Climate change and cetacean health: impacts and future directions

Abstract

Climate change directly impacts the foraging opportunities of cetaceans (e.g. lower prey availability), leads to habitat loss, and forces cetaceans to move to other feeding grounds. The rise in ocean temperature, low prey availability and loss of habitat can have severe consequences for cetacean survival, particularly those species that are already threatened or those with a limited habitat range. In addition, it is predicted that the concentration of contaminants in aquatic environments will increase owing to Arctic meltwater and increased rainfall events leading to higher rates of land-based runoff in downstream coastal areas. These persistent and mobile contaminants can bioaccumulate in the ecosystem, and lead to ecotoxicity with potentially severe consequences on the reproductive organs, immune system and metabolism of marine mammals. There is a need to measure and assess the cumulative impact of multiple stressors, given that climate change, habitat alteration, low prey availability and contaminants do not act in isolation. Human-caused perturbations to cetacean foraging abilities are becoming a pervasive and prevalent threat to many cetacean species on top of climate change-associated stressors. We need to move to a greater understanding of how multiple stressors impact the metabolism of cetaceans and ultimately their population trajectory.

This article is part of the theme issue ‘Nurturing resilient marine ecosystems’.

1. Introduction

The change in climate during the past decades is having a devastating effect on our ecosystem with a gradual change in temperature, ocean circulation, ice coverage, sea level and acidity and with more sudden increases in extreme weather events. In their 1996 paper, MacGravin & Simmonds predicted that climate change will affect cetaceans by both a reduction in prey availability and a shift in the distribution of prey species. They speculated that this will be caused by changes in water temperature, turbulence, and surface salinity of our oceans [1]. Over the last two decades, Arctic surface air temperature has indeed increased by more than double the global average, resulting in loss of sea ice but also a disproportionate increase in global ocean heat [2]. For example, in 2014, the Pacific Decadal Oscillation changed to a positive phase with a rise in sea surface temperatures, and coastal upwellings weakened as a result [3]. Coinciding with this climate event, a massive lens of warm water developed in the North East Pacific and moved east in the summer of 2014, spreading along the shelf of North America and coastal Alaska [4]. This led to sea surface temperature increases greater than +3°C in certain areas [5]. This marine heatwave had detrimental impacts on the marine ecosystem, recording not only mass strandings of marine mammals and seabirds but also a geographical shift of species [5]. Extreme climatic events, which are predicted to increase in frequency as a result of climate change [6], can induce ecosystem change and alter patterns of resource availability, as observed in a habitat shift of bottlenose dolphins (Tursiops truncatus) following seagrass die-off from the 2011 La Niña event [7].

Using quantitative models to estimate global terrestrial, freshwater and marine diversity scenarios containing information on extinctions, changes in species abundance, habitat loss and distribution shifts indicate that there will be a continuous decline in biodiversity over the twenty-first century [8]. For example, the overexploitation of important fish stocks to top marine predators in combination with this rise in ocean temperature can cause a decline in the availability of fishes. In Europe, a shift has been observed in the tropic-web of fish communities and a decline in mean trophic level [9]. In addition, the increase in harmful algal blooms is associated with climate change [10–12]. These algal blooms can produce biotoxins and can further bioaccumulate in filter-feeding shellfish, transferring toxins to higher trophic levels [13]. Recurring harmful algal blooms are also linked to loss of foraging fishes and a decline in plankton dynamics [14], leading to an overall decline in prey availability for marine top predators. In addition, these biotoxins produced by the harmful algal blooms can impact physiological functions and lead to an overall decline in health and body condition of marine mammals [15,16].

Changes in ocean temperature and prey availability can have particularly dramatic consequences for marine mammals [17], and trait-based approaches show that threatened species or local resident populations are the most vulnerable to climate change [18,19]. Species may be impacted, for example, by the loss of suitable habitat for functional behaviours. For example, many currently occupied humpback whale (Megaptera novaeangliae) breeding grounds are predicted to be unsuitable (greater than 28°C) by the end of the twenty-first century [20]. Genetic data combined with predictive habitat models for the year 2100 also predict that grey whales (Eschrichtius robustus) will expand beyond their habitat to the Atlantic, potentially via Arctic migration routes [21]. Similarly, beluga (Delphinapterus leucas) habitats are predicted to continue to decline for the year 2100, resulting in a distribution shift northwards and leading to a population decline in some populations [22]. Shifts in distribution ranges appear to have been successfully employed in the past in response to climate change, at least in some species. For example, ancient DNA revealed that the bowhead whale (Balaena mysticetus) lineage survived the change in the Late Pleistocene climate by shifting habitats northwards [23]. Foote et al. predict that the response to climate change will be species-specific and suitable habitat for bowhead whales will probably be halved by the end of this century. The combination of the rise in ocean temperature, low prey availability, and the loss of habitat can have severe consequences for the survival of many cetacean species, particularly those that are already threatened or those with a limited habitat range [24]. Here, we will discuss the consequences of climate change on cetacean health by looking at impacts on distribution, abundance, phenology and behaviour, reproductive success and pollutant burden. Finally, we will discuss how health is currently being measured to assess environmental impacts and the novel approaches taken to increase our knowledge of the physiological constraints limited prey availability might cause.

2. Consequences on distribution, abundance, phenology and behaviour

Changes in habitat usage/diversity and abundance are one of the most common responses of marine biota to the rise in ocean temperature. Similarly, the distributions of many cetacean species are expected to shift towards the poles, resulting in range contraction for polar species and range expansion for warm water species, as well as changes in population size [25–28]. Although effects on Arctic species are of particular concern (e.g. [29–31]), climate-driven impacts on cetaceans are projected to be global (e.g. [18,32,33]). Indeed, a recent systematic review (58 articles, 29 species) on climate change and distribution, migration and habitat use showed a poleward shift for many species [34]. Habitat usage is species-specific, meaning that while some species may move between different temperature zones, others might be more constrained. For example, the white-beaked dolphin (Lagenorhynchus albirostris) is a cold-water species whose relative abundance appears to be declining in northwest Scotland (UK), based on both frequencies of strandings between 1992 and 2003 and sighting surveys from 2002 and 2003 [35]. Indeed, statistical models show a negative relationship between white-beaked dolphin distribution and increasing water temperature [36]. On the other hand, the common dolphin (Delphinus delphis) has increased in abundance (both stranding and sightings), reflecting increased habitat usage of the warmer waters in northwest Scotland [35]. In addition, striped dolphins (Stenella coeruleoalba) are now regularly sighted in Scottish waters, despite never being recorded before 1988 [37]. Similar observations were documented in St Mary's Bay (Canada), which historically had few sightings of cetaceans. Owing to an increase in the local water temperature, this became a feeding ground for humpback whales in 2016 [38]. Changes in species abundance have also been reported in the North Atlantic, where sightings reported over the last 14 years showed an increase in humpback and fin (Balaenoptera physalus) whale abundance, but a significant decrease in common minke whale (Balaenoptera acutorostrata) abundance [39,40].

Similar shifts in distribution and abundance were observed in bowhead whales tracked by satellite between 2001 and 2011 in west Greenland. Bowhead whales showed a change in movement pattern and were found at higher latitudes during spring and summer [41], probably owing to the decrease in ice covering and the need to change their habitat usage. Bowhead whales feed on krill (Euphasia spp.) and the sea ice edge provides shelter from predators for krill and contains critical food resources (i.e. sea ice algae). As such, the receding of the sea ice edge results in a decline in krill availability [42]. On the other hand, the Pacific-Arctic bowhead whale was reported to be thriving during a period of rapid sea ice loss (longer duration of summer open water) and changes in upwelling potential (wind stress) with increased population size, body condition and calf counts over the last 25 years [43,44]. This was in combination with a substantial shift in habitat usage over those 25 years and reflects the findings of the bowhead whale lineage that survived the Late Pleistocene climate by shifting habitats [23]. Changes in habitat usage and abundance are not limited to colder regions and were also observed in cetaceans inhabiting tropical and subtropical regions of the Pacific Ocean. For example, the abundance of Bryde's whales (Balaenoptera edeni) increased between 2000 and 2010 in the Southern California Bight (USA), which was probably driven by prey availability [45]. Similarly, unusual sightings of Clymene dolphins (Stenella clymene) have been recorded on the northern coast of Spain [46], the Patagonian Coast (Argentina) [47] and the Brazilian coast [48], outside their usual habitat in the tropical waters of the Atlantic Ocean, Caribbean Sea and the Gulf of Mexico. Range shifts are believed to correlate with habitat expansion, leading to a functional feeding response of cetacean species to changes in the marine environment [40]. If climate-change impacts accelerate, such regime shifts are thought to become more widespread [49]. In general, range shifts are believed to be an indirect effect of climate change, as cetaceans adapt to changes in the distribution of prey (e.g. [40]). However, a recent study showed that pilot whales shifted polewards at a strikingly high rate that correlated with thermal niche, rather than shifts in prey distribution, thus suggesting a direct response to warming waters [50]. This decoupling between predator and prey distribution may potentially influence trophic interactions, reshaping marine communities and affecting cetacean populations. Future studies quantifying the rate of distribution shift in other populations and species will be crucial towards our understanding of the direct effects of climate change on cetaceans and the ecosystem-level consequences of these range shifts.

Environmental changes can impact food-web dynamics and may change entire marine ecosystems. They may lead, for example, to the introduction or increased occurrence of top predators, with consequences propagating through the entire food chain. For example, as the Arctic sea ice cover diminishes as a result of warming waters, killer whales (Orcinus orca) are expanding to ice-free areas of Hudson Bay (Canada) [51]. These animals are reported to feed on other marine mammals including seals and other whales (e.g. narwhal (Monodon monoceros) and bowhead whales) [52,53]. The expansion of inhabitable Arctic water is likely to continue to lead to an increasing presence of those killer whales that prey on marine mammals, putting severe pressure on marine mammal stocks and the Arctic marine ecosystem [52]. Behavioural studies of belugas, narwhals and bowhead whales show that in the presence of killer whales, these species change their habitat usage which can lead to increased stress and decreased fitness [54–56]. Such nonconsumptive effects on prey species may cause cumulative consequences for energy acquisition in habitat that may already be of poorer quality owing to climate change effects on resource availability. In addition, the shift of cetaceans to new feeding grounds can have an impact on the body condition of other non-cetacean species (e.g. Adelie (Psygoscelis adeliae) and Emperor penguins (Aptendytes forsteri)) [57].

Phenology and behavioural changes have also been reported as a result of climate changes. For migratory species, the impacts of climate change can be particularly challenging as these species time their migration to maximize exploitation of prey in feeding areas, which is only available temporarily. Changes in the period of prey availability will lead to mismatches between the arrival of migrants and the availability of prey, leading predators to shift their migration timing. However, there may be limits to the degree to which such timings can be adjusted before other important functional behaviours are affected. Baleen whales that migrate between feeding and breeding grounds provide an excellent example of these impacts. For example, in the Gulf of St Lawrence, fin and humpback whales were shown to shift arrival date over a period of 30 years, arriving and leaving earlier to and from their feeding grounds [58]. While both species were initially able to maintain temporal niche separation, there were indications of increasing temporal overlap, leading to higher competition for prey resources. The high rate of change in migration timing observed also suggested that if environmental changes continued at the same pace, both species would need to substantially change their annual life cycle to adapt to the timing of prey availability. Similar changes in migration timing have also been observed in other species [34]. Additionally, changes in behaviour as a result of climate change have also been reported, such as in group size. For example, bottlenose dolphins in the Moray Firth (UK) and killer whales in Johnstone Strait (Canada), seemed to change their group size in relation to changes in ocean climate over a period of 9–11 years [59]. Climate indicators correlated with local prey abundance and smaller groups were observed during periods of lower salmon availability in both areas. This seemed to recur every 2 years after a low phase of North Atlantic and Pacific Decadal Oscillations [59].

Clearly, climate change can impact not only the distribution range and abundance of cetaceans but also impact migration timing and behaviour, all of which may eventually lead to poorer health owing to decreased access to preferred prey or decreased foraging success. Those cetacean species that are limited by their habitat usage may face a greater challenge to cope with the temperate change, and thus may lead to extinction events. By contrast, those that can change their habitats, such as the bowhead whale, may ensure the survival of the species as demonstrated by historical climate events. Shifts in habitat usage will lead to increased sightings of uncommon species in some areas, which could have repercussions across the food chain, and ultimately alter whole ecosystems. As such, monitoring schemes and policy makers should take into account the predicted trajectory of habitat usage and those species that have a limited range when managing Marine Protected Areas.

3. Consequences on reproductive success

The rise in ocean temperature can impact the metabolism of marine mammals and their overall health. For example, following a heatwave, Indo-Pacific bottlenose dolphins (Tursiops aduncus) inhabiting Shark Bay (Western Australia) showed a significant decline in female reproductive rates [60]. Those that use tools for foraging had a higher survival rate compared to those that did not. The lower survival rate persisted post-heatwave and Wild et al. speculate that habitat loss may prolong negative impacts on higher trophic level marine predators. Wild et al. also speculate that the decline in population numbers is probably owing to (i) females spending more time foraging leaving calves open to predators; (ii) a trade-off between energy available and reproduction; and (iii) suppression of the reproductive system owing to low body weight.

The amount of energy available (e.g. fat) is tightly linked to the ability to invest in reproduction, and blubber thickness is linked to reproductive success [61–65]. When in poorer body condition (e.g. owing to low prey availability) early-term abortion or less investment in foetus growth has been observed in cetaceans as a measure to save energy and protect the mother's survival [62,63,66]. In addition, suppressed ovulation or delayed sexual maturity may also occur when females are below a certain threshold of body weight [67]. As such, the impact of climate change may have long-term effects on reproduction rates and lead to severe population declines over longer periods. For example, coinciding with the changes in the Pacific Decadal Oscillation and other climate events, the mother-calf rates of humpback whales sighted at Au'Au Channel Maui (Hawaii) dropped by 76.5% between 2013 and 2018, showing a rapid decline in reproductive rates [68]. There has been a decline in abundance and apparent survival rates of fin whales over the last 35 years [69] and a reduction in the reproductive success of humpback whales at the Gulf of St Lawrence (Canada) [70]. In humpback whales observed between 2004 and 2018, 39% of the identified pregnancies were unsuccessful over this 15 year period [70]. Both species also displayed changes in their migratory timing [58]. One of the likely drivers for these changes is the reduced prey availability caused by environmental shifts as a result of reduced sea ice extent [69].

Continued increasing water temperatures and sea ice reduction may also have major effects on ecosystem energy flux altering the ratio of phytoplankton and zooplankton species production [71]. With a gradual shift in the composition of Atlantic zooplankton species, lipid-rich prey species such as amphipods may contain less energy [72]. Marine predators such as common minke whales feeding on these less-energy rich species then fail to build up energy reserves for migration to breeding areas and may lead to a decline in producing offspring [73]. Similar patterns are observed with the southern right whale (Eubalaena australis) preying on krill [74]. Data collected between 1997 and 2013 showed a strong correlation between whale breeding success in southern Brazil and krill density. During that period, krill density was correlated with global climate indices and thus reduced krill is likely to slow down the current recovery rate of these historically overexploited species [74].

For some cetacean predators, consequences of environmental changes may be stronger owing to low flexibility for dietary shifts. For example, population trends of killer whales in the northeastern Pacific Ocean are strongly correlated with the availability of their principle prey, the Chinook salmon (Oncorhynchus tshawytscha) [75]. The lack of this key prey is associated with low reproductive success and high rates of unsuccessful pregnancies in the southern resident killer whale population [76]. Although other prey exists in the environment, the strong preference for this specific prey species can lead to population demographic consequences in killer whales. This dependence on a single prey species stems from fixed behavioural traditions within a pod, acting as important social isolating mechanisms which ultimately lead to the evolution of genetically distinct populations [77]. Thus, genetic diversity is also threatened under climate change. The decline in population size allows for inbreeding depression by reducing the genetic diversity and increasing recessive homozygotes created by consanguineous mating [78–80]. That would lead to a weakened resilience of populations against climate change effects and other anthropogenic pressures [81].

Prey switching to provide sufficient energy when other sources are low may not be an optimal response either, as it can lead to a decrease in body condition if suboptimal prey are consumed. Beluga whales in the eastern Beaufort Sea (Arctic region) primarily prey on Arctic cod, which is a fish species sensitive to climate change. Data collected between 2011 and 2014 showed that the diet of belugas containing cod declined and a prey switch occurred to capelin. The lowest body condition (maximum girth and blubber thickness) measured in 2014 coincided with the lowest consumption of cod and the highest of capelin, and this predominantly affected females and juveniles [82,83].

Climate change impacts reproductive success indirectly by reducing the food availability and thus worsening body condition. Given the trade-off between survival and reproducing when fat stores are low, climate change can lead to less offspring being born and thus could lead over time to an overall population decline. In addition, those species that migrate to their breeding grounds may encounter a loss of those grounds, change their migratory patterns, or fail to reproduce as migration can be energetically costly.

4. Consequences on pollutant burden

Climate change has the potential to impact the current environmental distribution of chemical toxicants and their associated biological effects on the marine ecosystem (see review [84]). With the increase in arctic ice melting and change in regional precipitation patterns, the concentration of contaminants in the meltwater and aquatic environments will increase [85,86]. As a warmer atmosphere can hold more water vapour, climate change models predict an intensification and an increase of rainfall events in certain areas [87–90]. This can lead to higher rates of land-based runoff in downstream coastal areas, elevating pollutant concentrations. Over time, this could contribute to increased contaminant exposure on cetaceans and affect survival rates of entire populations [91,92]. For example, model forecasts predict that greater than 50% of world killer whale populations are threatened by polychlorinated biphenyls (PCB)-mediated effects [93]. This is likely to be more severe in coastal populations, that are and will be exposed to higher concentrations of pollutants than those with an oceanic habitat. Persistent and mobile contaminants (PMCs) are globally distributed, persist long after their emissions (most banned in the 1960s) and can bioaccumulate in the ecosystem, leading to ecotoxicity [94]. Environmental exposure to these PMCs can continue for years and decades, with long-lasting adverse health effects on many organisms including marine species [95]. These effects include immunotoxicity and endocrine disruptions, which leads to changes in reproductive success [95–97].

Cetaceans are particularly vulnerable to these pollutants as they are apex predators, feed on top of the food chain and have a thick blubber layer where these chemicals bioaccumulate [98]. These contaminants then recirculate in periods of low prey availability (using energy stores), exposing vital organs to toxic risks [99]. Further, the immunosuppressive effects of PCBs make it more likely for an individual to die from infectious disease [100]. Although there has been a general decline in persistent organic pollutants (POPs) since the 1980s in blubber samples of cetaceans [101,102], the current change in climate could lead to a resuspension and reintroduction of these contaminants into the aquatic environment. Especially those species inhabiting coastal and Arctic regions may be most at risk of an increased contaminant exposure and there is evidence of PMCs transferring maternally in several species [103–106]. For example, following a severe weather event in 2011 resulting in an influx of contaminated freshwater into coastal waters in Queensland (Australia), unusually high mortality was observed in several dolphin species [91]. A rise in dichlorodiphenyltrichloroethane (DDT), PCB and hexachlorobenzene levels (i.e. POPs) in blubber samples was also recorded between 2011 and 2015 following this event in coastal Australian humpback dolphins (Sousa sahulensis) and Australian snubfin dolphins (Orcaella heinsohni) [107]. Further, sustained periods of elevated freshwater discharge may contribute to a higher mortality of resident inshore cetaceans [91]. This could potentially impact their health and reproductive success owing to the increased exposure to infectious pathogens [108] and contaminants with immunosuppressive effects [109], making the animal more vulnerable to disease.

Shifts in habitat usage and prey, owing to the low availability of preferred prey, may also result in higher exposure to pollutants [110]. Pollutant burdens are strongly influenced by geographical distribution [111], and the shift of species to new feeding grounds/habitats could expose cetaceans to higher levels of pollutants.

5. Measuring health in cetaceans: current and novel approaches

The ability of an animal to reproduce is highly dependent on the amount of energy that is available to invest in reproduction. When fat reserves are low, one's own survival is prioritized with a shut-down of processes related to reproduction. Therefore, the amount of fat stores is widely used in mammals to assess body condition or used as a health proxy [112–114], including in cetaceans (i.e. blubber thickness) [115]. However, using blubber thickness alone to infer body condition has led to inconclusive results (see review [65]). In some cetacean species, blubber thickness may not reflect whether individuals are in negative energy status or not [116–121]. This is probably because blubber also serves other functions than an energy storage, such as buoyancy aid, insulator and gives structural support. For example, bowhead whale blubber thickness did not vary with seasons or life stages but showed an increase in structural fibre density within the blubber layers [122]. As such, blubber thickness did not change but the morphology of the blubber did, with a reduced fat cell size. In addition, dolphins exhibit a unique fasting profile after 24 h, with a rapid switch to lipids and amino acids as fuel [123]. This is in agreement with Kershaw et al. [124] who argued that muscle mass may be used as fuel during periods of starvation to protect the blubber's other functions [124]. As such, novel approaches are being developed that consider other metrics than blubber thickness to infer health/body condition in cetaceans (see reviews [125,126]). As Castrillon et al. [125] extensively reviewed traditional and other approaches in evaluating cetacean body condition, we will here focus on the recent developments in molecular approaches.

We currently do not fully understand how the physiological system in cetaceans responds to low food availability and new insights in this complex system-wide response are emerging [123]. For example, nucleic acid-derived indices have recently been successfully applied as ecophysiological indicators in bottlenose dolphins and pilot whales, showing differences between species and animals with different residency patterns [127]. This approach shows promise and may have wide future applications, as it can be used in samples obtained via biopsying, a technique widely used for tissue sampling of several cetacean species. With recent advances in technology, we are also now able to characterize many thousands of genes, metabolites, lipids and proteins associated with phenotypic traits and this is key to the discovery of health biomarkers in for example human diseases (see reviews [128–132]). Omics technologies are now emerging as novel methods in the field of cetacean health research and to unravel how their metabolism may cope with stressors. For example, evidence for a Dynamic Network Marker (DNM), originally created for early human disease detection, emerged within the plasma metabolomic network of 24 h fasted dolphins [123]. This DNM hinted that dolphins may enter a ‘fat conservation’ state more rapidly than expected and shows a tipping point is emerging in energy state transitions [123]. Managed or stranded cetaceans can be used as ‘model species’ to create a more comprehensive understanding of cetacean health and the physiological/metabolic response to stressors as a way to create biomarkers to assess wild populations [123,133–139]. For example, in managed whales, a correlation was found between lipidomics (i.e. lipid profile) and blood parameters related to metabolism [135]. As such, lipidomics shows great promise to assess the change in energy body reserves and thus body condition in free-ranging cetaceans [99,133,140,141]. Other omics approaches such as proteomics and metabolomics are also emerging as novel methods to increase our understanding of cetacean metabolism [137,142–145]. Finally, we also lack an understanding of how cetacean metabolism and nutrient requirements influence feeding ecology. For example, selective feeding, whereby only certain portions of the prey are eaten or only certain prey are targeted, may be driven by nutrient balancing, rather than simple maximization of energy intake [146]. Lipid-rich or protein-rich prey or parts of prey may be preferred, depending on the nutrient needs of predators. Climate change may impact not only prey availability but also prey nutrient composition, thus affecting the nutrient balance required by cetacean predators. Thus, a shift in the focus of future studies away from only caloric measurements and applying a nutrient geometry framework may be useful to further our understanding of the impacts of climate change on feeding decision-making of cetacean predators and its consequences to their health.

6. Conclusion

The impacts of climate change on cetaceans are species or population-specific, with some being able to expand their habitat while others are forced to constrain their habitat range. Those with a limited habitat range may suffer from declining population sizes mainly caused by a range shift in prey availability across the food chain. Impacts may also differ depending on habitat type, however, knowledge on the effects of climate change in populations inhabiting oceanic or remote areas is still lacking. However, conclusive to most cetaceans is that with rising ocean temperature, food availability is declining and thus so is body condition. This will lead to a change in metabolism with a negative energy status and thus lead to a decline in reproductive rates. This is attributed to the trade-off between survival and reproduction as cetaceans cannot invest in reproduction when energy reserves are already low. Finally, changes in precipitation and sea ice loss caused by warming and changing climate can resuspend or introduce contaminants in the water column, potentially causing adverse effects on cetacean metabolism (e.g. endocrine disruption). The worsened body condition resulting from low food availability and the pollutants bioaccumulated in the thick blubber layer can impact cetacean health.

There is a need to measure and assess the cumulative impact of multiple stressors, given that climate change, habitat alteration, low prey availability and contaminants do not act in isolation. Human-caused perturbations to cetacean foraging abilities are becoming a pervasive and prevalent threat to many cetacean species on top of climate change-associated stressors. Multiple stressors can lead to a decline in population growth by reducing the amount of energy that is available to invest in reproduction, which may lead to extinction events. Approaches such as modelling and/or trait-based methods for assessment of climate change vulnerability can be helpful in identifying local or regional management units that are at particular risk. As such, monitoring schemes and policy makers should take into account the predicted trajectory of habitat usage and those species that have a limited range when managing Marine Protected Areas and their exposure to anthropogenic stressors. We need to begin to address the knowledge gaps regarding the interactions between multiple stressors and unravel the complex physiological mechanisms regulating cetacean metabolism, reproduction and body condition to better understand the consequences of future environmental changes. With approximately 25% of cetacean species classified as threatened (International Union for Conservation of Nature, December 2020), it is critical to understand the physiological effects of climate change on these apex predators to protect vulnerable cetacean species. The field of omics is showing great potential for biological markers to assess health in free ranging cetaceans.

Lastly, the majority of the papers focus on the impact of climate change on prey availability and cascading through the food-web, but little work has been done to discuss the direct consequences of oceanic acidification for cetaceans. It is important to point out that with an increase in atmospheric CO₂ levels, the ocean plays an increasing role in the carbon cycle with a higher biological uptake of CO₂ per unit area [147]. This can have indirect effects on cetaceans via their food chain by altering the quality of food available for cetaceans. However, very little is known what the direct impacts of increased CO₂ levels may be on cetacean's metabolism. There is indication from experimental work on other species that ocean acidification directly impacts metabolism. For example, molluscs show a substantial change to their energy metabolism with a shift in metabolic pathways when exposed to parameters mimicking ocean acidification [148]. In large pelagic fishes, elevated CO₂ increased resting oxygen uptake rates compared to fishes with normal conditions [149]. Other work on notothenioid fishes suggests that some species may require a physiological trade-off to compensate for the energetic costs of acclimations to both temperature increase and CO₂ changes [149]. If the rise in ocean acidity requires cetaceans to increase their resting oxygen uptake levels with potentially extra energetic costs, this could lead to cetaceans having to rely more on their stored energy reserves. The change in acidification could lead to a reduced body condition, reduced reproductive success and increased susceptibility to diseases. As mentioned earlier, climate change-associated impacts such as a change in temperature, increased ocean acidification and a decline in prey availability are cumulative. We need to move to a greater understanding of how multiple stressors impact the metabolism of cetaceans and ultimately their population trajectory.

Data accessibility

This article has no additional data.

Authors' contributions

A.K.: writing—original draft; F.S.: writing—original draft, writing—review and editing; D.D.: conceptualization, writing—original draft, writing—review and editing.

All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

Conflict of interest declaration

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Funding

We received no funding for this study.