Previously, we showed that the evolution of high acuity vision in fishes was directly associated with their unique pH-sensitive hemoglobins that allow O2 to be delivered to the retina at PO2s more than ten-fold that of arterial blood (Damsgaard et al., 2019). Here, we show strong evidence that vacuolar-type H+-ATPase and plasma-accessible carbonic anhydrase in the vascular structure supplying the retina act together to acidify the red blood cell leading to O2 secretion. In vivo data indicate that this pathway primarily affects the oxygenation of the inner retina involved in signal processing and transduction, and that the evolution of this pathway was tightly associated with the morphological expansion of the inner retina. We conclude that this mechanism for retinal oxygenation played a vital role in the adaptive evolution of vision in teleost fishes.

A novel acidification mechanism for greatly enhanced oxygen supply to the fish retina.

This review explores the long-standing question: 'Why do cardiovascular shunts occur?' An historical perspective is provided on previous research into cardiac shunts in vertebrates that continues to shape current views. Cardiac shunts and when they occur is then described for vertebrates. Nearly 20 different functional reasons have been proposed as specific causes of shunts, ranging from energy conservation to improved gas exchange, and including a plethora of functions related to thermoregulation, digestion and haemodynamics. It has even been suggested that shunts are merely an evolutionary or developmental relic. Having considered the various hypotheses involving cardiovascular shunting in vertebrates, this review then takes a non-traditional approach. Rather than attempting to identify the single 'correct' reason for the occurrence of shunts, we advance a more holistic, integrative approach that embraces multiple, non-exclusive suites of proposed causes for shunts, and indicates how these varied functions might at least co-exist, if not actually support each other as shunts serve multiple, concurrent physiological functions. It is argued that deposing the 'monolithic' view of shunting leads to a more nuanced view of vertebrate cardiovascular systems. This review concludes by suggesting new paradigms for testing the function(s) of shunts, including experimentally placing organ systems into conflict in terms of their perfusion needs, reducing sources of variation in physiological experiments, measuring possible compensatory responses to shunt ablation, moving experiments from the laboratory to the field, and using cladistics-related approaches in the choice of experimental animals.

Cardiovascular shunting in vertebrates: a practical integration of competing hypotheses

Acute exposure to low oxygen (hypoxia) places conflicting demands on the heart. Whilst an increase in heart rate (tachycardia) may compensate systemic oxygen delivery as arterial oxygenation falls, the heart itself is an energetically expensive organ that may benefit from slowing (bradycardia) to reduce work when oxygen is limited. Both strategies are apparent in vertebrates, with tetrapods (mammals, birds, reptiles, and amphibians) classically exhibiting hypoxic tachycardia and fishes displaying characteristic hypoxic bradycardia. With a richer understanding of the ontogeny and evolution of the responses, however, we see similarities in the underlying mechanisms between vertebrate groups. For example, in adult mammals, primary bradycardia results from the hypoxic stimulation of carotid body chemoreceptors that are overwhelmed by mechano‐sensory feedback from the lung associated with hyperpnoea. Fish‐like bradycardia prevails in the mammalian foetus (which, at this stage, is incapable of pulmonary ventilation), and in fish and foetus alike, the bradycardia ensues despite an elevation of circulating catecholamines. In both cases, the reduced heart rate may primarily serve to protect the heart. Thus, the comparative perspective offers fundamental insight into how and why different vertebrates regulate heart rate in different ways during periods of hypoxia.

Regulation of heart rate in vertebrates during hypoxia: A comparative overview

In the pirarucu (Arapaima gigas), gill surface area and thus gas exchange capacity of the gills are reduced with proceeding development. It, therefore, is expected that A. gigas, starting as a water breather, progressively turns into an obligate air-breathing fish using an air-breathing organ (ABO) for gas exchange. We assessed the air-breathing activity, O2 and CO2 exchange into air and water, ammonia-N and urea-N excretion, ion flux rates, and activities of ion transport ATPases in large versus small pirarucu. We found that even very young A. gigas (4–6 g, 2–3 weeks post-hatch) with extensive gills are air-breathers (18.1 breaths*h−1) and cover most (63%) of their O2 requirements from the air whereas 600–700-g animals (about 3–4 months post-hatch), with reduced gills, obtain 75% of their O2 from the air (10.8 breaths*h−1). Accordingly, the reduction in gill surface area hardly affected O2 uptake, but development had a significant effect on aerial CO2 excretion, which was very low (3%) in small fish and increased to 12% in larger fish, yielding a hyper-allometric scaling coefficient (1.12) in contrast to 0.82–0.84 for aquatic and total CO2 excretion. Mass-specific ammonia excretion decreased in approximate proportion to mass-specific O2 consumption as the fish grew, but urea-N excretion dropped from 18% (at 4–6 g) to 8% (at 600–700 g) of total N-excretion; scaling coefficients for all these parameters were 0.70–0.80. Mass-specific sodium influx and efflux rates, as well as potassium net loss rates, departed from this pattern, being greater in larger fish; hyper-allometric scaling coefficients were > 1.0. Gill V-type H+ ATPase activities were greater than Na+, K+-ATPase activities, but levels were generally low and comparable in large and small fish, and similar activities were detected in the ABO. A. gigas is a carnivorous fish throughout its lifecycle, and, despite fasting, protein oxidation accounted for the major portion (61–82%) of aerobic metabolism in both large and small animals. ABO PO2 and PCO2 (measured in 600–700-g fish) were quite variable, and aerial hypoxia resulted in lower ABO PO2 values. Under normoxic conditions, a positive correlation between breath volume and ABP PO2 was detected, and on average with a single breath more than 50% of the ABO volume was exchanged. ABO PCO2 values were in the range of 1.95–3.89 kPa, close to previously recorded blood PCO2 levels. Aerial hypoxia (PO2 down to 12.65 kPa) did not increase either air-breathing frequency or breath volume.

Gills and air-breathing organ in O2 uptake, CO2 excretion, N-waste excretion, and ionoregulation in small and large pirarucu (Arapaima gigas)

A swimbladder is a special organ present in several orders of Actinopterygians. As a gas-filled cavity it contributes to a reduction in overall density, but on descend from the water surface its contribution as a buoyancy device is very limited because the swimbladder is compressed by increasing hydrostatic pressure. It serves, however, as a very efficient organ for aerial gas exchange. To avoid the loss of oxygen to hypoxic water at the gills many air-breathing fish show a reduced gill surface area. This, in turn, also reduces surface area available for other functions, so that breathing air is connected to a number of physiological adjustments with respect to ion homeostasis, acid-base regulation and nitrogen excretion. Using the swimbladder as a buoyancy structure resulted in the loss of its function as an air-breathing organ and required the development of a gas secreting mechanism. This was achieved via the Root effect and a countercurrent arrangement of the blood supply to the swimbladder. In addition, a detachable air space with separated blood supply was necessary to allow the resorption of gas from the swimbladder. Gas secretion as well as gas resorption are slow phenomena, so that rapid changes in depth cannot instantaneously be compensated by appropriate volume changes. As gas-filled cavities the respiratory swimbladder and the buoyancy device require surfactant. Due to high oxygen partial pressures inside the bladder air-exposed tissues need an effective reactive oxygen species defense system, which is particularly important for a swimbladder at depth.

https://onlinelibrary.wiley.com/doi/pdf/10.1002/jez.2460

Using the swimbladder as a respiratory organ and/or a buoyancy structure-Benefits and consequences.

Air-breathing and amphibious fishes are essential study organisms to shed insight into the required physiological shifts that supported the full transition from aquatic water-breathing fishes to terrestrial air-breathing tetrapods. While the origin of air-breathing in the evolutionary history of the tetrapods has received considerable focus, much less is known about the evolutionary physiology of air-breathing among fishes. This review summarizes recent advances within the field with specific emphasis on the cardiorespiratory regulation associated with air-breathing and terrestrial excursions, and how respiratory physiology of these living transitional forms are affected by development and personality. Finally, we provide a detailed and re-evaluated model of the evolution of air-breathing among fishes that serves as a framework for addressing new questions on the cardiorespiratory changes associated with it. This review highlights the importance of combining detailed studies on piscine air-breathing model species with comparative multi-species studies, to add an additional dimension to our understanding of the evolutionary physiology of air-breathing in vertebrates.

Evolutionary and cardio-respiratory physiology of air-breathing and amphibious fishes

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Evolutionary and cardio-respiratory physiology of air-breathing and amphibious fishes