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.

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.

Australian long-finned pilot whales (Globicephala melas) emit stereotypical, variable, biphonic, multi-component, and sequenced vocalisations, similar to those recorded in the northern hemisphere.

While in the northern hemisphere, many studies have been conducted on the vocal repertoire of long-finned pilot whales (Globicephala melas), no such study has been conducted in the southern hemisphere. Presented here, is the first study on the vocalisations of long-finned pilot whales along the southern coast of mainland Australia. Multiple measures were taken of 2028 vocalisations recorded over five years in several locations. These vocalisations included tonal sounds with and without overtones, sounds of burst-pulse character, graded sounds, biphonations, and calls of multiple components. Vocalisations were further categorised based on spectrographic features into 18 contour classes. Altogether, vocalisations ranged from approximately 200 Hz to 25 kHz in fundamental frequency and from 0.03 s to 2.07 s in duration. These measures compared well with those from northern hemisphere pilot whales. Some call types were almost identical to northern hemisphere vocalisations, even though the geographic ranges of the two populations are far apart. Other call types were unique to Australia. Striking similarities with calls of short-finned pilot whales (Globicephala macrorhynchus) and sometimes sympatric killer whales (Orcinus orca) were also found. Theories for call convergence and divergence are discussed.

Propensity for Risk in Reproductive Strategy Affects Susceptibility to Anthropogenic Disturbance.

AbstractAnimals initiate, interrupt, or invest resources in reproduction in light of their physiology and the environment. The energetic risks entailed in an individual's reproductive strategy can influence the ability to cope with additional stressors, such as anthropogenic climate change and disturbance. To explore the trade-offs between internal state, external resource availability, and reproduction, we applied state-dependent life-history theory (SDLHT) to a dynamic energy budget (DEB) model for long-finned pilot whales (Globicephala melas). We investigated the reproductive strategies emerging from the interplay between fitness maximization and propensity to take energetic risks, as well as the resulting susceptibility of individual vital rates to disturbance. Without disturbance, facultative reproductive behavior from SDLHT and fixed rules in the DEB model led to comparable individual fitness. However, under disturbance, the reproductive strategies emerging from SDLHT increased vulnerability to energetic risks, resulting in lower fitness than fixed rules. These fragile strategies might therefore be unlikely to evolve in the first place. Heterogeneous resource availability favored more cautious (and thus more robust) strategies, particularly when knowledge of resource variation was accurate. Our results demonstrate that the assumptions regarding the dynamic trade-offs underlying an individual's decision-making can have important consequences for predicting the effects of anthropogenic stressors on wildlife populations.

Ecophysiological traits of highly mobile large marine predators inferred from nucleic acid derived indices.

Nucleic acid-derived indices such as RNA/DNA ratios have been successfully applied as ecophysiological indicators to assess growth, nutritional condition and health status in marine organisms given that they provide a measure of tissue protein reserves, which is known to vary depending on changes in the environment. Yet, the use of these biochemical indices on highly mobile large predators is scarce. In this study, we tested the applicability of using nucleic acids to provide insights on the ecophysiological traits of two marine mammal species (common bottlenose dolphins and short-finned pilot whales) and explored potential related factors (species, sex, season, and residency pattern), using skin tissue (obtained from biopsy darts) of apparently healthy and adult free-ranging animals. Significantly higher RNA/DNA ratios were obtained for bottlenose dolphins (p < 0.001), and for visitor pilot whales when compared with resident pilot whales (p = 0.001). No significant changes were found between the sexes. Based on the percentile approach, the samples contain individuals in a general good condition (as the 10th percentile is not closer to the mean than the 75th percentile), suggesting that the studied region of Macaronesia may be considered an adequate habitat. The combination of this effective tool with genetic sexing and photographic-identification provided an overall picture of ecosystem health, and although with some limitations and still being a first approach, it has the applicability to be used in other top predators and ecosystems.

Deep-diving pilot whales make cheap, but powerful, echolocation clicks with 50 µL of air.

Echolocating toothed whales produce powerful clicks pneumatically to detect prey in the deep sea where this long-range sensory channel makes them formidable top predators. However, air supplies for sound production compress with depth following Boyle's law suggesting that deep-diving whales must use very small air volumes per echolocation click to facilitate continuous sensory flow in foraging dives. Here we test this hypothesis by analysing click-induced acoustic resonances in the nasal air sacs, recorded by biologging tags. Using 27000 clicks from 102 dives of 23 tagged pilot whales (Globicephala macrorhynchus), we show that click production requires only 50 µL of air/click at 500 m depth increasing gradually to 100 µL at 1000 m. With such small air volumes, the metabolic cost of sound production is on the order of 40 J per dive which is a negligible fraction of the field metabolic rate. Nonetheless, whales must make frequent pauses in echolocation to recycle air between nasal sacs. Thus, frugal use of air and periodic recycling of very limited air volumes enable pilot whales, and likely other toothed whales, to echolocate cheaply and almost continuously throughout foraging dives, providing them with a strong sensory advantage in diverse aquatic habitats.

Topography of vibration frequency responses on the bony tympano-periotic complex of the pilot whale Globicephala macrorhynchus.

In modern Cetacea, the ear bone complex comprises the tympanic and periotic bones forming the tympano-periotic complex (TPC), differing from temporal bone complexes of other mammals in form, construction, position, and possibly function. To elucidate its functioning in sound transmission, we studied the vibration response of 32 pairs of formaldehyde-glutaraldehyde-fixed TPCs of Globicephala macrorhynchus, the short-finned pilot whale (legally obtained in Taiji, Japan). A piezoelectric-crystal-based vibrator was surgically attached to a location on the cochlea near the exit of the acoustic nerve. The crystal delivered vibrational pulses through continuous sweeps from 5 to 50 kHz. The vibration response was measured as a function of frequency by Laser Doppler Vibrometry at five points on the TPC. The aim of the experiment was to clarify how the vibration amplitudes produced by different frequencies are distributed on the TPC. At the lowest frequencies (<12 kHz), no clear differential pattern emerged. At higher frequencies the anterolateral lip of the TP responded most sensitively with the highest displacement amplitudes, and response amplitudes decreased in orderly fashion towards the posterior part of the TPC. We propose that this works as a lever: high-frequency sounds are most sensitively received and cause the largest vibration amplitudes at the anterior part of the TP, driving movements with lower amplitude but greater force near the posteriorly located contact to the ossicular chain, which transmits the movements into the inner ear. Although force (pressure) amplification is not needed for impedance matching in water, it may be useful for driving the stiffly connected ossicles at the high frequencies used in echolocation.

Stomach contents of long-finned pilot whales, Globicephala melas mass-stranded in Tasmania.

New data are reported from analyses of stomach contents from 114 long-finned pilot whales mass-stranded at four locations around Tasmania, Australia from 1992-2006. Identifiable prey remains were recovered from 84 (74%) individuals, with 30 (26%) individuals (17 females and 13 males) having empty stomachs. Prey remains comprised 966 identifiable lower beaks and 1244 upper beaks, belonging to 17 families (26 species) of cephalopods. Ommastrephidae spp. were the most important cephalopod prey accounting for 16.9% by number and 45.6% by reconstructed mass. Lycoteuthis lorigera was the next most important, followed by Ancistrocheirus lesueurii. Multivariate statistics identified significant differences in diet among the four stranding locations. Long-finned pilot whales foraging off Southern Australia appear to be targeting a diverse assemblage of prey (≥10 species dominated by cephalopods). This is compared to other similar studies from New Zealand and some locations in the Northern Hemisphere, where the diet has been reported to be primarily restricted to ≤3 species dominated by cephalopods. This study emphasises the importance of cephalopods as primary prey for Southern long-finned pilot whales and other marine vertebrates, and has increased our understanding of long-finned pilot whale diet in Southern Ocean waters.

Hepatic phase I and II biotransformation responses and contaminant exposure in long-finned pilot whales from the Northeastern Atlantic.

Faroe Island pilot whales have been documented to have high body burdens of organohalogen contaminants (OHCs), including polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs), but low burdens of their respective hydroxylated metabolites (OH-PCBs and OH-PBDEs). The present study investigated the hepatic expression and/or catalytic activities of phase I and II biotransformation enzymes in relation to hepatic concentrations of target OHCs, including OH-PCBs and OH-PBDEs, in long-finned pilot whales (Globicephala melas) from the Northeastern Atlantic. CYP1A, 2B, 2E and 3A protein expressions were identified in juveniles and adult males, but not in adult females. Ethoxyresorufin-O-deethylase (EROD) activity was significantly lower in adult females than in juveniles and adult males. Using multivariate analyses to investigate relationships between biological responses and OHC concentrations, a positive relationship was identified between EROD and OHCs. The activity levels of phase II conjugating enzymes (uridine 5'-diphospho-glucuronosyltransferase [UDPGT], and glutathione S-transferase [GST]) were low. The analyses of mRNA expression did not show correlative relationships with OHC concentrations, but cyp1a and ahr transcripts were positively correlated with EROD activity. We suggest that the low concentrations of OH-PCBs and OH-PBDEs reported in pilot whales is probably due to the identified low phase I biotransformation activities in the species.

Acoustic properties of a short-finned pilot whale head with insight into temperature influence on tissues' sound velocity.

Acoustic properties of odontocete head tissues, including sound velocity, density, and acoustic impedance, are important parameters to understand dynamics of its echolocation. In this paper, acoustic properties of head tissues from a freshly dead short-finned pilot whale (Globicephala macrorhynchus) were reconstructed using computed tomography (CT) and ultrasound. The animal's forehead soft tissues were cut into 188 ordered samples. Sound velocity, density, and acoustic impedance of each sample were either directly measured or calculated by formula, and Hounsfield Unit values (HUs) were obtained from CT scanning. According to relationships between HUs and sound velocity, HUs and density, as well as HUs and acoustic impedance, distributions of acoustic properties in the head were reconstructed. The inner core in the melon with low-sound velocity and low-density is an evidence for its potential function of sound focusing. The increase in acoustic impedance of forehead tissues from inner core to outer layer may be important for the acoustic impedance matching between the outer layer tissue and seawater. In addition, temperature dependence of sound velocity in soft tissues was also examined. The results provide a guide to the simulation of the sound emission of the short-finned pilot whale.

High diving metabolic rate indicated by high-speed transit to depth in negatively buoyant long-finned pilot whales.

To maximize foraging duration at depth, diving mammals are expected to use the lowest cost optimal speed during descent and ascent transit and to minimize the cost of transport by achieving neutral buoyancy. Here, we outfitted 18 deep-diving long-finned pilot whales with multi-sensor data loggers and found indications that their diving strategy is associated with higher costs than those of other deep-diving toothed whales. Theoretical models predict that optimal speed is proportional to (basal metabolic rate/drag)1/3 and therefore to body mass0.05 The transit speed of tagged animals (2.7±0.3 m s-1) was substantially higher than the optimal speed predicted from body mass (1.4-1.7 m s-1). According to the theoretical models, this choice of high transit speed, given a similar drag coefficient (median, 0.0035) to that in other cetaceans, indicated greater basal metabolic costs during diving than for other cetaceans. This could explain the comparatively short duration (8.9±1.5 min) of their deep dives (maximum depth, 444±85 m). Hydrodynamic gliding models indicated negative buoyancy of tissue body density (1038.8±1.6 kg m-3, ±95% credible interval, CI) and similar diving gas volume (34.6±0.6 ml kg-1, ±95% CI) to those in other deep-diving toothed whales. High diving metabolic rate and costly negative buoyancy imply a 'spend more, gain more' strategy of long-finned pilot whales, differing from that in other deep-diving toothed whales, which limits the costs of locomotion during foraging. We also found that net buoyancy affected the optimal speed: high transit speeds gradually decreased during ascent as the whales approached neutral buoyancy owing to gas expansion.

Conservation Status of Long-Finned Pilot Whales, Globicephala melas, in the Mediterranean Sea.

Mediterranean Sea long-finned pilot whales (Globicephala melas) are currently classified as Data Deficient on the International Union for the Conservation of Nature (IUCN) Red List. Multiple lines of evidence, including molecular genetic and photo-identification mark-recapture analyses, indicate that the Strait of Gibraltar population (distributed from 5.8°W longitude to west of Djibouti Bank and Alborán Dorsal in the Alborán Sea) is differentiated from the Mediterranean Sea population (east of Djibouti Bank and the Alborán Dorsal up to the Ligurian Sea). There is low genetic diversity within the Mediterranean population, and recent gene flow with the Strait of Gibraltar population is restricted. Current total abundance estimates are lacking for the species in the Mediterranean. Pilot whales in the Alborán Sea region were negatively affected by a morbillivirus epizootic from 2006 to 2007, and recovery may be difficult. The Strait of Gibraltar population, currently estimated to be fewer than 250 individuals, decreased by 26.2% over 5 years after the morbillivirus epizootic. Population viability analyses predicted an 85% probability of extinction for this population over the next 100 years. Increasing maritime traffic, increased contaminant burdens, and occasional fisheries interactions may severely impair the capacity of the Strait of Gibraltar population to recover after the decline due to the pathogen.

Fatal Asphyxiation in Two Long-Finned Pilot Whales (Globicephala melas) Caused by Common Soles (Solea solea).

Long-finned pilot whales (Globicephala melas) are rare visitors to the southern North Sea, but recently two individual strandings occurred on the Dutch coast. Both animals shared the same, unusual cause of death: asphyxiation from a common sole (Solea solea) stuck in their nasal cavity. This is a rare cause of death in cetaceans. Whilst asphyxiation has been reported in smaller odontocetes, there are no recent records of this occurring in Globicephala species. Here we report the stranding, necropsy and diet study results as well as discuss the unusual nature of this phenomenon. Flatfish are not a primary prey species for pilot whales and are rarely eaten by other cetaceans, such as harbour porpoises (Phocoena phocoena), in which there are several reports of asphyxiation due to airway obstruction by soles. This risk may be due to the fish's flexible bodies which can enter small cavities either actively in an attempt to escape or passively due to the whale 'coughing' or 'sneezing' to rid itself of the blockage of the trachea. It is also possible that the fish enter the airways whilst the whale is re-articulating the larynx after trying to ingest large, oddly shaped prey. It is unlikely that the soles entered the airways after the death of the whales and we believe therefore that they are responsible for the death of these animals.

Characterizing a Foraging Hotspot for Short-Finned Pilot Whales and Blainville's Beaked Whales Located off the West Side of Hawai'i Island by Using Tagging and Oceanographic Data.

Satellite tagging data for short-finned pilot whales (Globicephala macrorhynchus) and Blainville's beaked whales (Mesoplodon densirostris) were used to identify core insular foraging regions off the Kona (west) Coast of Hawai'i Island. Ship-based active acoustic surveys and oceanographic model output were used in generalized additive models (GAMs) and mixed models to characterize the oceanography of these regions and to examine relationships between whale density and the environment. The regions of highest density for pilot whales and Blainville's beaked whales were located between the 1000 and 2500 m isobaths and the 250 and 2000 m isobaths, respectively. Both species were associated with slope waters, but given the topography of the area, the horizontal distribution of beaked whales was narrower and located in shallower waters than that of pilot whales. The key oceanographic parameters characterizing the foraging regions were bathymetry, temperature at depth, and a high density of midwater micronekton scattering at 70 kHz in 400-650 m depths that likely represent the island-associated deep mesopelagic boundary community and serve as prey for the prey of the whales. Thus, our results suggest that off the Kona Coast, and potentially around other main Hawaiian Islands, the deep mesopelagic boundary community is key to a food web that supports insular cetacean populations.

How effectively do horizontal and vertical response strategies of long-finned pilot whales reduce sound exposure from naval sonar?

The behaviour of a marine mammal near a noise source can modulate the sound exposure it receives. We demonstrate that two long-finned pilot whales both surfaced in synchrony with consecutive arrivals of multiple sonar pulses. We then assess the effect of surfacing and other behavioural response strategies on the received cumulative sound exposure levels and maximum sound pressure levels (SPLs) by modelling realistic spatiotemporal interactions of a pilot whale with an approaching source. Under the propagation conditions of our model, some response strategies observed in the wild were effective in reducing received levels (e.g. movement perpendicular to the source's line of approach), but others were not (e.g. switching from deep to shallow diving; synchronous surfacing after maximum SPLs). Our study exemplifies how simulations of source-whale interactions guided by detailed observational data can improve our understanding about motivations behind behaviour responses observed in the wild (e.g., reducing sound exposure, prey movement).

Classification of large acoustic datasets using machine learning and crowdsourcing: application to whale calls.

Vocal communication is a primary communication method of killer and pilot whales, and is used for transmitting a broad range of messages and information for short and long distance. The large variation in call types of these species makes it challenging to categorize them. In this study, sounds recorded by audio sensors carried by ten killer whales and eight pilot whales close to the coasts of Norway, Iceland, and the Bahamas were analyzed using computer methods and citizen scientists as part of the Whale FM project. Results show that the computer analysis automatically separated the killer whales into Icelandic and Norwegian whales, and the pilot whales were separated into Norwegian long-finned and Bahamas short-finned pilot whales, showing that at least some whales from these two locations have different acoustic repertoires that can be sensed by the computer analysis. The citizen science analysis was also able to separate the whales to locations by their sounds, but the separation was somewhat less accurate compared to the computer method.

Predicting cetacean habitats from their energetic needs and the distribution of their prey in two contrasted tropical regions.

To date, most habitat models of cetaceans have relied on static and oceanographic covariates, and very few have related cetaceans directly to the distribution of their prey, as a result of the limited availability of prey data. By simulating the distribution of six functional micronekton groups between the surface and ≃1,000 m deep, the SEAPODYM model provides valuable insights into prey distributions. We used SEAPODYM outputs to investigate the habitat of three cetacean guilds with increasing energy requirements: sperm and beaked whales, Globicephalinae and Delphininae. We expected High Energy Requirements cetaceans to preferentially forage in habitats of high prey biomass and/or production, where they might easily meet their high energetic needs, and Low Energy Requirements cetaceans to forage in habitats of either high or low prey biomass and/or production. Cetacean sightings were collected from dedicated aerial surveys in the South West Indian Ocean (SWIO) and French Polynesia (FP). We examined cetacean densities in relation to simulated distributions of their potential prey using Generalised Additive Models and predicted their habitats in both regions. Results supported their known diving abilities, with Delphininae mostly related to prey present in the upper layers of the water column, and Globicephalinae and sperm and beaked whales also related to prey present in deeper layers. Explained deviances ranged from 9% for sperm and beaked whales in the SWIO to 47% for Globicephalinae in FP. Delphininae and Globicephalinae appeared to select areas where high prey biomass and/or production were available at shallow depths. In contrast, sperm and beaked whales showed less clear habitat selection. Using simulated prey distributions as predictors in cetacean habitat models is crucial to understand their strategies of habitat selection in the three dimensions of the ocean.

Combining whistle acoustic parameters to discriminate Mediterranean odontocetes during passive acoustic monitoring.

Acoustic observation can complement visual observation to more effectively monitor occurrence and distribution of marine mammals. For effective acoustic censuses, calibration methods must be determined by joint visual and acoustic studies. Research is still needed in the field of acoustic species identification, particularly for smaller odontocetes. From 1994 to 2012, whistles of four odontocete species were recorded in different areas of the Mediterranean Sea to determine how reliably these vocalizations can be classified to species. Recordings were attributed to species by simultaneous visual observation. The results of this study highlight that the frequency parameters, which are linked to physical features of animals, show lower variability than modulation parameters, which are likely to be more dependent on complex eco-ethological contexts. For all the studied species, minimum and maximum frequencies were linearly correlated with body size. DFA and Classification Tree Analysis (CART) show that these parameters were the most important for classifying species; however, both statistical methods highlighted the need for combining them with the number of contour minima and contour maxima for correct classification. Generally, DFA and CART results reflected both phylogenetic distance (especially for common and striped dolphins) and the size of the species.

Hearing threshold measurements of five stranded short-finned pilot whales (Globicephala macrorhynchus).

On May 5, 2011, 23 short-finned pilot whales, Globicephala macrorhynchus, were stranded along the coastline near Cudjoe Key, FL. Five animals (two adult females, two juvenile females, and an adult male) were transported to a rehabilitation facility in Key Largo, FL. Auditory evoked potentials (AEPs) were recorded in response to amplitude modulated tone pips modulated at 1000 Hz. AEP thresholds were determined at 10, 20, 40, 80, and 120 kHz for the four females. However, the adult male was euthanized prior to testing. Short-finned pilot whales had peak sensitivity at lower frequencies than other odontocetes such as bottlenose dolphins. Greatest sensitivity was around 40 kHz for all whales, while thresholds for the two adult females were 25-61 dB higher at 80 kHz than the juveniles. Click evoked potentials were similar between the four whales and comparable to other echolocating odontocetes. Click evoked potential data from a fifth short-finned pilot whale that had stranded in Curacao showed no response. These findings add to the limited database of pilot whale (short- and long-finned) hearing studies, of which there are only two others [Schlundt et al. (2011). J. Acoust. Soc. Am. 129, 1111-1116 and Pacini et al. (2010). J. Exp. Biol. 213, 3138-3143].

Body contact and synchronous diving in long-finned pilot whales.

Synchronous behavior, as a form of social interaction, has been widely reported for odontocete cetaceans observed at the sea surface. However, few studies have quantified synchronous behavior underwater. Using data from an animal-borne data recorder and camera, we described how a pair of deep-diving odontocetes, long-finned pilot whales, coordinated diving behavior. Diving data during overlapping periods of 3.7 h were obtained from two whales within a stable trio. The tagged whales made highly synchronous movements, and their dive durations differed only slightly (3±3 s). The pair of whales maintained a constant and narrow vertical separation (ca. 3 m) throughout synchronous dives. The overall fluking rate for the same travel speed during synchronous dives was virtually the same as that during asynchronous dives, suggesting that synchronous behavior did not affect locomotion effort. In addition, a possible affiliative behavior was recorded by the animal-borne camera: another individual appeared in 8% of the frames, both with and without body contact to the tagged whale. The primary type of body contact was flipper-to-body. Our study, the first on underwater synchronous behavior and body contact of pilot whales, highlights the utility of using animal-borne devices for enabling new insights into social interactions.