Maria Wilson

Intense ultrasonic clicks from echolocating toothed whales do not elicit anti-predator responses or debilitate the squid Loligo pealeii.

Toothed whales use intense ultrasonic clicks to echolocate prey and it has been hypothesized that they also acoustically debilitate their prey with these intense sound pulses to facilitate capture. Cephalopods are an important food source for toothed whales, and there has probably been an evolutionary selection pressure on cephalopods to develop a mechanism for detecting and evading sound–emitting toothed whale predators. Ultrasonic detection has evolved in some insects to avoid echolocating bats, and it can be hypothesized that cephalopods might have evolved similar ultrasound detection as an anti–predation measure. We test this hypothesis in the squid Loligo pealeii in a playback experiment using intense echolocation clicks from two squid–eating toothed whale species. Twelve squid were exposed to clicks at two repetition rates (16 and 125 clicks per second) with received sound pressure levels of 199–226 dB re 1 μPa (pp) mimicking the sound exposure from an echolocating toothed whale as it approaches and captures prey. We demonstrate that intense ultrasonic clicks do not elicit any detectable anti–predator behaviour in L. pealeii and that clicks with received levels up to 226 dB re 1 μPa (pp) do not acoustically debilitate this cephalopod species.

Hearing in the African lungfish (Protopterus annectens): pre-adaptation to pressure hearing in tetrapods?

Lungfishes are the closest living relatives of the tetrapods, and the ear of recent lungfishes resembles the tetrapod ear more than the ear of ray-finned fishes and is therefore of interest for understanding the evolution of hearing in the early tetrapods. The water-to-land transition resulted in major changes in the tetrapod ear associated with the detection of air-borne sound pressure, as evidenced by the late and independent origins of tympanic ears in all of the major tetrapod groups. To investigate lungfish pressure and vibration detection, we measured the sensitivity and frequency responses of five West African lungfish (Protopterus annectens) using brainstem potentials evoked by calibrated sound and vibration stimuli in air and water. We find that the lungfish ear has good low-frequency vibration sensitivity, like recent amphibians, but poor sensitivity to air-borne sound. The skull shows measurable vibrations above 100 Hz when stimulated by air-borne sound, but the ear is apparently insensitive at these frequencies, suggesting that the lungfish ear is neither adapted nor pre-adapted for aerial hearing. Thus, if the lungfish ear is a model of the ear of early tetrapods, their auditory sensitivity was limited to very low frequencies on land, mostly mediated by substrate-borne vibrations.

Ultrasound detection in the Gulf menhaden requires gas-filled bullae and an intact lateral line.

SUMMARY Clupeiform fish species, including the Gulf menhaden (Brevoortia patronus) that belong to the subfamily Alosinae, can detect ultrasound. Clupeiform fishes are unique in that they have specialized gas-filled bullae in the head associated with the ear via the bulla membrane and with the lateral line via the lateral recess membrane. It has been hypothesized that the utricle of the inner ear is responsible for ultrasound detection through a specialized connection to the gas-filled bullae complex. Here, we show that the lateral line and its connection to the gas-filled bullae complex via the lateral recess are involved in ultrasound detection in Gulf menhaden. Removal of a small portion of the lateral line overlying the lateral recess membrane eliminates the ability of Gulf menhaden to detect ultrasound. We further show that the gas-filled bullae vibrates in response to ultrasound, that the gas-filled bullae are necessary for detecting ultrasound, and that the bullae connections to the lateral line via the lateral recess membrane play an important role in ultrasound detection. These results add a new dimension to the role of the lateral line and bullae as part of the ultrasonic detection system in Gulf menhaden.

Allis shad (Alosa alosa) exhibit an intensity-graded behavioral response when exposed to ultrasound

Most fish cannot hear frequencies above 3 kHz, but a few species belonging to the subfamily Alosinae (family Clupeidae) can detect intense ultrasound. The response of adult specimens of the European allis shad (Alosa alosa) to sinusoidal ultrasonic pulses at 70 and 120 kHz is tested. The fish showed an intensity-graded response to the ultrasonic pulses with a response threshold between 161 and 167 dB re 1 microPa (pp) for both frequencies. These response thresholds are similar to thresholds derived from juvenile American shad (Alosa sapidissima) in previous studies, supporting the suggestion that these members of Alosinae have evolved a dedicated ultrasound detector adapted to detect and respond to approaching echolocating toothed whales.

Particle acceleration noise generated by boats

The acoustic field consists of oscillating particles causing pressure fluctuations. Many aquatic organisms can detect the particle acceleration in the acoustic field and are therefore sometimes more susceptible to this component of the sound field rather than to the acoustic pressure (Kalmijn 1988). In this study, the particle acceleration generated by various boat types is measured using two hydrophones.

Sperm whale predator-prey interactions involve chasing and buzzing, but no acoustic stunning

The sperm whale carries a hypertrophied nose that generates powerful clicks for long-range echolocation. However, it remains a conundrum how this bizarrely shaped apex predator catches its prey. Several hypotheses have been advanced to propose both active and passive means to acquire prey, including acoustic debilitation of prey with very powerful clicks. Here we test these hypotheses by using sound and movement recording tags in a fine-scale study of buzz sequences to relate the acoustic behaviour of sperm whales with changes in acceleration in their head region during prey capture attempts. We show that in the terminal buzz phase, sperm whales reduce inter-click intervals and estimated source levels by 1–2 orders of magnitude. As a result, received levels at the prey are more than an order of magnitude below levels required for debilitation, precluding acoustic stunning to facilitate prey capture. Rather, buzzing involves high-frequency, low amplitude clicks well suited to provide high-resolution biosonar updates during the last stages of capture. The high temporal resolution helps to guide motor patterns during occasionally prolonged chases in which prey are eventually subdued with the aid of fast jaw movements and/or buccal suction as indicated by acceleration transients (jerks) near the end of buzzes.

Ultrasound Detection in Fishes and Frogs: Discovery and Mechanisms

The frequency range of hearing in fishes and frogs historically has been thought to be confined to relatively low frequencies in comparison to that of mammals. However, within the last 20 years, the audiograms of several fish and frog species have been shown to encompass ultrasonic (US) frequencies. Moreover, these animals have been shown to respond behaviorally to US playbacks. Although the evolution of US detection in these species is still an ongoing topic of study, both fishes and frogs have faced the challenge of producing very high-frequency responses from systems that evolved with low-frequency sensitivity. A short history of the behavioral responses and the electrophysiological mechanisms (when known) underlying the production and reception of US in fishes and frogs is presented, with a focus on the unique experimental approaches that have yielded this surprising upward extension of the hearing ranges of several specialized fishes and frogs.

Ultrasonic predator–prey interactions in water–convergent evolution with insects and bats in air?

Toothed whales and bats have independently evolved biosonar systems to navigate and locate and catch prey. Such active sensing allows them to operate in darkness, but with the potential cost of warning prey by the emission of intense ultrasonic signals. At least six orders of nocturnal insects have independently evolved ears sensitive to ultrasound and exhibit evasive maneuvers when exposed to bat calls. Among aquatic prey on the other hand, the ability to detect and avoid ultrasound emitting predators seems to be limited to only one subfamily of Clupeidae: the Alosinae (shad and menhaden). These differences are likely rooted in the different physical properties of air and water where cuticular mechanoreceptors have been adapted to serve as ultrasound sensitive ears, whereas ultrasound detection in water have called for sensory cells mechanically connected to highly specialized gas volumes that can oscillate at high frequencies. In addition, there are most likely differences in the risk of predation between insects and fish from echolocating predators. The selection pressure among insects for evolving ultrasound sensitive ears is high, because essentially all nocturnal predation on flying insects stems from echolocating bats. In the interaction between toothed whales and their prey the selection pressure seems weaker, because toothed whales are by no means the only marine predators placing a selection pressure on their prey to evolve specific means to detect and avoid them. Toothed whales can generate extremely intense sound pressure levels, and it has been suggested that they may use these to debilitate prey. Recent experiments, however, show that neither fish with swim bladders, nor squid are debilitated by such signals. This strongly suggests that the production of high amplitude ultrasonic clicks serve the function of improving the detection range of the toothed whale biosonar system rather than debilitation of prey.

Behavioural responses to infrasonic particle acceleration in cuttlefish

ABSTRACT Attacks by aquatic predators generate frontal water disturbances characterised by low-frequency gradients in pressure and particle motion. Low-frequency hearing is highly developed in cephalopods. Thus, we examined behavioural responses in juvenile cuttlefish to infrasonic accelerations mimicking main aspects of the hydrodynamic signals created by predators. In the experimental set-up, animals and their surrounding water moved as a unit to minimise lateral line activation and to allow examination of the contribution by the inner ear. Behavioural responses were tested in light versus darkness and after food deprivation following a ‘simulated’ hunting opportunity. At low acceleration levels, colour change threshold at 3, 5 and 9 Hz was 0.028, 0.038 and 0.035 m s−2, respectively. At higher stimulus levels, jet-propulsed escape responses thresholds in daylight were 0.043, 0.065 and 0.069 m s−2 at 3, 5 and 9 Hz, respectively, and not significantly different from the corresponding darkness thresholds of 0.043, 0.071 and 0.064 m s−2. In a simulated hunting mode, escape thresholds were significantly higher at 3 Hz (0.118 m s−2) but not at 9 Hz (0.134 m s−2). Escape responses were directional, and overall followed the direction of the initial particle acceleration, with mean escape angles from 313 to 33 deg for all three experiments. Thus, in the wild, particle acceleration might cause escape responses directed away from striking predators but towards suction-feeding predators. We suggest that cuttlefish jet-propulsed escape behaviour has evolved to be elicited by the early hydrodynamic disturbances generated during predator encounters, and that the inner ear plays an essential role in the acoustic escape responses. Editors’ Choice: Cuttlefish exhibit jet-propulsed escape responses adapted to the hydrodynamic signatures generated by predators in the initial approach phase of an attack.

BIG BANG? INTENSE ULTRASOUND DOES NOT HAVE ANY DETECTABLE EFFECTS ON THE SQUID LOLIGO PEALEII

There are two important sources of ultrasound in the aquatic environment. One is the anthropogenic source in the form of echosounders and the other is the biosonar system of toothed whales. Both systems are very powerful, with source sound pressure levels of more than 220 dB re 1 pPa (peak to peak) (Au 1993). Their widespread use means that many fish and cephalopods often are exposed to intense ultrasound, but only a few studies have been conducted on the effects of these exposures. In this experiment (Wilson et al. 2007), we exposed the squid, Loligo pealeii, to intense ultrasonic signals to test for behavioural responses and to test if toothed whales may use intense echolocation signals to debilitate their prey.