The multiple functions of male song within the humpback whale (Megaptera novaeangliae) mating system: review,evaluation, and synthesis

Humpback whales (Megaptera novaeangliae) are seasonal breeders, annually migrating from high‐latitude summer feeding grounds to low‐latitude winter breeding grounds. The social matrix on the winter grounds is a loose network of interacting individuals and groups and notably includes lone males that produce long bouts of complex song that collectively yield an asynchronous chorus. Occasionally, a male will sing while accompanying other whales. Despite a wealth of knowledge about the social matrix, the full characterization of the mating system remains unresolved, without any firm consensus, as does the function of song within that system. Here, I consider and critically analyse three proposed functions of song that have received the most attention in the literature: female attraction to individual singers, determining or facilitating male–male interactions, and attracting females to a male aggregation within the context of a lekking system. Female attraction suggests that humpback song is an advertisement and invitation to females, but field observations and song playback studies reveal that female visits to individual singers are virtually absent. Other observations suggest instead that females might convey their presence to singers (or to other males) through the percussive sounds of flipper or tail slapping or possibly through vocalizations. There is some evidence for male–male interactions, both dominance and affiliative: visits to singers are almost always other lone males not singing at that time. The joiner may be seeking a coalition with the singer to engage cooperatively in attempts to obtain females, or may be seeking to disrupt the song or to affirm his dominance. Some observations support one or the other intent. However, other observations, in part based on the brevity of most pairings, suggest that the joiner is prospecting, seeking to determine whether the singer is accompanying a female, and if not soon departs. In the lekking hypothesis, the aggregation of vocalizing males on a winter ground and the visits there by non‐maternal females apparently for mating meet the fundamental definition of a lekking system and its role though communal display in attracting females to the aggregation, although not to an individual singer. Communal singing is viewed as a form of by‐product mutualism in which individuals benefit one another as incidental consequences of their own selfish actions. Possibly, communal singing may also act to stimulate female receptivity. Thus, there are both limitations and merit in all three proposals. Full consideration of song as serving multiple functions is therefore necessary to understand its role in the mating system and the forces acting on the evolution of song. I suggest that song may be the prime vector recruiting colonists to new winter grounds pioneered by vagrant males as population pressures increase or as former winter grounds become unavailable or undesirable, with such instances documented relatively recently. Speculatively, song may have evolved historically as an aggregating call during the dynamic ocean conditions and resulting habitat uncertainties in the late Miocene–early Pliocene epochs when Megaptera began to proliferate. Early song may have been comprised of simpler precursor sounds that through natural selection and ritualization evolved into complex song.     

Diel patterns in singing activity of humpback whales in a winter breeding area in Okinawan (Ryukyuan) waters

Male humpback whales produce complex sounds known as songs during their breeding season. Previous studies have shown diel patterns of song in their breeding areas, but there had been no similar studies in the breeding area around Okinawa, Japan. To study diel patterns of song and the behavior of humpback whales in Okinawa, we conducted 24 hr recording with a fixed hydrophone in 2007, and vessel-based sighting surveys during 2014–2017. Song was monitored for 15 days, with peaks at sunrise and around 2200. Singing activity declined significantly between sunrise and sunset, then increased until 2200. Activity levels at night were higher and more stable than during the day. During 278 days of sighting surveys, 2,551 whales in 1,382 groups were observed. 79 individuals were confirmed as singers, all of which were lone whales. In six cases, singing individuals stopped singing before joining a group or began singing after leaving a group. Previous studies have shown that group size of humpback whales increases through the day. Considering the results from our study and the former studies, the decrease in singing activity as the day progresses may be a result of aggregation increasing, thus reducing the number of lone singers during the day.     

Temporal Aspects of Singing Interactions among Territorial Ovenbirds (Seiurus aurocapillus)

The temporal aspects of singing interactions among birds have received relatively little attention. To determine if the song delivery of one individual is affected by that of its territorial neighbor, I recorded singing interactions between territorial ovenbirds (Seiurus aurocapillus). Ovenbirds appeared to adopt one of two roles during singing interactions, Type I or Type II singers. Type II singers placed more of their songs immediately after the song of their neighbor than expected. The singing pattern of Type I singers could not be distinguished from a random pattern with respect to their neighbor's songs. In each observed pair of interacting birds, one individual was a Type I singer and one was a Type II singer. Although there was some intra-individual variation, most birds maintained the same role with each of their recorded territorial neighbors. Variation occurred between the two study sites in the extent that individuals overlapped the songs of their neighbors. Song overlap was common at one site, but occurred as, or less, often than expected at the other site.     

Constant Proportions of Mixed Singers in Tree Creeper Populations (Certhia familiaris)

Of 205 tree creeper males in 7 syntopic populations 69 (34%) were mixed singers. Of these, 17 sang complete short-toed tree creeper song, six sang incomplete and 46 sang only one element thereof. In three populations (Neuenburg, Wendhausen, Kenzingen) there was a dominance of mixed singers, in another population (Lorettowald) a large proportion was present. Only one mixed singer was found in each of the last three populations (Freiburg, Bodanrück, Seerücken). Three populations had high proportions of mixed singers between 1960 and 1970 and later in 1983 and/or 1984. Two other populations had only one mixed singer in both periods. A small isolated population of 4 to 5 tree creeper pairs (Lorettowald) with many mixed singers was surrounded by populations with low proportions of mixed singers (Bodanrück, Seerücken). The proportions of different forms of mixed songs in Neuenburg in 1983 and 1984 were almost identical to those in the 1960′s whereas highly significant changes occurred in Kenzingen. The pronounced differences in the songs of tree creepers and short-toed tree creepers probably do not result from contrast reinforcement. Mixed song is also probably not caused by character (vocal) convergence according to Cody (1969) and Dobkin (1979). Instead, it seems more probable that mixed song results from errors in copying, which are passed on to the next offspring by cultural transmission.     

Minimal similarity in songs suggests limited exchange between humpback whales (Megaptera novaeangliae) in the southern Indian Ocean

Comparing humpback whale song from different breeding assemblages can reveal similarities in song due to acoustically interacting males, and therefore indirectly test whether males from different breeding sites are mixing. Northern Hemisphere song comparisons illustrated that whales within ocean basins share similar songs and are subpopulations within a larger population, whereas whales in different ocean basins are isolated populations and therefore do not share songs. During the 2006 breeding season, recordings were collected in Madagascar and Western Australia, and were compared visually plus aurally. Both regions shared one theme, whereas each region had four and six private themes, respectively. This study had a substantially low number of shared themes. The co‐occurrence of one theme was interpreted as an indication of limited exchange between these breeding assemblages, and we speculate that limited song similarity is due to inter‐oceanic interactions. Male(s) from an Indian Ocean breeding group could be exposed to novel song when they geographically overlap, and acoustically interact, with males from a different ocean basin. Novel song could induce rapid temporal changes as new song content is incorporated, thereby minimizing song similarities between that breeding group and other Indian Ocean breeding groups that were not exposed to the novel song.     

Song similarity predicts hybridization in flycatchers

Given that population divergence in sexual signals is an important prerequisite for reproductive isolation, a key prediction is that cases of signal convergence should lead to hybridization. However, empirical studies that quantitatively demonstrate links between phenotypic characters of individuals and their likelihood to hybridize are rare. Here we show that song convergence between sympatric pied (Ficedula hypoleuca) and collared flycatchers (F. albicollis) influence social and sexual interactions between the two species. In sympatry, the majority of male pied flycatchers (65%) include various parts of collared flycatcher song in their song repertoire (but not vice versa). Playback experiments on male interactions demonstrate that male collared flycatchers respond similarly to this 'mixed' song as to conspecific song. Long-term data on pairing patterns show that males singing a converged song attract females of the other species: female collared flycatchers only pair with male pied flycatchers if the males sing the mixed song type. From the perspective of a male pied flycatcher, singing a mixed song type is associated with 30% likelihood of hybridization. This result, combined with our estimates of the frequency of mixed singers, accurately predicts the observed occurrence of hybridization among male pied flycatchers in our study populations (20.45% of 484 pairs; predicted 19.5%). Our results support the suggestion that song functions as the most important prezygotic isolation mechanism in many birds.     

Humpback Whale Song and Foraging Behavior on an Antarctic Feeding Ground

Reports of humpback whale (Megaptera novaeangliae) song chorusing occurring outside the breeding grounds are becoming more common, but song structure and underwater behavior of individual singers on feeding grounds and migration routes remain unknown. Here, ten humpback whales in the Western Antarctic Peninsula were tagged in May 2010 with non-invasive, suction-cup attached tags to study foraging ecology and acoustic behavior. Background song was identified on all ten records, but additionally, acoustic records of two whales showed intense and continuous singing, with a level of organization and structure approaching that of typical breeding ground song. The songs, produced either by the tagged animals or close associates, shared phrase types and theme structure with one another, and some song bouts lasted close to an hour. Dive behavior of tagged animals during the time of sound production showed song occurring during periods of active diving, sometimes to depths greater than 100 m. One tag record also contained song in the presence of feeding lunges identified from the behavioral sensors, indicating that mating displays occur in areas worthy of foraging. These data show behavioral flexibility as the humpbacks manage competing needs to continue to feed and to prepare for the breeding season during late fall. This may also signify an ability to engage in breeding activities outside of the traditional, warm water breeding ground locations.     

KILLER WHALE PREDATION ON SPERM WHALES: OBSERVATIONS AND IMPLICATIONS

In October 1997 we observed a herd of approximately 35 killer whales ( Orcinus orca ) attack a pod of nine sperm whales ( Physeter macrocephalus ) 130 km off the coast of central California. During the four hours we watched, adult female killer whales, including some with calves, attacked in waves of four to five animals in what was apparently a "wound and withdraw" strategy. Adult male killer whales stood by until the very end when one charged in and quickly killed a seriously wounded sperm whale that had been separated from the group. The sperm whales appeared largely helpless: their main defensive behavior was the formation of a rosette ("marguerite"-heads together, tails out). When the killer whales were successful in pulling an individual out of the rosette, one or two sperm whales exposed themselves to increased attack by leaving the rosette, flanking the isolated individual, and leading it back into the formation. Despite these efforts, one sperm whale was killed and eaten and the rest were seriously, perhaps mortally, wounded. We also present details of two other encounters between sperm whales and killer whales that we observed. Although sperm whales, because of various behavioral and morphological adaptations, were previously thought to be immune to predation, our observations clearly establish their vulnerability to killer whales. We suggest that killer whale predation has potentially been an important, and underrated, selective factor in the evolution of sperm whale ecology, influencing perhaps the development of their complex social behavior and at-sea distribution patterns.     

Song complexity and song structure in the Moustached Warbler Acrocephalus melanopogon

We examined different song parameters leading to a complex song configuration, and song output (production), and their relation in male Moustached Warblers and discuss them with reference to female choice. With more than 120 different syllables per two minutes of song, male Moustached Warblers can be regarded as one of the most complex singers within the genus Acrocephalus . We found significant differences between males for almost all song parameters investigated (repertoire size, switching and repetition rate, song speed and strophe length) but not for time spent singing per 20 minutes. This individual variation probably is an important cue for female mate choice. Male Moustached Warblers achieve song complexity mainly via frequent syllable switching. Song complexity seems to be consistent throughout the song and our results suggest that females could assess the overall song complexity of a singer by examining even very short song bouts. Furthermore, a high proportion of motifs – clusters of syllables with the same sequence – occurs within the song of each male which would also facilitate assessment of song complexity by females. However, repertoire size and strophe length were positively related, thus it remains to be investigated which song feature, if any, females actually use.     

Red Shift,Blue Shift: Investigating Doppler Shifts,Blubber Thickness,and Migration as Explanations of Seasonal Variation in the Tonality of Antarctic Blue Whale Song

The song of Antarctic blue whales (Balaenoptera musculus intermedia) comprises repeated, stereotyped, low-frequency calls. Measurements of these calls from recordings spanning many years have revealed a long-term linear decline as well as an intra-annual pattern in tonal frequency. While a number of hypotheses for this long-term decline have been investigated, including changes in population structure, changes in the physical environment, and changes in the behaviour of the whales, there have been relatively few attempts to explain the intra-annual pattern. An additional hypothesis that has not yet been investigated is that differences in the observed frequency from each call are due to the Doppler effect. The assumptions and implications of the Doppler effect on whale song are investigated using 1) vessel-based acoustic recordings of Antarctic blue whales with simultaneous observation of whale movement and 2) long-term acoustic recordings from both the subtropics and Antarctic. Results from vessel-based recordings of Antarctic blue whales indicate that variation in peak-frequency between calls produced by an individual whale was greater than would be expected by the movement of the whale alone. Furthermore, analysis of intra-annual frequency shift at Antarctic recording stations indicates that the Doppler effect is unlikely to fully explain the observations of intra-annual pattern in the frequency of Antarctic blue whale song. However, data do show cyclical changes in frequency in conjunction with season, thus suggesting that there might be a relationship among tonal frequency, body condition, and migration to and from Antarctic feeding grounds.     

NORTH PACIFIC HUMPBACK WHALE SONGS: A COMPARISON OF SOUTHEAST ALASKAN FEEDING GROUND SONGS WITH HAWAIIAN WINTERING GROUND SONGS

Humpback whales sing long, complex songs on their wintering grounds. On 25 August 1979 and 3 September 1981, we made recordings of humpback whale songs in southeastern Alaska, showing that humpback whales also sing on the summer feeding grounds. Both these Alaskan samples are songs in that they are repeating cyclical sound patterns and follow the known structure for humpback whale song. The Alaskan songs contain all the same material sung in the same order as that heard off Mexico and Hawaii in the surrounding wintering seasons. However, song, theme and some phrase durations are abbreviated in the Alaskan songs. The recording of these two songs represents the full sample of song recorded from 155 days over five years of attempting to record humpback whale song in Alaskan waters.     

Golden-bellied mangabeys (Cercocebus galeritus chrysogaster) at the Sacramento Zoo: Adult heterosexual pairs

The behaviors of three different adult male–adult female pairs of golden-bellied mangabeys (Cercocebus galeritus chrysogaster) were compared. Correlates of restricted social conditions and of the presence of offspring on adult behavior and direction of aggressive behaviors were noted. A captive pair displayed self-biting and other aberrant behaviors, a lone wild-caught pair showed redirected aggression related to sex, and a pair housed with its offspring showed close social proximity and protection of an infant. The implications of housing and experience for space and visitor exposure are discussed. Observer- vs. visitor-directed displays are seen as important measures of group and visitor effects.     

Increased density and male-male interactions reduce male longevity in the medfly, Ceratitis capitata

We investigated the effect of adult density on male and female longevity and behavioural interactions in a mass-reared strain of the medfly. Male survival decreased significantly, and male-male behavioural interactions increased significantly, with increasing male density (males were kept at 1, 2, 6 and 10 flies per 285 cm²in pots of 5.5 cm in diameter and 12 cm high). No such effects were observed in females over the same density range. This suggests that male survival decreased in response to the deleterious effects of male-male behavioural interactions. At the highest density, courtship wing fanning directed towards other males decreased significantly over time. In addition, as either density or male-biased sex ratio increased, males were increasingly likely to be engaged in courtship wing fanning that was not directed towards females. These results suggest that high adult density may significantly reduce male reproductive success, by decreasing survival and mating success. The results highlight the potentially high survival costs of male-male interactions and indicate differences in the nature of reproductive costs in the two sexes.     

Songbird cheaters pay a retaliation cost: evidence for auditory conventional signals

Conventional signals impose costs on senders through receiver retaliation rather than through investment in signal production. While several visual conventional signals have been described (mainly 'badges of status'), acoustic examples are rare; however, several aspects of repertoire use in songbirds are potential candidates. We performed interactive playback experiments to determine whether song-type matches (responding to a song with the same song type), repertoire matches (responding to a song with a different song type, but one in the repertoires of both singers) and unshared song types serve as conventional signals during male-male territorial interactions in banded wrens, Thryothorus pleurostictus. Our results demonstrate that these three signals incite varying levels of receiver aggression: song-type matches induce faster approach than do repertoire matches, and repertoire matches induce faster approach than do unshared song types. Production costs do not differ, while the receiver response does. Because territorial banded wrens approach opponents who signal aggressively, such opponents risk attack. This system will punish and prevent cheaters, as weak males signalling aggression will be subject to escalation by stronger or more-motivated opponents.     

RESPONSE OF NORTH ATLANTIC RIGHT WHALES (EUBALAENA GLACIALIS) TO PLAYBACK OF CALLS RECORDED FROM SURFACE ACTIVE GROUPS IN BOTH THE NORTH AND SOUTH ATLANTIC

The surface active group (SAG) is the most obvious social interaction of the North Atlantic right whale ( Eubalaena glacialis ). SAGs are typically composed of an adult female with two or more males engaged in social behavior near the surface. Distinct calls, believed to be produced by the female, are associated with these groups. Calls recorded from three North Atlantic right whale SAGs and three South Atlantic right whale ( Eubalaena australis ) SAGs were played back to North Atlantic right whales to determine if these sounds are sufficient to attract males to the groups. Playbacks of gunshot sounds produced by North Atlantic right whales were used as a control stimulus. Thirty-six trials were carried out from 1999 to 2001 in the Bay of Fundy, Canada. Whales approached 27 of 31 SAG playbacks and 0 of 5 gunshot playbacks. Where sex was determined ( n = 28), all approaches to North Atlantic SAG recordings were by males. Individuals ( n = 22) of all age and sex classes approached South Atlantic SAG playbacks. These trials indicate that SAG calls from both populations are sufficient to attract right whales to SAGs and that males and females respond differently to stimuli from the North Atlantic. The difference in response to North and South Atlantic SAG stimuli was unexpected. Novelty, species differences in calls, and different seasonal or behavioral context for the recorded stimuli may be responsible for the differences in response.     

Synchronous Seasonal Change in Fin Whale Song in the North Pacific

Fin whale (Balaenoptera physalus) song consists of down-swept pulses arranged into stereotypic sequences that can be characterized according to the interval between successive pulses. As in blue (B. musculus) and humpback whales (Megaptera novaeangliae), these song sequences may be geographically distinct and may correlate with population boundaries in some regions. We measured inter-pulse intervals of fin whale songs within year-round acoustic datasets collected between 2000 and 2006 in three regions of the eastern North Pacific: Southern California, the Bering Sea, and Hawaii. A distinctive song type that was recorded in all three regions is characterized by singlet and doublet inter-pulse intervals that increase seasonally, then annually reset to the same shorter intervals at the beginning of each season. This song type was recorded in the Bering Sea and off Southern California from September through May and off Hawaii from December through April, with the song interval generally synchronized across all monitoring locations. The broad geographic and seasonal occurrence of this particular fin whale song type may represent a single population broadly distributed throughout the eastern Pacific with no clear seasonal migratory pattern. Previous studies attempting to infer population structure of fin whales in the North Pacific using synchronous individual song samples have been unsuccessful, likely because they did not account for the seasonal lengthening in song intervals observed here.     

SEXUAL COMPOSITION and ANALYSIS OF REPRODUCTIVE FEMALES IN THE NORTH ATLANTIC RIGHT WHALE, EUBALAENA GLACIALIS, POPULATION

To test hypotheses involving reproduction and demographics, the sex of individuals must be established, but many species of Cetacea are not obviously dimorphic. In the North Atlantic right whale, Eubalaena glacialis , population, the sex of 61 males and 55 females had been determined previously by observation of the urogenital region, and the sex of 43 more females had been inferred from repeated sightings with a calf. To confirm the sex of some of these animals and to identify the sex of mote animals, genomic DNA was isolated from skin samples of 95 individual right whales (54 from among those described above and 41 additional recognizable individuals). The DNA was surveyed using the human Y-chromosome probe pDP1007. With Eco RI-digested DNA, a clear, sex-discriminating banding pattern was apparent. This method verified the sex of all 54 animals whose sex was previously known or inferred and identified the sex of an additional 41 recognizable individuals. A total of 89 male and 111 female right whales was identified in the population. The most unbiased estimate of sex ratio available is the 36 male and 34 female calves identified by genital morphology and DNA techniques. The sex ratio of this sample does not differ significantly from unity (P = 0.811). Only 38% (58/152) of the females in the North Atlantic population are known to have been reproductively successful compared with 54% in the population of right whales in the western South Atlantic. The population growth rate reported for the North Atlantic population is only 33% of that reported for right whales in the South Atlantic. Thirteen adult North Atlantic females have been identified that have not been known to calve during the past 11 yr. These data suggest that the absence of measurable recovery may be due to a combination of fewer actively reproducing females and lower reproductive rates of some females.     

Whale killers: Prevalence and ecological implications of killer whale predation on humpback whale calves off Western Australia

Reports of killer whales (Orcinus orca) preying on large whales have been relatively rare, and the ecological significance of these attacks is controversial. Here we report on numerous observations of killer whales preying on neonate humpback whales (Megaptera novaeangliae) off Western Australia (WA) based on reports we compiled and our own observations. Attacking killer whales included at least 19 individuals from three stable social groupings in a highly connected local population; 22 separate attacks with known outcomes resulted in at least 14 (64%) kills of humpback calves. We satellite‐tagged an adult female killer whale and followed her group on the water for 20.3 h over six separate days. During that time, they attacked eight humpback calves, and from the seven known outcomes, at least three calves (43%) were killed. Overall, our observations suggest that humpback calves are a predictable, plentiful, and readily taken prey source for killer whales and scavenging sharks off WA for at least 5 mo/yr. Humpback “escorts” vigorously assisted mothers in protecting their calves from attacking killer whales (and a white shark, Carcharodon carcharias). This expands the purported role of escorts in humpback whale social interactions, although it is not clear how this behavior is adaptive for the escorts.     

High Source Levels and Small Active Space of High-Pitched Song in Bowhead Whales (Balaena mysticetus)

The low-frequency, powerful vocalizations of blue and fin whales may potentially be detected by conspecifics across entire ocean basins. In contrast, humpback and bowhead whales produce equally powerful, but more complex broadband vocalizations composed of higher frequencies that suffer from higher attenuation. Here we evaluate the active space of high frequency song notes of bowhead whales (Balaena mysticetus) in Western Greenland using measurements of song source levels and ambient noise. Four independent, GPS-synchronized hydrophones were deployed through holes in the ice to localize vocalizing bowhead whales, estimate source levels and measure ambient noise. The song had a mean apparent source level of 185±2 dB rms re 1 µPa @ 1 m and a high mean centroid frequency of 444±48 Hz. Using measured ambient noise levels in the area and Arctic sound spreading models, the estimated active space of these song notes is between 40 and 130 km, an order of magnitude smaller than the estimated active space of low frequency blue and fin whale songs produced at similar source levels and for similar noise conditions. We propose that bowhead whales spatially compensate for their smaller communication range through mating aggregations that co-evolved with broadband song to form a complex and dynamic acoustically mediated sexual display.