Acoustic noise is one of the major anthropogenic impacts on marine mammal life. To date, the majority of studies have examined the effect of loud noise on hearing and behavioral response in marine mammals. On the other hand, physiological parameters are often used to evaluate the response and state of the autonomic nervous system of humans and terrestrial mammals under the conditions of anxiety and stress as well as when exposed to a fatiguing acoustic noise. The objectives of this study were to investigate the effect of acoustic noise on the heart rate (HR) and breathing pattern in belugas.

The study was conducted on 2 young belugas housed at the Utrish Marine Station of RAS. The belugas were exposed to an octave band acoustic noise (frequency: 9.5-13, 19-27, 27-38, 54-78, 78-108 kHz; intensity: 140-165dB; duration 1, 3, 10 and 30 min). The frequency of noise overlapped the range of best hearing for the beluga. Two series of experiments were conducted in beluga 1: 2 months after capture when the animal was about 1-year old and then one year later when the animal was about 2-year old. Beluga 2 was studied when it was 1.5-2.0 years, one year after it had been captured.

The HR of the beluga laying on the stretcher was characterized by expressed arrhythmia: periods of bradycardia (instantaneous HR decreased to 20 beats/min), which accounted for the phase of breath holding or apneas (respiration pauses longer than 60 s) that alternated with periods of accelerated HR (up to 85 beats/min) concurrent with a series of respiration acts (2–10 inspirations over 30s intervals).

In the first series of experiments, acoustic noise evoked a HR acceleration in beluga 1 (age about 1 year), manifesting tachycardia. The instantaneous HR reached the maximum (up to 100 beats/min, 15 beats/min greater than the baseline values). When the noise was continued (10-30 min) tachycardia lasted up to 5 min and was replaced by bradycardia. The minimal instantaneous HR at that time was 12 beats/min. The pattern of breathing changed simultaneously with the HR acceleration changes: the proportion of short BP (<20 sec) increased and the ratio of long BP (>60 sec) increased. In beluga 2 (age 1.5-2.0 years) the response to acoustic noise was opposite: the instantaneous HR decreased (5 beats/min during the first noise presentation) and remained low for 4 min. The changes of breathing pattern were also opposite: the proportion of short BP decreased while the proportion of long BP increased.

In both belugas1 (series 1) and 2 the expression and duration of the response to noise depended both on the noise intensity and frequency. In beluga 1 a 150 dB acoustic noise evoked a sharp HR acceleration at all noise frequencies. During the first 1-min of noise exposure the average HR increased to 210% of the baseline values. The magnitude of acceleration of HR in beluga 1 at frequencies of 19-27 and 27-38 kHz was much greater than at frequencies 54-78 and 78-108 kHz (paired comparison). The HR acceleration in response to a 1-min 140 dB noise (on average 127% greater than the baseline values; frequencies of 19-27 and 27-38 kHz) was smaller compared to 150 and 160 dB noise. In beluga 2 a 1-min 165 dB noise caused a deceleration of HR at all noise frequencies. During the first 1-min of noise exposure the average HR decreased to 20% of the baseline values. The magnitude of bradycardia was the highest at the noise frequency of 9.5-13 kHz (the average HR was 45% lower than the baseline values) and progressively decreased when the frequency was changed to 78-108 kHz (74%). However, the effect of the noise frequency on the HR response in beluga 2 was not significant. In beluga 2 the degree of evoked bradycardia was similar at all employed noise intensities (145-165 dB) varying between 50 and 64% of the HR baseline values.

In both beluga 1 (series 1) and 2, the HR changes caused by an acoustic noise lasting longer than 1 min were not limited to the first minute of the noise presentation. Thus, in beluga 1 for the noise frequency of 19-27 kHz the evoked tachycardia lasted for a minimum of 4 min, so the average 1-min HR significantly exceeded the baseline values during this time. For higher frequencies the increase of HR over the control values was significant only for the first minute of noise exposure. In beluga 2 the bradycardia caused by the noise within the frequencies of 9.5-13, 19-27 and 38-54 kHz was much lower than the average HR during the first 3 min of the exposure.

In beluga 1 in the second series (age of 1.5-2.0 years) the instantaneous HR increased during the 1st min of the noise exposure. However, this increase was significant only for the lowest frequency – 9.5-13 kHz. The tachycardia and bradycardia recorded in belugas 1and 2 are physiological reactions to startling. Acceleration of HR recorded in beluga 1 (a calf aged about 1 year old captured 2 months before the study) in response to noise is the first component of the ―acoustic startle response which has been studied in details in humans and terrestrial mammals. When familiar conditions change, HR can increase up to 60% compared to the normal values. This acceleration is considered the cardiovascular component of the stress reaction and is accompanied by activation of the sympathetic nervous system, which in turn may cause cardiovascular and other medical problems. In beluga 1 tachycardia developed at the intensities of 140 dB; at higher intensities, the HR reached a twofold increase over the baseline values and lasted at least 5 min. Deceleration of HR recorded in beluga 2 in response to noise remains a startle response upon presentation of strong unexpected stimuli. A similar reaction was observed in manatees in response to approaching humans and it was interpreted as a cardiac response to a stressful impact.

At the same time, periodic HR accelerations and decelerations are normal for all marine mammals. In beluga 2 the temporal and frequency ranges of the HR were similar both during the normal respiratory cycle and in response to acoustic noise. However, the tachycardiac response caused by acoustic noise in beluga 1 is not typical for the normal condition and it is a stronger response to fatiguing noise.

We showed in these experiments that the response to noise in belugas is determined by parameters of noise as well as the animal individual response, their age and subsequent adaptation to the repeated noise. The intensity and duration of noise presented to the belugas in this study are lower than the levels of anthropogenic noise marine mammals may be exposed to in the ocean. Therefore, HR may serve as a criterion of physiological response to fatiguing acoustic noises, including anthropogenic, in belugas and, most likely, in other cetaceans. The breathing pattern is a less informative parameter because it depends on the HR pattern. Additional information on the animal state may be gathered via blood biochemistry.

Sourced from:

1. Severtsov Institute of Ecology and Evolution, RAS, Moscow, Russia

2. Utrish Dolphinarium Ltd., Moscow, Russia

3. University of California in Los Angeles and Sepulveda Research Corporation of Veteran Administration, USA

Lyamin O.I. (1,2,3), Korneva S.M. (2), Rozhnov V.V. (1), Mukhametov L.M. (1,2).

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