Toxic arsenolipids bioaccumulate in the developing brain of pilot whales.

Arsenic-containing hydrocarbons (AsHC), a subclass of arsenolipids (AsL), have been proven to exert neuro- and cytotoxic effects in in-vitro and in-vivo studies and were shown to pass through biological barriers like the blood-brain barrier. However, there has been no connection as to the environmental relevance of these findings, meaning there is no study based on samples from free living animals that are exposed to these compounds. Here, we report the identification of two AsHC as well as 3 arsenosugar phospholipids (AsPL) in the brains of a pod of stranded long-finned pilot whales (Globicephala melas) as well as the absence of arsenobetaine (AsB) which is often found to be a dominant As species in fish. We show data which suggests that there is an age-dependent accumulation of AsL in the brains of the animals. The results show that, in contrast to other organs, total arsenic as well as arsenolipids accumulate in an asymptotic pattern in the brains of the animals. Total As concentrations were found to range from 87 to 260 µg As/kg wet weight and between 0.6 and 27.6 µg As/kg was present in the form of AsPL958 in the brains of stranded pilot whales which was the most dominant lipophilic species present. The asymptotic relationship between total As, as well as AsPL, concentration in the brain and whale age may suggest that the accumulation of these species takes place prior to the full development of the blood-brain barrier in young whales. Finally, comparison between the organs of local squid, a common source of food for pilot whales, highlighted a comparable AsL profile which indicates a likely bioaccumulation pathway through the food chain.

Investigating the effects of underwater noise from two vessels on the behaviour of short-finned pilot whales.

Multiple whale-watching vessels may operate around cetaceans at any one time, and targeted animals may experience underwater noise effects. We hypothesised that the cumulative noise of two vessels with low source levels (SLs) will elicit lower behavioural disturbance in short-finned pilot whales (Globicephala macrorhynchus) compared to a single vessel with a higher SL. We measured the behaviour of whales during 26 controls (stationary vessel >300 m) and 44 treatments off Tenerife (Canary Islands, Spain). Treatments consisted of vessel approaches mimicking whale-watch scenarios (distance ∼60 m, speed 1.5 kn). Approaches with two simultaneous vessels, with maximum cumulative mid and low-frequency (0.2-110 kHz) weighted source levels (SLsMF-LF) 137-143 dB, did not affect mother-calf pairs' resting, nursing, diving, respiration rate or inter-breath interval. However, a louder single vessel approach with twin petrol engines at SLsMF-LF 139-151 dB significantly decreased the proportion of time resting for the mother. The results suggest that if a single or two vessels are present, if the cumulative SL is < 143 dB, the behavioural disturbance on the whales will be negligible. By examining noise effects from multiple vessels on the behaviour of pilot whales, the importance of incorporating a noise threshold into whale-watching guidelines was emphasised.

Phthalate contamination in marine mammals off the Norwegian coast.

Phthalates are used in plastics, found throughout the marine environment and have the potential to cause adverse health effects. In the present study, we quantified blubber concentrations of 11 phthalates in 16 samples from stranded and/or free-living marine mammals from the Norwegian coast: the killer whale (Orcinus orca), sperm whale (Physeter macrocephalus), long-finned pilot whale (Globicephala melas), white-beaked dolphin (Lagenorhynchus albirostris), harbour porpoise (Phocoena phocoena), and harbour seal (Phoca vitulina). Five compounds were detected across all samples: benzyl butyl phthalate (BBP; in 50 % of samples), bis(2-ethylhexyl) phthalate (DEHP; 33 %), diisononyl phthalate (DiNP; 33 %), diisobutyl phthalate (DiBP; 19 %), and dioctyl phthalate (DOP; 13 %). Overall, the most contaminated individual was the white-beaked dolphin, whilst the lowest concentrations were measured in the killer whale, sperm whale and long-finned pilot whale. We found no phthalates in the neonate killer whale. The present study is important for future monitoring and management of these toxic compounds.

POPs in long-finned pilot whales mass stranded in Iceland as a proxy for their physiological condition.

Long-finned pilot whales (Globicephala melas) are the most frequently stranded cetaceans in the world; however, the predominant drivers of these events are poorly understood. In this study the levels of persistent organic pollutants from pilot whales stranded in North-east Iceland were quantified and compared to historical data and physical parameters to investigate whether contaminant load may have influenced the physiological state of stranded individuals, how these loads fluctuate with sex and age group, and if this is consistent with the literature. Historical comparison was also carried out to discern how pollutant contamination has changed throughout the past few decades. DDE, transnonachlor and PCB-153 were the top three pollutants respectively. The accumulation of POPs was greater on average in immature individuals than adults, whilst among adults, males had higher concentration than females. Moreover, despite an indication of decreasing POP loads throughout the years, knowledge of harmful thresholds remains exceedingly limited.

Cetaceans playing with single-use plastics (SUPs): A widespread interaction with likely severe impacts.

Play is a common behaviour in wild cetaceans that includes the manipulation of natural, as well as artificial objects such as marine debris. Yet, very little is known about these interactions despite the potential impacts on cetacean health. We combined a detailed review of the scientific literature and social media with 12 years of observations to examine cetacean interactions with plastic litter. A total of 11 odontocete species (Tursiops truncatus, Stenella longirostris, Delphinus delphis, Grampus griseus, Steno bredanensis, Stenella frontalis, Sotalia guianensis, Pseudorca crassidens, Orcinus orca, Globicephala melas and Physeter macrocephalus) were documented in 59 events carrying or throwing plastic litter with their head and/or flippers suggesting a form of play. Interactions occurred in the Atlantic, Pacific, Indian Ocean, Mediterranean, and Red Sea, with single-use plastics composing the main typology registered. While these interactions appeared harmless to the observers, they can pose a significant risk through subsequent entanglement or ingestion.

Carbon, nitrogen, and oxygen stable isotope ratios of striped dolphins and short-finned pilot whales stranded in Hokkaido, northern Japan, compared with those of other cetaceans stranded and hunted in Japan.

Strandings of striped dolphins (SD) and short-finned pilot whales (PW) in Hokkaido, northern Japan, are rare but have recently increased, probably due to global warming. We quantified δ13C, δ15N, and δ18O in muscles of SD (n = 7) and PW (n = 3) stranded in Hokkaido and compared these values with those in muscles (red meat products) of hunted SD and PW in three areas of central and southern Japan. δ18O in stranded SD, except for the calf, decreased with increasing body length (BL), whereas δ13C increased, with no BL-related changes in δ15N. The variability of δ18O (range of maximum and minimum) was larger in the stranded SD (7.5 ‰) than of the hunted SD in three areas (0.9, 1.9, and 1.4 ‰), whereas that of δ15N was smaller in the stranded SD than in the hunted SD. Similarly, the variability of δ18O was larger in the stranded PW in Hokkaido (3.3 ‰) than in the hunted PW in central Japan (1.4 ‰). The larger variability of δ18O and smaller variability of δ15N in stranded SD imply long-term sojourning in coastal waters and feeding on small amounts of limited prey species at low trophic levels before death.

The first full-congener analysis of 209 polychlorinated biphenyls (PCBs) in the blubber of short-finned pilot whales (Globicephala macrorhynchus) stranded along the coast of Savu Island, Indonesia.

Short-finned pilot whales (SFPW) are a group of cetaceans found globally in tropical and temperate seas and are commonly stranded in the group, but the reason behind their stranding is still unknown. No detailed information on the contamination status and bioaccumulation of halogenated organic compounds, including polychlorinated biphenyls (PCBs), in the SFPW from Indonesian waters has been reported. Therefore, we analyzed all 209 PCB congeners in the blubber of 20 SFPW specimens stranded along the coast of Savu Island, East Nusa Tenggara, Indonesia, in October 2012 to explain the status of contamination, congener profiles, potential risk of PCBs to cetaceans, and the determination of unintentionally produced PCBs (u-PCBs) in the blubber of SFPW. Concentrations of Σ209PCBs, Σ7in-PCBs, Σ12dl-PCBs, and Σ21u-PCBs were between 48 and 490 (mean:240 ± 140), 22-230 (110 ± 60), 2.6-38 (17 ± 10), and 1.0-13 (6.3 ± 3.7) ng g-1 lipid weight (lw), respectively. Congener-specific profiles of PCBs among sex and estimated age groups were observed; relatively high proportions of tri-to penta-CBs in juveniles and highly chlorinated recalcitrant congeners in structure-activity groups (SAGs) in sub-adult females were noted. The estimated toxic equivalency (TEQs) value for dl-PCBs ranged from 2.2 to 60 TEQWHO pg/g lw, with juveniles containing high TEQ values than sub-adults and adults. Although the TEQs and concentrations of PCBs in SFPW stranded along Indonesian coasts were lower than those reported for similar whale species from other North Pacific regions, further research is needed to assess the long-term impact of halogenated organic pollutants on their survival and health.

Study of the long-finned pilot whale (Globicephala melas) bile content - An indicator of ocean health.

Globicephala melas has been harvested in the Faroe Islands for centuries. Given the distances travelled by this species, tissue/body fluid samples represent unique matrices to be considered as an integration of environmental condition and pollution status of their prey. For the first time, bile samples were analysed for presence of polycyclic aromatic hydrocarbon (PAH) metabolites and protein content. Concentrations of 2- and 3-ring PAH metabolites ranged from 11 to 25 µg mL-1 pyrene fluorescence equivalents. In total, 658 proteins were identified and 61,5 % were common amongst all individuals. Identified proteins were integrated into in silico software and determined that the top predicted disease and functions were neurological diseases, inflammation, and immunological disorders. The metabolism of reactive oxygen species (ROS) was predicted to be dysregulated, which can have consequences to both the protection against ROS produced during dives and contaminant exposures. The obtained data is valuable for understanding metabolism and physiology of G. melas.

A genome and single-nucleus cerebral cortex transcriptome atlas of the short-finned pilot whale Globicephala macrorhynchus.

Cetaceans (dolphins, whales, and porpoises) have large and anatomically sophisticated brains. To expand our understanding of the cellular makeup of cetacean brains and the similarities and divergence between the brains of cetaceans and terrestrial mammals, we report a short-finned pilot whale (Globicephala macrorhynchus) single-nucleus transcriptome atlas. To achieve this goal, we assembled a chromosome-scale reference genome spanning 2.25 Gb on 22 chromosomes and profiled the gene expression of five major anatomical cortical regions of the short-finned pilot whale by single-nucleus RNA-sequencing (snRNA-seq). We identified six major cell lineages in the cerebral cortex (excitatory neurons, inhibitory neurons, oligodendrocytes, oligodendrocyte precursor cells, astrocytes, and endothelial cells), eight molecularly distinct subclusters of excitatory neurons, and four subclusters of inhibitory neurons. Finally, a comparison of snRNA-seq data from the short-finned pilot whale, human, and rhesus macaque revealed a broadly conserved cellular makeup of brain cell types. Our study provides genomic resources and molecular insights into cetacean brain evolution.

Short-Finned Pilot Whale Strandings Associated with Pilot Whale Morbillivirus, Brazil.

Cetacean morbillivirus (CeMV) causes illness and death in cetaceans worldwide; the CeMV strains circulating in the Southern Hemisphere are poorly known. We detected a pilot whale CeMV strain in 3 short-finned pilot whales (Globicephala macrorhynchus) stranded in Brazil during July-October 2020. Our results confirm this virus circulates in this species.

A novel expert-driven methodology to develop thermal response curves and project habitat thermal suitability for cetaceans under a changing climate.

Over the last decades, global warming has contributed to changes in marine species composition, abundance and distribution, in response to changes in oceanographic conditions such as temperature, acidification, and deoxygenation. Experimentally derived thermal limits, which are known to be related to observed latitudinal ranges, have been used to assess variations in species distribution patterns. However, such experiments cannot be undertaken on free-swimming large marine predators with wide-range distribution, like cetaceans. An alternative approach is to elicit expert's knowledge to derive species' thermal suitability and assess their thermal responses, something that has never been tested in these taxa. We developed and applied a methodology based on expert-derived thermal suitability curves and projected future responses for several species under different climate scenarios. We tested this approach with ten cetacean species currently present in the biogeographic area of Macaronesia (North Atlantic) under Representative Concentration Pathways 2.6, 4.5 and 8.5, until 2050. Overall, increases in annual thermal suitability were found for Balaenoptera edeni, Globicephala macrorhynchus, Mesoplodon densirostris, Physeter macrocephalus, Stenella frontalis, Tursiops truncatus and Ziphius cavirostris. Conversely, our results indicated a decline in thermal suitability for B. physalus, Delphinus delphis, and Grampus griseus. Our study reveals potential responses in cetaceans' thermal suitability, and potentially in other highly mobile and large predators, and it tests this method's applicability, which is a novel application for this purpose and group of species. It aims to be a cost-efficient tool to support conservation managers and practitioners.

Exploring lipid affinities of persistent organic pollutants and MeO-PBDEs in blubber of marine mammals.

Although lipophilic compounds have been the focus of numerous studies in marine mammals, their association with lipids is widely accepted, but rarely scrutinized. This pilot study aimed to investigate potential relationships between individual lipids from different lipid classes identified through a non-targeted Nuclear Magnetic Resonance (NMR) based lipidomics approach and legacy POPs in the blubber of long-finned pilot whales, sperm whales, common bottlenose dolphins, and Indo-Pacific bottlenose dolphins. Concentrations of selected POPs such as HCB and HCHs in sperm whales from Tasmania were found to differ from those in long-finned pilot whales and common bottlenose dolphins from the same location. Profiles of NMR spectra measured in blubber of sperm whales were also distinctly different compared to the pilot whales and common bottlenose dolphins. Two groups of Indo-Pacific bottlenose dolphins from South Australia that were 20 years apart showed highly comparable profiles of NMR signals despite having higher concentrations of several POP classes in the more recent group. More specific correlations were investigated between selected POPs (n = 12) and all detected NMR signals (n = 63) in all species. Outcomes were species-specific, but difficult to interpret due to the lack of available literature for marine mammals and the small sample sizes per species. Because of the key role of lipids in the bioaccumulation of POPs and in the incidence of diseases, more attention should be given to the identification and characterization of lipid species in future toxicological studies. However, future studies should focus on one marine mammal species to increase sample sizes and limit the number of confounding factors, such as diet, that can influence POP and lipid levels and profiles.

A field study of chemical senses in bottlenose dolphins and pilot whales.

For most marine vertebrates, chemical cues provide crucial information during navigation and foraging, but their use by cetaceans is still poorly understood. In contrast to baleen whales, toothed whales (odontocetes) are scarcely equipped for chemoreception: they lack the conventional anatomical structures (i.e., olfactory epithelium, nerves and bulbs) involved in olfaction and have reduced taste buds on the tongue. Several behavioral studies have however shown that captive dolphins can perceive chemical solutions, including odorants, in their oral cavity. To investigate whether odontocetes could use infochemicals in their foraging ecology, we implemented a behavioral response experiment in wild bottlenose dolphins and long-finned pilot whales. We tested dimethyl sulfide (DMS) as a potentially attractive stimulus since it is a chemical signature of highly productive marine areas, known to attract several marine predators including fishes and seabirds. We assessed cetacean responses to DMS exposure by analyzing their movements and surface behaviors recorded by onboard observers. In both species, results did not reveal any significant attraction or behavioral reaction toward DMS when compared to a control chemical stimulus, apart from a short-distance response in bottlenose dolphins. These results suggest that while odontocetes may perceive DMS in water, it apparently does not play a significant role in their foraging ecology. Testing potentially more attractive compounds such as prey extracts with the present method and analyzing surface, underwater and acoustic responses would provide further insights on odontocete feeding behavior. It would also provide valuable clues to studies on the anatomical structures involved in their chemosenses.

Decreased resting and nursing in short-finned pilot whales when exposed to louder petrol engine noise of a hybrid whale-watch vessel.

Vessel noise is a primary driver of behavioural disturbance in cetaceans, which are targeted during whale-watch activities. Despite the growing, global effort for implementing best-practice principles, to date, there are no regulations on whale-watch vessel noise levels. Here, we test the hypothesis that a whale-watch vessel with a low noise emission will not elicit short-term behavioural responses in toothed whales compared to a vessel with a louder engine. We measured behavioural responses (n = 36) of short-finned pilot whales (Globicephala macrorhynchus) to whale-watch vessel approaches (range 60 m, speed 1.5 kn). Treatment approaches with a quieter electric engine (136-140 dB) compared to the same vessel with a louder petrol engine (151-139 dB) (low-frequency-mid-frequency weighted source levels, re 1 µPa RMS @ 1 m) were examined. Focal whales were resting mother and calves in small group sizes. During petrol engine treatments, the mother's mean resting time decreased by 29% compared to the control (GLM, p = 0.009). The mean proportion of time nursing for the calf was significantly influenced by petrol engine vessel passes, with a 81% decrease compared to the control (GLM, p = 0.01). There were no significant effects on behaviour from the quieter electric engine. Thus, to minimise disturbance on the activity budget of pilot whales, whale-watch vessels would ideally have source levels as low as possible, below 150 dB re 1 µPa RMS @ 1 m and perceived above ambient noise.

Numerical-modeling-based investigation of sound transmission and reception in the short-finned pilot whale (Globicephala macrorhynchus).

The sound-transmission, beam-formation, and sound-reception processes of a short-finned pilot whale (Globicephala macrorhynchus) were investigated using computed tomography (CT) scanning and numerical simulation. The results showed that sound propagations in the forehead were modulated by the upper jaw, air components, and soft tissues, which attributed to the beam formation in the external acoustic field. These structures owned different acoustic impedance and formed a multiphasic sound transmission system that can modulate sounds into a beam. The reception pathways composed of the solid mandible and acoustic fats in the lower head conducted sounds into the tympano-periotic complex. In the simulations, sounds were emitted in the forehead transmission system and propagated into water to interrogate a steel cylinder. The resulting echoes can be interpreted from multiple perspectives, including amplitude, waveform, and spectrum, to obtain the acoustic cues of the steel cylinder. By taking the short-finned pilot whale as an example, this study provides meaningful information to further deepen our understanding of biosonar system operations, and may expand sound-reception theory in odontocetes.

Climate change vulnerability of cetaceans in Macaronesia: Insights from a trait-based assessment.

Over the last decades global warming has caused an increase in ocean temperature, acidification and oxygen loss which has led to changes in nutrient cycling and primary production affecting marine species at multiple trophic levels. While knowledge about the impacts of climate change in cetacean's species is still scarce, practitioners and policymakers need information about the species at risk to guide the implementation of conservation measures. To assess cetacean's vulnerability to climate change in the biogeographic region of Macaronesia, we adapted the Marine Mammal Climate Vulnerability Assessment (MMCVA) method and applied it to 21 species management units using an expert elicitation approach. Results showed that over half (62%) of the units assessed presented Very High (5 units) or High (8 units) vulnerability scores. Very High vulnerability scores were found in archipelago associated units of short-finned pilot whales (Globicephala macrorhynchus) and common bottlenose dolphins (Tursiops truncatus), namely in the Canary Islands and Madeira, as well as Risso's dolphins (Grampus griseus) in the Canary Islands. Overall, certainty scores ranged from Very High to Moderate for 67% of units. Over 50% of units showed a high potential for distribution, abundance and phenology changes as a response to climate change. With this study we target current and future information needs of conservation managers in the region, and guide research and monitoring efforts, while contributing to the improvement and validation of trait-based vulnerability approaches under a changing climate.

Density dependence can obscure nonlethal effects of disturbance on life history of medium-sized cetaceans.

Nonlethal disturbance of animals can cause behavioral and physiological changes that affect individual health status and vital rates, with potential consequences at the population level. Predicting these population effects remains a major challenge in ecology and conservation. Monitoring fitness-related traits may improve detection of upcoming population changes, but the extent to which individual traits are reliable indicators of disturbance exposure is not well understood, especially for populations regulated by density dependence. Here we study how density dependence affects a population's response to disturbance and modifies the disturbance effects on individual health and vital rates. We extend an energy budget model for a medium-sized cetacean (the long-finned pilot whale Globicephala melas) to an individual-based population model in which whales feed on a self-replenishing prey base and disturbance leads to cessation of feeding. In this coupled predator-prey system, the whale population is regulated through prey depletion and the onset of yearly repeating disturbances on the whale population at carrying capacity decreased population density and increased prey availability due to reduced top-down control. In populations faced with multiple days of continuous disturbance each year, female whales that were lactating their first calf experienced increased mortality due to depletion of energy stores. However, increased prey availability led to compensatory effects and resulted in a subsequent improvement of mean female body condition, mean age at first reproduction and higher age-specific reproductive output. These results indicate that prey-mediated density dependence can mask negative effects of disturbance on fitness-related traits and vital rates, a result with implications for the monitoring and management of marine mammal populations.

Topographic Variations in Mobilization of Blubber in Relation to Changes in Body Mass in Short-Finned Pilot Whales (Globicephala macrorhynchus).

AbstractFat-level measurements used to indicate individual body condition and fitness are useful only when taken at a region along the body where fat responds to variations in caloric intake. Investigations to identify appropriate species-specific regions are limited, especially for cetaceans that have a specialized fat (blubber) that serves as an energy reserve and provides insulation. Over 18 mo, body mass of six pilot whales varied (range: 50-172 kg), and although caloric intake increased when water temperatures were lower, generally the best-fitting state-space model for length-adjusted mass was based on a single factor, caloric intake. After correcting for body length (range: 330-447 cm), the slope for blubber thickness and "blubber ring" thickness (average blubber thickness along a girth) in relation to body mass was positive and had a P value of <0.10 at six of 16 blubber measurement sites and one of five girth measurement sites, respectively. The slope for body girth (a reflection of changes in underlying blubber thickness) in relation to body mass was positive and had a lower P value ([Formula: see text]) at three of five girth measurement sites. Results indicate that blubber from the anterior insertion of the pectoral fins to the posterior insertion of the dorsal fin is the most metabolically active region. This region includes the midflank site, a location where blubber thickness measurements have historically been taken to monitor cetacean body condition. Conversely, blubber in the peduncle region was comparatively inert. These findings must be considered when measuring blubber thickness and body width (i.e., photogrammetry) to monitor the condition of free-ranging cetaceans.

Circular DNA viruses identified in short-finned pilot whale and orca tissue samples.

Members of the Delphinidae family are widely distributed across the world's oceans. We used a viral metagenomic approach to identify viruses in orca (Orcinus orca) and short-finned pilot whale (Globicephala macrorhynchus) muscle, kidney, and liver samples from deceased animals. From orca tissue samples (muscle, kidney, and liver), we identified a novel polyomavirus (Polyomaviridae), three cressdnaviruses, and two genomoviruses (Genomoviridae). In the short-finned pilot whale we were able to identify one genomovirus in a kidney sample. The presence of unclassified cressdnavirus within two samples (muscle and kidney) of the same animal supports the possibility these viruses might be widespread within the animal. The orca polyomavirus identified here is the first of its species and is not closely related to the only other dolphin polyomavirus previously discovered. The identification and verification of these viruses expands the current knowledge of viruses that are associated with the Delphinidae family.

Echolocation click parameters of short-finned pilot whales (Globicephala macrorhynchus) in the wild.

Short-finned pilot whales (Globicephala macrorhynchus) are large, deep-diving predators with diverse foraging strategies, but little is known about their echolocation. To quantify the source properties of short-finned pilot whale clicks, we made 15 deployments off the coast of Tenerife of a deep-water hydrophone array consisting of seven autonomous time-synced hydrophone recorders (SoundTraps), enabling acoustic localization and quantification of click source parameters. Of 8185 recorded pilot whale clicks, 47 were classified as being recorded on-axis, with a mean peak-to-peak source level (SL) of 181 ± 7 dB re 1 µPa, a centroid frequency of 40 ± 4 kHz, and a duration of 57 ± 23 µs. A fit to a piston model yielded an estimated half-power (-3 dB) beam width of 13.7° [95% confidence interval (CI) 13.2°-14.5°] and a mean directivity index (DI) of 22.6 dB (95% CI 22.5-22.9 dB). These measured SLs and DIs are surprisingly low for a deep-diving toothed whale, suggesting we sampled the short-finned pilot whales in a context with little need for operating a long-range biosonar. The substantial spectral overlap with beaked whale clicks emitted in similar deep-water habitats implies that pilot whale clicks may constitute a common source of false detections in beaked whale passive acoustic monitoring efforts.