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Federal Register / Vol. 86, No. 23 / Friday, February 5, 2021 / Notices more generally, moderation in response to human disturbance Bejder et al., 2009. The opposite process is sensitization, when an unpleasant experience leads to subsequent responses, often in the form of avoidance, at a lower level of exposure.
As noted, behavioral state may affect the type of response. For example, animals that are resting may show greater behavioral change in response to disturbing sound levels than animals that are highly motivated to remain in an area for feeding Richardson et al., 1995; NRC, 2003; Wartzok et al., 2003.
Controlled experiments with captive marine mammals have showed pronounced behavioral reactions, including avoidance of loud sound sources Ridgway et al., 1997; Finneran et al., 2003. Observed responses of wild marine mammals to loud impulsive sound sources typically airguns or acoustic harassment devices have been varied but often consist of avoidance behavior or other behavioral changes suggesting discomfort Morton and Symonds, 2002; see also Richardson et al., 1995; Nowacek et al., 2007.
However, many delphinids approach low-frequency airgun source vessels with no apparent discomfort or obvious behavioral change e.g., Barkaszi et al., 2012, indicating the importance of frequency output in relation to the species hearing sensitivity.
Available studies show wide variation in response to underwater sound;
therefore, it is difficult to predict specifically how any given sound in a particular instance might affect marine mammals perceiving the signal. If a marine mammal does react briefly to an underwater sound by changing its behavior or moving a small distance, the impacts of the change are unlikely to be significant to the individual, let alone the stock or population. However, if a sound source displaces marine mammals from an important feeding or breeding area for a prolonged period, impacts on individuals and populations could be significant e.g., Lusseau and Bejder, 2007; Weilgart, 2007; NRC, 2005. However, there are broad categories of potential response, which we describe in greater detail here, that include alteration of dive behavior, alteration of foraging behavior, effects to breathing, interference with or alteration of vocalization, avoidance, and flight.
Changes in dive behavior can vary widely and may consist of increased or decreased dive times and surface intervals as well as changes in the rates of ascent and descent during a dive e.g., Frankel and Clark, 2000; Costa et al., 2003; Ng and Leung, 2003; Nowacek et al., 2004; Goldbogen et al., 2013a,b.

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Variations in dive behavior may reflect interruptions in biologically significant activities e.g., foraging or they may be of little biological significance. The impact of an alteration to dive behavior resulting from an acoustic exposure depends on what the animal is doing at the time of the exposure and the type and magnitude of the response.
Disruption of feeding behavior can be difficult to correlate with anthropogenic sound exposure, so it is usually inferred by observed displacement from known foraging areas, the appearance of secondary indicators e.g., bubble nets or sediment plumes, or changes in dive behavior. As for other types of behavioral response, the frequency, duration, and temporal pattern of signal presentation, as well as differences in species sensitivity, are likely contributing factors to differences in response in any given circumstance e.g., Croll et al., 2001; Nowacek et al.
2004; Madsen et al., 2006; Yazvenko et al., 2007. An understanding of the energetic requirements of the affected individuals and the relationship between prey availability, foraging effort and success, and the life history stage of the animal can facilitate the assessment of whether foraging disruptions are likely to incur fitness consequences.
Variations in respiration naturally vary with different behaviors and alterations to breathing rate as a function of acoustic exposure can be expected to co-occur with other behavioral reactions, such as a flight response or an alteration in diving.
However, respiration rates in and of themselves may be representative of annoyance or an acute stress response.
Various studies have shown that respiration rates may either be unaffected or could increase, depending on the species and signal characteristics, again highlighting the importance in understanding species differences in the tolerance of underwater noise when determining the potential for impacts resulting from anthropogenic sound exposure e.g., Kastelein et al., 2001, 2005, 2006; Gailey et al., 2007; Gailey et al., 2016.
Marine mammals vocalize for different purposes and across multiple modes, such as whistling, echolocation click production, calling, and singing.
Changes in vocalization behavior in response to anthropogenic noise can occur for any of these modes and may result from a need to compete with an increase in background noise or may reflect increased vigilance or a startle response. For example, in the presence of potentially masking signals, humpback whales and killer whales have been observed to increase the
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length of their songs Miller et al., 2000;
Fristrup et al., 2003; Foote et al., 2004, while North Atlantic right whales have been observed to shift the frequency content of their calls upward while reducing the rate of calling in areas of increased anthropogenic noise Parks et al., 2007. In some cases, animals may cease sound production during production of aversive signals Bowles et al., 1994.
Avoidance is the displacement of an individual from an area or migration path as a result of the presence of a sound or other stressors, and is one of the most obvious manifestations of disturbance in marine mammals Richardson et al., 1995. For example, gray whales are known to change directiondeflecting from customary migratory pathsin order to avoid noise from airgun surveys Malme et al., 1984. Avoidance may be short-term, with animals returning to the area once the noise has ceased e.g., Bowles et al., 1994; Goold, 1996; Stone et al., 2000;
Morton and Symonds, 2002; Gailey et al., 2007. Longer-term displacement is possible, however, which may lead to changes in abundance or distribution patterns of the affected species in the affected region if habituation to the presence of the sound does not occur e.g., Blackwell et al., 2004; Bejder et al., 2006; Teilmann et al., 2006.
A flight response is a dramatic change in normal movement to a directed and rapid movement away from the perceived location of a sound source.
The flight response differs from other avoidance responses in the intensity of the response e.g., directed movement, rate of travel. Relatively little information on flight responses of marine mammals to anthropogenic signals exist, although observations of flight responses to the presence of predators have occurred Connor and Heithaus, 1996. The result of a flight response could range from brief, temporary exertion and displacement from the area where the signal provokes flight to, in extreme cases, marine mammal strandings Evans and England, 2001. However, it should be noted that response to a perceived predator does not necessarily invoke flight Ford and Reeves, 2008, and whether individuals are solitary or in groups may influence the response.
Behavioral disturbance can also impact marine mammals in more subtle ways. Increased vigilance may result in costs related to diversion of focus and attention i.e., when a response consists of increased vigilance, it may come at the cost of decreased attention to other critical behaviors such as foraging or resting. These effects have generally not
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