Acclimation and thermal tolerance in Antarctic marine ectotherms

Abstract

Antarctic marine species have evolved in one of the coldest and most temperature-stable marine environments on Earth. They have long been classified as being stenothermal, or having a poor capacity to resist warming. Here we show that their ability to acclimate their physiology to elevated temperatures is poor compared with species from temperate latitudes, and similar to those from the tropics. Those species that have been demonstrated to acclimate take a very long time to do so, with Antarctic fish requiring up to 21-36 days to acclimate, which is 2-4 times as long as temperate species, and invertebrates requiring between 2 and 5 months to complete wholeanimal acclimation. Investigations of upper thermal tolerance (CT max ) in Antarctic marine species have shown that as the rate of warming is reduced in experiments, CT max declines markedly, ranging from 8 to 17.5°C across 13 species at a rate of warming of 1°C day, and from 1 to 6°C at a rate of 1°C month −1 . This effect of the rate of warming on CT max also appears to be present at all latitudes. A macrophysiological analysis of long-term CT max across latitudes for marine benthic groups showed that both Antarctic and tropical species were less resistant to elevated temperatures in experiments and thus had lower warming allowances (measured as the difference between long-term CT max and experienced environmental temperature), or warming resistance, than temperate species. This makes them more at risk from warming than species from intermediate latitudes. This suggests that the variability of environmental temperature may be a major factor in dictating an organism's responses to environmental change.

Can acclimation of thermal tolerance, in adults and across generations, act as a buffer against climate change in tropical marine ectotherms?

“…Whilst geographic patterns of acute thermal tolerance have been most widely studied ), acclimation capacity (Deutsch et al, 2008;Sunday et al, 2011;Sunday et al, 2014), the capacity of physiological systems to adjust to a new stable state in response to an altered environment (Somero, 2012) will likely be an important moderator of these patterns (Bozinovic et al, 2011;Peck et al, 2014). This increase in functionality can be measured at the biochemical level or at the level of the whole animal, in the form of an increased temperature tolerance (Fry et al, 1942).…”

“…A higher ARR indicates that a species has a greater capacity to shift physiological pathways in response to incubation temperature. In response to predictable warming, acclimation can provide an important buffer, improving the chances of species persisting in altered environments (Anderson et al, 2012;Barrett and Hendry, 2012;Bell, 2013;Charmantier et al, 2008;Hendry et al, 2011;Peck et al, 2014;Somero, 2012), resulting in improved physiological fitness of their progeny (Burgess and Marshall, 2011;Shama et al, 2014) through non-genetic inheritance, allowing more time for evolution to occur (Chevin and Lande, 2010;Somero, 2010).…”

“…While acclimation capacity in tropical marine ectotherms may be reduced compared to mid latitude species (Peck et al, 2014) and can therefore be considered less resilient to climate change, many tropical species have shorter generation times, thus possessing a greater potential for adaptive change than higher latitude species (Peck, 2011).…”

Antarctic notothenioid fish: what are the future consequences of ‘losses’ and ‘gains’ acquired during long-term evolution at cold and stable temperatures?

“…The oceanic environment has been heavily impacted as temperatures of the Upper Circumpolar Deep Water of the ACC have risen 0.17°C from the 1950s to the 1980s, and surface seawater temperatures have increased by 1°C over the past 50 years and are predicted to rise another 2°C in the coming century (Meredith and King, 2005;Murphy and Mitchell, 2005;Clarke et al, 2007). Needless to say, there has been considerable interest in how these rising temperatures will impact marine fauna (Pörtner et al, 2007;Somero, 2010;Patarnello et al, 2011;O'Brien and Crockett, 2013;Peck et al, 2014). Thus, we now consider how the highly specialized thermal adaptations of notothenioids might influence their vulnerability status and overall fitness in the context of global warming.…”

“…By no means are we the first to ponder the fate of notothenioids in a warming world. Climate change impact studies on Antarctic fauna have been ongoing for many years and a number of studies and reviews have addressed the topic (for reviews, see Coppes Petricorena and Somero, 2007;Pörtner et al, 2007;Somero, 2010;Patarnello et al, 2011;O'Brien and Crockett, 2013;Peck et al, 2014). Considering the current trends in increasing temperatures, in particular the rapid changes occurring in the Southern Ocean, examining the underlying physiological and biochemical mechanisms of thermal adaptation of notothenioids can help to better assess the vulnerability of these fishes to warming oceans (Somero, 2010).…”