Microsatellite genetic distances between oceanic populations of the humpback whale (Megaptera novaeangliae)

Mitochondrial DNA haplotypes of humpback whales show strong segregation between oceanic populations and between feeding grounds within oceans, but this highly structured pattern does not exclude the possibility of extensive nuclear gene flow. Here we present allele frequency data for four microsatellite loci typed across samples from four major oceanic regions: the North Atlantic (two mitochondrially distinct populations), the North Pacific, and two widely separated Antarctic regions, East Australia and the Antarctic Peninsula. Allelic diversity is a little greater in the two Antarctic samples, probably indicating historically greater population sizes. Population subdivision was examined using a wide range of measures, including Fst, various alternative forms of Slatkin's Rst, Goldstein and colleagues' delta mu, and a Monte Carlo approximation to Fisher's exact test. The exact test revealed significant heterogeneity in all but one of the pairwise comparisons between geographically adjacent populations, including the comparison between the two North Atlantic populations, suggesting that gene flow between oceans is minimal and that dispersal patterns may sometimes be restricted even in the absence of obvious barriers, such as land masses, warm water belts, and antitropical migration behavior. The only comparison where heterogeneity was not detected was the one between the two Antarctic population samples. It is unclear whether failure to find a difference here reflects gene flow between the regions or merely lack of statistical power arising from the small size of the Antarctic Peninsula sample. Our comparison between measures of population subdivision revealed major discrepancies between methods, with little agreement about which populations were most and least separated. We suggest that unbiased Rst (URst, see Goodman 1995) is currently the most reliable statistic, probably because, unlike the other methods, it allows for unequal sample sizes. However, in view of the fact that these alternative measures often contradict one another, we urge caution in the use of microsatellite data to quantify genetic distance.      

Singing through winter nights: Seasonal and diel occurrence of humpback whale (Megaptera novaeangliae) calls in and around the Gully MPA,offshore eastern Canada

Humpback whale use of areas off eastern Canada is poorly understood, a knowledge gap that could impact future conservation efforts. We describe the acoustic occurrence of humpback whales in and around the Gully Marine Protected Area (MPA), an eastern Scotian Shelf submarine canyon. Near‐continuous acoustic recordings sampling at 16 kHz were collected from the MPA and nearby slope areas from October 2012 to September 2014 using near‐bottom recorders. In an offshore region where humpbacks were thought to be rare, we observed calls from October to June with a peak in song and nonsong calls in December and January. This suggests that some individuals occur in Canadian waters in winter and the Gully region may be a North Atlantic humpback whale migratory corridor. Calls were predominantly songs indicating potential mating activities. Song and nonsong calls occurred more at sunset and during hours of darkness than during daylight. This study improves our understanding of the seasonal occurrence of humpback whales on the Scotian Slope and, more specifically, their use of an offshore protected area.     

The blubber adipocyte index: A nondestructive biomarker of adiposity in humpback whales (Megaptera novaeangliae)

The ability to accurately evaluate the energetic health of wildlife is of critical importance, particularly under conditions of environmental change. Despite the relevance of this issue, currently there are no reliable, standardized, nonlethal measures to assess the energetic reserves of large, free‐roaming marine mammals such as baleen whales. This study investigated the potential of adipocyte area analysis and further, a standardized adipocyte index (AI ), to yield reliable information regarding humpback whale (Megaptera novaeangliae ) adiposity. Adipocyte area and AI , as ascertained by image analysis, showed a direct correlation with each other but only a weak correlation with the commonly used, but error prone, blubber lipid‐percent measure. The relative power of the three respective measures was further evaluated by comparing humpback whale cohorts at different stages of migration and fasting. Adipocyte area, AI , and blubber lipid‐percent were assessed by binary logistic regression revealing that adipocyte area had the greatest probability to predict the migration cohort with a high level of redundancy attributed to the AI given their strong linear relationship (r = −.784). When only AI and lipid‐percent were assessed, the performance of both predictor variables was significant but the power of AI far exceeded lipid‐percent. The sensitivity of adipocyte metrics and the rapid, nonlethal, and inexpensive nature of the methodology and AI calculation validate the inclusion of the AI in long‐term monitoring of humpback whale population health, and further raises its potential for broader wildlife applications.     

Low levels of genetic differentiation characterize Australian humpback whale (Megaptera novaeangliae) populations

Humpback whales undertake long‐distance seasonal migrations between low latitude winter breeding grounds and high latitude summer feeding grounds. We report the first in‐depth population genetic study of the humpback whales that migrate to separate winter breeding grounds along the northwestern and northeastern coasts of Australia, but overlap on summer feeding grounds around Antarctica. Weak but significant differentiation between eastern and western Australia was detected across ten microsatellite loci (F_ST = 0.005, P = 0.001; D_EST = 0.031, P = 0.001, n = 364) and mitochondrial control region sequences (F_ST = 0.017 and Φ_ST = 0.069, P = 0.001, n = 364). Bayesian clustering analyses using microsatellite data could not resolve any population structure unless sampling location was provided as a prior. This study supports the emerging evidence that weak genetic differentiation is characteristic among neighboring Southern Hemisphere humpback whale breeding populations. This may be a consequence of relatively high gene flow facilitated by overlapping summer feeding areas in Antarctic waters.     

Mitochondrial DNA diversity of the Southwestern Atlantic humpback whale (Megaptera novaeangliae) breeding area off Brazil, and the potential connections to Antarctic feeding areas

In the Southwestern Atlantic Ocean, humpback whales migrate every winter to the Brazilian coast for breeding and calving in the Abrolhos Bank. This breeding stock represents the remnants of a larger population heavily exploited during the beginning of the 20th century. Despite its relevance to conservation efforts, the degree of current genetic variation and the migratory relationship with Antarctic feeding areas for this population are still largely unknown. To examine these questions, we sequenced ∼400 bp of the mitochondrial DNA control region from samples taken off the Brazilian coast (n = 171) and near the Antarctic Peninsula (n = 77). The genetic variability of the Brazilian humpback whale breeding population was high and similar to that found in other Southern Hemisphere breeding grounds. Phylogenetic analysis suggested the existence of a new mitochondrial clade that exists at low frequency among Southern Hemisphere populations. Direct comparison between the Brazilian and the Colombia breeding populations and the Antarctic Peninsula feeding population showed no genetic differentiation between this feeding region and the Colombian breeding area or between feeding Areas I and II near the Antarctic Peninsula. In contrast, these populations were genetically distinct from the Brazilian population. Two humpback whales sampled off South Georgia Islands, in the Scotia Sea, shared identical haplotypes to whales from Brazil. Our results, supported by photo-identification and satellite telemetry data, suggest that the main feeding area of the Southern Hemisphere humpback whale population is likely to be located near the South Georgia/South Sandwich Islands area and not in the Antarctic Peninsula.     

Behavioral responses of humpback whales (Megaptera novaeangliae) to whale-watching vessels on the southeastern coast of Australia

This study assessed the short-term responses of humpback whales to whale-watching vessels during their southward migration along the south coast of New South Wales (NSW), Australia. The behavior of pods was recorded from commercial whale-watching vessels during tours and compared to pods observed in the absence of vessels from the shore in the same area. While some individuals showed obvious signs of horizontal avoidance, others approached vessels, initiating interactions. Calf pods were more sensitive to the presence of vessels than non-calf pods. Dive times and the overall percentage of time whales spent submerged were higher in the presence of vessels, but respiration intervals did not differ. Some surface behaviors occurred less often in the presence of vessels. Whales' responses differed according to whether vessels were operating in accordance with regulations or not. Whales were more likely to avoid a vessel moving within the permitted 100 m approach limit than vessels outside the limit. Whales showed some behavioral changes when vessels operated in accordance with whale-watching regulations, compared with whales in the absence of vessels. Pods that showed no obvious horizontal responses to vessels changed their diving and surface activity when compared with pods in the absence of vessels. Because the long-term impacts of effects of vessels are unknown, management of the humpback whale-watching industry should adopt a conservative approach. Improved knowledge of long-term impacts of multiple exposures to vessels is required to inform management of the effects of whale-watching.     

The potential beginning of a postwhaling recovery in New Zealand humpback whales (Megaptera novaeangliae)

Between the 1940s and 1970s Southern Hemisphere populations of humpback whales (including eastern Australia and Oceania populations) were hunted to near extinction by extensive commercial whaling activities in Antarctica, with fewer whales taken in shore whaling operations in New Zealand, Australia (including Norfolk Island) and Tonga. Variable rates of recovery of these populations have been documented, ranging from recovery to prewhaling numbers in eastern Australian humpbacks to very little sign of recovery in many Oceania populations. Here we analyze recent sighting data collected over 12 yr, from annual surveys in Cook Strait, New Zealand. The data show an increase in sightings, at an estimated rate of 13% (95% CI of 4.9% and 21.7%) in 2015, of humpback whales migrating through Cook Strait. The wide confidence intervals preclude substantive conclusions about the rate of increase but suggest humpback whales are returning to this region in increasing numbers, indicating an influx of immigrants from neighboring areas, namely eastern Australia.     

Humpback whale (Megaptera novaeangliae) and killer whale (Orcinus orca) feeding aggregations for foraging on herring (Clupea harengus) in Northern Norway

Aggregations of predators on food patches have been documented for both terrestrial and marine animals. Here, we documented for the first time, and investigated, non-predatory aggregations occurring between humpback whales (Megaptera novaeangliae) and killer whales (Orcinus orca) while feeding on wintering Norwegian spring spawning herring (Clupea harengus) in Andfjord, northern Norway. Observational data were collected during 109 opportunistic surveys through three seasons 2013–2016. Killer whales were observed feeding on 59 occasions, with one to three humpback whales involved in 47 of these feeding events (79.7%), and there was an increased probability of finding feeding humpback whales when feeding killer whales also were observed. With killer whales identified as the initiating species in 94.4% of the feeding aggregations for which the first species was known, and with humpback whales joining and feeding on the fish ball afterwards, we suggest that humpback whales may benefit more from these aggregations than the opposite.     

Multiple processes drive genetic structure of humpback whale (Megaptera novaeangliae) populations across spatial scales

Elucidating patterns of population structure for species with complex life histories, and disentangling the processes driving such patterns, remains a significant analytical challenge. Humpback whale (Megaptera novaeangliae) populations display complex genetic structures that have not been fully resolved at all spatial scales. We generated a data set of nuclear markers for 3575 samples spanning the seven breeding stocks and substocks found in the South Atlantic and western and northern Indian Oceans. For the total sample, and males and females separately, we assessed genetic diversity, tested for genetic differentiation between putative populations and isolation by distance, estimated the number of genetic clusters without a priori population information and estimated rates of gene flow using maximum‐likelihood and Bayesian approaches. At the ocean basin scale, structure is governed by geographical distance (IBD P < 0.05) and female fidelity to breeding areas, in line with current understanding of the drivers of broadscale population structure. Consistent with previous studies, the Arabian Sea breeding stock was highly genetically differentiated (F_ST 0.034–0.161; P < 0.01 for all comparisons). However, the breeding stock boundary between west South Africa and east Africa was more porous than expected based on genetic differentiation, cluster and geneflow analyses. Instances of male fidelity to breeding areas and relatively high rates of dispersal for females were also observed between the three substocks in the western Indian Ocean. The relationships between demographic units and current management boundaries may have ramifications for assessments of the status and continued protections of populations still in recovery from commercial whaling.     

Behavioral ontogeny in humpback whale (Megaptera novaeangliae) calves during their residence in Hawaiian waters

The ontogeny of behavior in young offspring is a key component of a species life history, influencing short-term survival and life-long future fitness. In this study, we examine the behavioral ontogeny of humpback whale calves during their natal season on the winter breeding grounds. Behavioral data were collected during focal follows for 69 calves. Their relative age was estimated based on the degree of unfurling of the dorsal fin, and analysis of their time budgets revealed that behavior changed as the calves matured. Among the youngest group of calves ( n = 27), persistent travel accounted for median 85% (interquartile range 34%) of the calves' time budget, they spent little time alone at the surface and the breathing regime included frequent intermittent breaths. Within the oldest group of calves ( n = 26), time spent traveling dropped to a median 47% (IQR 42%) of the time budget, they spent more time at rest, surfaced alone more frequently, and the breathing regime more closely resembled that of adult humpbacks. We suggest potential functions for these and other components of calf behavior during this period, and review our findings in light of recent discussions on the role of predation pressure as a driving force in mysticete migration.     

Estimates of relatedness in groups of humpback whales (Megaptera novaeangliae) on two wintering grounds of the Southern Hemisphere

Group formation in humpback whales has been described in relation to different components of the migratory cycle, yet it is debated whether such groups represent real social bonding or ephemeral aggregations. Cooperative behaviours are exhibited during feeding activities, and it has been suggested that males may cooperate during competition for mates. Since most cooperative behaviours are expected to originate among kin, genetic relatedness represents a critical variable in the understanding of any social phenomenon, especially when cooperation cannot be confirmed unequivocally. Using an approach combining multi-locus microsatellite genotyping and several genetic relatedness estimators, we analyzed whale associations for two different wintering grounds in the Southern Hemisphere. The analyses included 648 whales sampled from 292 groups off the coast of Gabon and Northeast Madagascar, and screened for eleven microsatellite loci. Through simulations, we assessed the performance of three pairwise relatedness estimators. The individuals were molecularly sexed and their associations were investigated in the context of sex and group type. No significant association among relatives was found with the exception of mother-offspring pairs, supporting previous indications of extended maternal care. The analysis from the Gabon population also suggests that related males may avoid each other during competitive activities. Our results demonstrate that if cooperative behaviours occur on wintering grounds they are not favoured by kin selection.     

Acoustic monitoring on a humpback whale (Megaptera novaeangliae) feeding ground shows continual singing into late Spring

Singing by males is a major feature of the mating system of humpback whales, Megaptera novaeangliae (Borowski). Although a few songs have been opportunistically recorded on the whales' high-latitude feeding grounds, singing in these regions was thought to be only sporadic. We report results from the first continuous acoustic monitoring of a humpback whale feeding ground (off Cape Cod, MA, USA) in spring. Using autonomous sea-floor recording systems, we found singing on a daily basis over the entire 25 day monitoring period, from 14 May to 7 June 2000. For much of the period, song was recorded 24 h per day. These results, combined with evidence for aseasonal conceptions in whaling catch data, suggest that the humpback whale breeding season should no longer be considered as confined to lower-latitude regions in winter. Rather, we suggest breeding extends geographically and temporally onto feeding grounds into at least spring and early summer. Singing at these times represents either low-cost opportunistic advertising by (perhaps relatively few) males to court females that failed to conceive during the winter, and/or possibly an intrasexual display.     

Your attention please: increasing ambient noise levels elicits a change in communication behaviour in humpback whales (Megaptera novaeangliae)

High background noise is an important obstacle in successful signal detection and perception of an intended acoustic signal. To overcome this problem, many animals modify their acoustic signal by increasing the repetition rate, duration, amplitude or frequency range of the signal. An alternative method to ensure successful signal reception, yet to be tested in animals, involves the use of two different types of signal, where one signal type may enhance the other in periods of high background noise. Humpback whale communication signals comprise two different types: vocal signals, and surface-generated signals such as ‘breaching’ or ‘pectoral slapping’. We found that humpback whales gradually switched from primarily vocal to primarily surface-generated communication in increasing wind speeds and background noise levels, though kept both signal types in their repertoire. Vocal signals have the advantage of having higher information content but may have the disadvantage of loosing this information in a noisy environment. Surface-generated sounds have energy distributed over a greater frequency range and may be less likely to become confused in periods of high wind-generated noise but have less information content when compared with vocal sounds. Therefore, surface-generated sounds may improve detection or enhance the perception of vocal signals in a noisy environment.     

Sex‐related site fidelity of humpback whales (Megaptera novaeangliae) to the Fueguian Archipelago feeding area,Chile

We investigated sex‐related site fidelity by humpback whales to the Fueguian Archipelago, a new feeding area in the eastern South Pacific, by examining the resighting histories of 45 males and 39 females recorded from 2003 to 2012. Results indicated an overall annual return to the feeding area of 74.8%, and annual sex ratio is roughly equal in the population. The probability of an individual being resighted across years and in subsequent years was not significantly different for both males and females, however, the proportion of resighting within a year was significantly higher for individual males compared to females. Potential sources of sex‐related bias were analyzed, but none were found to be significant. Greater intraannual resighting frequency for males may reflect sex‐based differences in spatial occupation and short‐range movements due to potential differences in energy budgets.     

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.