SEISMIC AND VERY LOW FREQUENCY SOUND INDUCED BEHAVIORS IN CAPTIVE LOGGERHEAD MARINE TURTLES (CARETTA CARETTA}

Martin L. Lenhardt

Virginia Commonwealth University, Richmond VA 23298-0168 USA Virginia Institute of Marine Science, Gloucester Point VA 23062-1346 USA

Little is known about the hearing range of marine turtles and even less is known how they use their hearing in surviving. These animals possess ear structures similar to that of stem reptiles, from which modern reptiles, birds and mammals have evolved. It is very likely then, that a sense of hearing proved to be advantageous in biological adaptation.

The electrical responses of the ear, i.e. cochlear potentials, yield a reasonable estimate of the frequency and intensity range of hearing in reptiles (Wever, 1978). The cochlear potential audiogram for Chelonia mydas, performed by Ridgway et ai. (1969) 1s redrawn in Figure 1. These data were collected for air conduction hearing. An audiogram for a marine species in air is informative, in that sexually mature females spend a portion of their lives on shore, but that time is relatively short. Turtles do surface to breathe and, as a consequence, the is near the aidwater boundary. The effect of water loading the eardrum, with varying degrees of pressure has not been studied. Placing a turtle underwater changes the mechanical impedance matching demands of the ear, hence the sensitivity. Using the air-water cochlear potential threshold difference for Terrapene carolina (Wever, 1978) as an approximate correction factor, the projected underwater audiogram of Chelonia mydas also appears in Figure 1.

Audiograms can be divided into three parts, the upper frequency range, the range of maximum sensitivity and the lower frequency range in which hearing feeling and seismic/gravity reception merge. The area of maximal sensitivity in marine turtles is from 100 to 800 Hz. The upper limit is about 2000 Hz. Hearing below frequencies of 80 Hz is less sensitive, nonetheless potentially serviceable to the animal. Behavioral responses to low frequency stimulation will be assessed in this pilot study.

METHODS

Two Atlantic loggerheads (Caretta caretta), weighing about 25-30 kg were maintained in separate circular tanks 1 rn in depth. Turtles were acclimated to the tank before testing. A specialized water coupled speaker (Vibra-Caustics) was placed next to the tank, coupling the water bladder of the speaker to the tank wail. A low frequency accelerometer (1-200 Hz) was placed at the abutting surfaces. A second accelerometer (.5 Hz-1gHz) was affixed to the opposite tank wall. The first accelerometer monitored the transfer of acoustic pressure into the tank and the second the interaction of the speaker with tank mechanics. A hydrophone was also suspended in the tank to measure sound pressure.

Testing did not initiate until the turtle exhibited a repeatable breathing cycle of surfacing about every ten minutes. Following breathing the turtles would rest on the bottom. After the turtles were on the bottom and motionless for two minutes, low frequency sound was presented continuously near maximal output of the amplifier, but below the point of overdriving distortion as monitored by accelerometer input into a real time spectral analyzer. Tones at 1 /3 octave intervals (20, 25, 31.5, 40, 80 Hz) as well as linear ramps over the same frequency range were employed. The saltwater loaded tank did interact with the low frequency tones such that overtones were produced 20-30 dB down from the fundamental. No attempt to attenuate the overtones was made during this preliminary study. Sound stimulation terminated after one minute or upon activation of the turtle. Five trials were run in clear water and five in algae clouded water to control for inadvertent visual cues. 0th turtles always responded to low frequency sound by swimmin typical response to the onset of sound was to swim to the surface and remain there or stay slightly returned to the bottom or stoppe swimming. The maximal level of sound stimulation delivered to th tank is depicted as vibration (and labeled "startles") in Figure 2. The zero d reference is displacement re: one micrometer RMS. Ridgway et al. (1969) placed a vibrator on the eardrum of Chelonia mydas and produced a vibration (bone conduction) audiogram. His data are also redrawn in Figure 2. Note that the sound energy that elicited the startle responses are within the measured hearing range.

Stimuli from 30 to 80 Hz are probably treated as auditory in the sense that the is likely the strongest responder. The ear of Caretta caretta suggests that since the is connected to the bone by fibroelastic strands (Lenhardt et al., 1985) this organ is also stimulated by low frequency sound when the eardrum is displaced. Such displacement would be present in the intense sound field of the tank and was certainly present in eliciting cochlear potentials (Ridgway et al., 1969). It is quite possible that only the saccule (or perhaps the lagena too) is responding in this low range since neurons in the auditory brainstem have center frequencies no lower than 140 Hz (Maniey, 1970). The lower frequency response of some units with '140 Hz center frequency extend only to 50 Hz and only if the stimuli are of sufficient intensity. It is also possible that there is an increasing degree of overlap between saccular and auditory neural tuning in these low frequencies. Auditory and otolith organs are not the only possible receptors. With the frequencies and driving intensities employed, whole animal displacement is possible. Bodily displacement could also be differentiated by eardrum phase response difference and coded in eight nerve discharge patterns.

For frequencies under 40 Hz somatosensory receptors on the skin and around internal organs that can be set into sympathetic resonance with low frequency sound are also sources of neural activation. Sound, at comparable levels, could also activate the , which might induce positional disturbance. The turtle could lessen the effects of the sound by staying near the airlwater boundary, which appears to be the overwhelming response.

Sounds between 100 and 800 Hz can be detected at lower energy levels and are likely purely auditory. Far field evoked potentials have been recorded from loggerheads (see Moein et al. this volume) and thresholds using clicks delivered by a vibrator affixed to the eardrum are in good agreement with cochlear potentials thresholds (see Figure 2). Evoked potentials can also be recorded with the turtle submerged in sea water. The difference in far field evoked potential voltage between the animal in either medium is approximately 10 dB, adding external validity to the 10 dB less sensitivity estimate of the ear underwater contrasted to the ear in air.

The use of sound stimulation in the range of maximal sensitivity has been disappointing in that consistent responses were not observed placing into doubt the feasibility of an acoustic repellent. Although limited to data on two animals in tanks, the use of very low frequency and seismic frequencies is promising. Since the patented speaker used in this study is an air type modified with a water coupling (Alton, 1994), mounting the speaker against the inside of a boat hull would result in efficient delivery of sound underwater bypassing the problems of conventional underwater sources as projectors and airlwater guns. The cost of a hull mounted water coupled speaker would be economically viable for commercial marine operations.

ound Related Technologies of Virginia each VA kindly supplied the Vibra-Coustics hydroco oudspeaker, animal maintenance costs ere partially offset by a Grant-in-Aid to the acilities were graciously rovided by the S~hoo . vergi. Physiologic., 197

roc. Nat Acad Sci.,

Reptile Ear. Princeton U. Press, 1978. 1 p Pascal

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Frequency (Hz)

Startles

Evokes