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.     

Fine‐scale spatial differences in humpback whale diet composition near Kodiak,Alaska

On the North Pacific feeding grounds, humpback whales (Megaptera novaeangliae) are recovering from commercial whaling at a rapid rate (6.8%). The potential effect that this recovery will have on trophic dynamics involving these predators is currently unknown. To better elucidate complex trophic dynamics, variability in diet composition of apex predators on their respective feeding grounds needs to be understood. Thus, we explored the diet composition of two defined subaggregations of humpback whales of the Kodiak Archipelago population (“North,” “South”) using stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope ratios of humpback whale skin and regional prey samples in Bayesian dietary mixing models. Humpback whales in the “North” region consumed proportionally more fish, dominated by capelin (Mallotus villosus), whereas, whales in the “South” region consumed predominantly krill. The difference in diet composition appears to reflect regional differences in prey availability. Thus, regional variability in diet composition by humpback whales may have disproportionate impacts on prey resources of sympatric predators depending on available prey biomass. As a result, we suggest fine‐scale studies of apex predator diets are needed to better model trophic dynamics with accuracy.     

DNA methylation-based biomarkers for ageing long-lived cetaceans

Epigenetic approaches for estimating the age of living organisms are revolutionizing studies of long-lived species. Molecular biomarkers that allow age estimates from small tissue biopsies promise to enhance studies of long-lived whales, addressing a fundamental and challenging parameter in wildlife management. DNA methylation (DNAm) can affect gene expression, and strong correlations between DNAm patterns and age have been documented in humans and nonhuman vertebrates and used to construct “epigenetic clocks”. We present several epigenetic clocks for skin samples from two of the longest-lived cetaceans, killer whales and bowhead whales. Applying the mammalian methylation array to genomic DNA from skin samples we validate four different clocks with median errors of 2.3–3.7 years. These epigenetic clocks demonstrate the validity of using cytosine methylation data to estimate the age of long-lived cetaceans and have broad applications supporting the conservation and management of long-lived cetaceans using genomic DNA from remote tissue biopsies.     

Prey preferences of sympatric fin (Balaenoptera physalus) and humpback (Megaptera novaeangliae) whales revealed by stable isotope mixing models

Over‐exploitation of top predators and fish stocks has altered ecosystems towards less productive systems with fewer trophic levels. In the Celtic Sea (CS), discards and bycatch levels have prompted concern about some fisheries, while fin and humpback whales are recovering from centuries of over‐exploitation. A lack of empirical evidence on the preferred diet of some predators such as whales in the CS has hindered the implementation of effective conservation measures using an ecosystem‐based approach to fisheries management. Using a Bayesian framework (SIAR), stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope mixing models were used to assign proportionate diet solutions to fin and humpback whales (skin biopsies) and putative prey items: herring (Clupea harengus), sprat (Sprattus sprattus), and krill (Meganyctiphanes norvegica and Nyctiphanes couchii) in the CS. Krill was the single most important prey item in the diet of fin whales, but one of the least important for humpback whales (albeit based on a small sample of humpback whale samples). Age 0 sprat and herring comprised a large proportion of the diet of both species, followed by older sprat (age 1–2) and older herring (age 2–4). An ecosystem based approach to fisheries management will be required in the CS if we seek effective conservation of both fin and humpback whales, and sustainable fisheries.     

The diets of humpback whales (Megaptera novaeangliae) on the shelf and oceanic feeding grounds in the western North Pacific inferred from stable isotope analysis

Humpback whales feed on a variety of prey, but significant differences likely occur between regional feeding grounds. In this study, the diets of humpback whales were analyzed by comparing stable isotope ratios in animal tissues at three humpback whale feeding grounds in the Russian Far East: Karaginsky Gulf, Anadyr Gulf, and the Commander Islands. Anadyr Gulf is a neritic zone far from a shelf break, Karaginsky Gulf is a neritic zone close to a shelf break, and the Commander Islands represent an open oceanic ecosystem where whales feed off the shelf break. Samples from the Commander Islands had the lowest mean δ¹³C and δ¹⁵N values (mean ± SE: δ¹³C = ?18.7 ± 0.1, δ¹⁵N = 10.4 ± 0.1) compared to the samples from Karaginsky Gulf (δ¹³C = ?17.2 ± 0.1, δ¹⁵N = 12.7 ± 0.2) and Anadyr Gulf (δ¹³C= ?17.8 ± 0.1, δ¹⁵N = 14.0 ± 0.4). The samples from Anadyr Gulf had the highest δ¹⁵N values, while the samples from Karaginsky Gulf had the highest δ¹³C values. Both δ¹³C and δ¹⁵N values differed significantly among all three areas. Our data support the hypothesis that humpback whales tend to feed on fish in neritic areas and on plankton in deep oceanic waters.     

Migratory preferences of humpback whales between feeding and breeding grounds in the eastern South Pacific

Latitudinal preferences within the breeding range have been suggested for Breeding Stock G humpback whales that summer in different feeding areas of the eastern South Pacific. To address this hypothesis, humpback whales photo‐identified from the Antarctic Peninsula and the Fueguian Archipelago (southern Chile) were compared with whales photo‐identified from lower latitudes extending from northern Peru to Costa Rica. This comparison was performed over a time span that includes 18 austral seasons. A total of 238 whales identified from the Antarctic Peninsula and 25 whales from the Fueguian Archipelago were among those photo‐identified at the breeding grounds. Our findings showed that humpback whales from each feeding area were resighted unevenly across the breeding grounds, which suggests a degree of spatial structuring in the migratory pathway. Humpback whales that feed at the Antarctic Peninsula were more likely to migrate to the southern breeding range between northern Peru and Colombia, whereas whales that feed at the Fueguian Archipelago were more likely to be found in the northern range of the breeding ground off Panama. Further photo‐identification efforts and genetic sampling from poorly sampled or unsampled areas are recommended to confirm these reported connectivity patterns.     

CpG methylation frequency of TET2, GRIA2, and CDKN2A genes in the North Atlantic fin whale varies with age and between populations

Recovery rates for baleen whales that were decimated by exploitation vary between species and populations. Age determination is critical for the understanding of recovery trends and population structure, but determining age in free-ranging individuals remains challenging. Recent research has suggested that the methylation level of some genes in skin samples may provide age determinations with accuracy. We selected nine CpG sites from three genes (TET2, CDKN2A, and GRIA2) and analyzed them in 40 skin samples from known-age individuals pertaining to two different populations of fin whales from the North Atlantic. We observed significant correlations with age in five CpG sites. We used three of these CpG sites to perform an epigenetic age estimation. Predictions had a standard deviation of 2.94, but regression between observed and predicted ages showed a clear underestimation for older fin whales. For further development, we suggest: (1) screening for new CpG sites associated with age that exhibit higher variability between individuals, and (2) including older animals whenever the sampling allows it. We also observed subtle, but significant differences between the two populations studied in one of the CpG sites (TET2_CpG + 21). We attributed these differences to genetic differences or to the dissimilar environments that affect both populations.     

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.     

Rhyme-like Repetitions in Songs of Humpback Whales

Humpback whales (Megaptera novaeangliae) sing long, complex songs which continually change over time. In certain time periods the songs contain repeating patterns which structurally resemble human rhyming, and which, like human rhyming, tend to occur in highly rhythmical contexts. We speculate that humpback whales may use these repetitions as mnemonic devices, much as humans are thought to use rhymes. With this speculation in mind we examine 548 humpback whale songs from 7 years in the eastern North Pacific and 12 years in the western North Atlantic oceans. We find that rhyme-like structures are most likely to occur in songs containing the most material to be remembered.     

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.     

Potential vessel collisions with Southern Hemisphere humpback whales wintering off Pacific Panama

Vessel collision is a threat to many whale species, and the risk has increased with expanding maritime traffic. This compromises international conservation efforts and requires urgent attention from the world's maritime industry. Humpback whales (Megaptera novaeangliae) are at the top of the death toll, and although Central America is a wintering area for populations from both the Northern and Southern Hemispheres, existing efforts to reduce ship‐whale collisions are meager. Herein, we evaluated the potential collisions between vessels and humpback whales wintering off Pacific Panama by following the movements of 15 whales tagged with satellite transmitters and comparing these data with tracks plotted using AIS real‐time latitude‐longitude points from nearly 1,000 commercial vessels. Movements of whales (adults and calves) in the Gulf of Panama coincide with major commercial maritime routes. AIS vessel data analyzed for individual whale satellite tracks showed that 53% (8 whales) of whales had 98 encounters within 200 m with 81 different vessels in just 11 d. We suggest implementing a 65 nmi Traffic Separation Scheme and a 10 kn maximum speed for vessel routing into the Gulf of Panama during the wintering season. In so doing, the area for potential whale‐vessel collisions could be reduced by 93%.     

Against the current: an inter-oceanic whale migration event

Humpback whales seasonally migrate long distances between tropical and polar regions. However, inter-oceanic exchange is rare and difficult to document. Using skin biopsy samples collected in the Indian Ocean and in the South Atlantic Ocean, and a genetic capture-recapture approach based on microsatellite genotyping, we were able to reveal the first direct genetic evidence of the inter-oceanic migration of a male humpback whale. This exceptional migration to wintering grounds of two different ocean basins questions traditional notions of fidelity to an ocean basin, and demonstrates how the behaviour of highly mobile species may be elucidated from combining genetics with long-term field studies. Our finding has implications for management of humpback whale populations, as well as for hypotheses concerning cultural transmission of behaviour.     

Migratory movements of individual humpback whales photographed off the eastern coast of Australia

Humpback whales (Megaptera novaeangliae) migrate long distances each year on a return journey from low‐latitude breeding grounds to high‐latitude feeding grounds. Migration is influenced by subtle and complex social behaviors and the assumption that whales transit directly through the migratory corridor off the east coast of Australia requires further investigation. From 2003 to 2005, we followed the movements of 99 individual whales within one migratory cycle from three locations, off Byron Bay during the whales' northern migration and in Hervey Bay and at Ballina during the southern migration. The median sighting interval of whales between Byron Bay and Hervey Bay (n = 26) was 52 d (IQR = 42.5–75.5); between Byron Bay and Ballina (n = 21) was 59 d (IQR = 47.0–70.0); and between Hervey Bay and Ballina (n = 33) was 9 d (8.0–14.0). The overall pattern observed from these resightings suggests that Group E1 humpback whales spend approximately two months in the northern quarter of their range during the austral winter months. Intraseason resightings of whales at Ballina (n = 13, median sighting interval = 7 d) also suggest that some individuals, particularly adult males, may circle back north during their general southward journey along this part of the coast, perhaps in an attempt to increase mating opportunities.     

Evidence of two subaggregations of humpback whales on the Kodiak,Alaska, feeding ground revealed from stable isotope analysis

Knowledge of humpback whale (Megaptera novaeangliae) foraging on feeding grounds is becoming increasingly important as the growing North Pacific population recovers from commercial whaling and consumes more prey, including economically important fishes. We explored spatial and temporal (interannual, within‐season) variability in summer foraging by humpback whales along the eastern side of the Kodiak Archipelago as described by stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope ratios of humpback whale skin (n = 118; 2004–2013). The trophic level (TL) of individual whales was calculated using basal food web δ¹⁵N values collected within the study area. We found evidence for the existence of two subaggregations of humpback whales (“North,” “South”) on the feeding ground that fed at different TLs throughout the study period. Linear mixed models suggest that within an average year, Kodiak humpback whales forage at a consistent TL during the feeding season. TL estimates support mixed consumption of fish and zooplankton species in the “North” (mean ± SE; 3.3 ± 0.1) and predominant foraging on zooplankton in the “South” (3.0 ± 0.1). This trend appears to reflect spatial differences in prey availability, and thus, our results suggest North Pacific humpback whales may segregate on feeding aggregations and target discrete prey species.     

INTERCHANGE AND ISOLATION OF HUMPBACK WHALES OFF CALIFORNIA AND OTHER NORTH PACIFIC FEEDING GROUNDS

Humpback whales feed in several high-latitude areas of the North Pacific. We examined the interchange of humpback whales between one of these areas, off California, and those in other feeding grounds in the eastern North Pacific:. Fluke photographs of 597 humpback whales identified off California between 1986 and 1992 were compared with those off Oregon and Washington (29); British Columbia (81); southeastern Alaska (343); Prince William Sound, Alaska (141); Kodiak Island, Alaska (104); Shumagin Islands, Alaska (22); and in the Bering Sea (7). A high degree of interchange, both inter-and intrayear, was found among humpback whales seen off California, Oregon, and Washington., A low rate of interchange was found between British Columbia and California.: two whales seen near the British Columbia/Washington border were photographed off California in a different year, No interchange was found between California and the three feeding areas in Alaska. Humpback whales off California, Oregon, and Washington form a single intermixing feeding aggregation with only limited interchange with areas farther north. These findings are consistent with photographic identification studies in the North Atlantic and with genetic studies in both the North Atlantic and North Pacific.     

Factors driving the variability in diving and movement behavior of migrating humpback whales (Megaptera novaeangliae): Implications for anthropogenic disturbance studies

Humpback whales (Megaptera novaeangliae) undertake one of the longest migrations of any animal and while on a broad‐scale this journey appears direct, on a fine‐scale, behaviors associated with socializing and breeding are regularly observed. However, little is known about which social and environmental factors influence behavior during this time. Here we examined the effect of multiple factors on the movement (speed and course) and diving behavior (dive and surfacing duration) of humpback whales during migration off the eastern coast of Australia. Focal data (202 h) were collected on 94 different whale groups with simultaneous social and environmental context data. The environmental factors water depth and wind speed were found to be important predictors of dive and movement behavior, whereas social factors were less influential at this site. Groups tended to dive for longer with increased water depth but traveled more slowly in increasing wind speeds. These baseline studies are crucial when examining the effect of anthropogenic disturbance. Determining which natural factors significantly affect behavior ensures any observed behavioral changes are correctly attributed to the disturbance and are not a result of other factors. In addition, any responses observed can be put into biological context and their relative magnitude determined.     

Signals from the south; humpback whales carry messages of Antarctic sea‐ice ecosystem variability

Southern hemisphere humpback whales (Megaptera novaeangliae) rely on summer prey abundance of Antarctic krill (Euphausia superba) to fuel one of the longest‐known mammalian migrations on the planet. It is hypothesized that this species, already adapted to endure metabolic extremes, will be one of the first Antarctic consumers to show measurable physiological change in response to fluctuating prey availability in a changing climate; and as such, a powerful sentinel candidate for the Antarctic sea‐ice ecosystem. Here, we targeted the sentinel parameters of humpback whale adiposity and diet, using novel, as well as established, chemical and biochemical markers, and assembled a time trend spanning 8 years. We show the synchronous, inter‐annual oscillation of two measures of humpback whale adiposity with Southern Ocean environmental variables and climate indices. Furthermore, bulk stable isotope signatures provide clear indication of dietary compensation strategies, or a lower trophic level isotopic change, following years indicated as leaner years for the whales. The observed synchronicity of humpback whale adiposity and dietary markers, with climate patterns in the Southern Ocean, lends strength to the role of humpback whales as powerful Antarctic sea‐ice ecosystem sentinels. The work carries significant potential to reform current ecosystem surveillance in the Antarctic region.     

MSAP markers and global cytosine methylation in plants: a literature survey and comparative analysis for a wild‐growing species

Methylation of DNA cytosines affects whether transposons are silenced and genes are expressed, and is a major epigenetic mechanism whereby plants respond to environmental change. Analyses of methylation‐sensitive amplification polymorphism (MS‐AFLP or MSAP) have been often used to assess methyl‐cytosine changes in response to stress treatments and, more recently, in ecological studies of wild plant populations. MSAP technique does not require a sequenced reference genome and provides many anonymous loci randomly distributed over the genome for which the methylation status can be ascertained. Scoring of MSAP data, however, is not straightforward, and efforts are still required to standardize this step to make use of the potential to distinguish between methylation at different nucleotide contexts. Furthermore, it is not known how accurately MSAP infers genome‐wide cytosine methylation levels in plants. Here, we analyse the relationship between MSAP results and the percentage of global cytosine methylation in genomic DNA obtained by HPLC analysis. A screening of literature revealed that methylation of cytosines at cleavage sites assayed by MSAP was greater than genome‐wide estimates obtained by HPLC, and percentages of methylation at different nucleotide contexts varied within and across species. Concurrent HPLC and MSAP analyses of DNA from 200 individuals of the perennial herb Helleborus foetidus confirmed that methyl‐cytosine was more frequent in CCGG contexts than in the genome as a whole. In this species, global methylation was unrelated to methylation at the inner CG site. We suggest that global HPLC and context‐specific MSAP methylation estimates provide complementary information whose combination can improve our current understanding of methylation‐based epigenetic processes in nonmodel plants.