Long-term stability in the circumpolar foraging range of a Southern Ocean predator between the eras of whaling and rapid climate change.

Assessing environmental changes in Southern Ocean ecosystems is difficult due to its remoteness and data sparsity. Monitoring marine predators that respond rapidly to environmental variation may enable us to track anthropogenic effects on ecosystems. Yet, many long-term datasets of marine predators are incomplete because they are spatially constrained and/or track ecosystems already modified by industrial fishing and whaling in the latter half of the 20th century. Here, we assess the contemporary offshore distribution of a wide-ranging marine predator, the southern right whale (SRW, Eubalaena australis), that forages on copepods and krill from ~30°S to the Antarctic ice edge (>60°S). We analyzed carbon and nitrogen isotope values of 1,002 skin samples from six genetically distinct SRW populations using a customized assignment approach that accounts for temporal and spatial variation in the Southern Ocean phytoplankton isoscape. Over the past three decades, SRWs increased their use of mid-latitude foraging grounds in the south Atlantic and southwest (SW) Indian oceans in the late austral summer and autumn and slightly increased their use of high-latitude (>60°S) foraging grounds in the SW Pacific, coincident with observed changes in prey distribution and abundance on a circumpolar scale. Comparing foraging assignments with whaling records since the 18th century showed remarkable stability in use of mid-latitude foraging areas. We attribute this consistency across four centuries to the physical stability of ocean fronts and resulting productivity in mid-latitude ecosystems of the Southern Ocean compared with polar regions that may be more influenced by recent climate change.

Origin and expansion of the world's most widespread pinniped: Range-wide population genomics of the harbour seal (Phoca vitulina).

The harbour seal (Phoca vitulina) is the most widely distributed pinniped, occupying a wide variety of habitats and climatic zones across the Northern Hemisphere. Intriguingly, the harbour seal is also one of the most philopatric seals, raising questions as to how it colonized its current range. To shed light on the origin, remarkable range expansion, population structure and genetic diversity of this species, we used genotyping-by-sequencing to analyse ~13,500 biallelic single nucleotide polymorphisms from 286 individuals sampled from 22 localities across the species' range. Our results point to a Northeast Pacific origin of the harbour seal, colonization of the North Atlantic via the Canadian Arctic, and subsequent stepping-stone range expansions across the North Atlantic from North America to Europe, accompanied by a successive loss of genetic diversity. Our analyses further revealed a deep divergence between modern North Pacific and North Atlantic harbour seals, with finer-scale genetic structure at regional and local scales consistent with strong philopatry. The study provides new insights into the harbour seal's remarkable ability to colonize and adapt to a wide range of habitats. Furthermore, it has implications for current harbour seal subspecies delineations and highlights the need for international and national red lists and management plans to ensure the protection of genetically and demographically isolated populations.

A deepening understanding of animal culture suggests lessons for conservation.

A key goal of conservation is to protect biodiversity by supporting the long-term persistence of viable, natural populations of wild species. Conservation practice has long been guided by genetic, ecological and demographic indicators of risk. Emerging evidence of animal culture across diverse taxa and its role as a driver of evolutionary diversification, population structure and demographic processes may be essential for augmenting these conventional conservation approaches and decision-making. Animal culture was the focus of a ground-breaking resolution under the Convention on the Conservation of Migratory Species of Wild Animals (CMS), an international treaty operating under the UN Environment Programme. Here, we synthesize existing evidence to demonstrate how social learning and animal culture interact with processes important to conservation management. Specifically, we explore how social learning might influence population viability and be an important resource in response to anthropogenic change, and provide examples of how it can result in phenotypically distinct units with different, socially learnt behavioural strategies. While identifying culture and social learning can be challenging, indirect identification and parsimonious inferences may be informative. Finally, we identify relevant methodologies and provide a framework for viewing behavioural data through a cultural lens which might provide new insights for conservation management.

Speciation in the deep: genomics and morphology reveal a new species of beaked whale Mesoplodon eueu.

The deep sea has been described as the last major ecological frontier, as much of its biodiversity is yet to be discovered and described. Beaked whales (ziphiids) are among the most visible inhabitants of the deep sea, due to their large size and worldwide distribution, and their taxonomic diversity and much about their natural history remain poorly understood. We combine genomic and morphometric analyses to reveal a new Southern Hemisphere ziphiid species, Ramari's beaked whale, Mesoplodon eueu, whose name is linked to the Indigenous peoples of the lands from which the species holotype and paratypes were recovered. Mitogenome and ddRAD-derived phylogenies demonstrate reciprocally monophyletic divergence between M. eueu and True's beaked whale (M. mirus) from the North Atlantic, with which it was previously subsumed. Morphometric analyses of skulls also distinguish the two species. A time-calibrated mitogenome phylogeny and analysis of two nuclear genomes indicate divergence began circa 2 million years ago (Ma), with geneflow ceasing 0.35-0.55 Ma. This is an example of how deep sea biodiversity can be unravelled through increasing international collaboration and genome sequencing of archival specimens. Our consultation and involvement with Indigenous peoples offers a model for broadening the cultural scope of the scientific naming process.

Trypsin-Like Proteases and Their Role in Muco-Obstructive Lung Diseases.

Trypsin-like proteases (TLPs) belong to a family of serine enzymes with primary substrate specificities for the basic residues, lysine and arginine, in the P1 position. Whilst initially perceived as soluble enzymes that are extracellularly secreted, a number of novel TLPs that are anchored in the cell membrane have since been discovered. Muco-obstructive lung diseases (MucOLDs) are characterised by the accumulation of hyper-concentrated mucus in the small airways, leading to persistent inflammation, infection and dysregulated protease activity. Although neutrophilic serine proteases, particularly neutrophil elastase, have been implicated in the propagation of inflammation and local tissue destruction, it is likely that the serine TLPs also contribute to various disease-relevant processes given the roles that a number of these enzymes play in the activation of both the epithelial sodium channel (ENaC) and protease-activated receptor 2 (PAR2). More recently, significant attention has focused on the activation of viruses such as SARS-CoV-2 by host TLPs. The purpose of this review was to highlight key TLPs linked to the activation of ENaC and PAR2 and their association with airway dehydration and inflammatory signalling pathways, respectively. The role of TLPs in viral infectivity will also be discussed in the context of the inhibition of TLP activities and the potential of these proteases as therapeutic targets.

Perturbation drives changing metapopulation dynamics in a top marine predator.

Metapopulation theory assumes a balance between local decays/extinctions and local growth/new colonisations. Here we investigate whether recent population declines across part of the UK harbour seal range represent normal metapopulation dynamics or are indicative of perturbations potentially threatening the metapopulation viability, using 20 years of population trends, location tracking data (n = 380), and UK-wide, multi-generational population genetic data (n = 269). First, we use microsatellite data to show that two genetic groups previously identified are distinct metapopulations: northern and southern. Then, we characterize the northern metapopulation dynamics in two different periods, before and after the start of regional declines (pre-/peri-perturbation). We identify source-sink dynamics across the northern metapopulation, with two putative source populations apparently supporting three likely sink populations, and a recent metapopulation-wide disruption of migration coincident with the perturbation. The northern metapopulation appears to be in decay, highlighting that changes in local populations can lead to radical alterations in the overall metapopulation's persistence and dynamics.

Decadal shift in foraging strategy of a migratory southern ocean predator.

Rapid anthropogenic environmental change is expected to impact a host of ecological parameters in Southern Ocean ecosystems. Of critical concern are the consequences of these changes on the range of species that show fidelity to migratory destinations, as philopatry is hypothesized to help or hinder adaptation to climate change depending on the circumstances. Many baleen whales show philopatry to feeding grounds and are also capital breeders that meet migratory and reproductive costs through seasonal energy intake. Southern right whales (Eubalaena australis, SRWs) are capital breeders that have a strong relationship between reproductive output and foraging success. The population dynamics of South Africa's population of SRWs are characterized by two distinct periods: the 1990s, a period of high calving rates; and the late 2010s, a period associated with lowered calving rates. Here we use analyses of stable carbon (δ13 C) and nitrogen (δ15 N) isotope values from SRW biopsy samples (n = 122) collected during these two distinct periods to investigate foraging ecology of the South African population of SRWs over a time period coincident with the demographic shift. We show that South African SRWs underwent a dramatic northward shift, and diversification, in foraging strategy from 1990s to 2010s. Bayesian mixing model results suggest that during the 1990s, South African SRWs foraged on prey isotopically similar to South Georgia/Islas Georgias del Sur krill. In contrast, in the 2010s, South African SRWs foraged on prey isotopically consistent with the waters of the Subtropical Convergence, Polar Front and Marion Island. We hypothesize that this shift represents a response to changes in preferred habitat or prey, for example, the decrease in abundance and southward range contraction of Antarctic krill. By linking reproductive decline to changing foraging strategies for the first time in SRWs, we show that altering foraging strategies may not be sufficient to adapt to a changing ocean.

Genetic Diversity and Connectivity of Southern Right Whales (Eubalaena australis) Found in the Brazil and Chile-Peru Wintering Grounds and the South Georgia (Islas Georgias del Sur) Feeding Ground.

As species recover from exploitation, continued assessments of connectivity and population structure are warranted to provide information for conservation and management. This is particularly true in species with high dispersal capacity, such as migratory whales, where patterns of connectivity could change rapidly. Here we build on a previous long-term, large-scale collaboration on southern right whales (Eubalaena australis) to combine new (nnew) and published (npub) mitochondrial (mtDNA) and microsatellite genetic data from all major wintering grounds and, uniquely, the South Georgia (Islas Georgias del Sur: SG) feeding grounds. Specifically, we include data from Argentina (npub mtDNA/microsatellite = 208/46), Brazil (nnew mtDNA/microsatellite = 50/50), South Africa (nnew mtDNA/microsatellite = 66/77, npub mtDNA/microsatellite = 350/47), Chile-Peru (nnew mtDNA/microsatellite = 1/1), the Indo-Pacific (npub mtDNA/microsatellite = 769/126), and SG (npub mtDNA/microsatellite = 8/0, nnew mtDNA/microsatellite = 3/11) to investigate the position of previously unstudied habitats in the migratory network: Brazil, SG, and Chile-Peru. These new genetic data show connectivity between Brazil and Argentina, exemplified by weak genetic differentiation and the movement of 1 genetically identified individual between the South American grounds. The single sample from Chile-Peru had an mtDNA haplotype previously only observed in the Indo-Pacific and had a nuclear genotype that appeared admixed between the Indo-Pacific and South Atlantic, based on genetic clustering and assignment algorithms. The SG samples were clearly South Atlantic and were more similar to the South American than the South African wintering grounds. This study highlights how international collaborations are critical to provide context for emerging or recovering regions, like the SG feeding ground, as well as those that remain critically endangered, such as Chile-Peru.

Phylogenomic insights to the origin and spread of phocine distemper virus in European harbour seals in 1988 and 2002.

The 1988 and 2002 phocine distemper virus (PDV) outbreaks in European harbour seals Phoca vitulina are among the largest mass mortality events recorded in marine mammals. Despite its large impact on harbour seal population numbers, and 3 decades of studies, many questions regarding the spread and temporal origin of PDV remain unanswered. Here, we sequenced and analysed 7123 bp of the PDV genome, including the coding and non-coding regions of the entire P, M, F and H genes in tissues from 44 harbour seals to shed new light on the origin and spread of PDV in 1988 and 2002. The phylogenetic analyses trace the origin of the PDV strain causing the 1988 outbreak to between May 1987 and April 1988, while the origin of the strain causing the 2002 outbreak can be traced back to between June 2001 and May 2002. The analyses further point to several independent introductions of PDV in 1988, possibly linked to a southward mass immigration of harp seals in the winter and spring of 1987-1988. The vector for the 2002 outbreak is unknown, but the epidemiological analyses suggest the subsequent spread of PDV from the epicentre in the Kattegat, Denmark, to haul-out sites in the North Sea through several independent introductions.

Genomic Methods Take the Plunge: Recent Advances in High-Throughput Sequencing of Marine Mammals.

The dramatic increase in the application of genomic techniques to non-model organisms (NMOs) over the past decade has yielded numerous valuable contributions to evolutionary biology and ecology, many of which would not have been possible with traditional genetic markers. We review this recent progression with a particular focus on genomic studies of marine mammals, a group of taxa that represent key macroevolutionary transitions from terrestrial to marine environments and for which available genomic resources have recently undergone notable rapid growth. Genomic studies of NMOs utilize an expanding range of approaches, including whole genome sequencing, restriction site-associated DNA sequencing, array-based sequencing of single nucleotide polymorphisms and target sequence probes (e.g., exomes), and transcriptome sequencing. These approaches generate different types and quantities of data, and many can be applied with limited or no prior genomic resources, thus overcoming one traditional limitation of research on NMOs. Within marine mammals, such studies have thus far yielded significant contributions to the fields of phylogenomics and comparative genomics, as well as enabled investigations of fitness, demography, and population structure. Here we review the primary options for generating genomic data, introduce several emerging techniques, and discuss the suitability of each approach for different applications in the study of NMOs.

A pan-cetacean MHC amplicon sequencing panel developed and evaluated in combination with genome assemblies.

The major histocompatibility complex (MHC) is a highly polymorphic gene family that is crucial in immunity, and its diversity can be effectively used as a fitness marker for populations. Despite this, MHC remains poorly characterised in non-model species (e.g., cetaceans: whales, dolphins and porpoises) as high gene copy number variation, especially in the fast-evolving class I region, makes analyses of genomic sequences difficult. To date, only small sections of class I and IIa genes have been used to assess functional diversity in cetacean populations. Here, we undertook a systematic characterisation of the MHC class I and IIa regions in available cetacean genomes. We extracted full-length gene sequences to design pan-cetacean primers that amplified the complete exon 2 from MHC class I and IIa genes in one combined sequencing panel. We validated this panel in 19 cetacean species and described 354 alleles for both classes. Furthermore, we identified likely assembly artefacts for many MHC class I assemblies based on the presence of class I genes in the amplicon data compared to missing genes from genomes. Finally, we investigated MHC diversity using the panel in 25 humpback and 30 southern right whales, including four paternity trios for humpback whales. This revealed copy-number variable class I haplotypes in humpback whales, which is likely a common phenomenon across cetaceans. These MHC alleles will form the basis for a cetacean branch of the Immuno-Polymorphism Database (IPD-MHC), a curated resource intended to aid in the systematic compilation of MHC alleles across several species, to support conservation initiatives.

Phylogenetically controlled life history trait meta-analysis in cetaceans reveals unexpected negative brain size and longevity correlation.

The identification of patterns in trait evolution is essential to understand the interaction of evolutionary forces, and provides useful information for species management. Cetaceans are a phylogenetically well-resolved infraorder that exhibit distinct trait variation across behavioral, molecular, and life history dimensions, yet few researchers have applied a meta-analytic or comparative approach to these traits. To understand cetacean trait evolution, we used a phylogenetic generalized least squares approach to examine the cognitive buffer hypothesis (CBH). A large brain should buffer individuals against environmental challenges through increasing survival rates, and a longer lifespan should buffer individuals against the cost of extended development for larger brains according to the CBH, leading to an expected positive correlation between brain size and lifespan. In contrast to this expectation, previously observed in taxa including primates, we found a negative correlation between brain size and lifespan in cetaceans. This suggests cetaceans experience selective pressures different from most other mammals in these traits but may be more similar to some social mammalian carnivores that display alloparenting. We also provide a comprehensive dataset to explore additional aspects of trait evolution but which would greatly benefit from studies on behavioral ecology across cetaceans and increased focus on data deficient species.

Historical Mitogenomic Diversity and Population Structuring of Southern Hemisphere Fin Whales.

Fin whales Balaenoptera physalus were hunted unsustainably across the globe in the 19th and 20th centuries, leading to vast reductions in population size. Whaling catch records indicate the importance of the Southern Ocean for this species; approximately 730,000 fin whales were harvested during the 20th century in the Southern Hemisphere (SH) alone, 94% of which were at high latitudes. Genetic samples from contemporary whales can provide a window to past population size changes, but the challenges of sampling in remote Antarctic waters limit the availability of data. Here, we take advantage of historical samples in the form of bones and baleen available from ex-whaling stations and museums to assess the pre-whaling diversity of this once abundant species. We sequenced 27 historical mitogenomes and 50 historical mitochondrial control region sequences of fin whales to gain insight into the population structure and genetic diversity of Southern Hemisphere fin whales (SHFWs) before and after the whaling. Our data, both independently and when combined with mitogenomes from the literature, suggest SHFWs are highly diverse and may represent a single panmictic population that is genetically differentiated from Northern Hemisphere populations. These are the first historic mitogenomes available for SHFWs, providing a unique time series of genetic data for this species.

Paternity assignment and demographic closure in the New Zealand southern right whale.

The identification and characterization of reproductively isolated subpopulations or 'stocks' are essential for effective conservation and management decisions. This can be difficult in vagile marine species like marine mammals. We used paternity assignment and 'gametic recapture' to examine the reproductive autonomy of southern right whales (Eubalaena australis) on their New Zealand (NZ) calving grounds. We derived DNA profiles for 34 mother-calf pairs from skin biopsy samples, using sex-specific markers, 13 microsatellite loci and mtDNA haplotypes. We constructed DNA profiles for 314 adult males, representing 30% of the census male abundance of the NZ stock, previously estimated from genotypic mark-recapture modelling to be 1085 (95% CL 855, 1416). Under the hypothesis of demographic closure and the assumption of equal reproductive success among males, we predict: (i) the proportion of paternities assigned will reflect the proportion of the male population sampled and (ii) the gametic mark-recapture (GMR) estimate of male abundance will be equivalent to the census male estimate for the NZ stock. Consistent with these predictions, we found that the proportion of assigned paternities equalled the proportion of the census male population size sampled. Using the sample of males as the initial capture, and paternity assignment as the recapture, the GMR estimate of male abundance was 1001 (95% CL 542, 1469), similar to the male census estimate. These findings suggest that right whales returning to the NZ calving ground are reproductively autonomous on a generational timescale, as well as isolated by maternal fidelity on an evolutionary timescale, from others in the Indo-Pacific region.

Diet variation in a critically endangered marine predator revealed with stable isotope analysis.

Understanding the foraging ecology of animals gives insights into their trophic relationships and habitat use. We used stable isotope analysis to understand the foraging ecology of a critically endangered marine predator, the Maui dolphin. We analysed carbon and nitrogen isotope ratios of skin samples (n = 101) collected from 1993 to 2021 to investigate temporal changes in diet and niche space. Genetic monitoring associated each sample with a DNA profile which allowed us to assess individual and population level changes in diet. Potential prey and trophic level indicator samples were also collected (n = 166; 15 species) and incorporated in Bayesian mixing models to estimate importance of prey types to Maui dolphin diet. We found isotopic niche space had decreased over time, particularly since the 2008 implementation of a Marine Mammal Sanctuary. We observed a decreasing trend in ∂13C and ∂15N values, but this was not linear and several fluctuations in isotope values occurred over time. The largest variation in isotope values occurred during an El Niño event, suggesting that prey is influenced by climate-driven oceanographic variables. Mixing models indicated relative importance of prey remained constant since 2008. The isotopic variability observed here is not consistent with individual specialization, rather it occurs at the population level.

Genetic and particle modelling approaches to assessing population connectivity in a deep sea lobster.

The emergence of high resolution population genetic techniques, such as genotyping-by-sequencing (GBS), in combination with recent advances in particle modelling of larval dispersal in marine organisms, can deliver powerful new insights to support fisheries conservation and management. In this study, we used this combination to investigate the population connectivity of a commercial deep sea lobster species, the New Zealand scampi, Metanephrops challengeri, which ranges across a vast area of seafloor around New Zealand. This species has limited dispersal capabilities, including larvae with weak swimming abilities and short pelagic duration, while the reptant juvenile/adult stages of the lifecycle are obligate burrow dwellers with limited home ranges. Ninety-one individuals, collected from five scampi fishery management areas around New Zealand, were genotyped using GBS. Using 983 haplotypic genomic loci, three genetically distinct groups were identified: eastern, southern and western. These groups showed significant genetic differentiation with clear source-sink dynamics. The direction of gene flow inferred from the genomic data largely reflected the hydrodynamic particle modelling of ocean current flow around New Zealand. The modelled dispersal during pelagic larval phase highlights the strong connectivity among eastern sampling locations and explains the low genetic differentiation detected among these sampled areas. Our results highlight the value of using a transdisciplinary approach in the inference of connectivity among populations for informing conservation and fishery management.

Marine mammals and microplastics: A systematic review and call for standardisation.

Microplastics receive significant societal and scientific attention due to increasing concerns about their impact on the environment and human health. Marine mammals are considered indicators for marine ecosystem health and many species are of conservation concern due to a multitude of anthropogenic stressors. Marine mammals may be vulnerable to microplastic exposure from the environment, via direct ingestion from sea water, and indirect uptake from their prey. Here we present the first systematic review of literature on microplastics and marine mammals, composing of 30 studies in total. The majority of studies examined the gastrointestinal tracts of beached, bycaught or hunted cetaceans and pinnipeds, and found that microplastics were present in all but one study, and the abundance varied between 0 and 88 particles per animal. Additionally, microplastics in pinniped scats (faeces) were detected in eight out of ten studies, with incidences ranging from 0% of animals to 100%. Our review highlights considerable methodological and reporting deficiencies and differences among papers, making comparisons and extrapolation across studies difficult. We suggest best practices to avoid these issues in future studies. In addition to empirical studies that quantified microplastics in animals and scat, ten studies out of 30 (all focussing on cetaceans) tried to estimate the risk of exposure using two main approaches; i) overlaying microplastic in the environment (water or prey) with cetacean habitat or ii) proposing biological or chemical biomarkers of exposure. We discuss advice and best practices on research into the exposure and impact of microplastics in marine mammals. This work on marine ecosystem health indicator species will provide valuable and comparable information in the future.

Southern right whale vocalizations on foraging grounds in South Georgia.

Southern right whale vocalizations were recorded concurrently with visual observations off the sub-Antarctic Island of South Georgia, and the characteristics of these calls were described. Calls were also compared to those of humpback whales at South Georgia, to determine how the two species might reliably be distinguished acoustically. The southern right whale calls measured (which were all upcalls) had lower frequency with peak energy and were mostly shorter in duration than the calls measured from humpback whales. The frequency upsweep and the lack of harmonics of southern right whale calls were also diagnostic characteristics.

Satellite derived offshore migratory movements of southern right whales (Eubalaena australis) from Australian and New Zealand wintering grounds.

Southern right whales (Eubalaena australis) migrate between Austral-winter calving and socialising grounds to offshore mid- to high latitude Austral-summer feeding grounds. In Australasia, winter calving grounds used by southern right whales extend from Western Australia across southern Australia to the New Zealand sub-Antarctic Islands. During the Austral-summer these whales are thought to migrate away from coastal waters to feed, but the location of these feeding grounds is only inferred from historical whaling data. We present new information on the satellite derived offshore migratory movements of six southern right whales from Australasian wintering grounds. Two whales were tagged at the Auckland Islands, New Zealand, and the remaining four at Australian wintering grounds, one at Pirates Bay, Tasmania, and three at Head of Bight, South Australia. The six whales were tracked for an average of 78.5 days (range: 29 to 150) with average individual distance of 38 km per day (range: 20 to 61 km). The length of individually derived tracks ranged from 645-6,381 km. Three likely foraging grounds were identified: south-west Western Australia, the Subtropical Front, and Antarctic waters, with the Subtropical Front appearing to be a feeding ground for both New Zealand and Australian southern right whales. In contrast, the individual tagged in Tasmania, from a sub-population that is not showing evidence of post-whaling recovery, displayed a distinct movement pattern to much higher latitude waters, potentially reflecting a different foraging strategy. Variable population growth rates between wintering grounds in Australasia could reflect fidelity to different quality feeding grounds. Unlike some species of baleen whale populations that show movement along migratory corridors, the new satellite tracking data presented here indicate variability in the migratory pathways taken by southern right whales from Australia and New Zealand, as well as differences in potential Austral summer foraging grounds.

Correction: Satellite derived offshore migratory movements of southern right whales (Eubalaena australis) from Australian and New Zealand wintering grounds.

[This corrects the article DOI: 10.1371/journal.pone.0231577.].