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

Oellermann M, Lieb B, Pörtner HO, Semmens JM, Mark FC - Front. Zool. (2015)

Bottom Line: To 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.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.In warm water octopods, increasing oxygen affinities reduce the ability to release oxygen from haemocyanin at colder temperatures.

View Article: PubMed Central - PubMed

Affiliation: Alfred-Wegener-Institute Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany.

ABSTRACT

Introduction: 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. 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.

Results: To 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.

Conclusions: Adjustments 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.

No MeSH data available.


Related in: MedlinePlus

pH at which the pH-dependent release of oxygen by haemocyanin becomes maximal. Comparison between the Antarctic Pareledone charcoti, the South-east Australian Octopus pallidus and the Mediterranean Eledone moschata at an experimental temperature of 10°C. Calculations include pH oxygen-saturation curves from all analysed PO2. Letters indicate significant differences (P < 0.05) between species. Data from different PO2 were pooled due to similar effects by PO2 among species.
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Fig6: pH at which the pH-dependent release of oxygen by haemocyanin becomes maximal. Comparison between the Antarctic Pareledone charcoti, the South-east Australian Octopus pallidus and the Mediterranean Eledone moschata at an experimental temperature of 10°C. Calculations include pH oxygen-saturation curves from all analysed PO2. Letters indicate significant differences (P < 0.05) between species. Data from different PO2 were pooled due to similar effects by PO2 among species.

Mentions: Haemocyanin of Pareledone charcoti showed the lowest venous oxygen saturation at a common temperature of 10°C, at a venous PO2 of 1 kPa and a venous pH of 7.27 (Figure 2B). At 10°C the Antarctic haemocyanin thus has the potential to release far more oxygen (on average 76.7%, 95% CI 68.6% to 84.8%) upon each cycle than the warm-water octopods Octopus pallidus (33.0%, 5.0-60.9) and Eledone moschata (29.8%, 9.9-49.7, Figure 3C, D, G, Figure 4A). This is mostly due to an increased pH dependent release of oxygen by haemocyanin in Pareledone charcoti (Figure 3C, D, G), with maxima occurring 0.16 or 0.25 pH values above those of Octopus pallidus or Eledone moschata respectively (Figure 6).Figure 6


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

Oellermann M, Lieb B, Pörtner HO, Semmens JM, Mark FC - Front. Zool. (2015)

pH at which the pH-dependent release of oxygen by haemocyanin becomes maximal. Comparison between the Antarctic Pareledone charcoti, the South-east Australian Octopus pallidus and the Mediterranean Eledone moschata at an experimental temperature of 10°C. Calculations include pH oxygen-saturation curves from all analysed PO2. Letters indicate significant differences (P < 0.05) between species. Data from different PO2 were pooled due to similar effects by PO2 among species.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4403823&req=5

Fig6: pH at which the pH-dependent release of oxygen by haemocyanin becomes maximal. Comparison between the Antarctic Pareledone charcoti, the South-east Australian Octopus pallidus and the Mediterranean Eledone moschata at an experimental temperature of 10°C. Calculations include pH oxygen-saturation curves from all analysed PO2. Letters indicate significant differences (P < 0.05) between species. Data from different PO2 were pooled due to similar effects by PO2 among species.
Mentions: Haemocyanin of Pareledone charcoti showed the lowest venous oxygen saturation at a common temperature of 10°C, at a venous PO2 of 1 kPa and a venous pH of 7.27 (Figure 2B). At 10°C the Antarctic haemocyanin thus has the potential to release far more oxygen (on average 76.7%, 95% CI 68.6% to 84.8%) upon each cycle than the warm-water octopods Octopus pallidus (33.0%, 5.0-60.9) and Eledone moschata (29.8%, 9.9-49.7, Figure 3C, D, G, Figure 4A). This is mostly due to an increased pH dependent release of oxygen by haemocyanin in Pareledone charcoti (Figure 3C, D, G), with maxima occurring 0.16 or 0.25 pH values above those of Octopus pallidus or Eledone moschata respectively (Figure 6).Figure 6

Bottom Line: To 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.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.In warm water octopods, increasing oxygen affinities reduce the ability to release oxygen from haemocyanin at colder temperatures.

View Article: PubMed Central - PubMed

Affiliation: Alfred-Wegener-Institute Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany.

ABSTRACT

Introduction: 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. 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.

Results: To 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.

Conclusions: Adjustments 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.

No MeSH data available.


Related in: MedlinePlus