Animal Behaviour 161 (2020) 15e22 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav Seismic noise influences brood size dynamics in a subterranean insect 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 animals. 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 beetle Nicrophorus marginatus, a species that breeds below the soil surface on vertebrate car- casses and provides biparental care to offspring. Nicrophorus marginatus beetles 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