Swimming and diving energetics in dolphins: a stroke-by-stroke analysis for predicting the cost of flight responses in wild odontocetes

Abstract

Exponential increases in hydrodynamic drag and physical exertion occur when swimmers move quickly through water, and underlie the preference for relatively slow routine speeds by marine mammals regardless of body size. Because of this and the need to balance limited oxygen stores when submerged, flight (escape) responses may be especially challenging for this group. To examine this, we used open-flow respirometry to measure the energetic cost of producing a swimming stroke during different levels of exercise in bottlenose dolphins (Tursiops truncatus). These data were then used to model the energetic cost of high-speed escape responses by other odontocetes ranging in mass from 42 to 2738 kg. The total cost per stroke during routine swimming by dolphins, 3.31± 0.20 J kg ), representing the cost of moving the flukes, revealed that LC during routine swimming increased with body mass (M ) for odontocetes according to LC=1.46±0.0005M; a separate relationship described LC during high-speed stroking. Using these relationships, we found that continuous stroking coupled with reduced glide time in response to oceanic noise resulted in a 30.5% increase in metabolic rate in the beaked whale, a deep-diving odontocete considered especially sensitive to disturbance. By integrating energetics with swimming behavior and dive characteristics, this study demonstrates the physiological consequences of oceanic noise on diving mammals, and provides a powerful tool for predicting the biological significance of escape responses by cetaceans facing anthropogenic disturbances.

Understanding the population consequences of disturbance

“…Most studies (e.g., Williams, Lusseau, & Hammond, ) have evaluated the decrease in energy intake due to the observed behavioral responses. However, there have been efforts to quantify the change in energy expenditure associated with avoidance responses (Braithwaite et al., ; Christiansen, Rasmussen, & Lusseau, ; Miller et al., ; Williams, Blackwell, Richter, Sinding, & Heide‐Jørgensen, ; Williams, Kendall, et al., ). Measuring physiological responses to disturbance is more challenging than measuring behavioral responses, and may require the analysis of tissue, exhalations, or feces from wild animals (Hogg et al., ; Rolland et al., ), dedicated physiological tags (Karpovich, Skinner, Mondragon, & Blundell, ; Williams, Blackwell, et al., ; Wilson, Wikelski, Wilson, & Cooke, ), or experiments in captivity (Kvadsheim, Sevaldsen, Folkow, & Blix, ; Miksis et al., ; Thomas, Kastelein, & Awbrey, ).…”

Discrimination between bycatch and other causes of cetacean and pinniped stranding

“…Strenuous activity, such as the reaction of an animal when it realizes that it is entrapped, creates more metabolic demand than the animal may be adapted for. The metabolic rate of an odontocete may increase 30% in a flight response (Williams et al 2017). The mechanisms that marine mammals use to compensate for long periods of breath-holding at depths (alveolar collapse, tracheobronchial compression, and blood redistribution; Piantadosi & Thalmann 2004, Moore et al 2011) may inhibit inspiration during forced submersion (Berta et al 2006), leading to cardiac inhibition and severe laryngospasm, hy po xia, and convulsions (Papa dodima et al 2010).…”

Delphinid brain development from neonate to adulthood with comparisons to other cetaceans and artiodactyls

“…, Noren , Williams et al . ). The metabolic rate of adult bottlenose dolphins and killer whales is much higher than the value predicted by Kleiber's law, which states that an animal's metabolic rate scales to the 0.75 power of its body mass (Noren , Williams et al .…”