Behaviour 161 (2020) 15e22

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Animal Behaviour

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Seismic noise influences brood size dynamics in a subterranean with biparental care

* Mia E. Phillips a, b, c, , Gabriela Chio a, Carrie L. Hall a, Hannah M. ter Hofstede b, c, Daniel R. Howard a a Department of Biological Sciences, University of New Hampshire, Durham, NH, U.S.A. b Department of Biological Sciences, Dartmouth College, Hanover, NH, U.S.A. c Graduate Program in Ecology, Evolution, Environment and Society, Dartmouth College, Hanover, NH, U.S.A. article info Anthropogenic noise pollution is known to alter the behaviour of acoustically sensitive . Many fi Article history: animals also sense vibrations through solid substrates and use substrate-borne vibrations in conspeci c Received 8 July 2019 communication. The effects of substrate-borne noise pollution, however, remain largely unknown. Here, Initial acceptance 19 September 2019 we investigate the potential for seismic (soil-borne) noise to alter the reproductive behaviour of the Final acceptance 1 November 2019 burying Nicrophorus marginatus, a species that breeds below the soil surface on vertebrate car- casses and provides biparental care to offspring. Nicrophorus marginatus produce sound using MS. number: A19-00466R stridulatory structures on the elytra and abdomen, but no ears have been identified in these beetles, suggesting that stridulation might function to produce substrate-borne signals. We examined the timing Keywords: of stridulation during reproduction, measured neural responses of beetles to substrate-borne vibrations, anthropogenic noise and measured beetle reproduction in the presence and absence of seismic noise. We found that parental Coleoptera beetles stridulate throughout carcass preparation and the burial process and confirmed that adult beetles communication Nicrophorus are sensitive to low-frequency seismic vibrations. Variables related to brood size were affected in parental care treatments with seismic noise, with burying beetles producing smaller broods with lower total mass vibration than those in control treatments, providing support for the hypothesis that substrate-borne noise may impose fitness costs for soil-dwelling animals. The precise mechanisms leading to reduced brood size remain unknown but may relate to disruption of seismic communication or inaccurate assessment of resource size. Additional investigations are required to understand the degree to which human- generated seismic noise in natural settings influences other edaphic species, and whether these behavioural impacts lead to shifts in edaphic community structure or function. © 2019 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Noise is present in all environments and is a ubiquitous obstacle (anthrophony), which can differ in temporal and spectral structure faced by acoustically sensitive animals (Brumm & Slabbekoorn, from natural sources of noise, can constrain animal communication 2005; Forrest, 1994; Morton, 1975; Wiley, 2017; Wiley & by introducing a novel impediment to the senderereceiver dyad Richards, 1978). Environmental noise generally disrupts animal (Bee & Swanson, 2007; Halfwerk & Slabbekoorn, 2015; Ortega, communication by masking signals or distracting receivers (Chan, 2012). Behavioural plasticity may allow some animals to cope Giraldo-Perez, Smith, & Blumstein, 2010; Morris-Drake, Kern, & with noise pollution in the short term, but the rapid emergence of Radford, 2016; Purser & Radford, 2011; Romer,€ Bailey, & Dadour, anthropogenic noise across most landscapes has afforded little time 1989; Walsh, Arnott, & Kunc, 2017; Wollerman, 1999). Disruptive for less plastic animals to adapt (Rabin & Greene, 2002; Sih, Ferrari, noise imposes selective pressure on senders to optimize signalling & Harris, 2011). If the noise source is especially intense or chronic, it behaviour, and on receiver behaviour and sensory systems to may eventually lead to fixed behavioural changes, population de- effectively extract signals from noise (Ryan & Brenowitz, 1985; clines or changes in community composition (Barber, Crooks, & Slabbekoorn & Peet, 2003). Noise produced by humans Fristrup, 2010; Francis, Ortega, & Cruz, 2009). Most attention devoted to understanding anthropogenic noise effects on animal behaviour has focused on the influence of * Correspondence: M. E. Phillips, Department of Biological Sciences, Dartmouth airborne or waterborne sound (reviewed in Ortega, 2012; Shannon College, 78 College Street, Hanover, NH, 03755, U.S.A. et al., 2016; Slabbekoorn et al., 2010). Many animals, however, rely E-mail address: [email protected] (M. E. Phillips). https://doi.org/10.1016/j.anbehav.2019.12.010 0003-3472/© 2019 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 16 M. E. Phillips et al. / Animal Behaviour 161 (2020) 15e22 on substrate-borne vibrations as a primary source of information end of this range (Kurzweil, 1979; Roberts et al., 2017; Saccorotti (Hill, 2008, 2009; Narins, Lewis, Jarvis, & O’Riain, 1997; ter et al., 2011), so we tested the hypothesis that substrate-borne Hofstede, Schoneich,€ Robillard, & Hedwig, 2015; Warkentin, vibrational noise acts as a physiologically salient disturbance. 2005). This taxonomically diverse group is especially adept at Noise disturbance could alter the carcass burial process or disrupt sensing vibrations in their environment (Cocroft & Rodríguez, parental care behaviour, resulting in perturbations to brood size 2005; Devetak & Amon, 1997; Finck, 1981; Salmon & Horch, and structure. We compared the carcass handling behaviour and 1973; Cokl, 1983) and like animals that have evolved to extract fecundity of beetles that bred in experimentally induced seismic information from airborne signals in noisy environments, may be noise environments to that of beetles that bred in silent controls, pre-adapted to cope with natural forms of substrate-borne noise predicting that beetles breeding in noisy environments would take (Barth, Bleckmann, Bohnenberger, & Seyfarth, 1988; McNett, Luan, longer to bury carcasses and have fewer offspring. & Cocroft, 2010; Tishechkin, 2007). Many human enterprises pro- duce intense vibrations in the ground, including transportation, METHODS construction and energy production (Kurzweil, 1979; Roberts et al., 2017; Saccorotti, Piccinini, Cauchie, & Fiori, 2011). We know very Animal Collection and Care little, however, about how these anthropogenically produced vi- brations affect the behaviour of animals that live at or below the soil Adult N. marginatus beetles were captured at the Nature Con- surface (Morley, Jones, & Radford, 2014; Raboin & Elias, 2019; servancy's Tallgrass Prairie Preserve in Osage County, Oklahoma, Roberts et al., 2015, 2016). U.S.A. (365004600N, 962502300W) in July of 2017. The beetles were The behavioural biology of nicrophorine burying beetles sug- held in sex-segregated aquaria and transported to the laboratory at gests that substrate-borne vibration may play a key role in their life The University of New Hampshire (Durham, NH, U.S.A.). In the history. Burying beetles are necrophilous scavengers that exhibit laboratory, the beetles were housed in aquaria with moist peat biparental care: both parents cooperate to bury the carcass of a moss and provided raw meat (pork) and access to water ad libitum. small vertebrate, rear their larval brood below the soil surface on Beetles were kept in a temperature-controlled vivarium set at 23 C the sequestered food resource (Eggert, Reinking, & Müller, 1998; and 45% RH, with a 14:10 h light:dark cycle. Fetherston, Scott, & Traniello, 1990; Milne & Milne, 1944, 1976; Scott, 1998a) and manipulate brood size and structure to opti- Use of Stridulatory Signals during Reproduction mize fitness in competitive environments (Woelber, Hall, & Howard, 2018). Burying beetles produce sound using stridulatory We observed whether N. marginatus parental adults produced structures on the elytra and abdomen, and these signals are stridulatory signals during carcass burial and, if so, at what time thought to play an important role in courtship, carcass burial and points by recording carcass burial behaviour (N ¼ 8 pairs) using a parental care (Bredohl, 1984; Darwin, 1871; Hall et al., 2013, 2015; sound-triggered image capture preparation. Maleefemale Huerta, Halffter, & Fresneau, 1992; Lane & Rothschild, 1965; Milne N. marginatus pairs were provisioned with a single quail carcass & Milne, 1944, 1976; Niemitz, 1972; Niemitz & Krampe, 1972; (122.72 ± 9.8 g; RodentPro.com, Evansville, IN, U.S.A.) placed in a Pukowski, 1933; Schumacher, 1973). The exact role of these sig- 7.57 l plastic bucket filled with 20.0 cm of moistened peat substrate. nals remains poorly understood, but burying beetles that are pre- Positioned above the carcass was a Sennheiser ME 66 supercardioid vented from stridulating are known to exhibit reductions in brood phantom-powered microphone (Sennheiser electronic GmbH & Co. size (Hall et al., 2015; Huerta et al., 1992). It has also been suggested KG, Wedemark, Germany) attached to a Tascam DR100 MK3 digital that the parents stridulate to ‘call’ larvae towards the carcass audio recorder (TEAC Corporation, Montebello, CA, U.S.A.), which feeding site upon emergence from the asynchronously hatching was set to auto-record each time sound was detected above a fixed eggs (Niemitz & Krampe, 1972; Pukowski, 1933). Stridulation pro- threshold (44 dB recorder setting; ~45 dB SPL ambient). This duces both airborne sound and substrate-borne vibration (Hall chosen decibel level was approximately 1.5e2.0 dB SPL above the et al., 2013), and while tympanal hearing organs have been ambient noise floor, and the setting detected stridulations when described in two beetle families (Cicindelidae: Spangler, 1988; beetles were both above and below the soil surface. Five-second Scarabaeidae: Forrest, Read, Farris, & Hoy, 1997), auditory struc- audio recordings were captured at a sample rate of 16 bits/ tures have yet to be identified in any of the Nicrophorus species (C. L. 44.1 kHz and saved to an SD card as time-coded and sequentially Hall, personal observation). This lack of clear airborne sound re- numbered PCM WAV files. A line output cable from the audio ceptors suggests that the substrate-borne vibration produced by recorder was attached to a Cognisys Stopshot high-speed photog- stridulation may carry relevant information through the soil sub- raphy controller (Cognisys Inc., Traverse City, MI, U.S.A.), which strate rather than through the air. If stridulation produces soil- controlled image acquisition in a Sony RX10 III DSLR camera fitted borne (seismic) vibrational signals that function to facilitate coop- with a Zeiss Vario-Sonnar F2.4-4 large aperture 24e600 mm lens erative carcass burial and/or parental care, then seismic noise positioned directly above the breeding container to capture 20.1 pollution could alter the reproductive behaviour and ultimately megapixel images of breeding behaviour in the region of interest impose fitness costs in these soil-breeding animals. inside the container. Accordingly, each time the microphone Here, we examined the sensitivity to substrate-borne vibration detected and recorded a beetle stridulation from the preparation, in the Nicrophorus marginatus, and asked whether the camera was triggered to capture a single time-coded and this sensitivity leaves them vulnerable to seismic noise. We first sequentially numbered still image that could then be cross- examined the use of stridulatory signals during carcass burial, then referenced to an audio recording for purposes of evaluating strid- tested for vibrational sensitivity in adult burying beetles using ulation time points and beetle spatial position at the time of sound extracellular physiological techniques, focusing on the response to production. Each breeding container was recorded from the time substrate-borne vibration receptors found in the leg. Other the maleefemale beetle pair was introduced to the container until (Cocroft & Rodríguez, 2005), including other beetles (Breidbach, the carcass was completely buried. Stridulations were quantified in 1986; Takanashi, Fukaya, Nakamuta, Skals, & Nishino, 2016), are each 5 s recording by manually counting individual pulses from sensitive to low-frequency vibrations; therefore, we expected spectrograms using Adobe Audition v.3.0 (Adobe Systems Incor- Nicrophorus leg responses to be broadly tuned to vibrations below porated, San Jose, CA, U.S.A.), and identifying their production time 1000 Hz. Anthropogenic seismic noise typically falls at the lower during the burial sequence (h:min:s). As total burial times varied M. E. Phillips et al. / Animal Behaviour 161 (2020) 15e22 17 across the eight breedings, we assigned percentiles to sound pro- comparing the amplitude of compound action potentials occurring duction time points to standardize the overall time sequence of before each pulse train (background activity) with those occurring stridulatory recordings (0e1) and used the captured images to during each pulse. Neural activity was coded as a response to the assess behaviour and to construct a time-lapse video of carcass vibrational stimulus if it exceeded 2.0 SD above the average back- preparation and burial. We then created a contour plot of the ground activity level, with detection thresholds for each frequency number of stridulatory signals produced during carcass burial to identified when response activity exceeded the signal-to-noise gauge the temporal pattern of sound production during carcass ratio (S:N) parameter in at least three of the five pulses in the burial in N. marginatus. stimulus train. The lowest intensity (mm/s) to meet this criterion was considered to be the detection threshold for each tested Sensitivity to Substrate-borne Vibration frequency.

We recorded the neural activity of 10 female N. marginatus Behavioural Responses to Seismic Noise beetles while exposing them to substrate-borne vibrations. Nicro- phorus marginatus is not sexually dimorphic and, like other burying To produce a substrate-borne noise condition for behavioural beetles, both sexes stridulate, producing signals of similar acoustic trial, we synthesized a vibrational .wav file (44.1 kHz sampling rate, structure (Hall et al., 2013). Therefore, we concluded that it was 16 bits/sample) stimulus in Adobe Audition v.3.0 with a pulse unlikely that males and females would have substantially different duration of 500 ms and an interpulse interval of 700 ms, producing vibration detection thresholds. a stimulus presentation of 0.833 pulses/s. We selected an inter- To collect neural response to substrate-borne vibration, beetles mittent rather than continuous stimulus to represent the rhythmic were placed dorsal side up on a plastic block and fixed with a low- temporal pattern of anthropogenic noise sources such as rotating temperature wax. Each beetle was positioned so that the right wind turbines and oil/gas pumps. Temporal patterns were hindleg could move freely, and the tibia and tarsi were then fixed approximated from data presented in Hubbard and Shepherd with wax to the end of a stainless steel 10e32 threaded rod (1991). To synthesize stimuli, we used an FFT filter (25e300 Hz attached to an electromagnetic mini-shaker (KCF ESO20, KCF band-pass) on brown noise in Adobe Audition v.3.0, to encompass Technologies, State College, PA, U.S.A.). The leg was bent at the both the frequency range of anthropogenic substrate-borne noise femuretibia joint to approximate a natural position when standing sources and the hypothesized sensitivity range of the beetle's on the soil or carcass substrate, with the recording preparation sensory system (Saccorotti et al., 2011). We looped the stimulus assembled on a Vision Station PG4 vibration isolation table inside a continuously via a digital music player (Sansa Clipþ, Western copper Faraday cage (Newport Corporation, Irvine, CA, U.S.A.). Digital Technologies, Inc., Milpitas, CA, U.S.A.), with the signal Stimuli for presentation during neural tests were created in amplified by a Dayton Audio MA1260 12-channel amplifier (89 W Adobe Audition v.3.0, and consisted of a train of five 500 ms pure- per channel at 4 U; Dayton Audio, Springboro, OH, U.S.A.) con- tone frequency pulses (16 bits/44.1 kHz WAV format), spaced 1.0 s nected to an Aurasound AST-2B-4 Pro Bass Shaker (Aurasound, Inc., apart. The right hindleg of each beetle was vibrated at 17 fre- Santa Ana, CA, U.S.A.). Each shaker was permanently affixed with quencies at third octave-band intervals (19, 23.6, 30, 37.5, 47.5, 60, four attachment bolts to a 15.14 l breeding container (US Plastics 75, 95, 118, 150, 190, 236, 300, 375, 475, 600, 750 Hz). The order of Corporation, Lima, OH, U.S.A.), positioned over a 10 cm circular frequencies presented was randomized for each beetle. Files were opening on the side of the container that was covered with two played back in Avisoft Recorder software (Avisoft Bioacoustics, layers of 4 mil PVC sheathing to create a waterproof but flexible Glienicke, Germany) connected to a NI-DAQmx data acquisition soil-transducer contact surface. Each container was filled to a depth board (National Instruments, Austin, TX, U.S.A.) with the mini- of 25 cm with a 1:1 mixture of peat moss and loam soil from a local shaker driven by a two-channel amplifier (SLA1, Applied Research nursery (Stratham Circle Nursery, Stratham, NH, U.S.A.). and Technology, Niagara Falls, NY, U.S.A.). Vibrational intensity was Shakers were driven to the maximum output level of the calibrated prior to and measured during playback with a Polytec amplifier, and the vibrational intensity in each breeding container PDV-100 laser Doppler vibrometer (LDV; Polytec GmbH, Wald- was measured using a Polytec PDV-100 laser Doppler vibrometer bronn, Germany) connected to a Tektronix TDS2024C oscilloscope connected to a Tektronix TDS2024C oscilloscope. Soil surface vi- (Tektronix, Inc., Beaverton, OR, U.S.A.). The laser was focused on a bration measurements were taken sequentially from the reflective piece of reflective tape attached to the horizontal attachment rod, surface of brass thumbtacks inserted flush with the surface at nine ~5 mm from the leg attachment point. positions across the exposed substrate of the breeding preparation. Two extracellular 0.172 mm diameter tungsten electrodes (A-M Vibrational velocity measurements (mm/s) were measured at each Systems, Sequim, WA, U.S.A.) were placed in the anterior side of the sampling point, and mean seismic velocities were calculated for beetle femur: one in the proximal femur, near the coxa, and a each container (mean ¼ 6.38 ± 0.8 mm/s). This level of amplifica- reference electrode in the distal femur. Since the vibration-sensitive tion achieved vibrational intensities comparable to those employed organ in N. marginatus is unknown, this electrode placement was by Tsubaki, Hosoda, Kitajima, and Takanashi (2014) and Takanashi sufficient to detect neural responses throughout the leg, regardless et al. (2016) in behavioural experiments with cerambycid beetles. of the exact position of the organ. Voltage signals from the electrodes Breeding containers lacking the vibrational stimulus but replicated were amplified by a microelectrode AC amplifier (Model 1800; A-M in all other parameters were set up as controls. Systems, Sequim, WA, U.S.A.), and recorded as one channel of a Within each breeding container, we placed one female and one stereo .wav file, paired with the synced signal from the LDV as the male N. marginatus adult on top of a single quail carcass. We then second channel, in Avisoft Recorder software via the NI-DAQmx. To measured parental reproductive behaviour and reproductive suc- find detection thresholds at each frequency, we presented pulses of a cess by quantifying the following variables: (1) latency to initiate single frequency at intensities just above the ambient noise floor and carcass burial (h), (2) duration of burial from start to completion increased intensity until neural activity was observed in response to (h), (3) total time to burial (latency þ duration, h), (4) number of all pulses. Beetles that underwent electrophysiological recording offspring (late-instar-dispersing larvae), (5) brood mass (g), (6) were immediately euthanized via freezing after the experiment. mass per larva (g; brood mass/number of offspring). Recordings were analysed in Adobe Audition v.3.0, with neural Once parents were placed in each container, we performed vi- responses to substrate-borne vibrational stimuli determined by sual checks every 0.5 h and measured the progress of carcass burial. 18 M. E. Phillips et al. / Animal Behaviour 161 (2020) 15e22

We stopped recording carcass handling behaviour once the quail 35 was completely buried. If beetle pairs failed to bury the carcass after 24 h, they were removed from the container and the process was 30 restarted with a fresh carcass and new maleefemale beetle pair. Since some burying beetle reproductive behaviours and brood 25 dynamics can be influenced by carcass size variation (Trumbo, & fi 1990b; Wilson Fudge, 1984), we rst tested for correlations be- 20 tween carcass mass and our measured variables. For variables fi found to exhibit a signi cant linear relationship with carcass mass, 15 we saved the residuals of these regressions for use in subsequent analyses. We then standardized the values for all data and ran a 10 principal component analysis (PCA) on the six measured variables (or their residuals). PCA was used to reduce the dimensionality of a Percentage of stridulations Percentage 5 data set that contained correlated variables (e.g. offspring number and brood mass, latency and total burial time), reducing the 0 severity of Bonferroni correction and allowing us to identify broader categories of variables influenced by the vibration treat- 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1 ment. Standardized residuals for total offspring and offspring mass Burial time (std.) were used, but latency to initiate burial, although correlated with carcass mass, remained persistently resistant to transformation to Figure 2. Temporal pattern of stridulations produced by N. marginatus parents during achieve normality and thus standardized raw data were used in cooperative carcass burial. Burial time was standardized and binned by one 10th of the total time. Each pair of parental burying beetles is represented by a different colour, for PCA analyses. We retained principal components (PCs) with ei- both data points and line of best fit, with mean values for the data set fitted with a genvalues at or near 1.0, and subsequently tested these PCs for dashed black line. differences between control and treatment using a Wilcoxon rank- sum test, two-sample normal approximation, with a Bonferroni correction of our alpha value to account for multiple comparisons. Sensitivity to Substrate-borne Vibrations All analyses were carried out in RStudio v.1.0.136 (RStudio, Boston, MA, U.S.A.) and JMP Pro v.13 (SAS Institute Inc., Cary, NC, U.S.A.). We recorded the neural response of 10 female N. marginatus adults across 17 third octave-band frequencies between 19 Hz and 750 Hz. In five instances, threshold amplitudes could not be measured at a particular frequency due to limitations in the output RESULTS of our equipment or to excess noise in the recording (95 Hz, 190 Hz, 600 Hz (N ¼ 2) and 750 Hz). In all other cases, we documented Use of Stridulatory Signals during Reproduction neural responses to substrate-borne vibration at all tested fre- quencies. Average detection thresholds were below 10 mm/s for all We observed stridulatory signal production during all eight frequencies presented, with highest sensitivities associated with breeding trials (mean ± SE ¼ 769.6 ± 123.6 stridulation signals/ those frequencies between 19 Hz and 200 Hz (Fig. 3). Thresholds burial), with wide variation in the range of total stridulations tended to increase with frequency, suggesting a sensory system recorded during carcass burial (range 216e1341; Fig. 1). Carcass bias towards lower-frequency stimuli. burial times varied widely as well (mean ± SE ¼ 6.89 ± 1.21 h; range 212e815 min). Most stridulations produced by parental Behavioural Responses to Seismic Noise beetles occurred during the first half of the carcass burial process (Fig. 2), when most copulatory behaviour is thought to occur in this Nicrophorus marginatus parents took on average 2.5 ± 2.8 h to species. begin carcass handling behaviours after introduction to breeding trials (N ¼ 48). Parents then invested an average of 7.6 ± 3.3 h burying the carcass, with a mean total carcass handling time of 20 10.2 ± 4.2 h. Nicrophorus marginatus parents produced an average of 41.1 ± 14.5 offspring per brood, with the average total brood 15 mass of 27.2 ± 7.8 g (average mass per larva across the 48 breedings ¼ 0.68 ± 0.1 g). While all N. marginatus parental pairs 10 buried carcasses irrespective of breeding treatment, we detected differences in brood structure between control (N ¼ 24) and ¼ 5 treatment (N 24) conditions (Table 1). We extracted three principal components from the standardized

Frequency (kHz) 0 reproductive data using PCA and incorporated these PCs in a comparison of control and treatment conditions (Table 2). PC1 described general brood structure, loaded by data related to offspring number and mass, and captured 40.68% of the variation 012345 from the original data set. PC2 described carcass handling costs, Time (s) loaded by metrics of burial time and total carcass handling time, and captured 31.47% of the variation in the data set. PC3 described Figure 1. Spectrogram (top) and waveform (bottom) of the airborne component of the latency to begin burial of the carcass after the trial began and stridulatory signals produced by N. marginatus parents during carcass burial. Pulses of captured 16.59% of the variation in the original data. Overall these sound are produced as beetles move a set of stridulatory files located on the dorsal side of the abdomen across a pair of scrapers located on the underside of the hardened three principal components explained 88.75% of the variation in the elytra. original data. The values for PC1 differed between control and M. E. Phillips et al. / Animal Behaviour 161 (2020) 15e22 19

20 (a)

15

10

5 Amplitude (mm/s)

0 0 200 400 600 (b) 100 ) 2 75

50

25 Amplitude (m/s 0

0 200 400 600 Frequency (Hz)

Figure 3. Vibration sensitivity thresholds of 10 female burying beetles across 17 frequencies. The median threshold curve is shown in black. Threshold data are shown in units of velocity (a) and acceleration (b). Threshold amplitudes were not achieved at five points (see Results). vibration conditions (Wilcoxon rank-sum test: S ¼ 764, Z ¼ 3.62, explanation for sound production in the group, although the role of P ¼ 0.001; Fig. 4), while neither PC2 (S ¼ 668, Z ¼ 1.64, P ¼ 0.303; these stridulatory signals in facilitating cooperative carcass burial Fig. 4) nor PC3 (S ¼ 479, Z ¼2.24, P ¼ 0.076; Fig. 4) differed be- deserves additional study. Given that burying beetles putatively tween the two treatments. lack auditory organs to detect airborne sound, it is feasible that the sound produced via stridulation serves a role in interspecific DISCUSSION communication, whereas the substrate-borne component trans- mitted through the substrate and detected via mechanoreceptors in The production of stridulatory signals appears to be linked to the receiver's legs acts as the salient intraspecific signal. If so, then cooperative carcass burial behaviours in N. marginatus burying substrate-borne vibrational noise, depending upon its spectral beetles. We observed beetle parents producing large but variable characteristics and intensity, may act as a masking agent that im- amounts of stridulatory sound from the earliest stages of carcass pairs information transfer between parents. preparation and burial, generally while positioned atop the carcass We found that adult N. marginatus burying beetles are sensitive or soil substrate adjacent to the carcass, until the carcass was to low-frequency (19e750 Hz) substrate-borne vibrations at am- completely buried. Pairs also stridulated during copulation, which plitudes often less than 1 mm/s. This spectral sensitivity range is generally occurred early in the carcass handling process and may consistent with the behavioural responses to vibration documented explain the increased density of recorded sound early in the burial in the Japanese pine sawyer beetle, Monochamus alternatus sequence. Hall et al. (2013) previously described stridulation in the (Takanashi et al., 2016). Similarly, the leaf-dwelling cerambycid species during handling that simulated a predatorial attack, but our beetle fortunei exhibited its highest behavioural sensi- findings represent the first recorded observations of stridulatory tivity to substrate-borne vibration at 75e500 Hz (Tsubaki et al., sound produced by burying beetles during reproduction. Interest- 2014). In both studies the behaviours measured were startle and ingly, Darwin (1871) speculated that the sound produced by freeze responses, with the observed response thresholds much nicrophorine burying beetles represented a sexual signal, and here higher than those we measured at the putative sensory organ in we report evidence that supports in part this functional N. marginatus. In our behavioural trials, burying beetles buried

Table 1 Mean ± SD of variables measured in control and vibration treatment conditions in trials with N. marginatus parents

Control Vibration Carcass mass correlation

Latency to begin burial (h) 2.05 ± 2.72 3.02 ± 2.92 r ¼ 0.285, P ¼ 0.049 Burial duration (h) 6.23 ± 1.64 9.03 ± 3.84 r ¼ 0.149, P ¼ 0.313 Total burial time (h) 8.29 ± 2.84 12.05 ± 4.61 r ¼0.077, P ¼ 0.604 Offspring number 46.21 ± 13.96 35.92 ± 13.48 r ¼ 0.341, P ¼ 0.018 Brood mass (g) 30.48 ± 6.45 23.91 ± 7.76 r ¼ 0.468, P < 0.001 Mass per larva (g) 0.68 ± 0.10 0.68 ± 0.11 r ¼ 0.077, P ¼ 0.602 N 24 24 48

Pearson correlation coefficients between each variable and carcass mass are shown, with significant correlations shown in bold. Residuals were used for these variables in subsequent analyses (see Methods). 20 M. E. Phillips et al. / Animal Behaviour 161 (2020) 15e22

Table 2 parental care behaviours take place underground and are not easily Loading matrix from a principal component analysis (PCA) of the measured repro- measured (Milne & Milne, 1976). If parent beetle stridulations are ductive variables utilized as vibrational signals during parental care, it is possible that PC1 PC2 PC3 seismic noise could disrupt signal transmission and impair infor- Number of offspring 0.891 0.407 0.154 mation exchange, leading to suboptimal brood care and offspring Total brood mass (g) 0.847 0.217 0.257 production, as observed in eastern bluebirds, Sialia sialis, exposed Mass per larva (g) 0.546 0.516 0.077 to airborne noise during reproduction (Kight, Saha, & Swaddle, Latency to bury (h) 0.528 0.361 0.764 2012). Preliminary data from recordings of substrate-borne vibra- Burial duration (h) 0.245 0.768 0.555 Total burial time (h) 0.514 0.830 0.085 tions produced by stridulation suggest that the dominant fre- % Variance explained 40.68 31.47 16.59 quency of the signal lies somewhere below 600 Hz (M. E. Phillips, Cumulative % 40.68 72.15 88.75 personal observation), and our neurophysiological recordings PC1 represented brood structure, PC2 represented carcass handling time, and PC3 confirm that the beetles are sensitive to frequencies in this range. represented latency to begin carcass burial. Thus, seismic noise conditions may have partially masked these signals, leading to the disruption of parental communication, which in turn could result in fewer eggs produced, lower hatching rates carcasses and were able to reproduce in conditions with vibrational and/or lower larval survivorship, as observed in nesting house noise levels comparable to those in which Takanashi et al. (2016) sparrows, Passer domesticus (Schroeder, Nakagawa, Cleasby, & and Tsubaki et al. (2014) observed startle and freeze responses in Burke, 2012), and blue tits, Cyanistes caeruleus (Lucass, Eens, & cerambycid beetles. While we did not observe obvious behavioural Müller, 2016), exposed to anthropogenic airborne noise. Alterna- changes in response to seismic noise, burying beetle parents tively, seismic noise could have disrupted communication between fi incurred signi cant reproductive costs, producing broods with parents and offspring, as burying beetles are known to stridulate fewer offspring and lower overall brood mass (Table 1). Average throughout the parental care process, and have been suggested to mass per individual larva remained unchanged between treat- ‘call’ larvae to the carcass resource (Niemitz & Krampe, 1972; ments, which further suggests that reduced mean brood mass may Pukowski, 1933). Future experiments using a similar set-up could fi simply relate to producing fewer offspring. While not signi cant, help pinpoint the time at which seismic noise affects reproductive we did observe a pattern of slightly longer latency to initiate carcass output. Presentation of seismic noise during either carcass burial or burial in vibration treatments, and thus some dimensions of after larval hatching could show whether the noise affected fl N. marginatus burial behaviour may be in uenced by seismic parental communication or parenteoffspring communication, disturbance. Other animals have been shown to change their respectively. Alternatively, manipulation of parental presence dur- behavioural patterns in response to anthropogenic noise (Gross, ing noise presentation could isolate the effects of interparent & & Pasinelli, Kunc, 2010; Sih et al., 2011; Slabbekoorn Peet, communication, as broods can be reared successfully by a single fi 2003), although the associated tness costs are rarely docu- parent (Fetherston, Scott, & Traniello, 1994; Scott, 1998b). Charac- & mented (Read, Jones, Radford, 2014). Here we have demonstrated terization of the soil-borne vibrations produced by burying beetle that even in the absence of observable behavioural change, stridulation and exploration of the function of stridulation during fi anthropogenic noise can negatively affect animal tness. parental care will shed further light on these results. Although overall carcass handling time remained relatively Seismic noise may also affect parental infanticide behaviour. unchanged in conditions of seismic noise, the reduction in brood Parental burying beetles adjust the size of their broods through size and brood mass could have resulted from disruption to below- facultative infanticide during the first through the third larval instar ground parental care behaviours. In nicrophorine burying beetles, (Bartlett, 1987; Oldekop, Smiseth, Piggins, & Moore, 2007; Trumbo, 2006), presumably as an adaptation to fluctuating environmental conditions (Glass, Holt, & Slade, 1985; Trumbo, 1990a). This Control behaviour is thought to be related to resource utilization such that 4 surviving larvae reach dispersal at an optimal size (Bartlett, 1987). Vibration Burying beetles assess the volume of the carcass resource prior to * reproduction (Trumbo & Fernandez, 1995), and they appear to make brood size decisions based on initial assessment of carcass 2 size (Trumbo, 1990a, 1990b, 1992; Bartlett & Ashworth, 1988; Nagano & Suzuki, 2007; Scott & Traniello, 1990) along with other environmental cues related to food availability and conspecific 0 competition (Woelber et al., 2018). Seismic noise may have dis- PC value rupted the parent beetles’ ability to properly assess carcass size, leading to an increase in larval culling and underproduction of offspring. Other insects, like Trichogramma parasitoid wasps, also –2 vary offspring number based on resource size (Klomp & Teerink, 1962). Parent wasps are thought to track the amount of time it takes to circumnavigate the host as a way to assess host size & PC1 PC2 PC3 (Schmidt Smith, 1987). The mechanism Nicrophorus beetles use to assess resource size is not entirely clear, but seismic noise may Principal component perturb the fine-scale mechanosensory elements of resource Figure 4. Box plots comparing median, upper and lower quartile values, and data assessment via a sensory pollution process. Additional experiments ranges between values of PC1, PC2 and PC3 for control (N ¼ 24) and vibration (N ¼ 24) examining the direct effect of seismic noise on culling behaviour treatments. PC1 represented general brood structure, loaded by metrics of offspring are needed to assess the possibility that noise may drive increased number and mass. PC2 represented carcass burial timing, loaded by metrics of burial parental infanticide. duration and total time to carcass burial. PC3 loaded mostly by latency to begin carcass burial. Asterisk indicates a significant difference between treatments at an alpha level Alternatively, seismic noise may have resembled a predator cue of 0.01. to the beetles. Burrowing insectivorous mammals are known to M. E. Phillips et al. / Animal Behaviour 161 (2020) 15e22 21 produce vibrations in the ground, and these vibrations have been with research supported by the U.S. Department of Agriculture shown to elicit antipredator behaviour in earthworms (Catania, National Institute of Food and Agriculture Hatch Project NH00646. 2008). If the seismic noise presented in our experiment was Additional funding was provided by the Animal Behavior Society perceived as a threatening cue, parent beetles may have altered via a Student Research Grant to M.E.P. In-kind support was pro- their behaviour in ways that reduced reproductive output. vided by the Dartmouth College Department of Biology, the Uni- Attempting to flee in response to vibrations may have temporarily versity of New Hampshire, and The Nature Conservancy (TNC). We disrupted parental care behaviours. As evidenced in Takanashi et al. thank Dr Peggy Hill for her expert assistance and Bob Hamilton for (2016) and Tsubaki et al. (2014), cerambycid beetles will startle or access to the TNC field site, which is located on the traditional lands freeze in response to discrete pulses of substrate vibrations. Simi- of the Wazhazhe (Osage) and Oceti Sakowi s (Sioux) people. Field larly, vibrational predator cues have been shown to elicit freezing and lab assistance were provided by Jasmine Buteau, Abbie behaviours in wolf spiders, preventing them from expressing Dempsey, Sarah Dodgin, Emily Dunlop, Tim Golden, Stacey Han- courtship displays (Lohrey, Clark, Gordon, & Uetz, 2009). 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