Building time-budgets from bioacoustic signals to measure population-level changes in behavior: a case study with sperm whales in the Gulf of Mexico

Evaluating changes in the collective behavior of a population can be an indirect method for inferring organismal responses to changing environmental conditions. Apex predators, such as the sperm whale (Physeter macrocephalus), can provide valuable insights into the ecosystem processes of the deep sea, where little direct observation can be made. Sperm whales are often difficult to observe at sea, as they inhabit deep, offshore waters and spend most of their lives beneath the surface. However, sperm whales are extremely amenable to passive acoustic monitoring, as their vocalizations are well-studied, highly distinguishable, produced regularly, and can be detected at relatively long ranges (>10 km). Sperm whales produce distinct clicks in two behavioral contexts (social interaction or foraging/prey capture); thus, we can use acoustic detection of these vocalizations to infer patterns of large-scale, collective behavior, which is similar to studying calling frogs or insects indicating their reproductive phenology. We recorded behaviorally-specific sperm whale vocalizations at three sites in the Northern Gulf of Mexico in July 2010 and 2011. We used these recordings to construct population-level time budgets, an empirical collective metric of behavior, based on the ratio of hours in a day with social clicks to the hours in a day with foraging clicks, and represented this as an “acoustic activity index.” Our index showed significant differences in the proportions of social and foraging behavior across the range of sperm whales in the Northern Gulf of Mexico, and the proportion of social activity increased by more than a factor of two from 2010 to 2011. These differences support previous evidence of differential habitat use by sperm whales in the Gulf of Mexico, and suggest possible changes in environmental conditions between years. Thus, the acoustic activity index may provide a powerful way to evaluate changes in behavior and link them to changing ecological conditions. This novel application of bioacoustics to constructing time budgets and creating a behaviorally-based index at the population scale can serve as an indicator of ecological change, and greatly enhance our ability to understand the behavior and ecology of many acoustically active species.     

TWO TYPES OF BLUE WHALE CALLS RECORDED IN THE GULF OF ALASKA

At one time blue whales were found throughout the Gulf of Alaska, however, none have been sighted there in post-whaling era surveys. To determine if blue whales ( Balaenoptera musculus ) might now occur in the Gulf of Alaska, an array of hydrophones was deployed there in October 1999. Data were retrieved in May 2000 and in June 2001. Spectrograms from a random subsample comprising 15% of the ∼63,000 h of data were visually examined for blue whale calls. Call types attributed to both northeastern and northwestern Pacific blue whales were recorded. Both of these call types were recorded seasonally from the initial deployment date in October 1999 through the third week of December 1999 and then from July 2000 through mid-December 2000. Both call types were regularly recorded on the same hydrophone at the same time indicating clear temporal and spatial overlap of the animals producing these calls. Two blue whale call types were recorded in the Gulf of Alaska suggesting that perhaps two stocks use this area. The northeastern call type has now been documented from the equator up to at least 55°N in the eastern North Pacific.     

ESTIMATES OF SPERM WHALE ABUNDANCE IN THE NORTHEASTERN TEMPERATE PACIFIC FROM A COMBINED ACOUSTIC AND VISUAL SURVEY

We estimate the abundance of sperm whales in a 7.8 million km² study area in the eastern temperate North Pacific using data from a ship-based acoustic and visual line-transect survey in spring 1997. Sperm whales were detected acoustically using a hydrophone array towed at 15 km/h and 100 m depth. The hydrophone array was towed for 14,500 km, and locations were estimated acoustically for 45 distinct sperm whale groups. Whales producing slow clicks (>2-s period) were detected at greater distance (up to 37 km), and the estimation of effective strip widths was stratified based on initial click period. Visual survey effort (using 25° binoculars and naked eyes) covered 8,100 km in Beaufort sea states 0–5 and resulted in only eight sightings. The effective strip width for visual detections was estimated from previous surveys conducted using the same methods and similar vessels in the eastern Pacific. Estimated sperm whale abundance in the study area was not significantly different between acoustic (32,100, CV = 0.36) and visual (26,300, CV = 0.81) detection methods. Acoustic techniques substantially increased the number of sperm whales detected on this line-transect survey by increasing the range of detection and allowing nighttime surveys; however, visual observations were necessary for estimating group size.     

'Megapclicks': acoustic click trains and buzzes produced during night-time foraging of humpback whales (Megaptera novaeangliae)

Humpback whales (Megaptera novaeangliae) exhibit a variety of foraging behaviours, but neither they nor any baleen whale are known to produce broadband clicks in association with feeding, as do many odontocetes. We recorded underwater behaviour of humpback whales in a northwest Atlantic feeding area using suction-cup attached, multi-sensor, acoustic tags (DTAGs). Here we describe the first recordings of click production associated with underwater lunges from baleen whales. Recordings of over 34000 'megapclicks' from two whales indicated relatively low received levels at the tag (between 143 and 154dB re 1 microPa pp), most energy below 2kHz, and interclick intervals often decreasing towards the end of click trains to form a buzz. All clicks were recorded during night-time hours. Sharp body rolls also occurred at the end of click bouts containing buzzes, suggesting feeding events. This acoustic behaviour seems to form part of a night-time feeding tactic for humpbacks and also expands the known acoustic repertoire of baleen whales in general.     

CLICK CHARACTERISTICS OF NORTHERN BOTTLENOSE WHALES (HYPEROODON AMPULLATUS)

Sounds produced by northern bottlenose whales ( Hyperoodon ampullatus ) recorded in the Gully, a submarine canyon off Nova Scotia, consisted predominately of clicks. In 428 min of recordings no whistles were heard which could unequivocally be attributed to bottlenose whales. There were two major types of click series, initially distinguished by large differences in received amplitude. Loud clicks (produced by nearby whales socializing at the surface) were rapid, with short and variable interclick intervals (mean 0.07 sec; CV 71%). The frequency spectra of these were variable and often multimodal, with peak frequencies ranging between 2 and 22 kHz (mean 11 kHz, CV 59%). Clicks received at low amplitude (produced by distant whales, presumably foraging at depth) had more consistent interclick intervals (mean 0.40 sec, CV 12.5%), generally unimodal frequency spectra with a mean peak frequency of 24 kHz (CV 7%) and 3 dB bandwidth of 4 kHz. Echolocation interclick intervals may reflect the approximate search distance of an animal, in this case 300 m, comparable to that found for sperm whales. The relationship between click frequency and the size of object being investigated, suggests that 24 kHz would be optimal for an object of approximately 6 cm or more, consistent with the size range of their squid prey.     

Sperm whale depredation of sablefish longline gear in the northeast Pacific Ocean

Interactions between marine mammals and fisheries include competition for prey (catch), marine mammal entanglement in fishing gear, and catch removal off fishing gear (depredation). We estimated the magnitude of sperm whale depredation on a major North Pacific longline fishery (sablefish) using data collected during annual longline surveys. Sperm whale depredation occurs while the longline gear is off‐bottom during retrieval. Sperm whales were observed on 16% of longline survey sampling days, mostly (95% of sightings) over the continental slope. Sightings were most common in the central and eastern Gulf of Alaska (98% of sightings), occasional in the western Gulf of Alaska and Aleutian Islands, and absent in the Bering Sea. Longline survey catches were commonly preyed upon when sperm whales were present (65% of sightings), as evidenced by damaged fish. Neither sperm whale presence (P = 0.71) nor depredation rate (P = 0.78) increased significantly from 1998 to 2004. Longline survey catch rates were about 2% less at locations where depredation was observed, but the effect was not significant (P = 0.34). Estimated sperm whale depredation was <1% of the annual sablefish longline fishery catch off Alaska during 1998 to 2004.     

KILLER WHALES, WHALING, AND SEQUENTIAL MEGAFAUNAL COLLAPSE IN THE NORTH PACIFIC: A COMPARATIVE ANALYSIS OF THE DYNAMICS OF MARINE MAMMALS IN ALASKA AND BRITISH COLUMBIA FOLLOWING COMMERCIAL WHALING

The hypothesis that commercial whaling caused a sequential megafaunal collapse in the North Pacific Ocean by forcing killer whales to eat progressively smaller species of marine mammals is not supported by what is known about the biology of large whales, the ecology of killer whales, and the patterns of ecosystem change that took place in Alaska, British Columbia, and elsewhere in the world following whaling. A comparative analysis shows that populations of seals, sea lions, and sea otters increased in British Columbia following commercial whaling, unlike the declines noted in the Gulf of Alaska and Aleutian Islands. The declines of seals and sea lions that began in western Alaska around 1977 were mirrored by increases in numbers of these species in British Columbia. A more likely explanation is that the seal and sea lion declines and other ecosystem changes in Alaska stem from a major oceanic regime shift that occurred in 1977. Killer whales are unquestionably a significant predator of seals, sea lions, and sea otters—but not because of commercial whaling.     

Size Distribution of Sperm Whales Acoustically Identified during Long Term Deep-Sea Monitoring in the Ionian Sea

The sperm whale (Physeter macrocephalus) emits a typical short acoustic signal, defined as a “click”, almost continuously while diving. It is produced in different time patterns to acoustically explore the environment and communicate with conspecifics. Each emitted click has a multi-pulse structure, resulting from the production of the sound within the sperm whale’s head. A Stable Inter Pulse Interval (Stable IPI) can be identified among the pulses that compose a single click. Applying specific algorithms, the measurement of this interval provides useful information to assess the total length of the animal recorded. In January 2005, a cabled hydrophone array was deployed at a depth of 2,100 m in the Central Mediterranean Sea, 25 km offshore Catania (Ionian Sea). The acoustic antenna, named OνDE (Ocean noise Detection Experiment), was in operation until November 2006. OνDE provided real time acoustic data used to perform Passive Acoustic Monitoring (PAM) of cetacean sound emissions. In this work, an innovative approach was applied to automatically measure the Stable IPI of the clicks, performing a cepstrum analysis to the energy (square amplitude) of the signals. About 2,100 five-minute recordings were processed to study the size distribution of the sperm whales detected during the OνDE long term deep-sea acoustic monitoring. Stable IPIs were measured in the range between 2.1 ms and 6.4 ms. The equations of Gordon (1991) and of Growcott (2011) were used to convert the IPIs into measures of size. The results revealed that the sperm whales recorded were distributed in length from about 7.5 m to 14 m. The size category most represented was from 9 m to 12 m (adult females or juvenile males) and specimens longer than 14 m (old males) seemed to be absent.     

Phenological changes in North Atlantic right whale habitat use in Massachusetts Bay

The North Atlantic right whale (Eubalaena glacialis) is one of the world's most highly endangered baleen whales, with approximately 400–450 individuals remaining. Massachusetts Bay (MB) and Cape Cod Bay (CCB) together comprise one of seven areas in the Gulf of Maine where right whales seasonally congregate. Here, we report on acoustically detected presence of right whales in MB over a nearly 6 year period, July 2007–April 2013, a time of both rapid ocean warming throughout the Gulf of Maine and apparent changes in right whale migratory dynamics. We applied an automated detection algorithm to assess hourly presence of right whale “up‐calls” in recordings from a 19‐channel acoustic array covering approximately 4,000 km² in MB. Over the survey, up‐calls were detected in 95% of 8 day periods. In each year, as expected, we observed a “peak season” of elevated up‐call detections in late winter and early spring corresponding to the season when right whales congregate to feed in CCB. However, we also saw an increase in right whale occurrence during time periods thought to be part of the “off‐season.” With the exception of 2009–2010, when acoustic presence was unusually low, the mean percent of hours in which up‐calls were detected increased every year, both during the peak season (from 38% in 2008 to 70% in 2012), and during the summer–fall season (from 2% in 2007 to 13% in 2012). Over the entire study, the peak season start date varied between 17 January and 26 February. Changes in right whale phenology in MB likely reflect broadscale changes in habitat use in other areas within the species range. This study demonstrates the value of continuous long‐term survey datasets to detect and quantify shifts in cetacean habitat use as environmental conditions change and the long‐term continued survival of right whales remains uncertain.     

SPERM WHALES IN THE GULF OF CALIFORNIA: RESIDENCY, MOVEMENTS, BEHAVIOR, AND THE POSSIBLE INFLUENCE OF VARIATION IN FOOD SUPPLY

Sperm whale movements, residency, population structure, and behavior were investigated in the Gulf of California in 1998 and 1999. Variations in sperm whale movement patterns and behavior were related to changes in prey abundance (jumbo squid, Dosidicus gigas ) determined by fishery statistics. Photo-identification data revealed that seven female sperm whales moved into the Gulf of California from the Galapagos Islands, traveling up to 3,803 km. These are among the longest documented movements for female sperm whales. There were significant differences in speed and distance traveled during a dive cycle between 1998 and 1999 (low and high squid abundance). In 1999 there were also significant differences in small-scale movements and behavior between the northern and the southern part of the study area (high and low prey abundance). These results suggest that when food resources are low, sperm whales travel in straighter lines, dive for longer periods, travel larger distances during dive cycles, and at higher speed. In 1999 there were significant differences in time spent socializing in areas of high prey abundance versus areas of low abundance. All of these changes in behavior were consistent with increased foraging effort when squid abundance was low. A high proportion of mature males and first-year calves were observed in the Gulf of California, suggesting that it is an important sperm whale breeding ground.     

First record of humpback whale songs in Southern Chile: Analysis of seasonal and diel variation

Male humpback whales (Megaptera novaeangliae) produce complex, patterned songs that are traditionally recorded on their breeding grounds. In this work, we report results from the first continuous acoustic monitoring of a humpback whale feeding ground off southern Chile, Corcovado Gulf. Using an autonomous continuously recording system anchored to the seafloor and an automatic signal detector, we used the units within a song to analyze the temporal distribution and diel patterns of humpback whales. Acoustic recordings were made at the end of the austral summer and autumn of 2012. Songs occurred over the entire 130 d monitoring period, from 1 February to 15 June 2012. The percentage of units detected increased throughout the monitored period with the highest detections in the last recorded month (June), despite recording for fewer days that month. Furthermore, songs were detected during all light regimes studied, but most frequently during darkness. This study provides further evidence that, far from being rare or sporadic, humpback whale songs occur commonly at a feeding ground in high latitudes over different light conditions and in all months, with a peak in autumn.     

POPULATION CHARACTERISTICS AND MIGRATION OF SUMMER AND LATE-SEASON HUMPBACK WHALES (MEGAPTERA NOVAEANGLIAE) IN SOUTHEASTERN ALASKA

A total of 326 humpback whales (Megaptera novaeangliae) were individually identified in southeastern Alaska during five summer seasons (July to September) and four late seasons (November to February) spanning the years 1979 to 1983. Peak numbers of whales were found late in August or early in September. Whales arrived 1–2 wk later in 1982 than in 1981. Whales sighted in both the summer and late seasons of 1981 and 1982 remained about 3.7 mo and one whale remained for at least 4.9 mo. Humpback whales from southeastern Alaska wintered in Hawaiian or Mexican waters, but generally did not travel to other feeding regions. The most rapid migratory transit between Hawaii and southeastern Alaska was 79 d. Based on mark-recapture analyses of the photographic data, we estimate a population of 270–372 whales in the southeastern Alaska feeding herd.     

The influence of habitat and time of day on the occurrence of odontocete vocalizations in Onslow Bay,North Carolina

To determine whether the occurrence and duration of odontocete vocal events varied by depth or time of day in Onslow Bay, North Carolina, we analyzed acoustic data collected by five underwater recorders. These recorders were deployed in July 2008 at three depths: two in shallow (64–73 m), one in medium (236 m), and two in deep (~366 m) water. We found that habitat influenced the occurrence of odontocete vocalizations, with significantly greater daily vocal activity from delphinids on recorders in deeper waters and sperm whale clicks recorded only on the medium and deep recorders. These findings suggest that a greater diversity and occurrence of animals are located in waters beyond the shelf break in this area, a conclusion supported by visual surveys. We also found an increase in the occurrence of delphinid clicks at night on the shallow and deep recorders, likely reflecting nocturnal foraging activity, and a regular nocturnal occurrence of sperm whale clicks on the medium‐depth recorder located near the shelf break, suggesting that one or more sperm whales moved into that area to feed at night. These observations improve our understanding of the occurrence and behavior of odontocetes in this region of the U.S. Atlantic seaboard.     

THERMAL INFRARED RADIATION FROM FREE LIVING WHALES

As part of a search for new detection techniques, and for obtaining information on whale surface temperatures, an Agema Thermovision 880 thermal imaging system was used to detect thermal infrared radiation from whales. The study took place along the northern coast of Norway and the northwest coast of Svalbard (68° to 80° N latitude). The emphasis of the study was on minke whales, but humpback, fin, blue and sperm whales were also observed. The apparent radiation temperature was strongly dependent on sea conditions, signal angle, and atmospheric interference; detection depended thus upon weather. During the study, sea surface temperatures varied as much as 7°C but the sea and minke whale body trunk surfaces were usually within 0.0° to 0.1°C of each other. The other species observed had temperature differences of 0.0° to 1.0°C relative to the sea surface. Temperature differences between sea water and whale appendages ranged from 0.0° to 6.0°C. The indicated maximum difference between sea water and blow (i.e., expired air) was 4.0°;C, while the maximum difference for the blowhole was 4.1°C. The results from all whales observed support the belief that the main body trunk is normally not a heat window, this function being reserved for the appendages. However, the results also indicate a regulated dermal blood flow determining heat loss from the body trunk. Detection of whales by thermal infrared radiation from the body trunk appears unreliable; in contrast, the blow and blowhole provided a consistent positive signal with apparent temperature differences to the surroundings ranging from 0.2° to 4.1°C.     

The relationship between the acoustic behaviour and surface activity of killer whales (<Emphasis Type="Italic">Orcinus orca</Emphasis>) that feed on herring (<Emphasis Type="Italic">Clupea harengus</Emphasis>)

We describe the acoustic behaviour of piscivorous killer whales in Norwegian and Icelandic waters. Whales were assigned to one of three activities (feeding, travelling or other), and sound recordings were made in their proximity with a single hydrophone and a digital audiotape (DAT) recorder. A quantitative analysis of the production of pulsed calls, whistles and echolocation clicks in the three activities revealed that there was a significant effect of activity on the production of these sound types. Both killer whales in Icelandic and Norwegian waters produced high rates of clicks and calls during feeding and low rates of click, calls and whistles during travelling. The differences can be used as acoustical markers and provides new possibilities for acoustic monitoring of killer whales in these areas. Based on the similarity between their prey choice, hunting strategies, phenotype and acoustic behaviour, we suggest that the killer whales in Icelandic and Norwegian waters belong to the same ecotype: Scandinavian herring-eating killer whales.     

Vocal clans in sperm whales (Physeter macrocephalus)

Cultural transmission may be a significant source of variation in the behaviour of whales and dolphins, especially as regards their vocal signals. We studied variation in the vocal output of 'codas' by sperm whale social groups. Codas are patterns of clicks used by female sperm whales in social circumstances. The coda repertoires of all known social units (n = 18, each consisting of about 11 females and immatures with long-term relationships) and 61 out of 64 groups (about two social units moving together for periods of days) that were recorded in the South Pacific and Caribbean between 1985 and 2000 can be reliably allocated into six acoustic 'clans', five in the Pacific and one in the Caribbean. Clans have ranges that span thousands of kilometres, are sympatric, contain many thousands of whales and most probably result from cultural transmission of vocal patterns. Units seem to form groups preferentially with other units of their own clan. We suggest that this is a rare example of sympatric cultural variation on an oceanic scale. Culture may thus be a more important determinant of sperm whale population structure than genes or geography, a finding that has major implications for our understanding of the species' behavioural and population biology.     

Predation by killer whales (Orcinus orca) and the evolution of whistle loss and narrow-band high frequency clicks in odontocetes

A disparate selection of toothed whales (Odontoceti) share striking features of their acoustic repertoires including the absence of whistles and high frequency but weak (low peak-to-peak source level) clicks that have a relatively long duration and a narrow bandwidth. The non-whistling, high frequency click species include members of the family Phocoenidae, members of one genus of delphinids, Cephalorhynchus, the pygmy sperm whale, Kogia breviceps, and apparently the sole member of the family Pontoporiidae. Our review supports the 'acoustic crypsis' hypothesis that killer whale predation risk was the primary selective factor favouring an echolocation and communication system in cephalorhynchids, phocoenids and possibly Pontoporiidae and Kogiidae restricted to sounds that killer whales hear poorly or not at all (< 2 and > 100 kHz).     

CHARACTERIZATION OF BEAKED WHALE (ZIPHIIDAE) AND SPERM WHALE (PHYSETER MACROCEPHALUS) SUMMER HABITAT IN SHELF-EDGE AND DEEPER WATERS OFF THE NORTHEAST U. S.

Sperm whales ( Physeter macrocephalus ) and beaked whales ( Mesoplodon spp. and Ziphius cavirostris ) are deep-diving cetaceans that frequent shelf-edge and Gulf Stream waters off the northeast U. S. coast. Sighting data collected during seven summer (1990, 1991, 1993, and 1995–1998) shipboard surveys were analyzed using a geographic information system to determine habitat use based on bathymetric and oceanographic features. Although sighting rates were lower for beaked whales, both taxa occupied similar habitats. Beaked whales were concentrated at the colder shelf edge, whereas sperm whales were associated with warmer off-shelf water. Mean sighting rates for both taxa were higher in canyon features, but only beaked whale sighting rates were significantly different between canyon and non-canyon habitat (Wilcoxon signed rank test P = 0.007). Within the shared habitat, the two taxa were separated at fine-scale based on oceanographic features.