 361

Fig. 1. The experimental set inside thermostat for registration of Polygraphus proximus

362

signals during male-female interactions (A – condenser microphone in glass tube, B – the arena

363

with beetles inside marked by arrows).

364 365 366

Fig. 2. The graphical descriptions of temporal parameters of stridulatory signals in the four-eyed fir bark beetle measured in this study

367 368

Fig. 3. Temporal characteristics of simple chirps during male-female interactions under

369

tested temperature settings: A. – inter syllable interval; B – the number of chirps per syllable; C–

370

chirp rate; D – chirp duration; E – inter chirp interval; F – number of tooth-strikes; G –

371

intertooth-strikes interval; H – syllable duration.

372 373 374 375

15

376

16

377

378

379

Highlights 17

380 381 382



Stridulation is first way of communication between individuals of bark beetles occurring at the imago stage.

383 384



Temporal parameters of P. proximus acoustic signals are temperature-dependent.

385 386 387



Among the analyzed characteristics of P. proximus signals a high correlation were between temperature and the chirp rate

388 389 390



Presence of females in limited area not inside entrance hole provokes producing of a rivalry signaling by males.

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18