T. Aran Mooney

An ecological acoustic recorder (EAR) for long-term monitoring of biological and anthropogenic sounds on coral reefs and other marine habitats

Keeping track of long-term biological trends in many marine habitats is a challenging task that is exacerbated when the habitats in question are in remote locations. Monitoring the ambient sound field may be a useful way of assessing biological activity because many behavioral processes are accompanied by sound production. This article reports the preliminary results of an effort to develop and use an Ecological Acoustic Recorder (EAR) to monitor biological activity on coral reefs and in surrounding waters for periods of 1 year or longer. The EAR is a microprocessor-based autonomous recorder that periodically samples the ambient sound field and also automatically detects sounds that meet specific criteria. The system was used to record the sound field of coral reefs and other marine habitats on Oahu, HI. Snapping shrimp produced the dominant acoustic energy on the reefs examined and exhibited clear diel acoustic trends. Other biological sounds recorded included those produced by fish and cetaceans, which also exhibited distinct temporal variability. Motor vessel activity could also be monitored effectively with the EAR. The results indicate that acoustic monitoring may be an effective means of tracking biological and anthropogenic activity at locations where continuous monitoring by traditional survey methods is impractical.

Sound detection by the longfin squid (Loligo pealeii) studied with auditory evoked potentials: sensitivity to low-frequency particle motion and not pressure

SUMMARY Although hearing has been described for many underwater species, there is much debate regarding if and how cephalopods detect sound. Here we quantify the acoustic sensitivity of the longfin squid (Loligo pealeii) using near-field acoustic and shaker-generated acceleration stimuli. Sound field pressure and particle motion components were measured from 30 to 10,000 Hz and acceleration stimuli were measured from 20 to 1000 Hz. Responses were determined using auditory evoked potentials (AEPs) with electrodes placed near the statocysts. Evoked potentials were generated by both stimuli and consisted of two wave types: (1) rapid stimulus-following waves, and (2) slower, high-amplitude waves, similar to some fish AEPs. Responses were obtained between 30 and 500 Hz with lowest thresholds between 100 and 200 Hz. At the best frequencies, AEP amplitudes were often >20 μV. Evoked potentials were extinguished at all frequencies if (1) water temperatures were less than 8°C, (2) statocysts were ablated, or (3) recording electrodes were placed in locations other than near the statocysts. Both the AEP response characteristics and the range of responses suggest that squid detect sound similarly to most fish, with the statocyst acting as an accelerometer through which squid detect the particle motion component of a sound field. The modality and frequency range indicate that squid probably detect acoustic particle motion stimuli from both predators and prey as well as low-frequency environmental sound signatures that may aid navigation.

Hearing measurements from a stranded infant Risso's dolphin, Grampus griseus.

SUMMARY An infant Rissos dolphin (Grampus griseus) was rescued from the beach in Southern Portugal, and an audiogram was measured using auditory evoked potentials (AEP) and envelope following response (EFR) techniques for frequencies from 4 to 150 kHz. The stimuli used were custom sinusoidally amplitude-modulated (SAM) tone-bursts, and the AEP responses were collected, averaged and analyzed to quantify the animals physiological response and, thereby, hearing thresholds. The infant animal showed a wide range of best sensitivity, with the lowest threshold of 49.5 dB re. 1 μPa at 90 kHz. The audiogram showed a typical mammalian ∪-shape with a gradual, low-frequency slope of 16.4 dB octave-1 and a sharp high-frequency increase of 95 dB octave-1. When compared with an audiogram of an older Rissos dolphin obtained using behavioral methods, the threshold values at upper frequencies were much lower for this infant animal, and this infant heard higher frequencies. These results redefine the hearing capabilities of Rissos dolphins by demonstrating very high-frequency sensitivity.

Predicting temporary threshold shifts in a bottlenose dolphin (Tursiops truncatus): The effects of noise level and duration

Noise levels in the ocean are increasing and are expected to affect marine mammals. To examine the auditory effects of noise on odontocetes, a bottlenose dolphin (Tursiops truncatus) was exposed to octave-band noise (4-8 kHz) of varying durations (<2-30 min) and sound pressures (130-178 dB re 1 microPa). Temporary threshold shift (TTS) occurrence was quantified in an effort to (i) determine the sound exposure levels (SELs) (dB re 1 microPa(2) s) that induce TTS and (ii) develop a model to predict TTS onset. Hearing thresholds were measured using auditory evoked potentials. If SEL was kept constant, significant shifts were induced by longer duration exposures but not for shorter exposures. Higher SELs were required to induce shifts in shorter duration exposures. The results did not support an equal-energy model to predict TTS onset. Rather, a logarithmic algorithm, which increased in sound energy as exposure duration decreased, was a better predictor of TTS. Recovery to baseline hearing thresholds was also logarithmic (approximately -1.8 dB/doubling of time) but indicated variability including faster recovery rates after greater shifts and longer recoveries necessary after longer duration exposures. The data reflected the complexity of TTS in mammals that should be taken into account when predicting odontocete TTS.

Hearing and Auditory Evoked Potential Methods Applied to Odontocete Cetaceans

Auditory evoked potential (AEP) procedures have been increasingly used to measure hearing processes in aquatic mammals. They have been demonstrated to be useful in measuring the audiograms of stranded animals like infant sperm whales (Physeter macrocephalus) and Risso’s dolphins (Grampus griseus). Modulation rate transfer functions (MRTF) demonstrating appropriate stimulus presentation rates are usually measured prior to recording audiograms with odontocetes. Measures comparing behavioral and AEP audiograms with the same animals have generally shown good correspondence between data gathered using the two procedures. AEPs and acoustic brainstem responses (ABRs) also have been used to measure hearing while an animal is actively echolocating. This technique of measuring the animal’s ability to hear its own outgoing signals, as well as the returning echoes, allows experimenters to develop a new understanding of the processes underlying echolocation.

Hearing in cetaceans: from natural history to experimental biology.

Sound is a primary sensory cue for most marine mammals, and this is especially true for cetaceans. To passively and actively acquire information about their environment, cetaceans have some of the most derived ears of all mammals, capable of sophisticated, sensitive hearing and auditory processing. These capabilities have developed for survival in an underwater world where sound travels five times faster than in air, and where light is quickly attenuated and often limited at depth, at night, and in murky waters. Cetacean auditory evolution has capitalized on the ubiquity of sound cues and the efficiency of underwater acoustic communication. The sense of hearing is central to cetacean sensory ecology, enabling vital behaviours such as locating prey, detecting predators, identifying conspecifics, and navigating. Increasing levels of anthropogenic ocean noise appears to influence many of these activities. Here, we describe the historical progress of investigations on cetacean hearing, with a particular focus on odontocetes and recent advancements. While this broad topic has been studied for several centuries, new technologies in the past two decades have been leveraged to improve our understanding of a wide range of taxa, including some of the most elusive species. This chapter addresses topics including how sounds are received, what sounds are detected, hearing mechanisms for complex acoustic scenes, recent anatomical and physiological studies, the potential impacts of noise, and mysticete hearing. We conclude by identifying emerging research topics and areas which require greater focus.

Adverse Effects of Ocean Acidification on Early Development of Squid (Doryteuthis pealeii)

Anthropogenic carbon dioxide (CO2) is being absorbed into the ocean, altering seawater chemistry, with potentially negative impacts on a wide range of marine organisms. The early life stages of invertebrates with internal and external aragonite structures may be particularly vulnerable to this ocean acidification. Impacts to cephalopods, which form aragonite cuttlebones and statoliths, are of concern because of the central role they play in many ocean ecosystems and because of their importance to global fisheries. Atlantic longfin squid (Doryteuthis pealeii), an ecologically and economically valuable taxon, were reared from eggs to hatchlings (paralarvae) under ambient and elevated CO2 concentrations in replicated experimental trials. Animals raised under elevated pCO2 demonstrated significant developmental changes including increased time to hatching and shorter mantle lengths, although differences were small. Aragonite statoliths, critical for balance and detecting movement, had significantly reduced surface area and were abnormally shaped with increased porosity and altered crystal structure in elevated pCO2-reared paralarvae. These developmental and physiological effects could alter squid paralarvae behavior and survival in the wild, directly and indirectly impacting marine food webs and commercial fisheries.

Detecting the Unexpected: A Research Framework for Ocean Acidification

The threat that ocean acidification (OA) poses to marine ecosystems is now recognized and U.S. funding agencies have designated specific funding for the study of OA. We present a research framework for studying OA that describes it as a biogeochemical event that impacts individual species and ecosystems in potentially unexpected ways. We draw upon specific lessons learned about ecosystem responses from research on acid rain, carbon dioxide enrichment in terrestrial plant communities, and nitrogen deposition. We further characterize the links between carbon chemistry changes and effects on individuals and ecosystems, and enumerate key hypotheses for testing. Finally, we quantify how U.S. research funding has been distributed among these linkages, concluding that there is an urgent need for research programs designed to anticipate how the effects of OA will reverberate throughout assemblages of species.

Long-duration anesthetization of squid (Doryteuthis pealeii)

Cephalopods, and particularly squid, play a central role in marine ecosystems and are a prime model animal in neuroscience. Yet, the capability to investigate these animals in vivo has been hampered by the inability to sedate them beyond several minutes. Here, we describe methods to anesthetize Doryteuthis pealeii, the longfin squid, noninvasively for up to 5 h using a 0.15 mol magnesium chloride (MgCl2) seawater solution. Sedation was mild, rapid (<4 min), and the duration could be easily controlled by repeating anesthetic inductions. The sedation had no apparent effect on physiological evoked potentials recorded from nerve bundles within the statocyst system, suggesting the suitability of this solution as a sedating agent. This simple, long-duration anesthetic technique opens the possibility for longer in vivo investigations on this and related cephalopods, thus expanding potential neuroethological and ecophysiology research for a key marine invertebrate group.

Baseline hearing abilities and variability in wild beluga whales (Delphinapterus leucas)

While hearing is the primary sensory modality for odontocetes, there are few data addressing variation within a natural population. This work describes the hearing ranges (4–150 kHz) and sensitivities of seven apparently healthy, wild beluga whales (Delphinapterus leucas) during a population health assessment project that captured and released belugas in Bristol Bay, Alaska. The baseline hearing abilities and subsequent variations were addressed. Hearing was measured using auditory evoked potentials (AEPs). All audiograms showed a typical cetacean U-shape; substantial variation (>30 dB) was found between most and least sensitive thresholds. All animals heard well, up to at least 128 kHz. Two heard up to 150 kHz. Lowest auditory thresholds (35–45 dB) were identified in the range 45–80 kHz. Greatest differences in hearing abilities occurred at both the high end of the auditory range and at frequencies of maximum sensitivity. In general, wild beluga hearing was quite sensitive. Hearing abilities were similar to those of belugas measured in zoological settings, reinforcing the comparative importance of both settings. The relative degree of variability across the wild belugas suggests that audiograms from multiple individuals are needed to properly describe the maximum sensitivity and population variance for odontocetes. Hearing measures were easily incorporated into field-based settings. This detailed examination of hearing abilities in wild Bristol Bay belugas provides a basis for a better understanding of the potential impact of anthropogenic noise on a noise-sensitive species. Such information may help design noise-limiting mitigation measures that could be applied to areas heavily influenced and inhabited by endangered belugas.