No distinct local cuisines among humpback whales: A population diet comparison in the Southern Hemisphere.

Southern hemisphere humpback whale (Megaptera novaeangliae, SHHW) breeding populations follow a high-fidelity Antarctic krill (Euphausia superba) diet while feeding in distinct sectors of the Southern Ocean. Their capital breeding life history requires predictable ecosystem productivity to fuel migration and migration-related behaviours. It is therefore postulated that populations feeding in areas subject to the strongest climate change impacts are more likely to show the first signs of a departure from a high-fidelity krill diet. We tested this hypothesis by investigating blubber fatty acid profiles and skin stable isotopes obtained from five SHHW populations in 2019, and comparing them to Antarctic krill stable isotopes sampled in three SHHW feeding areas in the Southern Ocean in 2019. Fatty acid profiles and δ13C and δ15N varied significantly among all five populations, however, calculated trophic positions did not (2.7 to 3.1). Similarly, fatty acid ratios, 16:1ω7c/16:0 and 20:5ω3/22:6ω3 were above 1, showing that whales from all five populations are secondary heterotrophs following an omnivorous diet with a diatom-origin. Thus, evidence for a potential departure from a high-fidelity Antarctic krill diet was not seen in any population. δ13C of all populations were similar to δ13C of krill sampled in productive upwelling areas or the marginal sea-ice zone. Consistency in trophic position and diet origin but significant fatty acid and stable isotope differences demonstrate that the observed variability arises at lower trophic levels. Our results indicate that, at present, there is no evidence of a divergence from a high-fidelity krill diet. Nevertheless, the characteristic isotopic signal of whales feeding in productive upwelling areas, or in the marginal sea-ice zone, implies that future cryosphere reductions could impact their feeding ecology.

Morphology of nares associated with stereo-olfaction in baleen whales.

The sensory mechanisms used by baleen whales (Mysticeti) for locating ephemeral, dense prey patches in vast marine habitats are poorly understood. Baleen whales have a functional olfactory system with paired rather than single blowholes (nares), potentially enabling stereo-olfaction. Dimethyl sulfide (DMS) is an odorous gas emitted by phytoplankton in response to grazing by zooplankton. Some seabirds use DMS to locate prey, but this ability has not been demonstrated in whales. For 14 extant species of baleen whale, nares morphometrics (imagery from unoccupied aerial systems, UAS) was related to published trophic level indices using Bayesian phylogenetic mixed modelling. A significant negative relationship was found between nares width and whale trophic level (ß = -0.08, lower 95% CI = -0.13, upper 95% CI = -0.03), corresponding with a 39% increase in nares width from highest to lowest trophic level. Thus, species with nasal morphology best suited to stereo-olfaction are more zooplanktivorous. These findings provide evidence that some baleen whale species may be able to localize odorants e.g. DMS. Our results help direct future behavioural trials of olfaction in baleen whales, by highlighting the most appropriate species to study. This is a research priority, given the potential for DMS-mediated plastic ingestion by whales.

Evaluating short- to medium-term effects of implantable satellite tags on southern right whales Eubalaena australis.

Improving our understanding of the effects of satellite tags on large whales is a critical step in ongoing tag development to minimise potential health effects whilst addressing important research questions that enhance conservation management policy. In 2014, satellite tags were deployed on 9 female southern right whales Eubalaena australis accompanied by a calf off Australia. Photo-identification resights (n = 48) of 4 photo-identified individuals were recorded 1 to 2894 d (1-8 yr) post-tagging. Short-term (<22 d) effects observed included localised and regional swelling, depression at the tag site, blubber extrusion, skin loss and pigmentation colour change. Broad swelling observable from lateral but not aerial imagery (~1.2 m diameter or ~9% of body length) and depression at the tag site persisted up to 1446 d post-tagging for 1 individual, indicating a persistent foreign-body response or infection. Two tagged individuals returned 4 yr post-tagging in 2018 with a calf, and the medium-term effects were evaluated by comparing body condition of tagged whales with non-tagged whales. These females calved in a typical 4 yr interval, suggesting no apparent immediate impact of tagging on reproduction for these individuals, but longer-term monitoring is needed. There was no observable difference in the body condition between the 2 tagged and non-tagged females. Ongoing monitoring post-tagging is required to build on the sample size and statistical power. We demonstrate the value of long-term monitoring programmes and a collaborative approach for evaluating effects from satellite-tagging cetaceans to support species management.

Growth in marine mammals: a review of growth patterns, composition and energy investment.

Growth of structural mass and energy reserves influences individual survival, reproductive success, population and species life history. Metrics of structural growth and energy storage of individuals are often used to assess population health and reproductive potential, which can inform conservation. However, the energetic costs of tissue deposition for structural growth and energy stores and their prioritization within bioenergetic budgets are poorly documented. This is particularly true across marine mammal species as resources are accumulated at sea, limiting the ability to measure energy allocation and prioritization. We reviewed the literature on marine mammal growth to summarize growth patterns, explore their tissue compositions, assess the energetic costs of depositing these tissues and explore the tradeoffs associated with growth. Generally, marine mammals exhibit logarithmic growth. This means that the energetic costs related to growth and tissue deposition are high for early postnatal animals, but small compared to the total energy budget as animals get older. Growth patterns can also change in response to resource availability, habitat and other energy demands, such that they can serve as an indicator of individual and population health. Composition of tissues remained consistent with respect to protein and water content across species; however, there was a high degree of variability in the lipid content of both muscle (0.1-74.3%) and blubber (0.4-97.9%) due to the use of lipids as energy storage. We found that relatively few well-studied species dominate the literature, leaving data gaps for entire taxa, such as beaked whales. The purpose of this review was to identify such gaps, to inform future research priorities and to improve our understanding of how marine mammals grow and the associated energetic costs.

Energy expenditure of southern right whales varies with body size, reproductive state and activity level.

Quantifying the energy expenditure of animals is critical to understanding the cost of anthropogenic disturbance relative to their overall energy requirements. We used novel drone focal follows (776 follows, 185 individuals) and aerial photogrammetry (5372 measurements, 791 individuals) to measure the respiration rate and body condition loss of southern right whales (Eubalaena australis) on a breeding ground in Australia. Respiration rates were converted to oxygen consumption rate and field metabolic rate (FMR) using published bioenergetic models. The intra-seasonal loss in body condition of different reproductive classes (calves, juveniles, adults, pregnant and lactating females) was converted to blubber energy loss and total energy expenditure (TEE). Using these two metrics, we tested the effects of body size, reproductive state and activity level on right whale energy expenditure. Respiration rates and mass-specific FMR decreased exponentially with an increase in body size, as expected based on allometric scaling. FMR increased curvilinearly with an increase in swim speed, probably as a result of increased drag and increased locomotion costs. Respiration rates and FMR were 44% higher for pregnant and lactating females compared with those of adults, suggesting significant costs of fetal maintenance and milk production, respectively. The estimated FMR of adults based on their respiration rates corresponded well with the estimated TEE based on body condition loss. The rate of decline in body condition of pregnant and lactating females was considerably higher than expected based on respiration rates, which probably reflects the milk energy transfer from mothers to calves, which is not reflected in their FMR.

Cheap gulp foraging of a giga-predator enables efficient exploitation of sparse prey.

The giant rorqual whales are believed to have a massive food turnover driven by a high-intake lunge feeding style aptly described as the world's largest biomechanical action. This high-drag feeding behavior is thought to limit dive times and constrain rorquals to target only the densest prey patches, making them vulnerable to disturbance and habitat change. Using biologging tags to estimate energy expenditure as a function of feeding rates on 23 humpback whales, we show that lunge feeding is energetically cheap. Such inexpensive foraging means that rorquals are flexible in the quality of prey patches they exploit and therefore more resilient to environmental fluctuations and disturbance. As a consequence, the food turnover and hence the ecological role of these marine giants have likely been overestimated.

Decadal decline in maternal body condition of a Southern Ocean capital breeder.

The changing physical properties of the Southern Ocean are known to impact the recruitment and survival of Antarctic krill (Euphausia superba). For oceanic krill predators, the resulting reduced energy intake may lead to population-level effects likely preceded by an alteration in the animals' body condition. This is especially true for capital breeders that rely on stored energy for successful reproduction. One such Southern Ocean capital breeder, the southern right whale (Eubalaena australis), has been monitored over the past 43 years in their South African wintering ground. Changes in the population have been documented in the past decade, including a decreased reproductive rate and a shift in foraging strategy. To evaluate if a reduced foraging success is an underlying factor, we assessed the temporal variation in morphological body condition through aerial photogrammetry. Results showed a 23% reduction in maternal body condition, potentially contributing to the decreased reproductive rate of the population. To the best of our knowledge, this is the first study to quantify a decadal reduction in the body condition of a capital breeder dependent on Southern Ocean productivity. Understanding the bioenergetic consequences of environmental change is vital to predicting species' resilience to climate change.

3D visualization processes for recreating and studying organismal form.

The study of biological form is a vital goal of evolutionary biology and functional morphology. We review an emerging set of methods that allow scientists to create and study accurate 3D models of living organisms and animate those models for biomechanical and fluid dynamic analyses. The methods for creating such models include 3D photogrammetry, laser and CT scanning, and 3D software. New multi-camera devices can be used to create accurate 3D models of living animals in the wild and captivity. New websites and virtual reality/augmented reality devices now enable the visualization and sharing of these data. We provide examples of these approaches for animals ranging from large whales to lizards and show applications for several areas: Natural history collections; body condition/scaling, bioinspired robotics, computational fluids dynamics (CFD), machine learning, and education. We provide two datasets to demonstrate the efficacy of CFD and machine learning approaches and conclude with a prospectus.

Key questions in marine mammal bioenergetics.

Bioenergetic approaches are increasingly used to understand how marine mammal populations could be affected by a changing and disturbed aquatic environment. There remain considerable gaps in our knowledge of marine mammal bioenergetics, which hinder the application of bioenergetic studies to inform policy decisions. We conducted a priority-setting exercise to identify high-priority unanswered questions in marine mammal bioenergetics, with an emphasis on questions relevant to conservation and management. Electronic communication and a virtual workshop were used to solicit and collate potential research questions from the marine mammal bioenergetic community. From a final list of 39 questions, 11 were identified as 'key' questions because they received votes from at least 50% of survey participants. Key questions included those related to energy intake (prey landscapes, exposure to human activities) and expenditure (field metabolic rate, exposure to human activities, lactation, time-activity budgets), energy allocation priorities, metrics of body condition and relationships with survival and reproductive success and extrapolation of data from one species to another. Existing tools to address key questions include labelled water, animal-borne sensors, mark-resight data from long-term research programs, environmental DNA and unmanned vehicles. Further validation of existing approaches and development of new methodologies are needed to comprehensively address some key questions, particularly for cetaceans. The identification of these key questions can provide a guiding framework to set research priorities, which ultimately may yield more accurate information to inform policies and better conserve marine mammal populations.

Fetal growth, birth size and energetic cost of gestation in southern right whales.

The cost of reproduction greatly affects a species' life history strategy. Baleen whales exhibit some of the fastest offspring growth rates in the animal kingdom. We quantified the energetic cost of gestation for southern right whales (Eubalaena australis) by combining whaling catch records of pregnant females with photogrammetry data on southern right whale mothers and calves from two breeding grounds in Argentina and Australia. The relationship between calf birth size and maternal length was determined from repeated measurements of individual females before and after giving birth. Fetal growth was determined from generalized linear models fitted to fetal length data from whaling operations between 1961 and 1967. Fetal length was converted to volume and mass, using the volume-to-length relationship of newborn southern right whales calves, and published tissue composition and energy content estimates. Fetal maintenance costs (heat of gestation) and the energy content of the placenta were predicted from published relationships and added to the fetal growth cost to calculate the total cost of gestation. Our findings showed that fetal growth rates and birth size increased linearly with maternal length, with calves being born at ∼35% maternal length. Fetal length increased curvilinearly through gestation, which resulted in an exponential increase in fetal volume and mass. Consequently, the cost of gestation was very low during the first (0.1% of total cost) and second trimester (4.9%), but increased rapidly during the last trimester (95.0%). The heat of gestation incurred the highest cost for pregnant females (73.8%), followed by fetal growth (21.2%) and the placental energy content (5.0%). KEY POINTS: Baleen whales exhibit some of the fastest fetal growth rates in the animal kingdom. Despite this, the energetic cost of gestation is largely unknown, as well as the influence of maternal body size on fetal growth rates and calf birth sizes. We combined historical whaling records and drone photogrammetry data to determine fetal growth rates and birth sizes in southern right whales (Eubalaena australis), from which we estimated the cost of gestation. Calf birth size, and consequent fetal growth rates, increased positively with maternal body size. The cost of gestation was negligible for southern right whale females during the first two trimesters, but increased rapidly during the last trimester. These results show that late gestation incurs a significant cost for baleen whale females, and needs to be accounted for in bioenergetic models.

Cryptic vocal behavior of foraging humpback whales on feeding grounds in West Greenland.

Male humpback whales (Megaptera novaeangliae) sing in mating aggregations in the form of song displays, but much less is known about how both sexes use sound on their feeding grounds. Here, we test different hypotheses about the function of vocalizations in 14 foraging humpback whales tagged with sound and movement recording Dtags in Greenland. We show that this population of foraging humpback whales have an overall low call rate of 11.9 calls h-1 (inter-quartile range = 12.1) with no support for the hypotheses that they employ sound in the localization or manipulation of prey nor in the coordination of lunge feeding. The calls had a mean received level of 135 ± 5dB re 1 µPa, which is some 30 dB lower than maximum levels of song recorded on similar deployed tags, suggesting a much smaller active space of these vocalizations. This reduced active space might, in concert with low call rates, serve to mitigate eavesdropping by predatory killer whales or conspecifics competing for the same prey resources. We conclude that feeding humpback whales in Greenland produce low level, infrequent calls suggesting that calling is not a prerequisite for successful feeding, but likely serves to mediate within group social interactions.

Tour boats affect the activity patterns of bottlenose dolphins (Tursiops truncatus) in Bocas del Toro, Panama.

Bottlenose dolphins (Tursiops truncatus) of the Bocas del Toro archipelago are targeted by the largest boat-based cetacean watching operation in Panama. Tourism is concentrated in Dolphin Bay, home to a population of resident dolphins. Previous studies have shown that tour boats elicit short-term changes in dolphin behavior and communication; however, the relationship of these responses to the local population's biology and ecology is unclear. Studying the effects of tour boats on dolphin activity patterns and behavior can provide information about the biological significance of these responses. Here, we investigated the effects of tour boat activity on bottlenose dolphin activity patterns in Bocas del Toro, Panama over 10 weeks in 2014. Markov chain models were used to assess the effect of tour boats on dolphin behavioral transition probabilities in both control and impact scenarios. Effect of tour boat interactions was quantified by comparing transition probabilities of control and impact chains. Data were also used to construct dolphin activity budgets. Markov chain analysis revealed that in the presence of tour boats, dolphins were less likely to stay socializing and were more likely to begin traveling, and less likely to begin foraging while traveling. Additionally, activity budgets for foraging decreased and traveling increased as an effect of tour boat presence. These behavioral responses are likely to have energetic costs for individuals which may ultimately result in population-level impacts. Boat operator compliance with Panamanian whale watching regulations is urgently needed to minimize potential long-term impacts on this small, genetically distinct population and to ensure the future viability of the local tourism industry.

Variation in outer blubber lipid concentration does not reflect morphological body condition in humpback whales.

An animal's body condition provides valuable information for ecophysiological studies, and is an important measure of fitness in population monitoring and conservation. While both the external body shape of an animal and its internal tissues (i.e. fat content) can be used as a measure of body condition, the relationship between the two is not always linear. We compared the morphological body condition (external metric obtained through aerial photogrammetry) of migrating humpback whales (Megaptera novaeangliae) with their outer blubber lipid concentration (internal metric obtained through blubber biopsy sampling) off the coast of south-west Australia early and late in the breeding season (spanning ∼4.5 months). The external body condition index of juvenile and adult humpback whales decreased by 26.9 (from 18.8% to -8.1%) and 12.0 percentage points (from 8.6% to -3.4%), respectively, between the early and late phase. In contrast, we found no intra-seasonal change in blubber lipid concentration, and no difference between reproductive classes (juveniles, adults and lactating females); however, the small sample size prevented us from effectively testing these effects. Importantly, however, in the 33 animals for which paired metrics were obtained, we found no correlation between the morphometric body condition index and the blubber lipid concentration of individual whales. The lack of a linear relationship suggests that changes in outer blubber lipid concentration do not reflect external changes in body shape, thus limiting the utility of outer blubber lipid reserves for individual body condition evaluation. The wider spectrum of change in body morphometry captured with aerial photogrammetry supports the use of body morphometry as a reliable and well-tested method.

Morphological differences between coastal bottlenose dolphin (Tursiops aduncus) populations identified using non-invasive stereo-laser photogrammetry.

Obtaining morphometric data on free-ranging marine megafauna is difficult, as traditional methods rely on post-mortem or live-capture techniques. We linked stereo-laser photogrammetry with long-term demographic data to compare length-at-age (LaA) growth curves of two well-studied populations of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in south-western (SW) and Shark Bay (SB), mid-western Australia. First, we determined the relationship between total length (TL) and blowhole-to-dorsal fin (BH-DF) length from post-mortem subjects (R2 = 0.99, n = 12). We then predicted TL from laser-derived BH-DF measurements of 129 and 74 known-age individuals in SW and SB, respectively. Richards growth models best described our LaA data. While birth length (103-110 cm) was similar between study regions, TL estimates at 1, 3, 12, and 25 years differed significantly (p < 0.001). Asymptotic length of adult males (SW = 246 cm, SB = 201 cm) and females (SW = 244 cm, SB = 200 cm) also differed significantly. Morphotypic variations likely reflect regional adaptations to local water temperatures, with the temperate SW having cooler waters than sub-tropical SB. We demonstrate the effectiveness of a non-invasive technique to understand ecological, demographic and life-history characteristics of long-lived marine megafauna, which are critical parameters for informing conservation and management actions.

Acoustic crypsis in southern right whale mother-calf pairs: infrequent, low-output calls to avoid predation?

Southern right whales (Eubalaena australis) invest substantial amounts of energy in their calves, while facing the risk of having them predated upon by eavesdropping killer whales (Orcinus orca). We tested the hypothesis that southern right whale mother-calf pairs employ acoustic crypsis to reduce acoustic detectability by such predators. Specifically, we deployed multi-sensor DTAGs on nine lactating whales for a total of 62.9 h in a Western Australian breeding ground, and used a SoundTrap to estimate the concomitant acoustic background noise. Vocalisations were recorded at low rates of <10 calls h-1 (1 call per dive) and at low received levels between 123±8 and 134±10 dB re. 1 µPa RMS depending on call type. We conclude that such acoustic crypsis in southern right whales and other baleen whales decreases the risk of alerting potential predators and hence jeopardizing a substantial energetic investment by the mother.

Chronic exposure of Hawaii Island spinner dolphins (Stenella longirostris) to human activities.

Habitat selection is strongly influenced by spatial variations in habitat quality and predation risk. Repeated exposure of wildlife to anthropogenic activities in important habitats may affect habitat selection, leading to negative biological consequences. We quantified the cumulative human exposure of a small, genetically isolated and behaviourally constrained spinner dolphin (Stenella longirostris) population, off Hawaii Island, and exposure effects on their daytime cumulative activity budget. Dolphins were exposed to human activities within 100 m for 82.7% of the daytime, with a median duration of 10 min between exposure events. Individual dolphins spent on average 61.7% (s.d. = 6.5) of their daytime resting. Of their total rest time, greater than 90% occurred inside sheltered bays. Despite high levels of human exposure, we did not observe an effect on dolphin resting behaviour. The short intervals between exposure events probably prevent dolphins from returning to a natural resting state before the next event. Consequently, 'control' observations may represent a resting behaviour of a more vigilant nature. Chronic levels of exposure to human activities could lead to rest deprivation, displacement from preferred resting habitats and ultimately negative population level effects. These results have implications for new proposed legislation aiming to reduce dolphin exposure to human activities.

El Niño Southern Oscillation influences the abundance and movements of a marine top predator in coastal waters.

Large-scale climate modes such as El Niño Southern Oscillation (ENSO) influence population dynamics in many species, including marine top predators. However, few quantitative studies have investigated the influence of large-scale variability on resident marine top predator populations. We examined the effect of climate variability on the abundance and temporary emigration of a resident bottlenose dolphin (Tursiops aduncus) population off Bunbury, Western Australia (WA). This population has been studied intensively over six consecutive years (2007-2013), yielding a robust dataset that captures seasonal variations in both abundance and movement patterns. In WA, ENSO affects the strength of the Leeuwin Current (LC), the dominant oceanographic feature in the region. The strength and variability of the LC affects marine ecosystems and distribution of top predator prey. We investigated the relationship between dolphin abundance and ENSO, Southern Annular Mode, austral season, rainfall, sea surface salinity and sea surface temperature (SST). Linear models indicated that dolphin abundance was significantly affected by ENSO, and that the magnitude of the effect was dependent upon season. Dolphin abundance was lowest during winter 2009, when dolphins had high temporary emigration rates out of the study area. This coincided with the single El Niño event that occurred throughout the study period. Coupled with this event, there was a negative anomaly in SST and an above average rainfall. These conditions may have affected the distribution of dolphin prey, resulting in the temporary emigration of dolphins out of the study area in search of adequate prey. This study demonstrated the local effects of large-scale climatic variations on the short-term response of a resident, coastal delphinid species. With a projected global increase in frequency and intensity of extreme climatic events, resident marine top predators may not only have to contend with increasing coastal anthropogenic activities, but also have to adapt to large-scale climatic changes.

Correction: The effects of marine traffic on the behaviour of Black Sea harbour porpoises (Phocoena phocoena relicta) within the Istanbul Strait, Turkey.

[This corrects the article DOI: 10.1371/journal.pone.0172970.].

Temporally and spatially partitioned behaviours of spinner dolphins: implications for resilience to human disturbance.

Selective forces shape the evolution of wildlife behavioural strategies and influence the spatial and temporal partitioning of behavioural activities to maximize individual fitness. Globally, wildlife is increasingly exposed to human activities which may affect their behavioural activities. The ability of wildlife to compensate for the effects of human activities may have implications for their resilience to disturbance. Resilience theory suggests that behavioural systems which are constrained in their repertoires are less resilient to disturbance than flexible systems. Using behavioural time-series data, we show that spinner dolphins (Stenella longirostris) spatially and temporally partition their behavioural activities on a daily basis. Specifically, spinner dolphins were never observed foraging during daytime, where resting was the predominant activity. Travelling and socializing probabilities were higher in early mornings and late afternoons when dolphins were returning from or preparing for nocturnal feeding trips, respectively. The constrained nature of spinner dolphin behaviours suggests they are less resilient to human disturbance than other cetaceans. These dolphins experience the highest exposure rates to human activities ever reported for any cetaceans. Over the last 30 years human activities have increased significantly in Hawaii, but the spinner dolphins still inhabit these bays. Recent abundance estimates (2011 and 2012) however, are lower than all previous estimates (1979-1981, 1989-1992 and 2003), indicating a possible long-term impact. Quantification of the spatial and temporal partitioning of wildlife behavioural schedules provides critical insight for conservation measures that aim to mitigate the effects of human disturbance.