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

Abstract

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...

Amphibious fishes: evolution and phenotypic plasticity

“…Gracey, 2008). However, we have found that this is not the case in K. marmoratus (Turko et al, 2014). Here, terrestrial acclimation results in a significant increase in the affinity of Hb for O 2 , which is not observed in hypoxiaacclimated K. marmoratus in water.…”

“…To increase blood flow and facilitate O 2 transfer across respiratory surfaces, including the cutaneous surface, there are rapid circulatory adjustments (Table 3). It is not clear in various amphibious fishes whether these gas exchange organs are primed and ready for aerial respiration, such as in the mudskipper P. schlosseri (Gonzales et al, 2011), or whether angiogenesis occurs in these extrabranchial respiratory surfaces as they acclimate to air exposure, as in the mangrove rivulus K. marmoratus; here, there is evidence of angiogenesis in the bucco-opercular lining, skin and fins after 7 days out of water relative to control fish in water Turko et al, 2014).…”

Rates of hypoxia induction alter mechanisms of O2 uptake and the critical O2 tension of goldfish

“…Most fishes possess mechanisms that enhance O 2 extraction and delivery to tissues as Pw O2 is reduced, such as increased haemoglobin (Hb) synthesis (Gracey et al, 2001) and concentration in the blood (Affonso et al, 2002), increased haematocrit (Lai et al, 2006;Turko et al, 2014), increased Hb-O 2 binding affinity (Turko et al, 2014), increased ventilation frequency and amplitude (Holeton and Randall, 1967;Itazawa and Takeda, 1978;Tzaneva et al, 2011;Vulesevic and Perry, 2006), and a redistribution of blood supply to critical tissues (Sundin et al, 1995). Some fishes, including goldfish and numerous other species, also have the ability to dramatically increase lamellar surface area in response to hypoxia exposure through apoptotic reductions to the inter-lamellar cell mass (ILCM; Anttila et al, 2015;Borowiec et al, 2015;Crispo and Chapman, 2010;Dhillon et al, 2013;Ong et al, 2007;Sollid et al, 2003Sollid et al, , 2005Turko et al, 2012).…”

Amphibious fish jump better on land after acclimation to a terrestrial environment

“…Can short-term acclimation to terrestrial environments also cause reversible plasticity in skeletal muscle and locomotory performance in amphibious fishes? The amphibious mangrove rivulus Kryptolebias marmoratus reversibly remodels respiratory surfaces and blood O 2 transport after a week out of water remaining relatively quiescent (Ong et al, 2007;Turko et al, 2014); however, it is unknown whether locomotory performance is also altered.…”