Physiological responses of narwhals to anthropogenic noise: a case study with seismic airguns and vessel traffic in the Arctic

Limited polar geographical range, narrowly defined migratory routes, and
deep-diving behaviors make narwhals exceptionally vulnerable to
anthropogenic disturbances including oceanic noise. Although behavioral
studies indicate marked responses of cetaceans to disturbance, the link
between fear reactions and possible injury from noise exposure is limited
for most species. To address this, we deployed custom-made heart
rate-accelerometer-depth recorders on 13 adult narwhals in Scoresby Sound,
East Greenland across a five-year period (2014-2018). Physiological
responses of the cetaceans were monitored in the absence (n = 13 animals)
or presence (n = 2 animals across 3 acoustic events) of experimentally
directed, seismic airgun pulses and associated vessels (full volume source
level = 241 dB re 1 μPa-m). We found that anthropogenic noise resulted in
marked cardiovascular, respiratory and locomotor reactions by two narwhals
exposed to seismic pulses across three acoustic events. The general
behavioral response to seismic and vessel noise included an 80% reduction
in the duration of gliding during dive descents by seismic-exposed
narwhals compared to controls, and the prolongation of high-intensity
activity (ODBA > 0.20 g) with elevated stroke frequencies exceeding
40 strokes per minute. Noise exposure also resulted intense (< 10
bpm) bradycardia that was decoupled from stroking frequency. This
decoupling instigated increased variability in heart rate, with the heart
switching rapidly between bradycardia and exercise tachycardia during
noise exposure. Maximum respiratory frequency following seismic exposure,
12 breaths.min-1, was 1.5 times control levels. Overall, the effect of
seismic/ship noise exposure on wild narwhals was a 2.0 – 2.2-fold increase
in the energetic cost of diving, which paradoxically occurred during
suppression of the cardiac exercise response. This unusual relationship
between diving heart rate and exercise intensity represents a new metric
for characterizing the level of fear reactions of wild marine mammals
exposed to different environmental stressors. Together, the multi-level
reactions to anthropogenic noise by this deep-diving cetacean demonstrated
how a cascade of effects along the entire oxygen pathway could challenge
physiological homeostasis especially if disturbance is prolonged.