200 kHz Commercial Sonar Systems Generate Lower Frequency Side Lobes Audible to Some Marine Mammals

The spectral properties of pulses transmitted by three commercially available 200 kHz echo sounders were measured to assess the possibility that marine mammals might hear sound energy below the center (carrier) frequency that may be generated by transmitting short rectangular pulses. All three sounders were found to generate sound at frequencies below the center frequency and within the hearing range of some marine mammals, e.g. killer whales, false killer whales, beluga whales, Atlantic bottlenose dolphins, harbor porpoises, and others. The frequencies of these sub-harmonic sounds ranged from 90 to 130 kHz. These sounds were likely detectable by the animals over distances up to several hundred meters but were well below potentially harmful levels. The sounds generated by the sounders could potentially affect the behavior of marine mammals within fairly close proximity to the sources and therefore the exclusion of echo sounders from environmental impact analysis based solely on the center frequency output in relation to the range of marine mammal hearing should be reconsidered.     

Responses of mosquitoes and German cockroaches to ultrasound emitted from a random ultrasonic generating device

The repellency of ultrasound to females of two species of mosquitoes, Anopheles quadrimaculatus Say and Anopheles gambiae Giles (Diptera: Culicidae), and male and female German cockroaches, Blattella germanica (L.) (Blattodea: Blattellidae), was evaluated under laboratory conditions using a random ultrasonic device developed at Kansas State University. This device produces ultrasound in the 20–100 kHz frequency range and random sound patterns at any frequency range. Under the particular settings described in the paper, this ultrasonic device produced sound pressure levels from 91 to 101, 91 to 102, and 90 to 100 dB at the top, bottom, and side panels of the test chamber, respectively (0 dB = 20 micropascals). Sound pressure levels recorded at the center of the top, bottom, and side panels were higher than those recorded at the panel edges. Ultrasound from the random ultrasonic device failed to repel mosquitoes and German cockroaches at the different frequency ranges evaluated. Our results confirm previous findings with commercial devices producing constant sound patterns that ultrasound in general is not a promising tool for repelling mosquitoes and cockroaches.     

Hearing in reindeer (Rangifer tarandus)

The audiogram of two yearling male reindeer (Rangifer tarandus tarandus) were determined using a conditioned suppression/avoidance procedure. During testing, the animal was drinking from a metal bowl while pure tone signals were played at random intervals and followed by an electric shock in the bowl. By breaking contact with the bowl at sound signals, the animal avoided the shock. The animals detected sounds at intensities of 60 dB or less from 70 Hz to 38 kHz. The frequency range of best sensitivity was relatively flat from 1 kHz to 16 kHz, with a best sensitivity of 3 dB at 8 kHz. The hearing ability of reindeer is similar to the hearing ability of other ungulates.     

Role of cage material, working style and hearing sensitivity in perception of animal care noise

During daily care, laboratory animals are exposed to a variety of sounds which may have effects on welfare and also cause physiological and behavioural changes. So far, almost no attention has been paid to individual sounds or the sound level caused by animal care or the sound level inside the animal cage. In this study, sounds from selected rat care procedures were recorded: pulling cage out of the rack, placing it onto a table and replacing the cage back into the rack; with measurements made inside the rat cage and in the adjacent cage. Diet was poured into the food hopper and sounds were recorded inside the cage and also the adjacent cage. The work was repeated in a calm and also in a hurried style, using stainless steel and polycarbonate cages. Finally, the sounds produced by running tap water were recorded. Differences between rat and human hearing were compared using novel species-specific sound level weightings: R-weighting for rats dB(R) and H-weighting for human dB(H). Hurried work with steel caused sound exposure levels exceeding 90 dB(R) when the cages were placed into the rack and about 80 dB(R) when pulling them out of the rack or placing onto a table. With polycarbonate, the levels were 10-15 dB(R) lower. Unhurried calm working produced lower sound exposure levels than hurried working in many procedures. When the procedures were repeated with measurements in the adjacent cage, the sound exposure levels were lower, but the results were similar. Pouring food pellets into a hopper above the rat's head caused 15 dB(R) higher sound exposure levels than pouring food to an adjacent cage. In general, humans hear these sounds about 10-15 dB louder than rats. In conclusion, cage material, working style and hearing sensitivity all have an impact on the sound exposure level in the rodent cage. With correct working methods, high sound levels can be efficiently avoided in most cases.     

Pacific herring hearing does not include ultrasound

Recent studies have shown that some clupeid fishes, including shad and menhaden, can detect ultrasound (sound with frequencies higher than 20 kHz) and actively avoid it. However, other clupeids, including sardines and anchovies, do not detect ultrasound. The hearing abilities of herring are of particular interest because of their commercial importance, our reliance on acoustics to monitor their populations and behavioural evidence of responses to high-frequency sound by some clupeid species. We measured the hearing sensitivity of Pacific herring (Clupea pallasii) using the auditory brainstem response and found that they were unable to detect ultrasonic signals at received levels up to 185 dB re 1 microPa. Herring had hearing thresholds at lower frequencies (100-5000 Hz) that were typical of other non-ultrasound-detecting clupeids. This lower-frequency hearing sensitivity could explain the results of several earlier studies showing responses to broadband sounds.     

Ultrasonic singing by the blue-throated hummingbird: a comparison between production and perception

Blue-throated hummingbirds produce elaborate songs extending into the ultrasonic frequency range, up to 30 kHz. Ultrasonic song elements include harmonics and extensions of audible notes, non-harmonic components of audible syllables, and sounds produced at frequencies above 20 kHz without corresponding hearing range sound. To determine whether ultrasonic song elements function in intraspecific communication, we tested the hearing range of male and female blue-throated hummingbirds. We measured auditory thresholds for tone pips ranging from 1 kHz to 50 kHz using auditory brainstem responses. Neither male nor female blue-throated hummingbirds appear to be able to hear above 7 kHz. No auditory brainstem responses could be detected between 8 and 50 kHz at 90 dB. This high-frequency cutoff is well within the range reported for other species of birds. These results suggest that high-frequency song elements are not used in intraspecific communication. We propose that the restricted hummingbird hearing range may exemplify a phylogenetic constraint.     

SOUND AND ITS SIGNIFICANCE FOR LABORATORY ANIMALS

1. Several methods of varying accuracy have been used to assess what sounds small laboratory animals such as rodents are capable of hearing. Most rodents can detect sounds from 1000 Hz (the frequency of the Greenwich Time Signal) up to 100000 Hz, depending on the strain, with usually one or more commonly two peaks of sensitivity within this range. Dogs can detect sound most easily from 500 Hz to 55000 Hz, depending on the breed. 2. Rodents also produce sound signals as a behavioural response and for communication in a variety of situations. Ultrasonic calls in the range 22000–70000 Hz are the main communicating pathway during aggressive encounters, mating, and mothering. Similar calls have also been recorded from isolated animals associated with inactivity, rest and possibly even sleep. 3. Very loud sounds cause seizures in rats and mice, or can make them more susceptible to other sounds later in life. This effect is possible even when animals are fully anaesthetized. Sound tends to startle and reduce activity in several species of animal. Even offspring of mice that have been sound-stressed exhibit abnormal behaviour patterns. Sounds also elicit various responses in rats from increasing aggression to making them more tolerant to electric shocks. 4. Levels of sound above 100 dB are teratogenic in several species of animals and several hormonal, haematological and reproductive parameters are disturbed by sounds above 80 dB. When rats are chemically deafened the disturbance to their fertility disappears. Lipid metabolism is disrupted in rats when exposed to over 95 dB of sounds, leading to increases in plasma triglycerides. Atherosclerosis can be produced in rabbits by similar levels of sound. 5. It has also been shown in guinea pigs and cats that hearing damage is governed by the duration as well as the intensity of the sound and is irreversible. Work on chinchillas hs demonstrated that sounds above 95 dB lead to this injury, but that sounds of 80 dB have no permanent effect on hearing sensitivity.     

REACTIONS OF CAPTIVE HARBOR PORPOISES (PHOCOENA PHOCOENA) TO PINGER-LIKE SOUNDS

Pingers on gill nets can reduce bycatch of harbor porpoises. If harbor porpoises habituate to pingers, the effect may be reduced or lost. Two captive harbor porpoises were exposed to three sound types. All sounds were in the frequency band from 100 kHz to 140 kHz, 200 ms long, and presented once per 4 s. The source level was 153 dB re 1 μPa RMS at 1 m. Each session consisted of a 10‐min presound, a 5‐min sound, and a 10‐min postsound period. Behavior was recorded on video and on dataloggers placed on the dorsal fin of one animal. The loggers recorded heart rate, swimming speed, dive duration, and depth. The animals responded most strongly to the initial presentations of a sound. Surface time decreased, the heart rate dropped below the normal bradycardia, and echolocation activity decreased. The reactions of both animals diminished rapidly in the following sessions. Should the waning of responsiveness apply to wild animals, porpoises may adapt to the sounds but still avoid nets, or the bycatch may increase after some time. The success of long‐term use of pingers may then depend on the variety of sounds and rates of exposure.     

The ontogenetic development of auditory sensitivity, vocalization and acoustic communication in the labyrinth fish Trichopsis vittata

The anabantoid fish Trichopsis vittata starts vocalizing as 8-week-old juveniles. In order to determine whether juveniles are able to detect conspecific sounds, hearing sensitivities were measured in six size groups utilizing the auditory brainstem response-recording technique. Results were compared to sound pressure levels and spectra of sounds recorded during fighting. Auditory evoked potentials were present in all size groups and complete audiograms were obtained starting with 0.18 to 0.30 g juveniles. Auditory sensitivity during development primarily increased between 0.8 kHz and 3.0 kHz. The most sensitive frequency within this range shifted from 2.5 kHz to 1.5 kHz, whereas thresholds decreased by 14 dB. Sound production, on the other hand, started at 0.1 g and sound power spectra at dominant frequencies increased by 43 dB, while dominant frequencies shifted from 3 kHz to 1.5 kHz. Comparisons between audiograms and sound power spectra in similar-sized juveniles revealed no clear match between most sensitive frequencies and dominant frequencies of sounds. This also revealed that juveniles cannot detect conspecific sounds below the 0.31 to 0.65 g size class. These results indicate that auditory sensitivity develops prior to the ability to vocalize and that vocalization occurs prior to the ability to communicate acoustically.     

Oyster Larvae Settle in Response to Habitat-Associated Underwater Sounds

Following a planktonic dispersal period of days to months, the larvae of benthic marine organisms must locate suitable seafloor habitat in which to settle and metamorphose. For animals that are sessile or sedentary as adults, settlement onto substrates that are adequate for survival and reproduction is particularly critical, yet represents a challenge since patchily distributed settlement sites may be difficult to find along a coast or within an estuary. Recent studies have demonstrated that the underwater soundscape, the distinct sounds that emanate from habitats and contain information about their biological and physical characteristics, may serve as broad-scale environmental cue for marine larvae to find satisfactory settlement sites. Here, we contrast the acoustic characteristics of oyster reef and off-reef soft bottoms, and investigate the effect of habitat-associated estuarine sound on the settlement patterns of an economically and ecologically important reef-building bivalve, the Eastern oyster (Crassostrea virginica). Subtidal oyster reefs in coastal North Carolina, USA show distinct acoustic signatures compared to adjacent off-reef soft bottom habitats, characterized by consistently higher levels of sound in the 1.5–20 kHz range. Manipulative laboratory playback experiments found increased settlement in larval oyster cultures exposed to oyster reef sound compared to unstructured soft bottom sound or no sound treatments. In field experiments, ambient reef sound produced higher levels of oyster settlement in larval cultures than did off-reef sound treatments. The results suggest that oyster larvae have the ability to respond to sounds indicative of optimal settlement sites, and this is the first evidence that habitat-related differences in estuarine sounds influence the settlement of a mollusk. Habitat-specific sound characteristics may represent an important settlement and habitat selection cue for estuarine invertebrates and could play a role in driving settlement and recruitment patterns in marine communities.     

Directional hearing in the gray tree frog Hyla versicolor: Eardrum vibrations and phonotaxis

1. We used laser vibrometry to study the vibrational frequency response of the eardrum of female gray tree frogs for different positions of the sound source in three-dimensional space. Furthermore, we studied the accuracy of 3-D phonotaxis in the same species for sounds with different frequency contents. 2. The directionality of the eardrum was most pronounced in a narrow frequency range between 1.3 and 1.8 kHz. 3. The average 3-D, horizontal and vertical jump error angles for phonotactic approaches with a sound similar to the natural advertisement call (1.1 and 2.2 kHz frequency components) were 23 degrees, 19 degrees and 12 degrees, respectively. 4. 3-D jump error angle distributions for the 1.4 + 2.2 kHz, 1.0 kHz and 2.0 kHz sounds were not significantly different from that for the 1.1 + 2.2 kHz sound. 5. The average 3-D jump error angle for the 1.4 kHz sound was 36 degrees, and the distribution was significantly different from that for the 1.1 + 2.2 kHz sound. Hence, phonotactic accuracy was poorer in the frequency range of maximum eardrum directionality. 6. Head scanning was not observed and is apparently unnecessary for accurate sound localization in three-dimensional space. 7. Changes in overall sound pressure level experienced by the frog during phonotactic approaches are not an important cue for sound localization.     

BIOACOUSTIC PUBLICATIONS, 1989

ABSTRACT

Coruros Spalacopus cyanus, social fossorial rodents from Chile, use a complex acoustic repertoire with eleven different true vocalisations and one mechanical sound in various behavioural contexts. The complex of contact calls is particularly well differentiated. Juvenile coruros produced six true vocalisations of which four were structurally identical to adult calls. One vocalisation had components of two adult sounds and one occurred only in juvenile animals. Certain calls from the adult repertoire were lacking. The frequencies of sounds of juveniles were considerably higher than those of adults, with many sounds reaching the ultrasonic range. Nevertheless, pure ultrasonic sounds were not recorded.

The frequencies of the analysed sounds of coruros extended from 0.17 to 20.33 kHz with dominant frequency components between 0.17 and 10 kHz. The acoustic properties of calls are suitable for transmission above and below ground, thus providing further indirect evidence that coruros are not strictly confined to an underground way of life. Indeed, the great variability of frequency ranges, with lower frequencies always being included, reflects a specialisation for communication in variable acoustic environments.

The most distinctive and unique vocalisation of coruros is the long duration musical trilling (lasting up to two minutes), which is a long-distance call emitted in alarm and arousal contexts. Recordings of this call from natural burrows in the field in Chile showed similar structural features to vocalisations from captive colonies in the laboratory.

Our findings provide a further example of matching physical properties of vocalisations to the acoustic conditions of the habitat. However, vocalisations in subterranean rodents consist almost exclusively of short-distance calls, the trilling of coruros being the notable exception. Since the selective pressure of the acoustic environment upon the evolution of short-distance vocalisations is probably minimal, we suggest that during their evolution, subterranean mammals have matched their vocalisations primarily to their hearing range and not directly to the acoustics underground. Hearing probably has been the primary target of natural selection, serving not only for communication but also for detection of predators (and, in carnivores, of prey).     

Frequency discrimination by the bottle-nosed dolphin and the Northern fur seal depending on sound parameters and sound conduction pathways

Underwater differential frequency hearing thresholds in the Black Sea bottle-nosed dolphin (Tursiops truncatus p.) and the northern fur seal (Callorhinus ursinus) were measured depending on signal frequency and sound conduction pathways. The measurements were performed by the method of instrumental conditioned reflexes with food reinforcement under conditions of full and partial (with heads out of water at sound conduction through body tissues) submergence of animals into water. It was shown that in a frequency range of 5-100 kHz, underwater differential frequency hearing thresholds of the bottle-nosed dolphin changed from 0.46-0.60% to 0.21-0.34% and depended little on sound conduction pathways. The minimum underwater differential frequency hearing thresholds of the northern fur seal corresponded to the frequencies of maximum hearing sensitivity, changed from 1.7% to 1-2.3% in a frequency range of 1-20 kHz, sharply increased at the edges of the frequency hearing perception range, and depended little (in a range of 5-40 kHz) on sound conduction pathways. Thus, underwater sounds propagating through the body tissues of dolphin and fur seal reach the inner ear.     

Acoustically evoked potentials in midbrain auditory structures in sea lions (Pinnipedia)

Summary Twelve sea lions (Zalophus californianus) and one harbor seal (Phoca vitulina) were examined by recording evoked potentials in response to sound from the inferior colliculus and adjacent structures, under barbiturate or after implanting and coming out of anesthesia. Results were similar in air and under water.The averaged response evoked by a sharply rising tone consists of early, brief peaks and later, slow waves (Fig. 1). The latency of the earliest deflection is 3.5 to 4.8 ms from the moment of arrival of a sound pip at the ear. The potential increases in size with sound intensity approximately as a power function, over a dynamic range of 60–70 db (Fig. 2). Masking is qualitatively similar to that in common laboratory species.The properties of the midbrain response are strikingly different from those in porpoises, reported elsewhere. The pinniped is not so specialized for extremely short duration, fast rise time, sounds or for rapid recovery or ultrasonic frequencies (Figs. 3, 4, 7, 8). Evoked potentials fail to show response above 30–35 kHz at 100 db SPL; best frequency is about 4–6 kHz (Figs. 5, 6). Threshold by this method is about 20 db SPL in air. Frequency modulated tones are markedly more effective in some loci but less so than in porpoises under water. The receptive field is essentially total and directionality weak, in contrast with porpoises.Physiological results cannot settle the question whether echolocation is employed but they can indicate lack of high specialization for the types of sounds bats and porpoises use.This study was aided by the Office of Naval Research, the Air Force Office of Scientific Research, the National Science Foundation, and the National Institute of Neurological Diseases and Stroke through grants to T. H. Bullock, and by the Naval Undersea Research and Development Center through S. H. Ridgway.The assistance of R. F. Green in developing anatomical landmarks and that of R. H. Hamstra, Jr. in electronic problems was especially valuable. The staffs of both laboratories were the essence of cooperation.     

R-weighting provides better estimation for rat hearing sensitivity

Since sounds may induce physiological and behavioural changes in animals, it is necessary to assess and define the acoustic environment in laboratory animal facilities. Sound studies usually express sound levels as unweighted linear sound pressure levels. However, because a linear scale does not take account of hearing sensitivity-which may differ widely both between and within species at various frequencies-the results may be spurious. In this study a novel sound pressure level weighting for rats, R-weighting, was calculated according to a rat's hearing sensitivity. The sound level of a white noise signal was assessed using R-weighting, with H-weighting tailored for humans, A-weighting and linear sound pressure level combined with the response curves of two different loudspeakers. The sound signal resulted in different sound levels depending on the weighting and the type of loudspeaker. With a tweeter speaker reproducing sounds at high frequencies audible to a rat, R- and A-weightings gave similar results, but the H-weighted sound levels were lower. With a middle-range loudspeaker, unable to reproduce high frequencies, R-weighted sound showed the lowest sound levels. In conclusion, without a correct weighting system and proper equipment, the final sound level of an exposure stimulus can differ by several decibels from that intended. To achieve reliable and comparable results, standardization of sound experiments and assessment of the environment in animal facilities is a necessity. Hence, the use of appropriate species-specific sound pressure level weighting is essential. R-weighting for rats in sound studies is recommended.     

Thermocron iButton and iBBat temperature dataloggers emit ultrasound

Thermocron iButton dataloggers are widely used to measure thermal microclimates experienced by wild animals. The iBBat is a smaller version of the datalogger, also commercially available, that is used to measure animal skin or core body temperatures when attached externally or surgically implanted. Field observations of bats roosting under a bridge suggested that bats avoided locations with iButtons. A heterodyne bat detector revealed that the dataloggers emitted ultrasound which was detectable from a distance of up to 30 cm. We therefore recorded and quantified the acoustic properties [carrier frequency (Hz) and root mean square sound pressure level (dB SPL)] of iButton and iBBat dataloggers. All units emitted a 32.9 kHz pure tone that was readily picked up with a time expansion bat detector at a distance of 1 cm, and most were detected at a distance of 15 cm. The maximum amplitude of iButton dataloggers was 46.5 dB SPL at 1.0 cm—a level within the range of auditory sensitivity for most small mammals. Wrapping iButtons in plastic insulation severely attenuated the amplitude of ultrasound. Although there was a statistically significant reduction in rates of warming and cooling with insulation, this effect was small and we suggest that insulation may be a viable solution to eliminate unwanted ultrasonic noise in instances when small delays in thermal response dynamics are not a concern. We recommend behavioural studies to assess if the electronic signals emitted by iButtons are disturbing to small mammals.     

Sound reception in marine mammals depending on sound parameters and conduction pathways

The interaction of complex sounds with the body tissues of Black Sea dolphin (Tursiops truncatus) was studied by the method of instrumental conditioned reflexes with food reinforcement. The thresholds of detecting underwater acoustic signals of different frequencies for dolphin and northern fur seal (Callorhinus ursinus) were measured as a function of pulse duration under conditions of full and partial (head above water) submergence of animals into water. It was found that sound conduction through dolphin tissues was more effective than that in a northern fur seal in a wide frequency range. Presumably, the process of sound propagation in dolphin is accompanied by changes in the amplitude-frequency structure of broad-band sounds. The temporal summation in dolphin hearing was observed at all frequencies under conditions of full and partial submergence, whereas in northern fur seal it was nearly absent at a frequency of 5 kHz under the conditions of head lifting above water.     

Sound localization by the bottlenose porpoise Tursiops truncatus.

1. Sound localization was measured behaviourally for the Atlantic bottlenose porpoise (Tursiops truncatus) using a wide range of pure tone pulses as well as clicks simulating the species echolocation click. 2. Measurements of the minimum audible angle (MAA) on the horizontal plane give localization discrimination thresholds of between 2 and 3 degrees for sounds from 20 to 90 kHz and thresholds from 2-8 to 4 degrees at 6, 10 and 100 kHz. With the azimuth of the animal changed relative to the speakers the MAAs were 1-3-1-5 degrees at an azimuth of 15 degrees and about 5 degrees for an azimuth of 30 degrees. 3. MAAs to clicks were 0-7-0-8 degrees. 4. The animal was able to do almost as well in determining the position of vertical sound sources as it could for horizontal localization. 5. The data indicate that at low frequencies the animal may have been localizing by using the region around the external auditory meatus as a detector, but at frequencies about 20 kHz it is likely that the animal was detecting sounds through the lateral sides of the lower jaw. 6. Above 20 kHz, it is likely that the animal was localizing using binaural intensity cues. 7. Our data support evidence that the lower jaw is an important channel for sound detection in Tursiops.     

Sounds audible to migrating birds

We have measured sound levels from frog choruses in eastern New York State at altitudes of up to several hundred metres. Rana pipiens choruses from small ponds often could be recorded by a radio microphone up to 500 m, and on an especially favourable night with light winds they were clearly audible even at 965 m at about 20 dB SPL in the 1·5 to 2·5 2·5 kHz frequency band. Sound travels upward much farther and more predictably than along the surface. Many natural sounds, including those from frogs, insects, whitecaps, and perhaps wind-blown vegetation, arise from large areas and therefore act as extended sources. The intensities of such sounds decrease with altitude more slowly than expected from the inverse square law. Natural sound fields provide migrating birds with a potential source of information about the kind of land or water below them, and their progress over acoustic landmarks could inform them about wind velocity. Because atmospheric absorption increases with frequency, several hundred metres of air act as a low-pass filter, so that altitude could be estimated from the relative reduction of higher frequencies in a familiar sound.     

Adaptations in the Mouse Auditory System for Perception of Ultrasonic Communication Calls

Ultrasonic calls in the frequency range of 40–80 kHz play an important role in sound communication of house mice. The processing of ultrasounds is enhanced by overrepresentation of the corresponding frequency range in the inferior colliculus and auditory cortex. The latter has an ultrasonic field that is distinct from the tonotopy of the primary auditory cortex and has connections with brain areas of multi-sensory, motivational, and motor control. Mechanisms, such as critical band filtering and categorical perception, ensure that ultrasounds can easily be discriminated from other sounds of the mouse acoustic repertoire.