Communication in Cook Inlet beluga whales: Describing the vocal repertoire and masking of calls by commercial ship noise.

Many species rely on acoustic communication to coordinate activities and communicate to conspecifics. Cataloging vocal behavior is a first step towards understanding how individuals communicate information and how communication may be degraded by anthropogenic noise. The Cook Inlet beluga population is endangered with an estimated 331 individuals. Anthropogenic noise is considered a threat for this population and can negatively impact communication. To characterize this population's vocal behavior, vocalizations were measured and classified into three categories: whistles (n = 1264, 77%), pulsed calls (n = 354, 22%), and combined calls (n = 15, 1%), resulting in 41 call types. Two quantitative analyses were conducted to compare with the manual classification. A classification and regression tree and Random Forest had a 95% and 85% agreement with the manual classification, respectively. The most common call types per category were then used to investigate masking by commercial ship noise. Results indicate that these call types were partially masked by distant ship noise and completely masked by close ship noise in the frequency range of 0-12 kHz. Understanding vocal behavior and the effects of masking in Cook Inlet belugas provides important information supporting the management of this endangered population.

Oceanographic barriers, divergence, and admixture: Phylogeography and taxonomy of two putative subspecies of short-finned pilot whale.

Genomic phylogeography plays an important role in describing evolutionary processes and their geographic, ecological, or cultural drivers. These drivers are often poorly understood in marine environments, which have fewer obvious barriers to mixing than terrestrial environments. Taxonomic uncertainty of some taxa (e.g., cetaceans), due to the difficulty in obtaining morphological data, can hamper our understanding of these processes. One such taxon, the short-finned pilot whale, is recognized as a single global species but includes at least two distinct morphological forms described from stranding and drive hunting in Japan, the "Naisa" and "Shiho" forms. Using samples (n = 735) collected throughout their global range, we examine phylogeographic patterns of divergence by comparing mitogenomes and nuclear SNP loci. Our results suggest three types within the species: an Atlantic Ocean type, a western/central Pacific and Indian Ocean (Naisa) type, and an eastern Pacific Ocean and northern Japan (Shiho) type. mtDNA control region differentiation indicates these three types form two subspecies, separated by the East Pacific Barrier: Shiho short-finned pilot whale, in the eastern Pacific Ocean and northern Japan, and Naisa short-finned pilot whale, throughout the remainder of the species' distribution. Our data further indicate two diverging populations within the Naisa subspecies, in the Atlantic Ocean and western/central Pacific and Indian Oceans, separated by the Benguela Barrier off South Africa. This study reveals a process of divergence and speciation within a globally-distributed, mobile marine predator, and indicates the importance of the East Pacific Barrier to this evolutionary process.

Familial social structure and socially driven genetic differentiation in Hawaiian short-finned pilot whales.

Social structure can have a significant impact on divergence and evolution within species, especially in the marine environment, which has few environmental boundaries to dispersal. On the other hand, genetic structure can affect social structure in many species, through an individual preference towards associating with relatives. One social species, the short-finned pilot whale (Globicephala macrorhynchus), has been shown to live in stable social groups for periods of at least a decade. Using mitochondrial control sequences from 242 individuals and single nucleotide polymorphisms from 106 individuals, we examine population structure among geographic and social groups of short-finned pilot whales in the Hawaiian Islands, and test for links between social and genetic structure. Our results show that there are at least two geographic populations in the Hawaiian Islands: a Main Hawaiian Islands (MHI) population and a Northwestern Hawaiian Islands/Pelagic population (FST and ΦST p < .001), as well as an eastern MHI community and a western MHI community (FST p = .009). We find genetically driven social structure, or high relatedness among social units and clusters (p < .001), and a positive relationship between relatedness and association between individuals (p < .0001). Further, socially organized clusters are genetically distinct, indicating that social structure drives genetic divergence within the population, likely through restricted mate selection (FST p = .05). This genetic divergence among social groups can make the species less resilient to anthropogenic or ecological disturbance. Conservation of this species therefore depends on understanding links among social structure, genetic structure and ecological variability within the species.

Acoustic differentiation of Shiho- and Naisa-type short-finned pilot whales in the Pacific Ocean.

Divergence in acoustic signals used by different populations of marine mammals can be caused by a variety of environmental, hereditary, or social factors, and can indicate isolation between those populations. Two types of genetically and morphologically distinct short-finned pilot whales, called the Naisa- and Shiho-types when first described off Japan, have been identified in the Pacific Ocean. Acoustic differentiation between these types would support their designation as sub-species or species, and improve the understanding of their distribution in areas where genetic samples are difficult to obtain. Calls from two regions representing the two types were analyzed using 24 recordings from Hawai'i (Naisa-type) and 12 recordings from the eastern Pacific Ocean (Shiho-type). Calls from the two types were significantly differentiated in median start frequency, frequency range, and duration, and were significantly differentiated in the cumulative distribution of start frequency, frequency range, and duration. Gaussian mixture models were used to classify calls from the two different regions with 74% accuracy, which was significantly greater than chance. The results of these analyses indicate that the two types are acoustically distinct, which supports the hypothesis that the two types may be separate sub-species.

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.

Spatial and seasonal foraging patterns drive diet differences among north Pacific resident killer whale populations.

Highly social top marine predators, including many cetaceans, exhibit culturally learned ecological behaviours such as diet preference and foraging strategy that can affect their resilience to competition or anthropogenic impacts. When these species are also endangered, conservation efforts require management strategies based on a comprehensive understanding of the variability in these behaviours. In the northeast Pacific Ocean, three partially sympatric populations of resident killer whales occupy coastal ecosystems from California to Alaska. One population (southern resident killer whales) is endangered, while another (southern Alaska resident killer whales) has exhibited positive abundance trends for the last several decades. Using 185 faecal samples collected from both populations between 2011 and 2021, we compare variability in diet preference to provide insight into differences in foraging patterns that may be linked with the relative success and decline of these populations. We find broad similarities in the diet of the two populations, with differences arising from spatiotemporal and social variability in resource use patterns, especially in the timing of shifts between target prey species. The results described here highlight the importance of comprehensive longitudinal monitoring of foraging ecology to inform management strategies for endangered, highly social top marine predators.

Skin microbiome of beluga whales: spatial, temporal, and health-related dynamics.

BACKGROUND: Host-specific microbiomes play an important role in individual health and ecology; in marine mammals, epidermal microbiomes may be a protective barrier between the host and its aqueous environment. Understanding these epidermal-associated microbial communities, and their ecological- or health-driven variability, is the first step toward developing health indices for rapid assessment of individual or population health. In Cook Inlet, Alaska, an endangered population of beluga whales (Delphinapterus leucas) numbers fewer than 300 animals and continues to decline, despite more than a decade of conservation effort. Characterizing the epidermal microbiome of this species could provide insight into the ecology and health of this endangered population and allow the development of minimally invasive health indicators based on tissue samples. RESULTS: We sequenced the hypervariable IV region of bacterial and archaeal SSU rRNA genes from epidermal tissue samples collected from endangered Cook Inlet beluga whales (n = 33) and the nearest neighboring population in Bristol Bay (n = 39) between 2012 and 2018. We examined the sequences using amplicon sequence variant (ASV)-based analyses, and no ASVs were associated with all individuals, indicating a greater degree of epidermal microbiome variability among beluga whales than in previously studied cetacean species and suggesting the absence of a species-specific core microbiome. Epidermal microbiome composition differed significantly between populations and across sampling years. Comparing the microbiomes of Bristol Bay individuals of known health status revealed 11 ASVs associated with potential pathogens that differed in abundance between healthy individuals and those with skin lesions or dermatitis. Molting and non-molting individuals also differed significantly in microbial diversity and the abundance of potential pathogen-associated ASVs, indicating the importance of molting in maintaining skin health. CONCLUSIONS: We provide novel insights into the dynamics of Alaskan beluga whale epidermal microbial communities. A core epidermal microbiome was not identified across all animals. We characterize microbial dynamics related to population, sampling year and health state including level of skin molting. The results of this study provide a basis for future work to understand the role of the skin microbiome in beluga whale health and to develop health indices for management of the endangered Cook Inlet beluga whales, and cetaceans more broadly.

Marine mammal skin microbiotas are influenced by host phylogeny.

Skin-associated microorganisms have been shown to play a role in immune function and disease of humans, but are understudied in marine mammals, a diverse animal group that serve as sentinels of ocean health. We examined the microbiota associated with 75 epidermal samples opportunistically collected from nine species within four marine mammal families, including: Balaenopteridae (sei and fin whales), Phocidae (harbour seal), Physeteridae (sperm whales) and Delphinidae (bottlenose dolphins, pantropical spotted dolphins, rough-toothed dolphins, short-finned pilot whales and melon-headed whales). The skin was sampled from free-ranging animals in Hawai'i (Pacific Ocean) and off the east coast of the United States (Atlantic Ocean), and the composition of the bacterial community was examined using the sequencing of partial small subunit (SSU) ribosomal RNA genes. Skin microbiotas were significantly different among host species and taxonomic families, and microbial community distance was positively correlated with mitochondrial-based host genetic divergence. The oceanic location could play a role in skin microbiota variation, but skin from species sampled in both locations is necessary to determine this influence. These data suggest that a phylosymbiotic relationship may exist between microbiota and their marine mammal hosts, potentially providing specific health and immune-related functions that contribute to the success of these animals in diverse ocean ecosystems.