Gill morphology and acute hypoxia: responses of mitochondria-rich, pavement, and mucous cells in the Amazonian oscar (Astronotus ocellatus) and the rainbow trout (Oncorhynchus mykiss), two species with very different approaches to the osmo-respiratory compromise

Abstract

The hypoxia-intolerant rainbow trout (Oncorhynchus mykiss (Walbaum, 1792)) exhibits increased branchial ion permeability and Na + influx during acute exposure to moderate hypoxia (PO2 = 80 torr; 1 torr = 133.3224 Pa), manifesting the usual trade-off between gas exchange and electrolyte conservation. In contrast, the hypoxia-tolerant oscar (Astronotus ocellatus (Agassiz, 1831)) is unusual in exhibiting decreased branchial ion permeability to ions and Na + influx during acute exposure to severe hypoxia (PO2 = 10-20 torr). These different physiological approaches to the osmo-respiratory compromise correlate with rapid, oppositely directed changes in gill morphology. In oscar, pavement cells (PVCs) expanded, partially covering neighboring mitochondria-rich cells (MRCs), which were recessed and reduced in size. Those remaining open were transformed from "shallow-basin" to "deep-hole" forms with smaller openings, deeper apical crypts, and smaller numbers of subapical microvesicles, changes that were largely reversed during normoxic recovery. In contrast, moderate hypoxia caused outward bulging of MRCs in rainbow trout with increases in size, surface exposure, and number of subapical microvesicles, accompanied by PVC retraction. These changes were partially reversed during normoxic recovery. In both rainbow trout and oscar, hypoxia caused discharge of mucus from enlarged mucous cells (MCs). Rapid, divergent morphological changes play an important role in explaining two very different physiological approaches to the osmo-respiratory compromise.Résumé : La truite arc-en-ciel (Oncorhynchus mykiss (Walbaum, 1792)) qui est intolérante à l'hypoxie montre une perméa-bilité branchiale accrue aux ions et un influx de Na + durant une exposition aiguë à une hypoxie modérée (PO 2 = 80 torr; 1 torr = 133.3224 Pa), ce qui représente le compromis habituel entre les échanges gazeux et la conservation des électrolytes. À l'opposé, l'oscar (Astronotus ocellatus (Agassiz, 1831)), qui est tolérant à l'hypoxie, réagit de façon inhabituelle par une diminution de la perméabilité des branchies aux ions et de l'influx de Na + durant une exposition aiguë à une hypoxie sévère (PO 2 = 10-20 torr). Il y a une corrélation entre ces approches physiologiques différentes au compromis osmo-respiratoire et les changements rapides de la morphologie des branchies dans des directions opposées. Chez l'oscar, les cellules pavimenteuses (PVC) prennent de l'expansion et couvrent partiellement les cellules riches en mitochondries (MRC) voisines qui se rétractent et rapetissent. Celles qui restent ouvertes se transforment d'une forme de « bassin évasé » à une de « dépression profonde » avec des ouvertures réduites, de cryptes apicales plus accentuées et un nombre restreint de microvésicules subapicales, des modifications qui en grande partie régressent durant le rétablissement de la normoxie. Au contraire, l'hypoxie modérée chez la truite arc-en-ciel cause un ballonnement des MRC vers l'extérieur et une augmentation de taille, de la surface d'exposition et du nom...

Interactions between hypoxia tolerance and food deprivation in Amazonian oscars, Astronotus ocellatus (Agassiz)

“…This is thought to be the morphological correlate, and indeed perhaps the cause, of decreased transcellular permeability. Hypoxia-sensitive rainbow trout, Oncorhynchus mykiss, showed the opposite effects, with MRCs that were increasing in size and bulging out, and pavement cell retraction (Iftikar et al, 2010;Matey et al, 2011). Fed fish in our study show the same response under hypoxia as seen before (Wood et al, 2009;Matey et al, 2011): MRCs at the gill decreased in number and surface area, and MCs increased slightly in number.…”

“…In some species, such as the anoxia-tolerant crucian carp (Carassius carassius) and the goldfish (Carassius auratus), it can lead to gross morphological changes (Sollid et al, 2003;Sollid et al, 2005a;Sollid et al, 2005b;Sollid and Nilsson, 2006). In oscars, changes under hypoxia have been shown to be more modest but very rapid, including a reduced number and apical surface area of MRCs due to pavement cell expansion from the first hour of exposure onwards (Wood et al, 2009;Matey et al, 2011). This is thought to be the morphological correlate, and indeed perhaps the cause, of decreased transcellular permeability.…”

Distinct physiological strategies are used to cope with constant hypoxia and intermittent hypoxia in killifish (Fundulus heteroclitus)

“…This underlies the 'osmorespiratory compromise' that leads to trade-offs between respiratory gas exchange and osmoregulation (Randall et al, 1972;Nilsson, 2007). Correspondingly, some species reduce gill surface area and/or ion permeability in response to hypoxia exposure, presumably to minimize ionic disruption rather than facilitate O 2 uptake (McDonald and McMahon, 1977;Wood et al, 2007Wood et al, , 2009Matey et al, 2011;De Boeck et al, 2013). The killifish acclimated to constant hypoxia in this study decreased gill surface area and shifted their gill epithelium towards a freshwater morphology (Figs 4 and 5; Table 1).…”

Physiological tradeoffs may underlie the evolution of hypoxia tolerance and exercise performance in sunfish (Centrarchidae)

“…It is also well known that many active species (e.g. tuna, rainbow trout) are very sensitive to hypoxia, even though they possess extremely high O 2 transport capacities to support high rates of aerobic metabolism (Davis, 1975;Gooding et al, 1981;Bushnell et al, 1990;Matey et al, 2011). However, tradeoffs between hypoxia tolerance and exercise performance are not always observed.…”