Ions first: Na⁺uptake shifts from the skin to the gills before O₂uptake in developing rainbow trout,Oncorhynchus mykiss

Abstract

This is the first direct physiological evidence in support of the ionoregulatory hypothesis, challenging the long-held assumption that teleost gills develop initially for gas exchange. Resting unidirectional sodium (Na þ ) uptake and oxygen (O 2 ) uptake across the skin and gills were measured simultaneously in larval rainbow trout, Oncorhynchus mykiss, during development. In soft and hard water, Na þ uptake shifted to the gills by 15 and 16 days post-hatch (dph) while O 2 uptake took 50 -80% longer and shifted by 23 and 28 dph, respectively. This suggests that gills are required for ionoregulation prior to gas exchange in developing rainbow trout. The age of transition for Na þ uptake, gill Na þ , K þ -ATPase (NKA) a-subunit protein expression and gill NKA enzyme activity were not significantly different between soft and hard water-reared groups, which suggests a lack of plasticity in gill ionoregulatory development.In rainbow trout, the gills assume a dominant role in ionoregulation before gas exchange, suggesting that ionoregulation may be the initial driving force for gill development. Further investigation is required to determine whether this pattern is consistent with other teleosts and more basal fishes during early development to gain insight into the role of ionoregulation in vertebrate gill evolution.

Effects of climate change on fish reproduction and early life history stages

“…Although very little is known about the mechanisms and pathways of acid-base regulation in larval fishes, it is clear that they must be capable of acid-base homeostasis (Brauner 2009). Indeed, the early ontogenetic development of gills in larval fish may be more important in ionoregulation and maintaining acid-base balance than for oxygen delivery (Fu et al 2010). Similar to the egg stage, the 24-h LC50 for larval fish is generally above 10 000 ppm CO 2 for the few species tested to date (Kikkawa et al 2003;Ishimatsu et al 2008).…”

Growth hormone transgenesis and polyploidy increase metabolic rate, alter the cardiorespiratory response and influence HSP expression to acute hypoxia in Atlantic salmon (Salmo salar) yolk-sac alevins

“…It has been suggested that the embryonic heart beat might primarily serve alternative functions such as nutrient transport and angiogenesis (Burggren, 2004), whereas the gills serve in ionoregulation (Fu et al, 2010). Alternatively, the absence of a cardiorespiratory response to hypoxia could be explained by a lack of chemosensory feedback at this life stage.…”

Different mechanisms of Na+ uptake and ammonia excretion by the gill and yolk sac epithelium of early life stage rainbow trout

“…The first or 'traditional' divided chamber (Fig. 1A) was designed to separate the head and gills from the rest of the body in CYA fish (Fu et al, 2010) and the protocol was almost identical to those described in previous studies (Zimmer et al, 2014c;Zimmer and Wood, 2015). CYA trout (∼200 mg; 30 days post-hatch) were initially anaesthetized to stage 3 anesthesia (McFarland, 1959) using 0.1 g l −1 neutralized MS-222 with 0.05 g l −1 neutralized MS-222 used to maintain anesthesia in the chambers.…”

“…In most mature freshwater fish, J Na,in and J amm occur primarily across the gills (Smith, 1929;Maetz and Garcia-Romeu, 1964;Cameron and Heisler, 1983;Wright and Wood, 1985;Smith et al, 2012;Zimmer et al, 2014a), although the skin, kidney, and gastrointestinal system play minor roles. However, in post-hatch larval fish, the gills are underdeveloped and the skin ( primarily that overlying the yolk sac) represents the dominant site for both J Na,in and J amm (Esaki et al, 2007;Shih et al, 2008;Fu et al, 2010;Zimmer et al, 2014c).…”