Heard off Heard: Acoustic detections of sperm whales (Physeter macrocephalus) and other cetaceans off Heard Island.

An underwater acoustic recorder was moored off Heard Island from September 2017 through March 2018 to listen for marine mammals. Analysis of data was initially conducted by visual inspection of long-term spectral averages to reveal sounds from sperm whales, Antarctic and pygmy blue whales, fin whales, minke whales, odontocete whistles, and noise from nearby ships. Automated detection of sperm whale clicks revealed they were seldom detected from September through January (n = 35 h) but were detected nearly every day of February and March (n = 684 h). Additional analysis of these detections revealed further diel and demographic patterns.

Cetaceans are the next frontier for vocal rhythm research.

While rhythm can facilitate and enhance many aspects of behavior, its evolutionary trajectory in vocal communication systems remains enigmatic. We can trace evolutionary processes by investigating rhythmic abilities in different species, but research to date has largely focused on songbirds and primates. We present evidence that cetaceans-whales, dolphins, and porpoises-are a missing piece of the puzzle for understanding why rhythm evolved in vocal communication systems. Cetaceans not only produce rhythmic vocalizations but also exhibit behaviors known or thought to play a role in the evolution of different features of rhythm. These behaviors include vocal learning abilities, advanced breathing control, sexually selected vocal displays, prolonged mother-infant bonds, and behavioral synchronization. The untapped comparative potential of cetaceans is further enhanced by high interspecific diversity, which generates natural ranges of vocal and social complexity for investigating various evolutionary hypotheses. We show that rhythm (particularly isochronous rhythm, when sounds are equally spaced in time) is prevalent in cetacean vocalizations but is used in different contexts by baleen and toothed whales. We also highlight key questions and research areas that will enhance understanding of vocal rhythms across taxa. By coupling an infraorder-level taxonomic assessment of vocal rhythm production with comparisons to other species, we illustrate how broadly comparative research can contribute to a more nuanced understanding of the prevalence, evolution, and possible functions of rhythm in animal communication.

Determination of water balance maintenance in Orcinus orca and Tursiops truncatus using oxygen isotopes.

The secondary adaptation of Cetacea to a fully marine lifestyle raises the question of their ability to maintain their water balance in a hyperosmotic environment. Cetacea have access to four potential sources of water: surrounding salt oceanic water, dietary free water, metabolic water and inhaled water vapour to a lesser degree. Here, we measured the 18O/16O oxygen isotope ratio of blood plasma from 13 specimens belonging to two species of Cetacea raised under human care (four killer whales Orcinus orca, nine common bottlenose dolphins Tursiops truncatus) to investigate and quantify the contribution of preformed water (dietary free water, surrounding salt oceanic water) and metabolic water to Cetacea body water using a box-modelling approach. The oxygen isotope composition of Cetacea blood plasma indicates that dietary free water and metabolic water contribute to more than 90% of the total water input in weight for cetaceans, with the remaining 10% consisting of inhaled water vapour and surrounding water accidentally ingested or absorbed through the skin. Moreover, the contribution of metabolic water appears to be more important in organisms with a more lipid-rich diet. Beyond these physiological and conservation biology implications, this study opens up questions that need to be addressed, such as the applicability of the oxygen isotope composition of cetacean body fluids and skeletal elements as an environmental proxy of the oxygen isotope composition of present and past marine waters.

Small reductions in cargo vessel speed substantially reduce noise impacts to marine mammals.

Global reductions in the underwater radiated noise levels from cargo vessels are needed to reduce increasing cumulative impacts to marine wildlife. We use a vessel exposure simulation model to examine how reducing vessel source levels through slowdowns and technological modifications can lessen impacts on marine mammals. We show that the area exposed to ship noise reduces markedly with moderate source-level reductions that can be readily achieved with small reductions in speed. Moreover, slowdowns reduce all impacts to marine mammals despite the longer time that a slower vessel takes to pass an animal. We conclude that cumulative noise impacts from the global fleet can be reduced immediately by slowdowns. This solution requires no modification to ships and is scalable from local speed reductions in sensitive areas to ocean basins. Speed reductions can be supplemented by routing vessels away from critical habitats and by technological modifications to reduce vessel noise.

Voices in the ocean.

Toothed whales evolved a third way of making sounds similar to that of land mammals and birds.

Toothed whales use distinct vocal registers for echolocation and communication.

Echolocating toothed whales (odontocetes) capture fast-moving prey in dark marine environments, which critically depends on their ability to generate powerful, ultrasonic clicks. How their supposedly air-driven sound source can produce biosonar clicks at depths of >1000 meters, while also producing rich vocal repertoires to mediate complex social communication, remains unknown. We show that odontocetes possess a sound production system based on air driven through nasal passages that is functionally analogous to laryngeal and syringeal sound production. Tissue vibration in different registers produces distinct echolocation and communication signals across all major odontocete clades, and thus provides a physiological basis for classifying their vocal repertoires. The vocal fry register is used by species from porpoises to sperm whales for generating powerful, highly air-efficient echolocation clicks.

Assessing data bias in visual surveys from a cetacean monitoring programme.

Long-term monitoring datasets are fundamental to understand physical and ecological responses to environmental changes, supporting management and conservation. The data should be reliable, with the sources of bias identified and quantified. CETUS Project is a cetacean monitoring programme in the Eastern North Atlantic, based on visual methods of data collection. This study aims to assess data quality and bias in the CETUS dataset, by 1) applying validation methods, through photographic confirmation of species identification; 2) creating data quality criteria to evaluate the observer's experience; and 3) assessing bias to the number of sightings collected and to the success in species identification. Through photographic validation, the species identification of 10 sightings was corrected and a new species was added to the CETUS dataset. The number of sightings collected was biased by external factors, mostly by sampling effort but also by weather conditions. Ultimately, results highlight the importance of identifying and quantifying data bias, while also yielding guidelines for data collection and processing, relevant for species monitoring programmes based on visual methods.

Retia mirabilia: Protecting the cetacean brain from locomotion-generated blood pressure pulses.

Cetaceans have massive vascular plexuses (retia mirabilia) whose function is unknown. All cerebral blood flow passes through these retia, and we hypothesize that they protect cetacean brains from locomotion-generated pulsatile blood pressures. We propose that cetaceans have evolved a pulse-transfer mechanism that minimizes pulsatility in cerebral arterial-to-venous pressure differentials without dampening the pressure pulses themselves. We tested this hypothesis using a computational model based on morphology from 11 species and found that the large arterial capacitance in the retia, coupled with the small extravascular capacitance in the cranium and vertebral canal, could protect the cerebral vasculature from 97% of systemic pulsatility. Evolution of the retial complex in cetaceans-likely linked to the development of dorsoventral fluking-offers a distinctive solution to adverse locomotion-generated vascular pulsatility.

A machine learning pipeline for classification of cetacean echolocation clicks in large underwater acoustic datasets.

Machine learning algorithms, including recent advances in deep learning, are promising for tools for detection and classification of broadband high frequency signals in passive acoustic recordings. However, these methods are generally data-hungry and progress has been limited by challenges related to the lack of labeled datasets adequate for training and testing. Large quantities of known and as yet unidentified broadband signal types mingle in marine recordings, with variability introduced by acoustic propagation, source depths and orientations, and interacting signals. Manual classification of these datasets is unmanageable without an in-depth knowledge of the acoustic context of each recording location. A signal classification pipeline is presented which combines unsupervised and supervised learning phases with opportunities for expert oversight to label signals of interest. The method is illustrated with a case study using unsupervised clustering to identify five toothed whale echolocation click types and two anthropogenic signal categories. These categories are used to train a deep network to classify detected signals in either averaged time bins or as individual detections, in two independent datasets. Bin-level classification achieved higher overall precision (>99%) than click-level classification. However, click-level classification had the advantage of providing a label for every signal, and achieved higher overall recall, with overall precision from 92 to 94%. The results suggest that unsupervised learning is a viable solution for efficiently generating the large, representative training sets needed for applications of deep learning in passive acoustics.

Early giant reveals faster evolution of large body size in ichthyosaurs than in cetaceans.

Body sizes of marine amniotes span six orders of magnitude, yet the factors that governed the evolution of this diversity are largely unknown. High primary production of modern oceans is considered a prerequisite for the emergence of cetacean giants, but that condition cannot explain gigantism in Triassic ichthyosaurs. We describe the new giant ichthyosaur Cymbospondylus youngorum sp. nov. with a 2-meter-long skull from the Middle Triassic Fossil Hill Fauna of Nevada, USA, underscoring rapid size evolution despite the absence of many modern primary producers. Surprisingly, the Fossil Hill Fauna rivaled the composition of modern marine mammal faunas in terms of size range, and energy-flux models suggest that Middle Triassic marine food webs were able to support several large-bodied ichthyosaurs at high trophic levels, shortly after ichthyosaur origins.

Assessment of animal management and habitat characteristics associated with social behavior in bottlenose dolphins across zoological facilities.

Bottlenose dolphins are a behaviorally complex, social species that display a variety of social behaviors. Because of this, it is important for zoological facilities to strive to ensure animals display species-appropriate levels of social behavior. The current study is part of the multi-institutional study entitled "Towards understanding the welfare of cetaceans in zoos and aquariums" commonly referred to as the Cetacean Welfare Study. All participating facilities were accredited by the Alliance of Marine Mammal Parks and Aquariums and/or the Association of Zoos and Aquariums. Behavioral data were collected on 47 bottlenose dolphins representing two subspecies, Tursiops truncatus and Tursiops aduncus, at 25 facilities. The social behaviors of group related activity (group active) as well as interacting with conspecifics (interact with conspecific) were examined for their relationships to both animal management factors and habitat characteristics. The behavioral state of group active and the rate of interact with conspecific were both positively related to the frequency of receiving new forms of environmental enrichment. Both were inversely related to the random scheduling of environmental enrichment. Additional results suggested interact with conspecific was inversely related with daytime spatial experience and that males displayed group active more than females. Overall, the results suggested that animal management techniques such as the type and timing of enrichment may be more important to enhance social behavior than habitat characteristics or the size of the habitat. Information gained from this study can help facilities with bottlenose dolphins manage their enrichment programs in relation to social behaviors.

Towards understanding the welfare of cetaceans in accredited zoos and aquariums.

Cetaceans are long-lived, social species that are valued as ambassadors inspiring the public to engage in conservation action. Under professional care, they are critical partners with the scientific community to understanding the biology, behavior, physiology, health, and welfare requirements of this taxonomic group. The Cetacean Welfare Study was a highly collaborative research effort among zoos and aquariums accredited by the Alliance for Marine Mammal Parks and Aquariums and/or the Association of Zoos & Aquariums that provided important empirical and comparative information on the care and management of cetaceans. The goal was to identify factors that were related to the welfare of bottlenose dolphins and to develop reference intervals and values for common and novel indicators of health and welfare for common bottlenose dolphins (Tursiops truncatus), Indo-Pacific bottlenose dolphins (Tursiops aduncus), beluga whales (Delphinapterus leucas), and Pacific white-sided dolphins (Lagenorhynchus obliquidens). Data were collected from cetaceans at 43 accredited zoos and aquariums in seven countries in 2018 and 2019. This overview presents a summary of findings from the initial research articles that resulted from the study titled "Towards understanding the welfare of cetaceans in zoos and aquariums." With multiple related objectives, animal-based metrics were used to advance frameworks of clinical care and target key conditions that were associated with good welfare of cetaceans in zoo and aquarium environments. As a result of this collaboration, species-specific reference intervals and values for blood variables and fecal hormone metabolites were developed and are freely available in an iOS application called ZooPhysioTrak. The results suggested that environmental enrichment programs and social management factors were more strongly related to behaviors likely indicative of positive welfare than habitat characteristics for common and Indo-Pacific bottlenose dolphins. These findings can be widely applied to optimize care and future science-based welfare practice.

The isotopic niche of Atlantic, biting marine mammals and its relationship to skull morphology and body size.

Understanding the trophic niches of marine apex predators is necessary to understand interactions between species and to achieve sustainable, ecosystem-based fisheries management. Here, we review the stable carbon and nitrogen isotope ratios for biting marine mammals inhabiting the Atlantic Ocean to test the hypothesis that the relative position of each species within the isospace is rather invariant and that common and predictable patterns of resource partitioning exists because of constrains imposed by body size and skull morphology. Furthermore, we analyze in detail two species-rich communities to test the hypotheses that marine mammals are gape limited and that trophic position increases with gape size. The isotopic niches of species were highly consistent across regions and the topology of the community within the isospace was well conserved across the Atlantic Ocean. Furthermore, pinnipeds exhibited a much lower diversity of isotopic niches than odontocetes. Results also revealed body size as a poor predictor of the isotopic niche, a modest role of skull morphology in determining it, no evidence of gape limitation and little overlap in the isotopic niche of sympatric species. The overall evidence suggests limited trophic flexibility for most species and low ecological redundancy, which should be considered for ecosystem-based fisheries management.

Scaling of heart rate with breathing frequency and body mass in cetaceans.

Plasticity in the cardiac function of a marine mammal facilitates rapid adjustments to the contrasting metabolic demands of breathing at the surface and diving during an extended apnea. By matching their heart rate (fH) to their immediate physiological needs, a marine mammal can improve its metabolic efficiency and maximize the proportion of time spent underwater. Respiratory sinus arrhythmia (RSA) is a known modulation of fH that is driven by respiration and has been suggested to increase cardiorespiratory efficiency. To investigate the presence of RSA in cetaceans and the relationship between fH, breathing rate (fR) and body mass (Mb), we measured simultaneous fH and fR in five cetacean species in human care. We found that a higher fR was associated with a higher mean instantaneous fH (ifH) and minimum ifH of the RSA. By contrast, fH scaled inversely with Mb such that larger animals had lower mean and minimum ifHs of the RSA. There was a significant allometric relationship between maximum ifH of the RSA and Mb, but not fR, which may indicate that this parameter is set by physical laws and not adjusted dynamically with physiological needs. RSA was significantly affected by fR and was greatly reduced with small increases in fR. Ultimately, these data show that surface fHs of cetaceans are complex and the fH patterns we observed are controlled by several factors. We suggest the importance of considering RSA when interpreting fH measurements and particularly how fR may drive fH changes that are important for efficient gas exchange. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

Social survival: Humpback whales (Megaptera novaeangliae) use social structure to partition ecological niches within proposed critical habitat.

Animal culture and social bonds are relevant to wildlife conservation because they influence patterns of geography, behavior, and strategies of survival. Numerous examples of socially-driven habitat partitioning and ecological-niche specialization can be found among vertebrates, including toothed whales. But such social-ecological dynamics, described here as 'social niche partitioning', are not known among baleen whales, whose societies-particularly on foraging grounds-are largely perceived as unstructured and incidental to matters of habitat use and conservation. However, through 16 years of behavioral observations and photo-identifications of humpback whales (Megaptera novaeangliae) feeding within a fjord system in the Canadian Pacific (primarily within Gitga'at First Nation waters), we have documented long-term pair bonds (up to 12 years) as well as a complex societal structure, which corresponds closely to persistent patterns in feeding strategy, long-term site fidelity (extended occupancy and annual rate of return up to 75%), specific geographic preferences within the fjord system, and other forms of habitat use. Randomization tests of network congruency and clustering algorithms were used to test for overlap in patterns of social structure and habitat use, which confirmed the occurrence of social niche partitioning on the feeding grounds of this baleen whale species. In addition, we document the extensive practice of group bubble net feeding in Pacific Canada. This coordinated feeding behavior was found to strongly mediate the social structure and habitat use within this humpback whale society. Additionally, during our 2004-2019 study, we observed a shift in social network structure in 2010-2012, which corresponded with environmental and demographic shifts including a sudden decline in the population's calving rate. Our findings indicate that the social lives of humpback whales, and perhaps baleen whales generally, are more complex than previously supposed and should be a primary consideration in the assessment of potential impacts to important habitat.

Shifting trends: Detecting changes in cetacean population dynamics in shifting habitat.

The ability to monitor population dynamics and detect major changes in population trend is essential for wildlife conservation and management. However, this is often challenging for cetaceans as surveys typically cover only a portion of a population's range and conventional stock assessment methods cannot then distinguish whether apparent changes in abundance reflect real changes in population size or shifts in distribution. We developed and tested methods for estimating population size and trend and detecting changes in population trend in the context of shifting habitat by integrating additional data into distance-sampling analysis. Previous research has shown that incorporating habitat information can improve population size estimates for highly mobile species with dynamic spatial distributions. Here, using simulated datasets representative of a large whale population, we demonstrate that incorporating individual mark-recapture data can increase the accuracy and precision of trend estimation and the power to distinguish whether apparent changes in abundance reflect changes in population trend or distribution shifts. We recommend that similar simulation studies are conducted for specific cetacean populations to assess the potential for detecting changes in population dynamics given available data. This approach is especially important wherever population change may be confounded with long-term change in distribution patterns associated with regime shifts or climate change.

Cetacean occurrence and diversity in whale-watching waters off Mirissa, Southern Sri Lanka.

Scientific information is vital to the conservation of cetaceans and the management of whale-watching activities. The southern coastal waters of Sri Lanka are near a narrow continental shelf and biologically abundant in cetacean species. Although the occurrence of cetaceans has been investigated in certain waters of Sri Lanka, few surveys have been conducted along the southern coast. To fill this gap, we conducted boat-based surveys from January to May 2017 to investigate the occurrence, diversity, and behavior of cetaceans in the waters off Mirissa, covering a survey area of 788.9 km2 . During 55 survey days, we recorded a total of 242 cetacean sightings and identified at least 9 species (3 mysticetes and 6 odontocetes). The blue whale was the most common mysticete species (167 of 174 mysticete encounters), followed by the Omura's whale (4 of 174) and Bryde's whale (3 of 174). The spinner dolphin was the most common odontocete species (28 of 68 odontocete encounters), followed by the sperm whale (18 of 68), common bottlenose dolphin (13 of 68), short-finned pilot whale (5 of 68), melon-headed whale (2 of 68), and killer whale. Blue whales and sperm whales exhibited a clear preference for outer shelf and high slope areas, and blue whales were observed feeding along these waters. The present study provides near-baseline information on cetacean occurrence and diversity in whale-watching waters off southern Sri Lanka, and highlights the urgent need for proper management strategies for whale-watching activities.

Sensing ecosystem dynamics via audio source separation: A case study of marine soundscapes off northeastern Taiwan.

Remote acquisition of information on ecosystem dynamics is essential for conservation management, especially for the deep ocean. Soundscape offers unique opportunities to study the behavior of soniferous marine animals and their interactions with various noise-generating activities at a fine temporal resolution. However, the retrieval of soundscape information remains challenging owing to limitations in audio analysis techniques that are effective in the face of highly variable interfering sources. This study investigated the application of a seafloor acoustic observatory as a long-term platform for observing marine ecosystem dynamics through audio source separation. A source separation model based on the assumption of source-specific periodicity was used to factorize time-frequency representations of long-duration underwater recordings. With minimal supervision, the model learned to discriminate source-specific spectral features and prove to be effective in the separation of sounds made by cetaceans, soniferous fish, and abiotic sources from the deep-water soundscapes off northeastern Taiwan. Results revealed phenological differences among the sound sources and identified diurnal and seasonal interactions between cetaceans and soniferous fish. The application of clustering to source separation results generated a database featuring the diversity of soundscapes and revealed a compositional shift in clusters of cetacean vocalizations and fish choruses during diurnal and seasonal cycles. The source separation model enables the transformation of single-channel audio into multiple channels encoding the dynamics of biophony, geophony, and anthropophony, which are essential for characterizing the community of soniferous animals, quality of acoustic habitat, and their interactions. Our results demonstrated the application of source separation could facilitate acoustic diversity assessment, which is a crucial task in soundscape-based ecosystem monitoring. Future implementation of soundscape information retrieval in long-term marine observation networks will lead to the use of soundscapes as a new tool for conservation management in an increasingly noisy ocean.

A natural endocast of an early Miocene odontocete and its implications in cetacean brain evolution.

The natural endocast Museo di Geologia e Paleontologia of the Università degli Studi di Torino (MGPT)-PU 13873 is described and analyzed in order to interpret its taxonomic affinities and its potential significance on our understanding of cetacean brain evolution. The endocast is from the early Miocene of Piedmont (between ca. 19 and 16 million years ago), Northwestern Italy, and shows a number of plesiomorphic characters. These include: scarcely rounded cerebral hemispheres, cerebellum exposed in dorsal view with little superimposition by the cerebral hemispheres, short temporal lobe, and long sylvian fissure. The distance between the hypophysis and the rostral pons is particularly high, as it was determined by the calculus of the hypothalamus quotient, suggesting that the development of a deep interpeduncular fossa was not as advanced as in living odontocetes. The encephalization quotient (EQ) of MGPT-PU 13873 is ~1.81; therefore, this specimen shows an EQ in line with other fossil whales of the same geological age (early Miocene). Comparative analysis shows that there is a critical lack of data from the late Miocene and Pliocene that prevents us to fully understand the recent evolution of the EQ diversity in whales. Moreover, the past diversity of brain size and shape in mysticetes is virtually unknown. All these observations point to the need of additional efforts to uncover evolutionary patterns and processes on cetacean brain evolution.