Field assessment of behavioural responses of southern stingrays ( Hypanus americanus ) to acoustic stimuli

Abstract

The ability of elasmobranchs to detect and use sound cues has been heavily debated in previous research and has only recently received revived attention. To properly understand the importance of sound to elasmobranchs, assessing their responses to acoustic stimuli in a field setting is vital. Here, we establish a behavioural audiogram of free-swimming male and female southern stingrays ( Hypanus americanus ) exposed to low-frequency tones. We demonstrate that female stingrays exposed to tones (50–500 Hz) exhibit significant changes in swimming behaviours (increased time spent swimming, decreased rest time, increased surface breaches and increased side swimming with pectoral flapping) at 140 dB re 1 µPa (−2.08 to −2.40 dB re 1 m s −2 ) while males exposed to the same tones did not exhibit a change in these behaviours until 160 dB re 1 µPa (−1.13 to −1.21 dB re 1 m s −2 ). Our results are the first demonstration of field responses to sound in the Batoidea and show a distinct sensitivity to low-frequency acoustic inputs.

Towards a new understanding of elasmobranch hearing

“…Since elasmobranchs do not have a swim bladder or similar gas inclusions, they are unable to detect the pressure component of a propagating sound wave and only respond to the induced particle motion. Despite the lack of the ability of elasmobranchs to detect sound pressure, only Banner (1967); Kelly and Nelson (1975); Casper and Mann (2006, 2009; and Mickle et al (2020) account for particle motion in their characterization of elasmobranch hearing ability-the remainder of research in the field has focussed on pressure sensitivity.…”

“…The macula neglecta has a direct connection to the external surface of the head of Sound components (i.e. frequency, pressure level and power spectrum) get distorted in a tank setting (Akamatsu et al 2002) The starting point and distribution of animals is known and can be easily measured (Hueter et al 2004) Due to physical limitations of tanks, fish do not exhibit full extent of behaviours compared to wild studies (Parvulescu 1964(Parvulescu , 1967Popper and Hawkins 2019) Current knowledge on fish hearing is mainly from laboratory data collected under quiet conditions, which is not comparable to natural conditions where fish are exposed to a baseline ambient sound level (Wysocki and Ladich 2005) Fish live in environments where sound transmission is complex and not comparable to tank settings (Popper and Hawkins 2019) Acoustic field studies Less distortion of sound in a natural environment compared to tank settings (Akamatsu et al 2002) Difficult and often impossible to control environmental conditions (Akamatsu et al 2002) Behavioural observations are more likely to be accurate due to natural environmental setting (Parvulescu 1964(Parvulescu , 1967Akamatsu et al 2002) Without using physiological techniques such as AEP, it is difficult to know if the animal cannot hear the sound or can hear it and is not responding (Mickle et al 2020) If experiments include playback of free-swimming fish, the starting point of animal distribution is unknown (Hueter et al 2004) elasmobranchs through the endolymphatic duct and detects particle velocity from above the shark's head (Popper and Fay 1977;Myrberg 2001). While the basic structure of these end organs is conserved across the Elasmobranchii, the relative sizes of and connections between the end organs do differ between individual species (Maisey 2001;Evangelista et al 2010; Fig.…”

“…There have also been recent criticisms of laboratory studies in general, and evoked potential studies in particular (Popper and Hawkins 2019;Hawkins et al 2020), due to the distortion of sound components in small tanks (Parvulescu 1967;Akamatsu et al 2002;Rogers et al 2016; Table 2). Behavioural methods can be used on freeswimming animals as the hearing range of southern stingrays (Hypanus americanus) was determined with a change in activity levels (swimming/resting) used as a metric of behavioural response to sound, showing a clear ability of southern stingrays to detect sound (Mickle et al 2020). A drawback to the behavioural techniques used by Mickle et al ( 2020) is that the researchers were not able to definitively state that the animal's lack of response to a given frequency meant they could not hear it; they may have heard the sound and chosen not to respond.…”

“…Fig. 2 Measured hearing thresholds for: yellow stingray (Urobatis jamaicensis) and nurse shark (Ginglymostoma cirratum) using AEP (Casper and Mann 2006); little skate (Leucoraja erinacea) using behavioural conditioning and AEP (Casper et al 2003); southern stingray (Hypanus americanus) using behavioural threshold (M = male, F = female) (Mickle et al 2020); horn shark (Heterodon-tus francisci) using electrical shock and cardiac output (Kelly and Nelson 1975); lemon shark (Negaprion brevirostris) using compound action potential (Corwin 1981) and bull shark (Carcharhinus leucas) using operant conditioning (Kritzler and Wood 1961). Refer to text for details regarding techniques used…”

“…Ryan et al (2018) calls for more research on auditory sensitivity and frequency discrimination to determine the effects of sound on sharks and further uncover the potential for auditory-based shark repellants. The behavioural audiogram of southern stingrays (Hypanus americanus) was recently determined, suggesting that stingrays exhibit a behavioural response (change in activity, resting and surface breaching) to tones played from 50-500 Hz, with a significant difference in male and female response to sound level (Mickle et al 2020). An underwater baited camera rig was used to determine the behavioural response of seven reef and coastal shark species, and the white shark (Carcharodon carcharias) to killer whale and artificial sounds (Chapuis et al 2019).…”