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Concept: Whale surfacing behaviour

357

Almost all mammals communicate using sound, but few species produce complex songs. Two baleen whales sing complex songs that change annually, though only the humpback whale (Megaptera novaeangliae) has received much research attention. This study focuses on the other baleen whale singer, the bowhead whale (Balaena mysticetus). Members of the Spitsbergen bowhead whale population produced 184 different song types over a 3-year period, based on duty-cycled recordings from a site in Fram Strait in the northeast Atlantic. Distinct song types were recorded over short periods, lasting at most some months. This song diversity could be the result of population expansion, or immigration of animals from other populations that are no longer isolated from each other by heavy sea ice. However, this explanation does not account for the within season and annual shifting of song types. Other possible explanations for the extraordinary diversity in songs could be that it results either from weak selection pressure for interspecific identification or for maintenance of song characteristics or, alternatively, from strong pressure for novelty in a small population.

Concepts: Whale, Humpback whale, Whale surfacing behaviour, Baleen, Whaling, Bowhead whale

174

Southern Hemisphere humpback whales (Megaptera novaeangliae) generally undertake annual migrations from polar summer feeding grounds to winter calving and nursery grounds in subtropical and tropical coastal waters. Evidence for such migrations arises from seasonality of historic whaling catches by latitude, Discovery and natural mark returns, and results of satellite tagging studies. Feeding is generally believed to be limited to the southern polar region, where Antarctic krill (Euphausia superba) has been identified as the primary prey item. Non-migrations and / or suspended migrations to the polar feeding grounds have previously been reported from a summer presence of whales in the Benguela System, where feeding on euphausiids (E. lucens), hyperiid amphipods (Themisto gaudichaudii), mantis shrimp (Pterygosquilla armata capensis) and clupeid fish has been described. Three recent research cruises (in October/November 2011, October/November 2014 and October/November 2015) identified large tightly-spaced groups (20 to 200 individuals) of feeding humpback whales aggregated over at least a one-month period across a 220 nautical mile region of the southern Benguela System. Feeding behaviour was identified by lunges, strong milling and repetitive and consecutive diving behaviours, associated bird and seal feeding, defecations and the pungent “fishy” smell of whale blows. Although no dedicated prey sampling could be carried out within the tightly spaced feeding aggregations, observations of E. lucens in the region of groups and the full stomach contents of mantis shrimp from both a co-occurring predatory fish species (Thyrsites atun) and one entangled humpback whale mortality suggest these may be the primary prey items of at least some of the feeding aggregations. Reasons for this recent novel behaviour pattern remain speculative, but may relate to increasing summer humpback whale abundance in the region. These novel, predictable, inter-annual, low latitude feeding events provide considerable potential for further investigation of Southern Hemisphere humpback feeding behaviours in these relatively accessible low-latitude waters.

Concepts: Antarctica, Whale, Humpback whale, Whale surfacing behaviour, Fin whale, Whale watching, Krill, Whaling

110

The pulmonary system is a common site for bacterial infections in cetaceans, but very little is known about their respiratory microbiome. We used a small, unmanned hexacopter to collect exhaled breath condensate (blow) from two geographically distinct populations of apparently healthy humpback whales (Megaptera novaeangliae), sampled in the Massachusetts coastal waters off Cape Cod (n = 17) and coastal waters around Vancouver Island (n = 9). Bacterial and archaeal small-subunit rRNA genes were amplified and sequenced from blow samples, including many of sparse volume, as well as seawater and other controls, to characterize the associated microbial community. The blow microbiomes were distinct from the seawater microbiomes and included 25 phylogenetically diverse bacteria common to all sampled whales. This core assemblage comprised on average 36% of the microbiome, making it one of the more consistent animal microbiomes studied to date. The closest phylogenetic relatives of 20 of these core microbes were previously detected in marine mammals, suggesting that this core microbiome assemblage is specialized for marine mammals and may indicate a healthy, noninfected pulmonary system. Pathogen screening was conducted on the microbiomes at the genus level, which showed that all blow and few seawater microbiomes contained relatives of bacterial pathogens; no known cetacean respiratory pathogens were detected in the blow. Overall, the discovery of a shared large core microbiome in humpback whales is an important advancement for health and disease monitoring of this species and of other large whales. IMPORTANCE The conservation and management of large whales rely in part upon health monitoring of individuals and populations, and methods generally necessitate invasive sampling. Here, we used a small, unmanned hexacopter drone to noninvasively fly above humpback whales from two populations, capture their exhaled breath (blow), and examine the associated microbiome. In the first extensive examination of the large-whale blow microbiome, we present surprising results about the discovery of a large core microbiome that was shared across individual whales from geographically separated populations in two ocean basins. We suggest that this core microbiome, in addition to other microbiome characteristics, could be a useful feature for health monitoring of large whales worldwide.

Concepts: Bacteria, Microbiology, Pathogen, Cetacea, Whale, Humpback whale, Whale surfacing behaviour, Whaling

57

Humpback whales (Megaptera novaeangliae) were hunted commercially in Canada’s Pacific region until 1966. Depleted to an estimated 1,400 individuals throughout the North Pacific, humpback whales are listed as Threatened under Canada’s Species at Risk Act (SARA) and Endangered under the US Endangered Species Act. We conducted an 8-year photo-identification study to monitor humpback whale usage of a coastal fjord system in British Columbia (BC), Canada that was recently proposed as candidate critical habitat for the species under SARA. This participatory research program built collaborations among First Nations, environmental non-governmental organizations and academics. The study site, including the territorial waters of Gitga'at First Nation, is an important summertime feeding destination for migratory humpback whales, but is small relative to the population’s range. We estimated abundance and survivorship using mark-recapture methods using photographs of naturally marked individuals. Abundance of humpback whales in the region was large, relative to the site’s size, and generally increased throughout the study period. The resulting estimate of adult survivorship (0.979, 95% CI: 0.914, 0.995) is at the high end of previously reported estimates. A high rate of resights provides new evidence for inter-annual site fidelity to these local waters. Habitat characteristics of our study area are considered ecologically significant and unique, and this should be considered as regulatory agencies consider proposals for high-volume crude oil and liquefied natural gas tanker traffic through the area. Monitoring population recovery of a highly mobile, migratory species is daunting for low-cost, community-led science. Focusing on a small, important subset of the animals' range can make this challenge more tractable. Given low statistical power and high variability, our community is considering simpler ecological indicators of population health, such as the number of individuals harmed or killed each year by human activities, including ship strikes and entanglement in fishing gear.

Concepts: Hawaii, Endangered species, Whale, Humpback whale, Whale surfacing behaviour

41

The skin is the first line of defense between an animal and its environment, and disruptions in skin-associated microorganisms can be linked to an animal’s health and nutritional state. To better understand the skin microbiome of large whales, high-throughput sequencing of partial small subunit ribosomal RNA genes was used to study the skin-associated bacteria of 89 seemingly healthy humpback whales (Megaptera novaeangliae) sampled along the Western Antarctic Peninsula (WAP) during early (2010) and late (2013) austral summers. Six core genera of bacteria were present in 93% or more of all humpback skin samples. A shift was observed in the average relative abundance of these core genera over time, with the emergence of four additional core genera corresponding to a decrease in water temperature, possibly caused by seasonal or foraging related changes in skin biochemistry that influenced microbial growth, or other temporal-related factors. The skin microbiome differed between whales sampled at several regional locations along the WAP, suggesting that environmental factors or population may also influence the whale skin microbiome. Overall, the skin microbiome of humpback whales appears to provide insight into animal and environmental-related factors and may serve as a useful indicator for animal health or ecosystem alterations.IMPORTANCE The microbiomes of wild animals are currently understudied, but may provide information about animal health and/or animal-environmental interactions. In the largest sampling of any marine mammal microbiome, this study demonstrates conservation in the skin microbiome of 89 seemingly healthy humpback whales sampled in the Western Antarctic Peninsula, with shifts in the bacterial community composition related to temporal and regional variability. This study is important because it suggests that the skin microbiome of humpback whales could provide insight into animal nutritional or seasonal/environmental-related factors, which are becoming increasingly important to recognize due to unprecedented rates of climate change and anthropogenic impact on ocean ecosystems.

Concepts: Archaea, Bacteria, RNA, Ribosomal RNA, Ribosome, Whale, Humpback whale, Whale surfacing behaviour

33

Humpback whales migrate between relatively unproductive tropical or temperate breeding grounds and productive high latitude feeding areas. However, not all individuals of a population undertake the annual migration to the breeding grounds; instead some are thought to remain on the feeding grounds year-round, presumably to avoid the energetic demands of migration. In the Southern Hemisphere, ice and inclement weather conditions restrict investigations of humpback whale presence on feeding grounds as well as the extent of their southern range. Two years of near-continuous recordings from the PerenniAL Acoustic Observatory in the Antarctic Ocean (PALAOA, Ekström Iceshelf, 70°31’S, 8°13'W) are used to explore the acoustic presence of humpback whales in an Antarctic coastal area. Humpback whale calls were present during nine and eleven months of 2008 and 2009, respectively. In 2008, calls were present in January through April, June through August, November and December, whereas in 2009, calls were present throughout the year, except in September. Calls occurred in un-patterned sequences, representing non-song sound production. Typically, calls occurred in bouts, ranging from 2 to 42 consecutive days with February, March and April having the highest daily occurrence of calls in 2008. In 2009, February, March, April and May had the highest daily occurrence of calls. Whales were estimated to be within a 100 km radius off PALAOA. Calls were also present during austral winter when ice cover within this radius was >90%. These results demonstrate that coastal areas near the Antarctic continent are likely of greater importance to humpback whales than previously assumed, presumably providing food resources year-round and open water in winter where animals can breathe.

Concepts: Antarctica, Whale, Humpback whale, Whale surfacing behaviour, Southern Ocean, Whale watching

28

BACKGROUND: Telomeres, the protective cap of chromosomes, have emerged as powerful markers of biological age and life history in model and non-model species. The qPCR method for telomere length estimation is one of the most common methods for telomere length estimation, but has received recent critique for being too error-prone and yielding unreliable results. This critique coincides with an increasing awareness of the potentials and limitations of the qPCR technique in general and the proposal of a general set of guidelines (MIQE) for standardization of experimental, analytical, and reporting steps of qPCR. In order to evaluate the utility of the qPCR method for telomere length estimation in non-model species, we carried out four different qPCR assays directed at humpback whale telomeres, and subsequently performed a rigorous quality control to evaluate the performance of each assay. RESULTS: Performance differed substantially among assays and only one assay was found useful for telomere length estimation in humpback whales. The most notable factors causing these inter-assay differences were primer design and choice of using singleplex or multiplex assays. Inferred amplification efficiencies differed by up to 40 % depending on assay and quantification method, however this variation only affected telomere length estimates in the worst performing assays. CONCLUSION: Our results suggest that seemingly well performing qPCR assays may contain biases that will only be detected by extensive quality control. Moreover, we show that the qPCR method for telomere length estimation can be highly precise and accurate, and thus suitable for telomere measurement in non-model species, if effort is devoted to optimization at all experimental and analytical steps. We conclude by highlighting a set of quality controls which may serve for further standardization of the qPCR method for telomere length estimation, and discuss some of the factors that may cause variation in qPCR experiments.

Concepts: DNA, Quality control, DNA replication, Telomere, Whale, Humpback whale, Whale surfacing behaviour, Whale watching

17

We used network-based diffusion analysis to reveal the cultural spread of a naturally occurring foraging innovation, lobtail feeding, through a population of humpback whales (Megaptera novaeangliae) over a period of 27 years. Support for models with a social transmission component was 6 to 23 orders of magnitude greater than for models without. The spatial and temporal distribution of sand lance, a prey species, was also important in predicting the rate of acquisition. Our results, coupled with existing knowledge about song traditions, show that this species can maintain multiple independently evolving traditions in its populations. These insights strengthen the case that cetaceans represent a peak in the evolution of nonhuman culture, independent of the primate lineage.

Concepts: Mammal, Whale, Humpback whale, Whale surfacing behaviour, Whaling

14

Exposure to underwater sound can cause permanent hearing loss and other physiological effects in marine animals. To reduce this risk, naval sonars are sometimes gradually increased in intensity at the start of transmission (‘ramp-up’). Here, we conducted experiments in which tagged humpback whales were approached with a ship to test whether a sonar operation preceded by ramp-up reduced three risk indicators - maximum sound pressure level (SPLmax), cumulative sound exposure level (SELcum) and minimum source-whale range (Rmin) - compared with a sonar operation not preceded by ramp-up. Whales were subject to one no-sonar control session and either two successive ramp-up sessions (RampUp1, RampUp2) or a ramp-up session (RampUp1) and a full-power session (FullPower). Full-power sessions were conducted only twice; for other whales we used acoustic modelling that assumed transmission of the full-power sequence during their no-sonar control. Averaged over all whales, risk indicators in RampUp1 (n=11) differed significantly from those in FullPower (n=12) by -3.0 dB (SPLmax), -2.0 dB (SELcum) and +168 m (Rmin), but not significantly from those in RampUp2 (n=9). Only five whales in RampUp1, four whales in RampUp2 and none in FullPower or control sessions avoided the sound source. For RampUp1, we found statistically significant differences in risk indicators between whales that avoided the sonar and whales that did not: -4.7 dB (SPLmax), -3.4 dB (SELcum) and +291 m (Rmin). In contrast, for RampUp2, these differences were smaller and not significant. This study suggests that sonar ramp-up has a positive but limited mitigative effect for humpback whales overall, but that ramp-up can reduce the risk of harm more effectively in situations when animals are more responsive and likely to avoid the sonar, e.g. owing to novelty of the stimulus, when they are in the path of an approaching sonar ship.

Concepts: Sound, Whale, Humpback whale, Whale surfacing behaviour

14

Noise from shipping activity in North Atlantic coastal waters has been steadily increasing and is an area of growing conservation concern, as it has the potential to disrupt the behaviour of marine organisms. This study examines the impacts of ship noise on bottom foraging humpback whales (Megaptera novaeangliae) in the western North Atlantic. Data were collected from 10 foraging whales using non-invasive archival tags that simultaneously recorded underwater movements and the acoustic environment at the whale. Using mixed models, we assess the effects of ship noise on seven parameters of their feeding behaviours. Independent variables included the presence or absence of ship noise and the received level of ship noise at the whale. We found significant effects on foraging, including slower descent rates and fewer side-roll feeding events per dive with increasing ship noise. During 5 of 18 ship passages, dives without side-rolls were observed. These findings indicate that humpback whales on Stellwagen Bank, an area with chronically elevated levels of shipping traffic, significantly change foraging activity when exposed to high levels of ship noise. This measureable reduction in within-dive foraging effort of individual whales could potentially lead to population-level impacts of shipping noise on baleen whale foraging success.

Concepts: Whale, Humpback whale, Whale surfacing behaviour, Whale watching