We tagged ten humpback whales with non-invasive, suction cup acoustic tags (DTAGs [26]) in the waters off of the Western Antarctic Peninsula in the austral fall, between 12 May and 04 June 2010. Research locations included Wilhelmina Bay and Flandres Bay, which are northeast and southeast of Palmer Station, respectively (Figure 1). We worked from the United States Antarctic Program's RVIB Nathaniel B Palmer.

Tags were deployed for 24-hour periods, and during that time they continuously recorded acoustics (64 kHz sampling rate) as well as behavioral data from a suite of temperature, pressure, accelerometer, and magnetometer sensors (50 Hz sampling rate, decimated to 5 Hz for analysis). During daylight hours, tagged whales were visually tracked from small, rigid-hulled inflatable boats (RHIBs) conducting focal-individual follows [27], and from the Palmer at night via a VHF radio signal from the DTAG.

Acoustic records were visually scanned for periods of song by two experienced acoustic analysts using the eXtensible Bioacoustic Analysis Tool (XBAT) [28], running in Matlab 7.0. Periods of song (“bouts”) were identified based on high signal-to-noise ratio (SNR) and an obvious pattern in the order in which units were repeated. Designation was subjective, but at minimum, two different themes and repetition of phrases needed to be present before the section could be declared a song bout. Within-bout song units were then individually identified (manually delineated using XBAT), and root-mean-square (RMS) received levels (RLs) were calculated over the full bandwidth of the recording after the frequencies below 400 Hz were emphasized to compensate for the tag hardware's built-in high pass filter. The low frequency emphasis filter combined a high pass filter at 40 Hz and a low pass filter at 400 Hz, resulting in a gain of 20 dB between 40 and 400 Hz [22], [29]. Source levels for these sounds cannot be calculated using this type of data because of the placement of the hydrophone on the animal's body. Its location on the back of the animal, roughly 3 m caudal to the blowholes and approximately on the animal's dorsal midline, is likely behind the sound source and could be in the near-field of any sounds produced by the tagged animal. In addition, some unknown amount of attenuation and distortion may be occurring as the sound propagates through the animal's body and surrounding waters [30].

It is difficult to definitively ascribe calls recorded on a tag to the focal animal because sounds produced by another animal in close proximity could also appear as intense sounds on the tagged animal's acoustic record [30]. Because these tags had only one hydrophone, and humpbacks habitually travel in closely spaced groups, we could not identify focal calls based on a consistent angle of arrival of successive sounds, or based on a lack of nearby conspecifics [30]–[33]. However, it is likely that if an associate whale were producing song registering strongly on the tag, this whale would be in close enough proximity to be engaged in similar behaviors to the tagged animal [31]. Therefore, we assumed that our broad assessments of dive behavior and suitability of the area for foraging would also apply to other close associates in the group, in the case that some or all of the sounds were produced by a companion.

Sound production was related to behavior by integrating the individual song units with the kinematics record based on time. Periods of song were overlaid on the dive profile to compare timing of song production with tagged animal depth and dive behavior. In addition, the locations of presumed foraging lunges were detected automatically using the algorithm described in Ware et al. [34]. This technique identified vertical lunges based on a significant change in upward or downward acceleration, and all other lunges based on changes in the speed profile calculated using acoustic flow noise as a proxy for speed [35], [36]. Lunges are believed to imply directed feeding on layers of krill in the area [34], [37].

All field research was permitted under the U.S. Marine Mammal Protection Act by the National Marine Fisheries Service Permit 808–1735, the Antarctic Conservation Act Permit 2009-014, and Duke University Institutional Animal Care and Use Permit A041-09-02.

We named units based on their acoustic properties, using terms such as broadband burst (BB), pulsed (P), long (>1 second, L), short (<1 second, S), and high (>2 kHz, H). For example, alternating long and short units would be labeled “L/S”. The two whales produced similar phrases, and shared themes and overall structure, including five identifiable and organized themes (Figure 2). The L/S theme was the most common and had the highest number of phrase repetitions. Percent occurrence of phrase types and mean number of phrase repetitions within themes are shown in Table 1.

General structure on both records adhered roughly to the following pattern of themes: BB – PT – L/H – LM – L/S. Figure 3 shows an example of this pattern. The songs were not rigidly structured and sometimes not continuous (in some cases up to 28% unidentified phrases, Table 1), but this overall pattern of themes persisted.

One of the unique aspects of this dataset is the ability to examine the behavior of animals under water during the song recording. Figure 4 shows the dive profile of each whale over the duration of the tag attachment. Overlaid are locations of feeding lunges that were automatically detected via the acoustic record and verified by an experienced technician who cross-referenced the accelerometer data [34]. Whale mn132a's record had defined periods of feeding that did not overlap with the defined periods of song (the thick black lines in Figure 4). Conversely, whale mn133a's record had two bouts of song during dives that included feeding lunges. This foraging behavior appears to have begun before singing started, and continued well after singing ceased.

Given that song is less prevalent on the feeding grounds, the level of structure in the song we recorded was higher than expected. We found a clear pattern of themes sung in a specific order, which is characteristic of humpback whale song as first described by Payne and McVay [1], and this pattern held for both of the whales we recorded singing in this area. Similar phrases were evident in the background chorusing, though theme structure was more difficult to analyze in detail. The type of song units produced was consistent between the two songs as well.

However, our recordings of off-season, or perhaps more accurately, shoulder-season song on this Antarctic feeding ground were not as continuous as song on the breeding grounds during the breeding season, where singers often sing for hours at a time [3]. The two tagged animals' acoustic records here each contained one long bout of song during the 24 hour study period, but also had many shorter sections, which may be similar to the partial song or song fragments mentioned in early reports of humpback whale song recorded on feeding grounds [19], [21]. There were also interspersed unidentified phrases, periods of song that were not very refined (i.e. had no obvious pattern), and periods of non-song sound production.

We do not know for certain the breeding ground(s) of this population of humpback whales. Evidence of linkage between the Western Antarctic Peninsula humpbacks and the breeding ground off the coast of Bahia, Brazil has been gathered via satellite tracking [38]. However, humpbacks travel great distances, as inferred from evidence of acoustic interaction between populations on either side of the Atlantic [39], horizontal cultural transmission of song across the Pacific [14], and fluke matches showing movement of an individual between Brazil and Madagascar [40]. In fact, recent evidence based on fluke matching does show migration between this Western Antarctic feeding ground and a breeding area in American Samoa [41]. Thus, comparisons of this song with that from established breeding grounds will need to be geographically extensive, and will be an enlightening topic of further study. We have included acoustic example files of song units with this paper to facilitate future comparisons (see acoustic files S1 and S2).

Many of the focal whales observed during this research exhibited frequent periods of social activity in addition to feeding, including the two animals discussed here. Song production in a group of three adults (as was the case during the first two bouts of song production on the record of mn132a) is unusual in comparison to the breeding grounds and migration routes, where solitary singers or singers escorting mother/calf pairs are the norm [5], [15], [42]. Another key finding with this work is that the acoustic records of both tagged whales showed song production during periods of active diving, in some cases to depths greater than 100 m. This also differs from the typical singer behavior on the breeding grounds, where whales will frequently sing while remaining stationary at depths between 15 and 25 m [43]. Tagged blue whales also generally sing when at depths shallower than 35 m [32]. Sound production in diving cetaceans is complicated by changing ambient pressure due to depth changes, so these data showing that humpbacks are capable of song production at deeper depths may inform the search to describe the mechanism of sound production in baleen whales [44].

The close overlap between singing and feeding in the record of whale mn133a is surprising. As noted above, it is possible that the song during this portion of the record is actually produced by a companion whale in close proximity. If this were the case, the two individuals would have had to maintain a relatively close fixed-distance association for long periods in order for the song to appear to have been from one animal continuously, or the song levels on the tag may have faded out completely as the other (potentially singing) whale drifted away. As described in the results section, unit received levels did vary over a range greater than 40 dB. However, these levels did not fluctuate in a regular way, i.e. increasing steadily as an associate drifted closer or decreasing steadily as an associate drifted away. Humpback whales are in fact known to vary their source levels during song production. Au and colleagues documented fluctuations of 10 dB re 1 µPa RMS within a given unit type from a single individual, and 22 dB re 1 µPa RMS of variation overall across three individuals and several unit types, as measured using a vertical array with stationary animals [43]. Overall, measurements of sound levels from hydrophones that are possibly in the near field and on an animal's back (thus subject to shading by the body and varying amounts of flow noise from body movements), and that are measuring sounds that may already be fluctuating in intensity, are not a reliable method of identifying the location or identity of a sound-producing baleen whale.

Regardless, even if it were a companion whale singing, whale pairs often engage in similar behaviors when associated [45]–[47], so if one were feeding, its associate may have been as well. At minimum, for the levels to register this strongly on the tag, the companion would have to have been in close enough proximity that the dive depths would be similar between the two individuals, and both animals would have been immersed in the same prey patch.

Thus, this work highlights the issue of tradeoff between foraging and breeding/display behavior while still on the feeding grounds. Both animals appear to have switched between foraging and breeding/display behavior over the course of a 24-hour period, with even a conservative interpretation indicating that groups of animals may have some individuals feeding while others actively engage in mating displays. These results combined with the increasing number of reports of chorusing recorded on humpback feeding grounds [17], [19], [25], competition on the feeding grounds [48], and even occasional reports of feeding on the breeding grounds [49] indicate that “feeding” and “breeding” behavior may be more plastic both spatially and temporally than traditionally thought.

Given the large amount of food available [50], these whales do not necessarily need to feed continuously, which provokes the interesting question of when they would switch from display behavior to foraging and back. The concept of behavioral flexibility has been described as the ability to modify behavior adaptively based on surrounding conditions [51], and humpback whales have shown this ability by developing and learning new foraging behaviors in response to prey type and availability [52]. The whales studied in this Antarctic location showed similar flexibility, exhibiting both display and foraging behavior, and even singing amidst lunge-worthy prey patches.

Humpback whale behavior may be more tied to the time of year than to physical location, in which case this behavioral tradeoff between feeding and mating behaviors would be a common dilemma faced by whales remaining on the feeding grounds later in the year due to varying environmental conditions. Recent work on fin whale song patterns in the Arctic has shown fin whale presence much later into the year than previously thought [53]. The authors suggested that with changing sea ice conditions affecting whale distributions, the behavioral dichotomy of breeding vs. feeding behavior for this migratory species is too simplistic, and mating may be taking place at higher latitudes. Major changes in the extent and duration of sea ice cover around the Antarctic Peninsula [54] may similarly be providing conditions for increases in breeding behavior on the feeding grounds in humpback whales, meriting further study.