Gas Exchange and Control of Respiration in Air-Breathing Teleost Fish

Glass, Mogens L.; Rantin, Francisco Tadeu

doi:10.1007/978-3-540-93985-6_5

Cited by 15 publications

(13 citation statements)

References 73 publications

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“…Both have a physostomous swimbladder, but in the jeju the anterior portion of the posterior chamber is heavily vascularized (red in colour) whereas in the traira, the whole swimbladder is poorly vascularized (uniformly white in colour). Facultative air-breathing using the swimbladder is well documented in the jeju (Kramer 1978;Farrell and Randall 1978;Randall et al 1978;Stevens and Holeton 1978;Juca-Chagas 2004;Oliveira et al 2004;Perry et al 2004;McKenzie et al 2007;Lopes et al 2010), but has never been reported in the traira (Rantin et al 1992;Val and Almeida-Val 1995;Glass and Rantin 2009). In a companion behavioural study (Pelster et al submitted), we have confirmed this complete lack of air-breathing in the traira, even under intense hypoxia.…”

Section: Introductionsupporting

confidence: 88%

“…Johansen 1972;Lenfant and Johansen 1972;Dejours 1975;Kramer et al 1978;Randall et al 1981;Ultsch 1996;Graham 1997;Sayer 2005;Glass and Rantin 2009), but far less is known about the changes which must have occurred in ionoregulation, which is another major gill function. Very simply, as the gills became smaller, less ventilated, and less perfused, this critical function had to shift to another organ, and that organ was clearly not the swimbladder (i.e.…”

Section: Introductionmentioning

confidence: 97%

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The transition from water-breathing to air-breathing is associated with a shift in ion uptake from gills to gut: a study of two closely related erythrinid teleosts, Hoplerythrinus unitaeniatus and Hoplias malabaricus

et al. 2016

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The evolutionary transition from water-breathing to air-breathing involved not only a change in function of the organs of respiratory gas exchange and N-waste excretion, but also in the organs of ion uptake from the environment. A combination of in vivo and in vitro techniques was used to look at the relative importance of the gills versus the gut in Na(+), Cl(-), and K(+) balance in two closely related erythrinid species: a facultative air-breather, the jeju (Hoplerythrinus unitaeniatus) and an obligate water-breather, the traira (Hoplias malabaricus). The jeju has a well-vascularized physostomous swimbladder, while that in the traira is poorly vascularized, but the gills are much larger. Both species are native to the Amazon and are common in the ion-poor, acidic blackwaters of the Rio Negro. Under fasting conditions, the traira was able to maintain positive net Na(+) and Cl(-) balance in this water, and only slightly negative net K(+) balance. However, the jeju was in negative net balance for all three ions and had lower plasma Na(+) and Cl(-) concentrations, despite exhibiting higher branchial Na(+), K(+)ATPase and v-type H(+)ATPase activities. In the intestine, activities of these same enzymes were also higher in the jeju, and in vitro measurements of net area-specific rates of Na(+), Cl(-), and K(+) absorption, as well as the overall intestinal absorption capacities for these three ions, were far greater than in the traira. When acutely exposed to disturbances in water O2 levels (severe hypoxia ~15% or hyperoxia ~420% saturation), gill ionoregulation was greatly perturbed in the traira but less affected in the jeju, which could "escape" the stressor by voluntarily air-breathing. We suggest that a shift of ionoregulatory capacity from the gills to the gut may have occurred in the evolutionary transition to air-breathing in jeju, and in consequence branchial ionoregulation, while less powerful, is also less impacted by variations in water O2 levels.

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Section: Introductionsupporting

confidence: 88%

Section: Introductionmentioning

confidence: 97%

The transition from water-breathing to air-breathing is associated with a shift in ion uptake from gills to gut: a study of two closely related erythrinid teleosts, Hoplerythrinus unitaeniatus and Hoplias malabaricus

et al. 2016

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“…The enlargement of spiracles occurred during a time of Earth's history when oxygen levels trended downward (26,41). For aquatic animals, the Devonian decline of oxygen was exacerbated by the fact that water has 1/30th of the oxygen of air, while being 800 times denser (42,43). Therefore, respiration with water requires 800 × 30 = 24,000 times more mass flux through respiratory tissues per unit of extracted oxygen than aerial respiration with all other things being equal.…”

Section: Discussionmentioning

confidence: 99%

Massive increase in visual range preceded the origin of terrestrial vertebrates

MacIver

Schmitz

Mugan

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The evolution of terrestrial vertebrates, starting around 385 million years ago, is an iconic moment in evolution that brings to mind images of fish transforming into four-legged animals. Here, we show that this radical change in body shape was preceded by an equally dramatic change in sensory abilities akin to transitioning from seeing over short distances in a dense fog to seeing over long distances on a clear day. Measurements of eye sockets and simulations of their evolution show that eyes nearly tripled in size just before vertebrates began living on land. Computational simulations of these animal's visual ecology show that for viewing objects through water, the increase in eye size provided a negligible increase in performance. However, when viewing objects through air, the increase in eye size provided a large increase in performance. The jump in eye size was, therefore, unlikely to have arisen for seeing through water and instead points to an unexpected hybrid of seeing through air while still primarily inhabiting water. Our results and several anatomical innovations arising at the same time suggest lifestyle similarity to crocodiles. The consequent combination of the increase in eye size and vision through air would have conferred a 1 million-fold increase in the amount of space within which objects could be seen. The "buena vista" hypothesis that our data suggest is that seeing opportunities from afar played a role in the subsequent evolution of fully terrestrial limbs as well as the emergence of elaborated action sequences through planning circuits in the nervous system. fish-tetrapod transition | vision | visual ecology | terrestriality | prospective cognition B efore terrestrial vertebrates arose, their ancestors inhabited underwater environments, where vision is highly compromised compared with vision above water. The visual difference between life in water and life above it is comparable with driving fast on a foggy road, where our responses must be rapid and simple, vs. driving in clear daylight conditions, where deliberation over more complex choices is enabled by the vast increase in sensory range. Nonetheless, although an immense quantity of work has been done on the emergence of limbs during the evolution of land vertebrates, how visual capability changed during the transition from water to land has not been explored. In part, this lack of exploration is because computational visual ecology-necessary to interpret the fossil data-has not been combined with early tetrapod paleontology. Through combining these disciplines, here we probe the evolutionary history of the switch in our visual sensory ecology from water to air. Surprisingly, our results show that eyes tripled in size just before full-time life on land evolved. Convergent lines of evidence, including our own, strongly support the hypothesis that a crocodilian ecotype-using the greatly enhanced visual capabilities conferred by vision through air to prey on the bounty of unexploited invertebrates that long preceded the vertebrates onto ...

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“…gariepinus comprises paired suprabranchial chambers in the dorsal-posterior area of the branchial cavity, with extensions of the second and fourth gill arches that form the arborescent organs (for details see Glass and Rantin, 2009). Although the cardiorespiratory responses to hypoxia have been described in this species by Belão et al (2011), the mechanisms of oxygen sensing and the distribution and orientation of chemoreceptors mediating reflex responses still remain to be elucidated.…”

Section: Introductionmentioning

confidence: 96%