Using individual-based bioenergetic models to predict the aggregate effects of disturbance on populations: A case study with beaked whales and Navy sonar.

Anthropogenic activities can lead to changes in animal behavior. Predicting population consequences of these behavioral changes requires integrating short-term individual responses into models that forecast population dynamics across multiple generations. This is especially challenging for long-lived animals, because of the different time scales involved. Beaked whales are a group of deep-diving odontocete whales that respond behaviorally when exposed to military mid-frequency active sonar (MFAS), but the effect of these nonlethal responses on beaked whale populations is unknown. Population consequences of aggregate exposure to MFAS was assessed for two beaked whale populations that are regularly present on U.S. Navy training ranges where MFAS is frequently used. Our approach integrates a wide range of data sources, including telemetry data, information on spatial variation in habitat quality, passive acoustic data on the temporal pattern of sonar use and its relationship to beaked whale foraging activity, into an individual-based model with a dynamic bioenergetic module that governs individual life history. The predicted effect of disturbance from MFAS on population abundance ranged between population extinction to a slight increase in population abundance. These effects were driven by the interaction between the temporal pattern of MFAS use, baseline movement patterns, the spatial distribution of prey, the nature of beaked whale behavioral response to MFAS and the top-down impact of whale foraging on prey abundance. Based on these findings, we provide recommendations for monitoring of marine mammal populations and highlight key uncertainties to help guide future directions for assessing population impacts of nonlethal disturbance for these and other long-lived animals.

Discrete-space continuous-time models of marine mammal exposure to Navy sonar.

Assessing the patterns of wildlife attendance to specific areas is relevant across many fundamental and applied ecological studies, particularly when animals are at risk of being exposed to stressors within or outside the boundaries of those areas. Marine mammals are increasingly being exposed to human activities that may cause behavioral and physiological changes, including military exercises using active sonars. Assessment of the population-level consequences of anthropogenic disturbance requires robust and efficient tools to quantify the levels of aggregate exposure for individuals in a population over biologically relevant time frames. We propose a discrete-space, continuous-time approach to estimate individual transition rates across the boundaries of an area of interest, informed by telemetry data collected with uncertainty. The approach allows inferring the effect of stressors on transition rates, the progressive return to baseline movement patterns, and any difference among individuals. We apply the modeling framework to telemetry data from Blainville's beaked whale (Mesoplodon densirostris) tagged in the Bahamas at the Atlantic Undersea Test and Evaluation Center (AUTEC), an area used by the U.S. Navy for fleet readiness training. We show that transition rates changed as a result of exposure to sonar exercises in the area, reflecting an avoidance response. Our approach supports the assessment of the aggregate exposure of individuals to sonar and the resulting population-level consequences. The approach has potential applications across many applied and fundamental problems where telemetry data are used to characterize animal occurrence within specific areas.

Diving behaviour of Cuvier's beaked whales exposed to two types of military sonar.

Cuvier's beaked whales (Ziphius cavirostris) have stranded in association with mid-frequency active sonar (MFAS) use, and though the causative mechanism linking these events remains unclear, it is believed to be behaviourally mediated. To determine whether MFAS use was associated with behavioural changes in this species, satellite tags were used to record the diving and movements of 16 Cuvier's beaked whales for up to 88 days in a region of frequent MFAS training off the coast of Southern California. Tag data were combined with summarized records of concurrent bouts of high-power, surface-ship and mid-power, helicopter-deployed MFAS use, along with other potential covariates, in generalized additive mixed-effects models. Deep dives, shallow dives and surface intervals tended to become longer during MFAS use, with some variation associated with the total amount of overlapping MFAS during the behaviour. These changes in dives and surface intervals contributed to a longer interval between deep dives, a proxy for foraging disruption in this species. Most responses intensified with proximity and were more pronounced during mid-power than high-power MFAS use at comparable distances within approximately 50 km, despite the significantly lower source level of mid-power MFAS. However, distance-mediated responses to high-power MFAS, and increased deep dive intervals during mid-power MFAS, were evident up to approximately 100 km away.

First long-term behavioral records from Cuvier's beaked whales (Ziphius cavirostris) reveal record-breaking dives.

Cuvier's beaked whales (Ziphius cavirostris) are known as extreme divers, though behavioral data from this difficult-to-study species have been limited. They are also the species most often stranded in association with Mid-Frequency Active (MFA) sonar use, a relationship that remains poorly understood. We used satellite-linked tags to record the diving behavior and locations of eight Ziphius off the Southern California coast for periods up to three months. The effort resulted in 3732 hr of dive data with associated regional movements--the first dataset of its kind for any beaked whale--and included dives to 2992 m depth and lasting 137.5 min, both new mammalian dive records. Deep dives had a group mean depth of 1401 m (s.d. = 137.8, n = 1142) and duration of 67.4 min (s.d. = 6.9). The group mean time between deep dives was 102.3 min (s.d. = 30.8, n = 783). While the previously described stereotypic pattern of deep and shallow dives was apparent, there was considerable inter- and intra-individual variability in most parameters. There was significant diel behavioral variation, including increased time near the surface and decreased shallow diving at night. However, maximum depth and the proportion of time spent on deep dives (presumed foraging), varied little from day to night. Surprisingly, tagged whales were present within an MFA sonar training range for 38% of days locations were received, and though comprehensive records of sonar use during tag deployments were not available, we discuss the effects frequent acoustic disturbance may have had on the observed behaviors. These data better characterize the true behavioral range of this species, and suggest caution should be exercised when drawing conclusions about behavior using short-term datasets.

First direct measurements of behavioural responses by Cuvier's beaked whales to mid-frequency active sonar.

Most marine mammal- strandings coincident with naval sonar exercises have involved Cuvier's beaked whales (Ziphius cavirostris). We recorded animal movement and acoustic data on two tagged Ziphius and obtained the first direct measurements of behavioural responses of this species to mid-frequency active (MFA) sonar signals. Each recording included a 30-min playback (one 1.6-s simulated MFA sonar signal repeated every 25 s); one whale was also incidentally exposed to MFA sonar from distant naval exercises. Whales responded strongly to playbacks at low received levels (RLs; 89-127 dB re 1 µPa): after ceasing normal fluking and echolocation, they swam rapidly, silently away, extending both dive duration and subsequent non-foraging interval. Distant sonar exercises (78-106 dB re 1 µPa) did not elicit such responses, suggesting that context may moderate reactions. The observed responses to playback occurred at RLs well below current regulatory thresholds; equivalent responses to operational sonars could elevate stranding risk and reduce foraging efficiency.

Blue whales respond to simulated mid-frequency military sonar.

Mid-frequency military (1-10 kHz) sonars have been associated with lethal mass strandings of deep-diving toothed whales, but the effects on endangered baleen whale species are virtually unknown. Here, we used controlled exposure experiments with simulated military sonar and other mid-frequency sounds to measure behavioural responses of tagged blue whales (Balaenoptera musculus) in feeding areas within the Southern California Bight. Despite using source levels orders of magnitude below some operational military systems, our results demonstrate that mid-frequency sound can significantly affect blue whale behaviour, especially during deep feeding modes. When a response occurred, behavioural changes varied widely from cessation of deep feeding to increased swimming speed and directed travel away from the sound source. The variability of these behavioural responses was largely influenced by a complex interaction of behavioural state, the type of mid-frequency sound and received sound level. Sonar-induced disruption of feeding and displacement from high-quality prey patches could have significant and previously undocumented impacts on baleen whale foraging ecology, individual fitness and population health.

Sighting characteristics and photo-identification of Cuvier's beaked whales (Ziphius cavirostris) near San Clemente Island, California: a key area for beaked whales and the military?

The relationship between beaked whales and certain anthropogenic sounds remains poorly understood and of great interest. Although Cuvier's beaked whales (Ziphius cavirostris) are widely distributed, little is known of their behavior and population structure throughout much of their range. We conducted a series of five combined visual-acoustic marine mammal surveys from 2006 to 2008 in the southern San Nicolas Basin, a site of frequent naval activity off the southern California coast, west of San Clemente Island. The study area was defined by a 1,800 km2 array of 88 bottom-mounted hydrophones at depths up to 1,850 m. The array was used to vector visual observers toward vocalizing marine mammal species. Thirty-seven groups of Cuvier's beaked whales were encountered during the study period. The overall encounter rate was one group for every 21.0 h of survey effort, and was as high as one group per 10.2 h of effort during the October 2007 survey. Whales were encountered in the deepest portion of the study area, at a mean bottom depth of 1,580 m (SD 138). The average group size was 3.8 individuals (SD 2.4), which was higher than has been reported from other studies of this species. Twenty-four groups were observed over multiple surfacings (median = 4 surfacings, range 2-15). The mean encounter duration of extended sightings was 104 min (SD 98, range 12-466 min) and the mean distance moved over the course of sightings was 1.66 km (SD 1.56, range 0.08-6.65 km). Temporal surfacing patterns during extended encounters were similar to dive behavior described from Cuvier's beaked whales carrying time-depth recording tags. Seventy-eight photographic identifications were made of 58 unique individuals, for an overall resighting rate of 0.26. Whales were sighted on up to 4 days, with duration from first to last sighting spanning 2-79 days. For those whales sighted on subsequent days, the mean distance between subsequent sightings was 8.6 km (SD 7.9). Individuals resighted over 2-3 days were usually in association with previous group members. Approximately one-third of groups contained more than one adult male, and many of the repeated associations involved adult males. These observations suggest the basin west of San Clemente Island may be an important region for Cuvier's beaked whales, and also one which affords an unusual opportunity to collect detailed data on this species. Given its status as an active military range, it can also provide the ability to monitor the behavior of individuals in the presence of naval sonar, a critical step in the management of this and other beaked whale populations worldwide.