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.

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.

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.

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.

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].

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.

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.

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.

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.

Calling under pressure: short-finned pilot whales make social calls during deep foraging dives.

Toothed whales rely on sound to echolocate prey and communicate with conspecifics, but little is known about how extreme pressure affects pneumatic sound production in deep-diving species with a limited air supply. The short-finned pilot whale (Globicephala macrorhynchus) is a highly social species among the deep-diving toothed whales, in which individuals socialize at the surface but leave their social group in pursuit of prey at depths of up to 1000 m. To investigate if these animals communicate acoustically at depth and test whether hydrostatic pressure affects communication signals, acoustic DTAGs logging sound, depth and orientation were attached to 12 pilot whales. Tagged whales produced tonal calls during deep foraging dives at depths of up to 800 m. Mean call output and duration decreased with depth despite the increased distance to conspecifics at the surface. This shows that the energy content of calls is lower at depths where lungs are collapsed and where the air volume available for sound generation is limited by ambient pressure. Frequency content was unaffected, providing a possible cue for group or species identification of diving whales. Social calls may be important to maintain social ties for foraging animals, but may be impacted adversely by vessel noise.

Static inflation and deflation pressure-volume curves from excised lungs of marine mammals.

Excised lungs from eight marine mammal species [harp seal (Pagophilus groenlandicus), harbor seal (Phoca vitulina), gray seal (Halichoerus grypush), Atlantic white-sided dolphin (Lagenorhynchus acutus), common dolphin (Delphinus delphis), Risso's dolphin (Grampus griseus), long-finned pilot whale (Globicephala melas) and harbor porpoise (Phocoena phocoena)] were used to determine the minimum air volume of the relaxed lung (MAV, N=15), the elastic properties (pressure-volume curves, N=24) of the respiratory system and the total lung capacity (TLC). Our data indicate that mass-specific TLC (sTLC, l kg(-1)) does not differ between species or groups (odontocete vs phocid) and agree with that estimated (TLC(est)) from body mass (M(b)) by applying the equation: TLC(est)=0.135 M(b)(0.92). Measured MAV was on average 7% of TLC, with a range from 0 to 16%. The pressure-volume curves were similar among species on inflation but diverged during deflation in phocids in comparison with odontocetes. These differences provide a structural basis for observed species differences in the depth at which lungs collapse and gas exchange ceases.

Auditory evoked potentials in two short-finned pilot whales (Globicephala macrorhynchus).

The hearing sensitivities of two short-finned pilot whales (Globicephala macrorhynchus) were investigated by measuring auditory evoked potentials generated in response to clicks and sinusoidal amplitude modulated (SAM) tones. The first whale tested, an adult female, was a long-time resident at SeaWorld San Diego with a known health history. Click-evoked responses in this animal were similar to those measured in other echolocating odontocetes. Auditory thresholds were comparable to dolphins of similar age determined with similar evoked potential methods. The region of best sensitivity was near 40 kHz and the upper limit of functional hearing was between 80 and 100 kHz. The second whale tested, a juvenile male, was recently stranded and deemed non-releasable. Click-evoked potentials were not detected in this animal and testing with SAM tones suggested severe hearing loss above 10 kHz.

Comparison of echolocation clicks from geographically sympatric killer whales and long-finned pilot whales (L).

The source characteristics of biosonar signals from sympatric killer whales and long-finned pilot whales in a Norwegian fjord were compared. A total of 137 pilot whale and more than 2000 killer whale echolocation clicks were recorded using a linear four-hydrophone array. Of these, 20 pilot whale clicks and 28 killer whale clicks were categorized as being recorded on-axis. The clicks of pilot whales had a mean apparent source level of 196 dB re 1 µPa pp and those of killer whales 203 dB re 1 µPa pp. The duration of pilot whale clicks was significantly shorter (23 µs, S.E.=1.3) and the centroid frequency significantly higher (55 kHz, S.E.=2.1) than killer whale clicks (duration: 41 µs, S.E.=2.6; centroid frequency: 32 kHz, S.E.=1.5). The rate of increase in the accumulated energy as a function of time also differed between clicks from the two species. The differences in duration, frequency, and energy distribution may have a potential to allow for the distinction between pilot and killer whale clicks when using automated detection routines for acoustic monitoring.

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.

Audiogram of a formerly stranded long-finned pilot whale (Globicephala melas) measured using auditory evoked potentials.

Long-finned pilot whales are highly social odontocetes found in temperate and subpolar regions. This species is particularly known for its interaction with fisheries as well as its mass strandings. Recent tagging work has provided some information about pilot whales in the wild but, even though they have been successfully kept in captivity, little is known about their sensory capabilities. This study investigates the hearing abilities of a rehabilitated 2 year old male long-finned pilot whale. A complete audiogram was collected using auditory evoked potential techniques that included measurements of nine frequencies from 4 to 100 kHz presented as sinusoidally amplitude-modulated tones. The results indicated that the region of best hearing was between 11.2 and 50 kHz and the subject had relatively poor high frequency hearing compared with other odontocete species. This study emphasizes the importance of collecting basic hearing measurements from new species, understanding diagnostic life histories as well as continuously increasing the sample size of audiometry measurements within and between odontocete species as animals become available.

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.

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.

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.

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.