Abstract
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.
Highlights
The 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
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 a common temperature of 10°C the haemocyanin of the Antarctic octopod Pareledone charcoti displayed a lower affinity for oxygen than haemocyanin of the South-east Australian Octopus pallidus and the Mediterranean Eledone moschata, reflected in a 1.4- or 4.2-fold higher P50 (PO2 at which haemocyanin reaches half-maximum saturation with oxygen (50%)), respectively (Figure 2A, Table 1)
Summary
The 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. Cold temperatures may hamper oxygen supply by lowered diffusion across tissue and cellular boundaries, increased viscosity [10] and often a decreased ability of blood pigments like vertebrate haemoglobin or cephalopod haemocyanin to release oxygen to tissues as the pigment’s affinity for oxygen increases [11,12,13]. Antarctic fishes cope with these challenges by increased mitochondrial and membrane densities supporting diffusion [10], loss of blood cells reducing blood viscosity [14] or lowered oxygen affinity sustaining oxygen transport by their haemoglobins [15,16,17]. Little is known whether Antarctic ectotherms other than fish evolved comparable physiological adaptations to sustain oxygen supply in the cold
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