Patrick J. O. Miller

Sperm whale behaviour indicates the use of echolocation click buzzes 'creaks' in prey capture

During foraging dives, sperm whales (Physeter macrocephalus) produce long series of regular clicks at 0.5–2 s intervals interspersed with rapid–click buzzes called ‘creaks’. Sound, depth and orientation recording Dtags were attached to 23 whales in the Ligurian Sea and Gulf of Mexico to test whether the behaviour of diving sperm whales supports the hypothesis that creaks are produced during prey capture. Sperm whales spent most of their bottom time within one or two depth bands, apparently feeding in vertically stratified prey layers. Creak rates were highest during the bottom phase: 99.8% of creaks were produced in the deepest 50% of dives, 57% in the deepest 15% of dives. Whales swam actively during the bottom phase, producing a mean of 12.5 depth inflections per dive. A mean of 32% of creaks produced during the bottom phase occurred within 10 s of an inflection (13 x more than chance). Sperm whales actively altered their body orientation throughout the bottom phase with significantly increased rates of change during creaks, reflecting increased manoeuvring. Sperm whales increased their bottom foraging time when creak rates were higher. These results all strongly support the hypothesis that creaks are an echolocation signal adapted for foraging, analogous to terminal buzzes in taxonomically diverse echolocating species.

Swimming gaits, passive drag and buoyancy of diving sperm whales Physeter macrocephalus.

SUMMARY Drag and buoyancy are two primary external forces acting on diving marine mammals. The strength of these forces modulates the energetic cost of movement and may influence swimming style (gait). Here we use a high-resolution digital tag to record depth, 3-D orientation, and sounds heard and produced by 23 deep-diving sperm whales in the Ligurian Sea and Gulf of Mexico. Periods of active thrusting versus gliding were identified through analysis of oscillations measured by a 3-axis accelerometer. Accelerations during 382 ascent glides of five whales (which made two or more steep ascents and for which we obtained a measurement of length) were strongly affected by depth and speed at Reynolds numbers of 1.4–2.8×107. The accelerations fit a model of drag, air buoyancy and tissue buoyancy forces with an r2 of 99.1–99.8% for each whale. The model provided estimates (mean ± s.d.) of the drag coefficient (0.00306±0.00015), air carried from the surface (26.4±3.9 l kg-3 mass), and tissue density (1030±0.8 kg m-3) of these five animals. The model predicts strong positive buoyancy forces in the top 100 m of the water column, decreasing to near neutral buoyancy at 250–850 m. Mean descent speeds (1.45±0.19 m s-1) were slower than ascent speeds (1.63±0.22 m s-1), even though sperm whales stroked steadily (glides 5.3±6.3%) throughout descents and employed predominantly stroke-and-glide swimming (glides 37.7±16.4%) during ascents. Whales glided more during portions of dives when buoyancy aided their movement, and whales that glided more during ascent glided less during descent (and vice versa), supporting the hypothesis that buoyancy influences behavioural swimming decisions. One whale rested at∼ 10 m depth for more than 10 min without fluking, regulating its buoyancy by releasing air bubbles.

Quantitative measures of air-gun pulses recorded on sperm whales (Physeter macrocephalus) using acoustic tags during controlled exposure experiments

The widespread use of powerful, low-frequency air-gun pulses for seismic seabed exploration has raised concern about their potential negative effects on marine wildlife. Here, we quantify the sound exposure levels recorded on acoustic tags attached to eight sperm whales at ranges between 1.4 and 12.6 km from controlled air-gun array sources operated in the Gulf of Mexico. Due to multipath propagation, the animals were exposed to multiple sound pulses during each firing of the array with received levels of analyzed pulses falling between 131-167 dB re. 1 microPa (pp) [111-147 dB re. 1 microPa (rms) and 100-135 dB re. 1 microPa2 s] after compensation for hearing sensitivity using the M-weighting. Received levels varied widely with range and depth of the exposed animal precluding reliable estimation of exposure zones based on simple geometric spreading laws. When whales were close to the surface, the first arrivals of air-gun pulses contained most energy between 0.3 and 3 kHz, a frequency range well beyond the normal frequencies of interest in seismic exploration. Therefore air-gun arrays can generate significant sound energy at frequencies many octaves higher than the frequencies of interest for seismic exploration, which increases concern of the potential impact on odontocetes with poor low frequency hearing.

Female philopatry in coastal basins and male dispersion across the North Atlantic in a highly mobile marine species, the sperm whale (Physeter macrocephalus).

The mechanisms that determine population structure in highly mobile marine species are poorly understood, but useful towards understanding the evolution of diversity, and essential for effective conservation and management. In this study, we compare putative sperm whale populations located in the Gulf of Mexico, western North Atlantic, Mediterranean Sea and North Sea using mtDNA control region sequence data and 16 polymorphic microsatellite loci. The Gulf of Mexico, western North Atlantic and North Sea populations each possessed similar low levels of haplotype and nucleotide diversity at the mtDNA locus, while the Mediterranean Sea population showed no detectable mtDNA diversity. Mitochondrial DNA results showed significant differentiation between all populations, while microsatellites showed significant differentiation only for comparisons with the Mediterranean Sea, and at a much lower level than seen for mtDNA. Samples from either side of the North Atlantic in coastal waters showed no differentiation for mtDNA, while North Atlantic samples from just outside the Gulf of Mexico (the western North Atlantic sample) were highly differentiated from samples within the Gulf at this locus. Our analyses indicate a previously unknown fidelity of females to coastal basins either side of the North Atlantic, and suggest the movement of males among these populations for breeding.

Genetic differentiation among North Atlantic killer whale populations

Population genetic structure of North Atlantic killer whale samples was resolved from differences in allele frequencies of 17 microsatellite loci, mtDNA control region haplotype frequencies and for a subset of samples, using complete mitogenome sequences. Three significantly differentiated populations were identified. Differentiation based on microsatellite allele frequencies was greater between the two allopatric populations than between the two pairs of partially sympatric populations. Spatial clustering of individuals within each of these populations overlaps with the distribution of particular prey resources: herring, mackerel and tuna, which each population has been seen predating. Phylogenetic analyses using complete mitogenomes suggested two populations could have resulted from single founding events and subsequent matrilineal expansion. The third population, which was sampled at lower latitudes and lower density, consisted of maternal lineages from three highly divergent clades. Pairwise population differentiation was greater for estimates based on mtDNA control region haplotype frequencies than for estimates based on microsatellite allele frequencies, and there were no mitogenome haplotypes shared among populations. This suggests low or no female migration and that gene flow was primarily male mediated when populations spatially and temporally overlap. These results demonstrate that genetic differentiation can arise through resource specialization in the absence of physical barriers to gene flow.

Killer whales are capable of vocal learning

The production learning of vocalizations by manipulation of the sound production organs to alter the physical structure of sound has been demonstrated in only a few mammals. In this natural experiment, we document the vocal behaviour of two juvenile killer whales, Orcinus orca, separated from their natal pods, which are the only cases of dispersal seen during the three decades of observation of their populations. We find mimicry of California sea lion (Zalophus californianus) barks, demonstrating the vocal production learning ability for one of the calves. We also find differences in call usage (compared to the natal pod) that may reflect the absence of a repertoire model from tutors or some unknown effect related to isolation or context.

The Severity of behavioral changes observed during experimental exposures of killer (Orcinus orca), long-finned Pilot (Globicephala melas), and sperm (Physeter macrocephalus) whales to naval sonar

This study describes behavioral changes of wild cetaceans observed during controlled exposures of naval sonar. In 2006 through 2009, 14 experiments were conducted with killer (n = 4), long-finned pilot (n = 6), and sperm (n = 4) whales. A total of 14 6-7 kHz upsweep, 13 1-2 kHz upsweep, and five 1-2 kHz downsweep sonar exposures, as well as seven Silent vessel control exposure sessions and eight playbacks of killer whale sounds were conducted. Sonar signals were transmitted by a towable source that approached each tagged subject from a starting distance of 6 to 8 km with a ramp up of source levels (from 152 to 158 to a maximum of 198 to 214 dB re: 1 μPa m). This procedure resulted in a gradual escalation of the sonar received level at the whale, measured by towed hydrophones and by tags that record movement and sound (Dtags). Observers tracked the position of each tagged animal and recorded group-level surface behavior. Two expert panels independently scored the severity of diverse behavioral changes observed during each sonar and control exposure, using the 0 to 9 point severity scale of Southall et al. (2007), and then reached consensus with a third-party moderator. The most severe responses scored (i.e., most likely to affect vital rates) included a temporary separation of a calf from its group, cessation of feeding or resting, and avoidance movements that continued after the sonar stopped transmitting. Higher severity scores were more common during sonar exposure than during Silent control sessions. Scored responses started at lower sound pressure levels (SPLs) for killer whales and were more severe during sonar exposures to killer and sperm whales than to long-finned pilot whales. Exposure sessions with the higher source level of 1 to 2 kHz sonar had more changes and a trend for higher maximum severity than 6 to 7 kHz sessions, but the order of the sessions had no effect. This approach is helpful to standardize the description of behavioral changes that occurred during our experiments and to identify and describe the severity of potential responses of free-ranging cetaceans to sonar.

The influence of social affiliation on individual vocal signatures of northern resident killer whales (Orcinus orca)

Northern resident killer whales (Orcinus orca) live in highly stable groups and use group-specific vocal signals, but individual variation in calls has not been described previously. A towed beam-forming array was used to ascribe stereotyped pulsed calls with two independently modulated frequency contours to visually identified individual killer whales in Johnstone Strait, British Columbia. Overall, call similarity determined using neural networks differed significantly between different affiliation levels for both frequency components of all the call types analysed. This method distinguished calls from individuals within the same matriline better than different calls produced by a single individual and better than by chance. The calls of individuals from different matrilines were more distinctive than those within the same matriline, confirming previous studies based on group recordings. These results show that frequency contours of stereotyped calls differ among the individuals that are constantly associated with each other and use group-specific vocalizations, though across-group differences were substantially more pronounced.

Northern elephant seals adjust gliding and stroking patterns with changes in buoyancy: validation of at-sea metrics of body density

SUMMARY Many diving animals undergo substantial changes in their body density that are the result of changes in lipid content over their annual fasting cycle. Because the size of the lipid stores reflects an integration of foraging effort (energy expenditure) and foraging success (energy assimilation), measuring body density is a good way to track net resource acquisition of free-ranging animals while at sea. Here, we experimentally altered the body density and mass of three free-ranging elephant seals by remotely detaching weights and floats while monitoring their swimming speed, depth and three-axis acceleration with a high-resolution data logger. Cross-validation of three methods for estimating body density from hydrodynamic gliding performance of freely diving animals showed strong positive correlation with body density estimates obtained from isotope dilution body composition analysis over density ranges of 1015 to 1060 kg m–3. All three hydrodynamic models were within 1% of, but slightly greater than, body density measurements determined by isotope dilution, and therefore have the potential to track changes in body condition of a wide range of freely diving animals. Gliding during ascent and descent clearly increased and stroke rate decreased when buoyancy manipulations aided the direction of vertical transit, but ascent and descent speed were largely unchanged. The seals adjusted stroking intensity to maintain swim speed within a narrow range, despite changes in buoyancy. During active swimming, all three seals increased the amplitude of lateral body accelerations and two of the seals altered stroke frequency in response to the need to produce thrust required to overcome combined drag and buoyancy forces.

Nonlinear phenomena in the vocalizations of North Atlantic right whales (Eubalaena glacialis) and killer whales (Orcinus orca).

Nonlinear phenomena or nonlinearities in animal vocalizations include features such as subharmonics, deterministic chaos, biphonation, and frequency jumps that until recently were generally ignored in acoustic analyses. Recent documentation of these phenomena in several species suggests that they may play a communicative role, though the exact function is still under investigation. Here, qualitative descriptions and quantitative analyses of nonlinearities in the vocalizations of killer whales (Orcinus orca) and North Atlantic right whales (Eubalaena glacialis) are provided. All four nonlinear features were present in both species, with at least one feature occurring in 92.4% of killer and 65.7% of right whale vocalizations analyzed. Occurrence of biphonation varied the most between species, being present in 89.0% of killer whale vocalizations and only 20.4% of right whale vocalizations. Because deterministic chaos is qualitatively and quantitatively different than random or Gaussian noise, a program (TISEAN) designed specifically to identify deterministic chaos to confirm the presence of this nonlinearity was used. All segments tested in this software indicate that both species do indeed exhibit deterministic chaos. The results of this study provide confirmation that such features are common in the vocalizations of cetacean species and lay the groundwork for future studies.