| Summary: | The evolution of the Antarctic notothenioid fishes in the chronically cold waters of the Southern Ocean has resulted in a remarkably narrow thermal tolerance shared among most extant species. While most of these fishes have the capacity to accommodate the physiological challenges of low temperature, they show a greatly reduced tolerance to heat relative to fishes native to warmer waters. Though predominantly distributed in the Southern Ocean, today the Antarctic notothenioids are largely divided by their geographic distributions between three regionally endemic ichthyofaunas in the high-latitude High Antarctic Zone (HAZ), the lower-latitude Seasonal Pack-ice Zone, and cold-temperate waters of southern South America and the South Island of New Zealand. However, the extent to which regional differences in ice abundance and temperature affect the thermal tolerance of their endemic fishes is poorly understood. Within the Southern Ocean the Antarctic notothenioids are largely split between the constantly freezing High-Antarctic Zone (HAZ) and the more thermally variable Seasonal pack-Ice Zone (SPZ). For these fishes, the lower boundary of their thermal tolerance is effectively determined by their capacity for freeze avoidance and limited by their circulating levels of antifreeze proteins (AFPs). To investigate the differences in freeze avoidance between these regions’ endemic ichthyofaunas blood serum freezing points were measured in 11 of the 14 species of the Antarctic icefishes (family Channichthyidae). While the icefishes are a small monophyletic group within the suborder Notothenioidei, they mirror the larger group’s divisions in geographic distribution and lifestyle making this family a useful system for understanding the larger group. Within this family, blood serum freezing point was negatively correlated with the latitude of species’ geographic distributions with the three SPZ species showing the highest freezing points. Either equal to or higher than the freezing point of seawater, these serum freezing points left the SPZ species with insufficient protection from freezing to survive in the ice-laden waters inhabited by the HAZ species. When the contributions to freeze avoidance of serum osmolytes, antifreeze glycoproteins (AFGPs), and the antifreeze potentiating protein was assessed, the higher freeze avoidance of high-latitude HAZ icefishes was found to result predominantly from increasing antifreeze activity from the AFGPs. The reduced severity of some SPZ habitats which allows the survival of species with high freezing points may also be reflected in the development of notothenioid freeze avoidance during ontogeny. While prior work on larval Gymnodraco acuticeps has shown that HAZ notothenioids can reach adult levels of serum antifreeze activity within months of hatching, antifreeze activity has never been previously studied in any of the SPZ species. To do so, I investigated the freeze avoidance in juveniles of the high freezing point SPZ icefish Chaenocephalus aceratus which had the highest serum freezing point among the adult Antarctic icefishes. These maintained sub-adult levels of serum antifreeze activity through the 2+ year class, which were the oldest collected, and if the observed rate of increase was sustained they would not attain adult levels of antifreeze activity until 4.2 years after hatching. Though most of the Antarctic notothenioids share low freezing points, the absence of selection for heat tolerance in the chronically cold Southern Ocean has over evolutionary time resulted in their modern limited heat tolerance. To determine whether differences in environmental temperature between the HAZ and SPZ are also correlated with the heat tolerance of regionally endemic fishes, the critical thermal maximum (CTMax) was determined in 11 species of Antarctic fishes including six from the HAZ and five from the SPZ. Like freeze avoidance, heat tolerance among the Antarctic fishes could be separated according to their geographic distribution with the CTMaxs of five of the HAZ species significantly below those of the SPZ species when acclimatized to their natural freezing water temperatures. However, while these shared low heat tolerances in the eight species available in numbers allowing further study, all retained plasticity in their heat tolerance with significant and often proportionally large increases in CTMax following warm acclimation to 4°C. The Antarctic notothenioids also include at least 16 secondarily temperate species with origins in Antarctic waters but that are now permanent residents of the warmer waters around New Zealand and South America. Presumably these once shared the limited heat tolerance found currently among endemic Antarctic fishes however, it is not known whether this polar trait continues to exert an influence on their modern heat tolerance. To investigate, I determined the CTMax in two species of New Zealand notothenioids, the secondarily temperate N. angustata and the basal thorn fish Bovichtus variegatus that does not share the former’s evolutionary origins in polar waters but which inhabits a similar modern thermal environment. While N. angustata had significantly higher heat tolerance than its endemic Antarctic congener N. coriiceps, it showed significantly lower heat tolerance than B. variegatus, suggesting the continued presence of its presumed ancestral loss of heat tolerance. These studies showed species’ levels of freeze avoidance and heat tolerance are not homogeneous throughout the Antarctic notothenioids, but reflect regional differences even within the Southern Ocean where water temperatures range only between -1.9 and 3°C. Freeze avoidance was lowest among species restricted to the more northerly waters of the SPZ where they presumably survive in the perennially ice free waters found within this region, but which also likely limits their distributions to waters outside the more severe HAZ. The relaxed selection for freeze avoidance in some SPZ waters also allows for the slow onset of adult antifreeze activity in at least one species of icefish, C. aceratus. Similarly, while the Antarctic notothenioids largely share low heat tolerances when acclimatized to their natural freezing water temperatures, these show notable regional variation and a surprisingly high level of plasticity in response to warm acclimation. However, the comparably limited levels of heat tolerance in the secondarily temperate nototheniid, N. angustata, suggests that there may be substantial retention of its ancestral low heat tolerance which may impairing the Antarctic notothenioid’s ability to adapt to the rising water temperatures predicted from global climate change.
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