Strong and lasting impacts of past global warming on baleen whales and their prey.

Global warming is affecting the population dynamics and trophic interactions across a wide range of ecosystems and habitats. Translating these real-time effects into their long-term consequences remains a challenge. The rapid and extreme warming period that occurred after the Last Glacial Maximum (LGM) during the Pleistocene-Holocene transition (7-12 thousand years ago) provides an opportunity to gain insights into the long-term responses of natural populations to periods with global warming. The effects of this post-LGM warming period have been assessed in many terrestrial taxa, whereas insights into the impacts of rapid global warming on marine taxa remain limited, especially for megafauna. In order to understand how large-scale climate fluctuations during the post-LGM affected baleen whales and their prey, we conducted an extensive, large-scale analysis of the long-term effects of the post-LGM warming on abundance and inter-ocean connectivity in eight baleen whale and seven prey (fish and invertebrates) species across the Southern and the North Atlantic Ocean; two ocean basins that differ in key oceanographic features. The analysis was based upon 7032 mitochondrial DNA sequences as well as genome-wide DNA sequence variation in 100 individuals. The estimated temporal changes in genetic diversity during the last 30,000 years indicated that most baleen whale populations underwent post-LGM expansions in both ocean basins. The increase in baleen whale abundance during the Holocene was associated with simultaneous changes in their prey and climate. Highly correlated, synchronized and exponential increases in abundance in both baleen whales and their prey in the Southern Ocean were indicative of a dramatic increase in ocean productivity. In contrast, the demographic fluctuations observed in baleen whales and their prey in the North Atlantic Ocean were subtle, varying across taxa and time. Perhaps most important was the observation that the ocean-wide expansions and decreases in abundance that were initiated by the post-LGM global warming, continued for millennia after global temperatures stabilized, reflecting persistent, long-lasting impacts of global warming on marine fauna.

Runs of homozygosity in killer whale genomes provide a global record of demographic histories.

Runs of homozygosity (ROH) occur when offspring inherit haplotypes that are identical by descent from each parent. Length distributions of ROH are informative about population history; specifically, the probability of inbreeding mediated by mating system and/or population demography. Here, we investigated whether variation in killer whale (Orcinus orca) demographic history is reflected in genome-wide heterozygosity and ROH length distributions, using a global data set of 26 genomes representative of geographic and ecotypic variation in this species, and two F1 admixed individuals with Pacific-Atlantic parentage. We first reconstructed demographic history for each population as changes in effective population size through time using the pairwise sequential Markovian coalescent (PSMC) method. We found a subset of populations declined in effective population size during the Late Pleistocene, while others had more stable demography. Genomes inferred to have undergone ancestral declines in effective population size, were autozygous at hundreds of short ROH (<1 Mb), reflecting high background relatedness due to coalescence of haplotypes deep within the pedigree. In contrast, longer and therefore younger ROH (>1.5 Mb) were found in low latitude populations, and populations of known conservation concern. These include a Scottish killer whale, for which 37.8% of the autosomes were comprised of ROH >1.5 Mb in length. The fate of this population, in which only two adult males have been sighted in the past five years, and zero fecundity over the last two decades, may be inextricably linked to its demographic history and consequential inbreeding depression.

Tracking of marine predators to protect Southern Ocean ecosystems.

Southern Ocean ecosystems are under pressure from resource exploitation and climate change1,2. Mitigation requires the identification and protection of Areas of Ecological Significance (AESs), which have so far not been determined at the ocean-basin scale. Here, using assemblage-level tracking of marine predators, we identify AESs for this globally important region and assess current threats and protection levels. Integration of more than 4,000 tracks from 17 bird and mammal species reveals AESs around sub-Antarctic islands in the Atlantic and Indian Oceans and over the Antarctic continental shelf. Fishing pressure is disproportionately concentrated inside AESs, and climate change over the next century is predicted to impose pressure on these areas, particularly around the Antarctic continent. At present, 7.1% of the ocean south of 40°S is under formal protection, including 29% of the total AESs. The establishment and regular revision of networks of protection that encompass AESs are needed to provide long-term mitigation of growing pressures on Southern Ocean ecosystems.

The retrospective analysis of Antarctic tracking data project.

The Retrospective Analysis of Antarctic Tracking Data (RAATD) is a Scientific Committee for Antarctic Research project led jointly by the Expert Groups on Birds and Marine Mammals and Antarctic Biodiversity Informatics, and endorsed by the Commission for the Conservation of Antarctic Marine Living Resources. RAATD consolidated tracking data for multiple species of Antarctic meso- and top-predators to identify Areas of Ecological Significance. These datasets and accompanying syntheses provide a greater understanding of fundamental ecosystem processes in the Southern Ocean, support modelling of predator distributions under future climate scenarios and create inputs that can be incorporated into decision making processes by management authorities. In this data paper, we present the compiled tracking data from research groups that have worked in the Antarctic since the 1990s. The data are publicly available through biodiversity.aq and the Ocean Biogeographic Information System. The archive includes tracking data from over 70 contributors across 12 national Antarctic programs, and includes data from 17 predator species, 4060 individual animals, and over 2.9 million observed locations.

Persistent organic pollutants in blubber of fin whales (Balaenoptera physalus) from the Southern Ocean.

Persistent organic pollutants (POPs) were analyzed in eighteen blubber samples biopsied from fin whales (Balaenoptera physalus) during the feeding season near the Antarctic Peninsula in the summer of 2013. POP content (in ng g-1 lipid weight) ranged from 46.4 to 708 for polychlorinated biphenyls (∑PCBs), 6.77 to 123 for hexachlorobenzene (HCB), 10.1 to 489 for dichlorodiphenyltrichloroethane and derivatives (∑DDTs), 5.38 to 52.8 for hexachlorocyclohexanes (∑HCH) and <0.40 to 2.54 for polybrominated diphenyl ethers (∑PBDEs). The presence of those compounds in Southern Ocean fin whales is related to long-range transport and their diet based mainly on euphausiids (krill). Their contents were much lower compared to the same species in other locations, especially in the Northern Hemisphere, presumably due to differences in trophic position and the proximity of POP sources and contamination of prey items.

Killer whale genomes reveal a complex history of recurrent admixture and vicariance.

Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree-like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidate complex population histories. Killer whales have limited extrinsic barriers to dispersal and have radiated globally, and are therefore a good candidate model for the application of such tools. Here, we analyse a global data set of killer whale genomes in a rare attempt to elucidate global population structure in a nonhuman species. We identify a pattern of genetic homogenisation at lower latitudes and the greatest differentiation at high latitudes, even between currently sympatric lineages. The processes underlying the major axis of structure include high drift at the edge of species' range, likely associated with founder effects and allelic surfing during postglacial range expansion. Divergence between Antarctic and non-Antarctic lineages is further driven by ancestry segments with up to four-fold older coalescence time than the genome-wide average; relicts of a previous vicariance during an earlier glacial cycle. Our study further underpins that episodic gene flow is ubiquitous in natural populations, and can occur across great distances and after substantial periods of isolation between populations. Thus, understanding the evolutionary history of a species requires comprehensive geographic sampling and genome-wide data to sample the variation in ancestry within individuals.

Fin whale (Balaenoptera physalus) mitogenomics: A cautionary tale of defining sub-species from mitochondrial sequence monophyly.

The advent of massive parallel sequencing technologies has resulted in an increase of studies based upon complete mitochondrial genome DNA sequences that revisit the taxonomic status within and among species. Spatially distinct monophyly in such mitogenomic genealogies, i.e., the sharing of a recent common ancestor among con-specific samples collected in the same region has been viewed as evidence for subspecies. Several recent studies in cetaceans have employed this criterion to suggest subsequent intraspecific taxonomic revisions. We reason that employing intra-specific, spatially distinct monophyly at non-recombining, clonally inherited genomes is an unsatisfactory criterion for defining subspecies based upon theoretical (genetic drift) and practical (sampling effort) arguments. This point was illustrated by a re-analysis of a global mitogenomic assessment of fin whales, Balaenoptera physalus spp., published by Archer et al. (2013), which proposed to further subdivide the Northern Hemisphere fin whale subspecies, B. p. physalus. The proposed revision was based upon the detection of spatially distinct monophyly among North Atlantic and North Pacific fin whales in a genealogy based upon complete mitochondrial genome DNA sequences. The extended analysis conducted in this study (1676 mitochondrial control region, 162 complete mitochondrial genome DNA sequences and 20 microsatellite loci genotyped in 380 samples) revealed that the apparent monophyly among North Atlantic fin whales reported by Archer et al. (2013) to be due to low sample sizes. In conclusion, defining sub-species from monophyly (i.e., the absence of para- or polyphyly) can lead to erroneous conclusions due to relatively "trivial" aspects, such as sampling. Basic population genetic processes (i.e., genetic drift and migration) also affect the time to the most recent common ancestor and hence the probability that individuals in a sample are monophyletic.

Southern Right Whale (Eubalaena australis) Reproductive Success is Influenced by Krill (Euphausia superba) Density and Climate.

The reproductive success of southern right whale (Eubalaena australis) depends on body condition and, therefore, on foraging success. This, in turn, might be affected by climatically driven change in the abundance of the species main prey, krill (Euphausia superba), on the feeding grounds. Annual data on southern right whale number of calves were obtained from aerial surveys carried out between 1997 and 2013 in southern Brazil, where the species concentrate during their breeding season. The number of calves recorded each year varied from 7 to 43 ( = 21.11 ± 11.88). Using cross-correlation analysis we examined the response of the species to climate anomalies and krill densities. Significant correlations were found with krill densities (r = 0.69, p = 0.002, lag 0 years), Oceanic Niño Index (r = -0.65, p = 0.03, lag 6 years), Antarctic Oscillation (r = 0.76, p = 0.01, lag 7 years) and Antarctic sea ice area (r = -0.68, p = 0.002, lag 0 years). Our results suggest that global climate indices influence southern right whale breeding success in southern Brazil by determining variation in food (krill) availability for the species. Therefore, increased frequency of years with reduced krill abundance, due to global warming, is likely to reduce the current rate of recovery of southern right whales from historical overexploitation.

Killer whale (Orcinus orca) whistles from the western South Atlantic Ocean include high frequency signals.

Acoustic parameters of killer whale (Orcinus orca) whistles were described for the western South Atlantic Ocean and highlight the occurrence of high frequency whistles. Killer whale signals were recorded on December of 2012, when a pod of four individuals was observed harassing a group of sperm whales. The high frequency whistles were highly stereotyped and were modulated mostly at ultrasonic frequencies. Compared to other contour types, the high frequency whistles are characterized by higher bandwidths, shorter durations, fewer harmonics, and higher sweep rates. The results add to the knowledge of vocal behavior of this species.

Geographic and temporal dynamics of a global radiation and diversification in the killer whale.

Global climate change during the Late Pleistocene periodically encroached and then released habitat during the glacial cycles, causing range expansions and contractions in some species. These dynamics have played a major role in geographic radiations, diversification and speciation. We investigate these dynamics in the most widely distributed of marine mammals, the killer whale (Orcinus orca), using a global data set of over 450 samples. This marine top predator inhabits coastal and pelagic ecosystems ranging from the ice edge to the tropics, often exhibiting ecological, behavioural and morphological variation suggestive of local adaptation accompanied by reproductive isolation. Results suggest a rapid global radiation occurred over the last 350 000 years. Based on habitat models, we estimated there was only a 15% global contraction of core suitable habitat during the last glacial maximum, and the resources appeared to sustain a constant global effective female population size throughout the Late Pleistocene. Reconstruction of the ancestral phylogeography highlighted the high mobility of this species, identifying 22 strongly supported long-range dispersal events including interoceanic and interhemispheric movement. Despite this propensity for geographic dispersal, the increased sampling of this study uncovered very few potential examples of ancestral dispersal among ecotypes. Concordance of nuclear and mitochondrial data further confirms genetic cohesiveness, with little or no current gene flow among sympatric ecotypes. Taken as a whole, our data suggest that the glacial cycles influenced local populations in different ways, with no clear global pattern, but with secondary contact among lineages following long-range dispersal as a potential mechanism driving ecological diversification.

Levels and profiles of chlorinated and brominated contaminants in Southern Hemisphere humpback whales, Megaptera novaeangliae.

The study documents the levels and profiles of selected contaminants [polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs), polybrominated diphenyl ethers (PBDEs) and methoxylated PBDEs (MeO-PBDEs)] in blubber biopsy samples collected from humpback whales (Megaptera novaeangliae) in Antarctic Peninsula waters. In addition, we investigated year-to-year and sex-related differences in the bioaccumulation patterns. Except for hexachlorobenzene (HCB), whose concentrations were in the same range as those found in whales from the Northern Hemisphere, levels of all other compounds were lower in Southern Hemisphere whales compared to literature data on animals from the Arctic and subarctic region. The mean contribution to the sum of all anthropogenic organohalogen compounds (ΣOHC) decreased in the following order ΣPCBs (44%)>HCB (31%)>ΣDDXs (13%)>ΣCHLs (4.6%)>ΣHCHs (4.4%)>ΣPBDEs (0.9%). The predominant compounds within each chemical class were: PCBs 153, 149, 101 and 138; p,p'-DDE; γ-HCH; trans-nonachlor; PBDEs 99 and 47. The most dominant MeO-PBDE congener was 6-MeO-BDE 47. As samples were collected during three consecutive summer seasons, year-to-year trends could be assessed indicating a significant decrease from 2000 to 2003 for ΣCHL levels. Higher ΣPBDE concentrations and higher values of the ΣPBDE / ΣMeO-PBDE ratio, as well as higher ratios between the two MeO-BDEs (2'-MeO-BDE 68/6-MeO-BDE 47) were found in females compared to males. Higher ΣMeO-PBDE concentrations and higher values of the ratios between the lower chlorinated and the higher chlorinated PCBs were found in males than in females. In addition, five out of six significant differences found through discriminant function analysis were gender-related. The literature reports both feeding in mid- to low-latitudes and sex-related differences in migration patterns for humpback whales from the Southern Hemisphere, indicating that the hypothesis of dietary differences between males and females cannot be excluded. Nevertheless, additional studies are required for further investigation of this hypothesis.

Southern Hemisphere humpback whales wintering off Central America: insights from water temperature into the longest mammalian migration.

We report on a wintering area off the Pacific coast of Central America for humpback whales (Megaptera novaeangliae) migrating from feeding areas off Antarctica. We document seven individuals, including a mother/calf pair, that made this migration (approx. 8300km), the longest movement undertaken by any mammal. Whales were observed as far north as 11 degrees N off Costa Rica, in an area also used by a boreal population during the opposite winter season, resulting in unique spatial overlap between Northern and Southern Hemisphere populations. The occurrence of such a northerly wintering area is coincident with the development of an equatorial tongue of cold water in the eastern South Pacific, a pattern that is repeated in the eastern South Atlantic. A survey of location and water temperature at the wintering areas worldwide indicates that they are found in warm waters (21.1-28.3 degrees C), irrespective of latitude. We contend that while availability of suitable reproductive habitat in the wintering areas is important at the fine scale, water temperature influences whale distribution at the basin scale. Calf development in warm water may lead to larger adult size and increased reproductive success, a strategy that supports the energy conservation hypothesis as a reason for migration.