The Potential Role of Hypercarbia in the Transition from Water-Breathing to Air-Breathing in Vertebrates

Ultsch, Gordon R.

doi:10.2307/2409152

Cited by 22 publications

(20 citation statements)

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“…Circumstantial observations indicate higher sensitivity to hypocapnia of fauna living in marine sediments as compared to epibenthic or pelagic fauna. This line of thought is also supported by shifting CO 2 windows during evolution of air breathing ectotherms from water breathers (Ultsch 1987) and furthermore of endotherms from ectotherms.…”

Section: Physiological Principles Of Co 2 Vs Temperature Effects On mentioning

confidence: 69%

Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view

Pörtner

2008

Mar. Ecol. Prog. Ser.

733

542

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The oceans cover 70% of the earth's surface. Due to their large volume and the ability of seawater to buffer CO 2 , oceans have absorbed approximately half of all anthropogenic CO 2 emissions to the atmosphere, which amounts to more than 120 Gt C in total or 440 Gt CO 2 (Sabine et al. 2004) within the last 200 yr. CO 2 produced by human activities penetrates into the surface layers of the ocean and is transported by ocean currents to deeper waters. At present, the oceans take up about 2 of the 6 Gt C per annum from human activity. In this context, the contribution of ocean biology to CO 2 uptake is similarly large as that of the terrestrial biosphere. However, the ability of the ocean to take up CO 2 decreases with increasing atmospheric CO 2 concentrations due to the reduced buffering ability of seawater as CO 2 accumulates. The present increase in CO 2 levels in the atmosphere is approximately 100-fold faster than at the end of the last ice ages when CO 2 levels rose by about 80 ppm over 6000 yr (IPCC 2001(IPCC , 2007. Now exceeding 380 ppm, the present CO 2 content is the highest in the atmosphere for the last 420 000 and possibly more than 10 million yr (IPCC 2001(IPCC , 2007 ABSTRACT: Ocean warming and acidification occur at global scales and, in the case of temperature, have already caused shifts in marine ecosystem composition and function. In the case of CO 2 -induced ocean hypercapnia and acidification, however, effects may still be so small that evidence for changes in the field is largely lacking. Future scenarios indicate that marine life forms are threatened by the specific or synergistic effects of factors involved in these processes. The present paper builds on the view that development of a cause and effect understanding is required beyond empirical observations, for a more accurate projection of ecosystem effects and for quantitative scenarios. Identification of the mechanisms through which temperature-and CO 2 -related ocean physicochemistry affect organism fitness, survival and success, is crucial with this research strategy. I suggest operation of unifying physiological principles, not only of temperature but also CO 2 effects, across animal groups and phyla. Thermal windows of optimized performance emerge as a basic character defining species fitness and survival, including their capacity to interact with other species. Through effects on performance at the level of reproduction, behaviour and growth, ocean acidification acts especially on lower marine invertebrates, which are characterized by a low capacity to compensate for disturbances in extracellular ion and acid -base status and sensitivity of metabolism to such disturbances. Available data suggest that one key consequence of these features is a narrowing of thermal tolerance windows, as well as a reduced scope for performance at ecosystem level. These changes in bioenvelopes may have major implications for the ranges of geographical distribution of these organisms and in species interactions.

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Section: Physiological Principles Of Co 2 Vs Temperature Effects On mentioning

confidence: 69%

Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view

Pörtner

2008

Mar. Ecol. Prog. Ser.

733

542

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“…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 air versus water, can also impair the ability of hemoglobin (Hb) to bind and transport O 2 (Rahn, 1966;Ultsch, 1987). High blood partial pressure of CO 2 (P CO 2 ) may reduce intraerythrocytic pH and reduce the affinity of Hb for O 2 by the Bohr effect, which prevents O 2 loading at the gas-exchange surface (Bohr et al, 1904).…”

Section: Received 4 July 2014; Accepted 15 September 2014mentioning

confidence: 99%

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

Turko

Robertson

Bianchini

et al. 2014

Journal of Experimental Biology

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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...

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“…P. hypophthalmus inhabits tropical freshwater plains within the Mekong River Delta in South-East Asia. Such ecosystems are characterized by frequent high organic loading resulting in combined hypoxia and hypercapnia with Pw CO2 reaching 65 mmHg (Furch and Junk, 1997;Ultsch, 1987;Willmer, 1934). Furthermore, it is farmed extensively in severely hypoxic (Lefevre et al, 2011b) and hypercapnic (this study) water throughout South-East Asia.…”

Section: Introductionmentioning

confidence: 99%

High capacity for extracellular acid-base regulation in the air-breathing fishPangasianodon hypophthalmus

Damsgaard

Gam

Tuong

et al. 2015

Journal of Experimental Biology

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The evolution of accessory air-breathing structures is typically associated with reduction of the gills, although branchial ion transport remains pivotal for acid-base and ion regulation. Therefore, airbreathing fishes are believed to have a low capacity for extracellular pH regulation during a respiratory acidosis. In the present study, we investigated acid-base regulation during hypercapnia in the airbreathing fish Pangasianodon hypophthalmus in normoxic and hypoxic water at 28-30°C. Contrary to previous studies, we show that this air-breathing fish has a pronounced ability to regulate extracellular pH (pH e ) during hypercapnia, with complete metabolic compensation of pH e within 72 h of exposure to hypoxic hypercapnia with CO 2 levels above 34 mmHg. The high capacity for pH e regulation relies on a pronounced ability to increase levels of HCO 3 − in the plasma. Our study illustrates the diversity in the physiology of air-breathing fishes, such that generalizations across phylogenies may be difficult.

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The Potential Role of Hypercarbia in the Transition from Water-Breathing to Air-Breathing in Vertebrates

Cited by 22 publications

References 10 publications

Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view

Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view

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

High capacity for extracellular acid-base regulation in the air-breathing fishPangasianodon hypophthalmus

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