Temperature-induced changes in the oxygen equilibrium curve of the blood of the brown bullhead, Ictalurus nebulosus

Despite the abundance of oxygen in atmospheric air relative to water, the initial loss of respiratory surface area and accumulation of carbon dioxide in the blood of amphibious fishes during emersion may result in hypoxemia. Given that the ability to respond to low oxygen conditions predates the vertebrate invasion of land, we hypothesized that amphibious fishes maintain O 2 uptake and transport while emersed by mounting a co-opted hypoxia response. We acclimated the amphibious fish Kryptolebias marmoratus, which are able to remain active for weeks in both air and water, for 7 days to normoxic brackish water (15‰, ~21 kPa O 2 ; control), aquatic hypoxia (~3.6 kPa), normoxic air (~21 kPa) or aerial hypoxia (~13.6 kPa). Angiogenesis in the skin and bucco-opercular chamber was pronounced in air-versus water-acclimated fish, but not in response to hypoxia. Aquatic hypoxia increased the O 2 -carrying capacity of blood via a large (40%) increase in red blood cell density and a small increase in the affinity of hemoglobin for O 2 (P 50 decreased 11%). In contrast, air exposure increased the hemoglobin O 2 affinity (decreased P 50 ) by 25% without affecting the number of red blood cells. Acclimation to aerial hypoxia both increased the O 2 -carrying capacity and decreased the hemoglobin O 2 affinity . These results suggest that O 2 transport is regulated both by O 2 availability and also, independently, by air exposure. The ability of the hematological system to respond to air exposure independent of O 2 availability may allow extant amphibious fishes, and may also have allowed primitive tetrapods to cope with the complex challenges of aerial respiration during the invasion of land.KEY WORDS: Hemoglobin, Oxygen-carrying capacity, Hemoglobin-oxygen affinity, Air-breathing organ, Air-breathing fish, Mangrove rivulus INTRODUCTIONThe transition from aquatic to terrestrial life represents a major step in vertebrate evolution because the physical conditions between these environments are dramatically different. Oxygen solubility is relatively low in water and even well-oxygenated aquatic environments contain only about 3% of the O 2 available in atmospheric air (Dejours, 1988). Low concentrations of aquatic O 2 , particularly in hypoxic habitats, have often been hypothesized to be one of the driving forces behind the evolution of amphibious or terrestrial life histories because invasion of land would allow animals to exploit the O 2 -rich aerial environment (Graham, 1997). RESEARCH ARTICLEDepartment of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada.*Author for correspondence (aturko@uoguelph.ca) Received 4 July 2014; Accepted 15 September 2014Taking advantage of aerial O 2 presents several challenges for fishes. Water-breathing fishes exchange respiratory gases across the gills but during emersion the gill lamellae typically collapse and coalesce, reducing the surface area available for respiration. Accumulation of CO 2 in the blood of emersed fishes, resulting from the low solubility of CO 2 in...

Section: Research Articlementioning

confidence: 99%

mentioning

confidence: 99%

The amphibious fishKryptolebias marmoratususes alternate strategies to maintain oxygen delivery during aquatic hypoxia and air exposure

Turko

Robertson

Bianchini

et al. 2014

“…Greater oxygen uptake at a given P O 2 can be achieved by increasing haematocrit, haemoglobin concentration or erythrocyte number (Weber et al, 1976;Fernandes et al, 1999), blood oxygen affinity (i.e. decreased blood P 50 ) (Grigg, 1969;Weber et al, 1976;Albers et al, 1983;Andersen et al, 2009) or respiratory surface area (Sollid et al, 2005;Tzaneva et al, 2011;Nilsson et al, 2012). The Alaska blackfish does not appear to adopt any of these mechanisms.…”

Section: Research Articlementioning

confidence: 99%

Air breathing in the Arctic: influence of temperature, hypoxia, activity and restricted air access on respiratory physiology of Alaska blackfish (Dallia pectoralis)

Lefevre

Damsgaard

Pascale

et al. 2014

The Alaska blackfish (Dallia pectoralis) is an air-breathing fish native to Alaska and the Bering Sea islands, where it inhabits lakes that are ice-covered in the winter, but enters warm and hypoxic waters in the summer to forage and reproduce. To understand the respiratory physiology of this species under these conditions and the selective pressures that maintain the ability to breathe air, we acclimated fish to 5°C and 15°C and used respirometry to measure: standard oxygen uptake (Ṁ O2 ) in normoxia (19.8 kPa P O2 ) and hypoxia (2.5 kPa), with and without access to air; partitioning of standard Ṁ O2 in normoxia and hypoxia; maximum Ṁ O2 and partitioning after exercise; and critical oxygen tension (P crit ). Additionally, the effects of temperature acclimation on haematocrit, haemoglobin oxygen affinity and gill morphology were assessed. Standard Ṁ O2 was higher, but air breathing was not increased, at 15°C or after exercise at both temperatures. Fish acclimated to 5°C or 15°C increased air breathing to compensate and fully maintain standard Ṁ O2 in hypoxia. Fish were able to maintain Ṁ O2 through aquatic respiration when air was denied in normoxia, but when air was denied in hypoxia, standard Ṁ O2 was reduced by ~30-50%. P crit was relatively high (5 kPa) and there were no differences in P crit , gill morphology, haematocrit or haemoglobin oxygen affinity at the two temperatures. Therefore, Alaska blackfish depends on air breathing in hypoxia and additional mechanisms must thus be utilised to survive hypoxic submergence during the winter, such as hypoxia-induced enhancement in the capacities for carrying and binding blood oxygen, behavioural avoidance of hypoxia and suppression of metabolic rate.

“…It should be borne in mind that these interspecific specializations (decreased temperature sensitivity resulting from structural differences in the Hb molecules that increase effector interaction) are distinct from the decreases in temperature sensitivity seen in temperature-acclimated fish that result from downregulation of red cell effector levels at high temperatures (cf. Grigg, 1969).…”

Section: Biological Implicationsmentioning

confidence: 99%

ATP-induced temperature independence of hemoglobin–O2 affinity in heterothermic billfish

Weber

Campbell

Fago

et al. 2010

SUMMARYThe inverse relationship between temperature and hemoglobin-O 2 affinity resulting from the exothermic nature of heme oxygenation favors O 2 unloading from blood to warm, metabolically active tissues. However, this temperature sensitivity is maladaptive, and commonly countered in regional heterotherms, where it may hamper unloading (e.g. in cold extremities of arctic mammals) or increase the diffusive arterio-venous short-circuiting of O 2 (e.g. in counter-current heat exchangers of warm swimming muscles of tuna). We hypothesized analogous blood specializations in heterothermic billfish, whose warm eyes and brains increase the temporal resolution of vision, and measured hemoglobin-O 2 binding properties in three species over a wide pH range, at two temperatures, and in the absence and presence of the major red cell effector, ATP, permitting detailed assessment of overall oxygenation enthalpies (⌬HЈ) and contributions from oxygenation-linked proton and ATP dissociation. . Thus in addition to allosterically modulating hemoglobin-O 2 affinity, ATP diminishes its temperature sensitivity, reducing deleterious arterio-venous short-circuiting of oxygen in the cranial billfish heat exchangers. The mechanism underlying this reduction in oxygenation enthalpy differs fundamentally from that in tuna, supporting independent evolution of this trait in these scombroid lineages.