The search for body condition biomarkers in cetacean blubber has led to an increased appreciation of the complexity and pleiotropic nature of blubber tissue, and by extension, further insight into the extreme physiological adaptations of these animals. Blubber is unique to marine mammals, and appreciating how its functions may contribute to physiological homeostasis can give us insights into the development and maintenance of the life-cycles and adaptations of marine mammals to their environment.
The notion that the blubber’s primary function across all species is to act as an energy storage depot is too simplistic. Results from Chapters 1 and 2 demonstrate that the relationship between blubber thickness, blubber lipid content and overall body condition is not straightforward across different species. The importance of the blubber in terms of providing readily available energy reserves will likely be balanced with its roles in maintaining other optimal characteristics of the animals that allow them to occupy a particular ecological niche. The range of physiological demands on species, as a result of their ecology, will therefore affect the extent to which some functions are more important than others, and by extension, the extent to which the blubber is able to change in thickness and lipid content and still retain its structural integrity. A theoretical representation of this idea is shown in Fig. 8.1.
It appears that beaked whales are a great example of these trade-offs. The lack of variability in morphometric body condition indices or blubber lipid content shown in Chapters 1 and 2 suggests that these species may be adapted to live within very narrow physiological constraints, perhaps
driven by their extreme diving behaviour. Clues for why this may be the case come from previously published evidence of high wax ester content of the blubber. Other functional roles of the tissue in thermoregulation and buoyancy control that allow them to make continuous, prolonged, deep foraging dives (Tyack et al., 2006), unique to only a small number of cetacean species that share these blubber characteristics (Koopman, 2007), appear to be more important than energy storage. In contrast, baleen whales are able to take advantage of spatially and temporally separated breeding and feeding habitats through extreme fasting endurance. These species are therefore uniquely adapted to survive prolonged fasting periods where they rely heavily on energy reserves in the blubber.
Other, ‘intermediate’ species between these two extremes include some of the delphinidae family for example, and a number of pressures likely affect the blubber composition of the animals in this broad group. For example, hydrodynamic drivers that are responsible for high intensity or ‘sprint’ prey capture behaviours in some species (Aguilar Soto et al. 2008), will affect overall body shape through the deposition and mobilisation of the blubber to achieve optimum swimming efficiency (Koopman, 2007). Equally, some species will experience huge seasonal variation in ambient water temperatures which will dictate the extent to which the blubber layer is increased or reduced, and its conductance continually altered in line with the animals’ thermoregulatory capacities and/or requirements (Fougeres et al., 2008; Noren et al., 2009; Koopman, 2007). There are likely very complex relationships between body size, thermal habitat, diving behaviour, lipid stratification, blubber thickness, reliance on endogenous energy reserves and overall metabolism that affect the structural and chemical composition of the tissue.
Marine mammal species that have highly energetically costly life history strategies, including long distance migrations (Burton and Koch, 1999; Lockyer, 1981), prolonged breeding seasons (Boness et al., 2002), and an annual moult in many pinniped species (McConkey et al., 2002; Thompson and Rothery, 1987; Worthy et al., 1992), undergo extreme physiological changes. However, an understanding of the regulatory pathways and how the blubber plays a role in allowing animals to readily meet these extreme, cyclical demands on their energy stores is limited. The functional adaptations governing these highly energetically costly life-history strategies warrant further investigation. With the results from Chapters 5 and 6 that identified, for the first time, a large number of proteins involved in various metabolic pathways in blubber tissue, I suggest that it may be involved in the regulation of a number of paracrine and endocrine metabolic processes, similar to the roles of white adipose tissue in terrestrial mammals (Ahima and Flier, 2000; Kershaw and Flier, 2004).
It is still not known whether marine mammal blubber produces and secretes hormones in the same way, and to the same extent as other mammalian adipose tissues. If it does, its importance in energy regulation is not only through the storage of dietary fats, but also through the secretion of hormones, such as cortisol and adiponectin, that are involved in the control of lipid metabolism, fasting energetics and the regulation of physiological processes that take place during periods of high energy demand. Recent evidence suggests that there is metabolism of corticosteroids in the blubber with the interconversion of cortisol and cortisone (Galligan et al., 2018). Cetacean blubber is therefore likely a site of active steroid metabolism. The localised production of hormones involved in lipid metabolism may help to explain how cetaceans have evolved an enhanced capacity for inhibiting unrestricted lipolysis and are able to finely control the lipid content of the tissue (Wang et al., 2015).
It is likely that there are a wide range of cellular and tissue-specific processes occurring constantly, and simultaneously in the blubber, and this work has only begun to scratch the surface as to the complexity of the tissue. As the blubber makes up such a large proportion of the total body mass in cetaceans, and other marine mammals, it is possible that the other roles of adipose tissue in the regulation of appetite and energy balance, the immune response, inflammation and the acute-phase response, blood pressure, nutrient transport and haemostasis (Trayhurn and Wood, 2004), contribute greatly to the overall metabolism of these animals. In fact, if blubber does act as an endocrine and paracrine organ, its ability to contribute to whole body homeostasis during different parts of the life cycle could help to explain some of the extreme life-history strategies characteristic of some species. For example, finely controlled metabolism of available lipid stores could contribute to the extreme, long-term fasting endurance of baleen whales (Chivers, 2009). Fig. 8.1. Theoretical schematic demonstrating the relative importance of different blubber functions across three cetacean families with respect to the extent to which the tissue can vary in total lipid content. It is hypothesised that ziphiids prioritise the preservation of a constant blubber structure and lipid content to maintain the hydrodynamic, insulative and buoyant properties of the tissue. Balaenopterids however, show huge amounts of variability in blubber lipid content both within and between individuals, likely because they rely on blubber lipid stores during prolonged fasting periods of their life-cycles. Artwork by Chris Huh.
Endocrine signalling from the tissue could contribute to the mechanisms that signal the end of fasting and the initiation of feeding at the end of the extremely intense lactation periods of many female phocid seals (Schulz and Bowen, 2004). Finally, and very speculatively, combinations of the ability of the tissue to regulate vasoconstriction and vasodilation, together with the immune response and localised coordination of inflammatory and cellular defences, could help to explain how marine mammals are able to sustain severe injuries, often of anthropogenic origin, and survive (Barcenas-De la Cruz et al., 2017; Neilson et al., 2009).
These are speculative links between whole animal physiology and blubber tissue function, so further investigations of how the blubber contributes to different homeostatic processes are required. A major step forward in efforts to better understand blubber function is the recent use of blubber explants to investigate its metabolism in grey seals (Halichoerus grypus) (Bennett et al., 2017). Adipose explants are small pieces of tissue taken from live animals. Cells within the tissue are kept alive in a culture medium in order to maintain structure. Cells are therefore able to better retain their original metabolic characteristics compared to individual cells cultured in isolation. Experimental manipulations of these explants can be used to investigate adipose regulation in wildlife species when opportunities for whole organism experimental work are limited, as is the case for marine mammals (Bennett et al., 2017). Short term explant culture may therefore be a viable method to complement whole animal studies to improve our understanding of the molecular and cellular physiology of adipose tissue in general (Bennett et al., 2017). Future work should build on developing these novel experimental approaches to explore the pleiotropic nature of the blubber, and how it contributes to the extreme diving, fasting and breeding physiology of many marine mammal species.