Antarctic Ectotherms Research Articles

Upper thermal limits and risk of mortality of coastal Antarctic ectotherms

Antarctic marine animals face one of the most extreme thermal environments, characterized by a stable and narrow range of low seawater temperatures. At the same time, the Antarctic marine ecosystems are threatened by accelerated global warming. Determining the upper thermal limits (CTmax) is crucial to project the persistence and distribution areas of the Antarctic marine species. Using thermal death time curves (TDT), we estimated CTmax at different temporal scales from 1 minute to daily and seasonal, the predict vulnerability to the current thermal variation and two potential heatwave scenarios. Our results revealed that CTmax at 1 min are far from the temperature present in the marine intertidal area where our study species, showing Echinoderm species higher CTmax than the Chordata and Arthropods species. Simulations indicated that seasonal thermal variation from the intertidal zone contributed to basal mortality, which increased after considering moderate scenarios of heatwaves (+2°C) in the Shetland Archipelago intertidal zone. Our finding highlighted the relevance of including exposure time explicitly on the CTmax estimates, which deliver closer and more realistic parameters according to the species that may be experiencing in the field.

The biology and ecology of the Antarctic limpet Nacella concinna

Physiological studies suggest that Antarctic marine organisms are adversely affected by rising global temperatures and ocean acidification and have poor prospects for survival. However, according to ecological studies, their vulnerability might be less severe than initially thought. Thus, a realistic forecast of species survival and Antarctic biodiversity should be based on studies from a variety of species under consideration of ecological factors. The limpet Nacella concinna is often found in the rocky intertidal and sublittoral zones of the Antarctic Peninsula and adjacent subantarctic islands. This review summarizes most of the available information on the biology of this limpet, one of the most conspicuous invertebrates of the intertidal zone. There is some evidence that adult N. concinna are physiologically flexible and can acclimate to 3 °C. However, the requirements of the larval stage are poorly known, thus precluding realistic predictions of how elevated temperatures will affect N. concinna populations. Data on physiological performance (righting ability, tenacity and radula rasping rate) under different temperatures could provide a useful baseline for further field investigations on the effects of warming. The species could be used as model organism for investigating the biological effects of ongoing global warming on slow-growing Antarctic ectotherms. Nacella concinna might also be a better biomonitor for polycyclic aromatic hydrocarbons than other Antarctic mollusks.

Blue blood on ice: modulated blood oxygen transport facilitates cold compensation and eurythermy in an Antarctic octopod.

IntroductionThe Antarctic Ocean hosts a rich and diverse fauna despite inhospitable temperatures close to freezing, which require specialist adaptations to sustain animal activity and various underlying body functions. While oxygen transport has been suggested to be key in setting thermal tolerance in warmer climates, this constraint is relaxed in Antarctic fishes and crustaceans, due to high levels of dissolved oxygen. Less is known about how other Antarctic ectotherms cope with temperatures near zero, particularly the more active invertebrates like the abundant octopods. A continued reliance on the highly specialised blood oxygen transport system of cephalopods may concur with functional constraints at cold temperatures. We therefore analysed the octopod’s central oxygen transport component, the blue blood pigment haemocyanin, to unravel strategies that sustain oxygen supply at cold temperatures.ResultsTo identify adaptive compensation of blood oxygen transport in octopods from different climatic regions, we compared haemocyanin oxygen binding properties, oxygen carrying capacities as well as haemolymph protein and ion composition between the Antarctic octopod Pareledone charcoti, the South-east Australian Octopus pallidus and the Mediterranean Eledone moschata. In the Antarctic Pareledone charcoti at 0°C, oxygen unloading by haemocyanin was poor but supported by high levels of dissolved oxygen. However, lower oxygen affinity and higher oxygen carrying capacity compared to warm water octopods, still enabled significant contribution of haemocyanin to oxygen transport at 0°C. At warmer temperatures, haemocyanin of Pareledone charcoti releases most of the bound oxygen, supporting oxygen supply at 10°C. In warm water octopods, increasing oxygen affinities reduce the ability to release oxygen from haemocyanin at colder temperatures. Though, unlike Eledone moschata, Octopus pallidus attenuated this increase below 15°C.ConclusionsAdjustments of haemocyanin physiological function and haemocyanin concentrations but also high dissolved oxygen concentrations support oxygen supply in the Antarctic octopus Pareledone charcoti at near freezing temperatures. Increased oxygen supply by haemocyanin at warmer temperatures supports extended warm tolerance and thus eurythermy of Pareledone charcoti. Limited haemocyanin function towards colder temperatures in Antarctic and warm water octopods highlights the general role of haemocyanin oxygen transport in constraining cold tolerance in octopods.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-015-0097-x) contains supplementary material, which is available to authorized users.

Spatial and temporal variation in the heat tolerance limits of two abundant Southern Ocean invertebrates

While, in lower latitudes, population-level differences in heat tolerance are linked to temperature variability, in the Southern Ocean remarkably stable year-round temperatures prevail. Temporal variation in the physiology of Antarctic ectotherms is therefore thought to be driven by the intense seasonality in primary productivity. Here we tested for differences in the acute upper temperature limits (lethal and activity) of 2 Antarctic marine invertebrates (the omnivorous starfish Odontaster validus and the filter-feeding clam Laternula elliptica) across latitude, seasons and years. Acute thermal responses in the starfish (righting and feeding) and clam (burrowing) differed between populations collected at 77°S (McMurdo Sound) and 67°S (Marguerite Bay). Both species displayed significantly higher temperature performance at 67°S, where seawater can reach a maximum of +1.8°C in summer versus ?0.5°C at 77°S, showing that even the narrow spatial and temporal variation in environmental temperature in Antarctica is biologically meaningful to these stenothermal invertebrates. Temporal comparisons of heat tolerance also demonstrated seasonal differences in acute upper limits for survival that were consistent with physiological acclimatisation: lethal limits were lower in winter than summer and higher in warm years than cool years. However, clams had greater inter-annual variation of temperature limits than was observed for starfish, suggesting that variation in food availability is also an important factor, particularly for primary consumers. Teasing out the interaction of multiple factors on thermal tolerance will be important for refining species-specific predictions of climate change impacts.

Growth in the slow lane: protein metabolism in the Antarctic limpetNacella concinna(Strebel 1908)

Growth rates in Antarctic ectotherms are generally considered to be low in comparison to temperate and tropical species. Food consumption plays a major role in determining animal growth rates, but once food is ingested soft tissue growth rates are largely determined by the protein synthesis retention efficiency (PSRE), a measure of the efficiency with which proteins are synthesised and retained as protein growth. The effect of water temperatures on the PSRE of polar organisms has not previously been investigated, and it is possible that reduced PSRE at polar water temperatures may at least partially explain low growth rates in Antarctic organisms. We also currently lack any information on the potential effects of predicted increases in seawater temperatures on protein metabolism in Antarctic ectotherms. We have measured seasonal protein synthesis, degradation and growth rates in free-ranging Antarctic limpets (Nacella concinna), together with protein synthesis rates at temperatures ranging between -1.5 degrees C and 6.0 degrees C. PSRE were not significantly different in summer (15.69+/-4.41%) or winter (20.59+/-4.45%), but values were considerably lower than those previously reported in temperate and tropical species. A meta-analysis of published ectotherm PSRE suggested there was a positive relationship with temperature (y=449.9-114.9x, r(2)=28.8%, P<0.05). In turn, this suggests that temperature may be an important factor in determining ectotherm growth efficiency via an influence on PSRE. Maximal fractional and absolute protein synthesis rates occurred at approximately 1 degrees C in N. concinna, the approximate summer water temperature at the study site, and protein synthesis rates decreased above this temperature. In the absence of adaptation, predicted increases in Antarctic water temperatures would result in reduced, rather than increased, rates of protein synthesis and, in turn, possibly growth.

Thermal limits and adaptation in marine Antarctic ectotherms: an integrative view

A cause and effect understanding of thermal limitation and adaptation at various levels of biological organization is crucial in the elaboration of how the Antarctic climate has shaped the functional properties of extant Antarctic fauna. At the same time, this understanding requires an integrative view of how the various levels of biological organization may be intertwined. At all levels analysed, the functional specialization to permanently low temperatures implies reduced tolerance of high temperatures, as a trade-off. Maintenance of membrane fluidity, enzyme kinetic properties (Km and k(cat)) and protein structural flexibility in the cold supports metabolic flux and regulation as well as cellular functioning overall. Gene expression patterns and, even more so, loss of genetic information, especially for myoglobin (Mb) and haemoglobin (Hb) in notothenioid fishes, reflect the specialization of Antarctic organisms to a narrow range of low temperatures. The loss of Mb and Hb in icefish, together with enhanced lipid membrane densities (e.g. higher concentrations of mitochondria), becomes explicable by the exploitation of high oxygen solubility at low metabolic rates in the cold, where an enhanced fraction of oxygen supply occurs through diffusive oxygen flux. Conversely, limited oxygen supply to tissues upon warming is an early cause of functional limitation. Low standard metabolic rates may be linked to extreme stenothermy. The evolutionary forces causing low metabolic rates as a uniform character of life in Antarctic ectothermal animals may be linked to the requirement for high energetic efficiency as required to support higher organismic functioning in the cold. This requirement may result from partial compensation for the thermal limitation of growth, while other functions like hatching, development, reproduction and ageing are largely delayed. As a perspective, the integrative approach suggests that the patterns of oxygen- and capacity-limited thermal tolerance are linked, on one hand, with the capacity and design of molecules and membranes, and, on the other hand, with life-history consequences and lifestyles typically seen in the permanent cold. Future research needs to address the detailed aspects of these interrelationships.

Climate-dependent evolution of Antarctic ectotherms: An integrative analysis

Abstract The paper explores the climate-dependent evolution of marine Antarctic fauna and tries to identify key mechanisms involved as well as the driving forces that have caused the physiological and life history characteristics observed today. In an integrative approach it uses the recent concept of oxygen and capacity limited thermal tolerance to identify potential links between molecular, cellular, whole-organism, and ecological characteristics of marine animal life in the Antarctic. As a generalized pattern, minimization of baseline energy costs, for the sake of maximized growth in the cold, appears as one over-arching principle shaping the evolution and functioning of Antarctic marine ectotherms. This conclusion is supported by recent comparisons with (sub-) Arctic ectotherms, where elevated levels of energy turnover result at unstable, including cold temperatures, and are related to wide windows of thermal tolerance and associated metabolic features. At biochemical levels, metabolic regulation at low temperatures in general, is supported by the cold compensation of enzyme kinetic parameters like substrate affinities and turnover numbers, through minute structural modifications of the enzyme molecule. These involve a shift in protein folding, sometimes supported by the replacement of individual amino acids. The hypothesis is developed that efficient metabolic regulation at low rates in Antarctic marine stenotherms occurs through high mitochondrial densities at low capacities and possibly enhanced levels of Arrhenius activation energies or activation enthalpies. This contrasts the more costly patterns of metabolic regulation at elevated rates in cold-adapted eurytherms. Energy savings in Antarctic ectotherms, largely exemplified in fish, typically involve low-cost, diffusive oxygen distribution due to high density of lipid membranes, loss of haemoglobin, myoglobin and the heat shock response, reduced anaerobic capacity, large myocytes with low ion exchange activities, and the use of lipid body stores for neutral buoyancy. Important trade-offs result from obligatory energy savings in the permanent cold: low metabolic rates support cold-compensated growth but imply narrow windows of thermal tolerance and reduced scopes for activity. The degree of thermal specialization is not uniformly defined by cold temperature but varies with life style characteristics and activity levels and associated aerobic scope. Trade-offs for the sake of cold compensated growth parallel reduced capacities for exercise performance, exacerbated by the effect of high haemolymph magnesium levels in crustaceans and, possibly, other invertebrates. High magnesium levels likely exclude the group of reptant decapod crustaceans from Antarctic waters below 0 °C. The hypothesis is developed that energy savings imposed by the permanent cold bear specific life history consequences. Due to effects of allometry, energy savings are exacerbated at small body size, favouring passive lecithotrophic larvae. At all stages of life history, reduced energy turnover for the sake of growth causes delays and low rates in other higher functions, with the result of late maturity, fecundity and offspring release, as well as extended development. As a consequence, extended life spans evolved due to life history requirements. At the same time, polar gigantism is enabled by a combination of elevated oxygen levels in cold waters, of reduced metabolism and of extended periods of growth at slow developmental rates.

How does oxidative stress relate to thermal tolerance in the Antarctic bivalve Yoldia eightsi?

Short and long-term exposure to elevated temperatures were studied in the Antarctic stenothermal protobranch bivalve Yoldia eightsi (Courthouy) from Potter Cove, King George Island (South Shetland Islands, Antarctica). Above a breakpoint temperature of 2°C – the upper habitat temperature for the Potter Cove Y. eightsi stock – both routine (RMR) and standard metabolic rate (SMR) increased steeply. The fraction of metabolism allocated to SMR, as well as the number of intervals of elevated activity per hour increased significantly with temperature. During acute exposure, ATP concentrations in the foot muscle peaked at 2°C and fell at 5°C, whereas superoxide dismutase (SOD) activity decreased upon warming. Slow stepwise warming to a final temperature of 11°C resulted in a significant decrease of SOD activity. Malondialdehyde concentration increased compared with controls at 0°C. In contrast to the effect of short-term exposure, tissue adenylate concentrations displayed a mild increase at higher temperatures during slow warming, indicating an acclimation response. A switch to anaerobic energy production could not be observed up to 11°C, demonstrating a higher level of thermal tolerance than in other Antarctic ectotherms, or a failure of the relevant pathways in Y. eightsi. The imbalance between pro- and antioxidant processes upon warming indicate oxidative stress to be one feature accompanying early heat stress in Y. eightsi.

Estudo do metabolismo de rotina e excreção de amônia do antípoda antártico Waldeclàa obesa em duas temperaturas distintas

Realizaram-se estimativas, a 0ºC e a 3ºC, do consumo médio e específico de oxigênio e da excreção média e específica de amónia de anfípodas antárticos da espécie Waldeckia obesa, coletados na Baía do Almirantado, Ilha Rei George, Antártica. Os experimentos foram realizados na Estação Antártica Brasileira "Comandante Ferraz" e no Laboratório de Ecologia Polar do Instituto Oceanográfico da Universidade de São Paulo. Foram empregados animais entre 120 mg a 620 mg e entre 40 mg e 690 mg de peso úmido, nos experimentos a 0ºC e a 3ºC, respectivamente. Dentro dessas faixas de peso, o consumo médio de oxigênio, a 0ºC, variou de 2,22µl/h a 10,81µl/h e o específico de 0,011µl/mg/h a 0,018µl/mg/h. A 3ºC, o consumo médio de oxigênio variou de 1,83µl/h a 14,19µl/h e o específico de 0,033µl/mg/h a 0,022µl/mg/h. O Q10, calculado a partir das médias das classes, foi de 6,95. Por sua vez, a excreção média de amónia, a 0ºC, variou de 13,84 ng.at/h a 55,34 ng.at/h e a específica entre 0,090 ng.at/mg/h a 0,042 ng.at/mg/h. A 3ºC, a excreção média de amónia variou de 5,11 ng.at/h a 38,33 ng.at/h e a específica de 0,088 ng.at/mg/h a 0,059 ng.at/mg/h. A relação 0:N indica que uma mistura de proteínas e lipídios é utilizada como substrato para o catabolismo. A 3ºC, entretanto, há uma tendência a aumentar a contribuição dos lipídios nesse substrato. O consumo de oxigênio de Waldeckia obesa é bastante baixo estando de acordo com os valores encontrados, a 0ºC, por outros autores. Esses dados, juntamente com resultados recentes encontrados na literatura, indicam a fragilidade da hipótese de "adaptação metabólica ao frio", que supõe terem os animais marinhos ectotérmicos antárticos taxas metabólicas elevadas, como resposta adaptativa às baixas temperaturas. Os dados de consumo de oxigênio e excreção de amónia fornecem material básico para extrapolação a parâmetros populacionais, fornecendo subsídios para a avaliação do papel ecológico desses animais no ecossistema em que vivem.