Despite very cold waters, polar regions are very productive and support a large population of birds and mammals that rely on fish for their food. The challenge for fishes come largely in the winter, when thick ice limits atmospheric gas exchange, although high oxygen solubility in the cold may avoid serious problems, and the lack of sunlight shuts down primary production. This volume provides a timely overview of the physiology of fishes that have successfully adapted to one of the most challenging aquatic environments on earth. It updates one aspect of the wide-ranging ‘Antarctic Fish Biology’1, and various specialist books since, but importantly fills a gap for the Arctic fauna, where the biology and systematics are much less well served2. The authors address three important questions: What is special about the physiology of fish from the stenothermal Arctic and Antarctic environments? Are there common themes to the physiology for fishes that live in frigid waters but poles apart? How do polar fishes differ from more eurythermal temperate species that can acclimatize to seasonally cold waters?
Opening of the Drake Passage occurred about 25 m.y.a., and the circumpolar current thus formed physically isolated the waters around Antarctica that reached freezing point 10–15 m.y.a. This caused a loss of species diversity, with extinctions being replaced by a benthic blennioid ancestor, and the subsequent radiation into vacant niches. In contrast, Arctic ice cover is more recent, beginning only 2–3 m.y.a., and is an open system allowing migration to and from the warmer Atlantic and Pacific oceans, leading to a lower degree of endemism than in the Antarctic. An annotated list of fish families occurring in Arctic and Antarctic regions usefully updates and extends the scope of previous guides. Physical isolation led to a high degree of endemism and the dominance of the notothenioids around Antarctica, (which have attracted the lions share of research effort) although there appears to have been several invasions by deep water zoarcids and liparids. The Arctic fauna shows much less endemism and is dominated by phylogenetically young families, probably of both Pacific and Atlantic origins. A major challenge for evolutionary biologists is mapping physiological characteristics onto molecular phylogenies, especially as many families have not been studied in this way.
A particularly good example of how the physical environment largely shapes animal physiology is how geography of the two polar regions defines the two fish faunas. Perhaps the most important ecological process limiting polar fish diversity is the extreme seasonality of food resources and primary productivity. The year-round frigid waters and abundance of ice provided a powerful selection pressure driving adaptive radiation in the ancestral Antarctic fish stock, and exploitation of the shallow Arctic shelf regions. The younger Arctic fish fauna may be displaying an intermediate position on the evolutionary path towards a common polar phenotype. For example, freezing is always lethal in teleost fish as their bodies are hyposmotic to seawater, and colonization of the frigid Antarctic waters was made possible by evolution of a biological antifreeze system, with both similar and unrelated antifreezes found in Arctic fishes. Their identification and characterization provides a classic example of convergent evolution at the protein level, and the description of how these APs disrupt or arrest the growth of ice crystals is a real tour de force. Importantly for such a volume, the limited understanding of the in vivo role played by APs is highlighted, in particular how epithelial surfaces resist ice entry and the fate of ice that enters the gut.
The metabolic physiology, biochemistry, and functional genomics of cold adaptation in marine fish is nicely outlined. One of the major challenges for ectothermic animals is to generate sufficient energy for activity, growth and reproduction, as physiological processes are depressed by a factor of 2–3 for every 10°C drop (Q10 of 2–3). The limits and benefits of thermal specialization require an understanding of the trade-offs and constraints in thermal adaptation, and a particularly emphasis is placed on oxygen delivery. A conceptual framework is developed that involves pejus (‘getting worse’) temperatures that characterize the onset of thermal limitation at high and low temperature thresholds, with shifts in thermal tolerance being of interest in light of global warming. Thermal acclimatization or adaptation to permanent cold may include increased aerobic metabolism, reduced proton leakage and ionoregulation, and modifications to protein synthesis and structure. With the possible exception of the haemoglobinless icefish, it seems unlikely that the role of branchial or cutaneous oxygen uptake in transfer of oxygen from water to tissue is fundamentally different to that in temperate fishes, so other adaptations must provide for the maintenance of aerobically-based metabolic activity. The long-running debate over metabolic cold adaptation, where polar species were assumed to have a higher metabolic rate than temperate counterparts at the same temperature, is extensively discussed and shown to be an artifact of earlier studies. This has important implications for maintenance costs in fish that have to synthesize antifreeze proteins and maintain high muscle mitochondrial densities, and complements a discussion about repartitioning of the energy budget.
A perennial problem in comparative physiology, how can one be sure that observed traits in one of the polar regions are adaptations to low temperature that have arisen through natural selection, or the consequences of genetic drift or phylogenetic constraints, is explored by means of the cardiovascular system and oxygen transport. While the effects of cold on blood viscosity, splennic control of haematocrit and vascular resistance are all thought to reduce cardiac afterload, and the low heart rate and high stroke volume (particularly in icefishes) is explained by unusual autonomic control, differences in vascular control may reflect phylogeny rather than temperature. Some unusual findings are of unknown function, e.g. an apparently widespread blunted catecholamine-mediated stress response, but the unusual response to exercise and hypoxia may reflect the few species examined and/or experimental protocols adopted, highlighting the need to study sub-Antarctic and temperate relatives to distinguish between true adaptations to the cold and phylogenetic traits, and for bipolar comparisons. A further caution, however, is that given the limited ecological opportunities offered by the deep Antarctic continental shelf, the slower rate of cooling, and the development of secondary pelagicism in the endemic species, there is no a priori reason that their adaptations for energy expenditure should parallel those seen in Arctic fishes.
Notothenioid fish are not great swimmers, using sluggish labriform locomotion, but red muscle has an extremely high mitochondrial content (> 50% of fibre volume in pectoral muscle) supporting other evidence that cold adaptation has maintained aerobic capacity. However, the low capillary density suggest limitations for peripheral oxygen exchange which contrast nicely with those described for oxygen uptake. While specific protein isoforms mean that it is energetically cheaper for Antarctic fishes to maintain muscle tension and its development appears to be temperature independent, contraction velocity and fuel use show little thermal compensation. Consequently, sprint performance is comparable to that of temperate species over a 9°C range. More significant for the consequences of global warming is exciting new data showing that notothenioids are capable of distinct warm acclimation, rather than just tolerating higher temperatures, which calls into question the dogma that Antarctic fishes are extreme stenotherms. As with these other processes, the principles of adaptation to the cold, dark and relatively quiet world they inhabit should be common to both faunas with respect to neuro/sensory physiology where it is important to distinguish between resistance adaptations (change in tolerance of physiological processes outside of normal limits) and capacitance adaptations (compensatory changes to offset the effects of cold). It appears that nerve conduction velocities are higher than temperate species at a common temperature, but with the trade-off that they fail at relatively low temperature, providing interesting parallels between fishes of high latitudes and deep sea (see vol. 16).
This is an excellent summary of current knowledge written by the acknowledged experts in the field. It will be a valuable resource about the physiology of fishes living at high latitudes for many years, as well as providing a good overview of general topics in fish physiology. With its emphasis on the challenges and adaptations of fishes at high latitudes, it is also timely for those with an interest in the effects of global change in polar regions. The audience will include comparative physiologists, thermobiologists, ichthyologists, and fishery scientists. It is highly recommended.
