Abstract

When in seawater, rainbow trout (Oncorhynchus mykiss) drink to avoid dehydration and display stroke volume (SV) mediated elevations in cardiac output (CO) and an increased proportion of CO is diverted to the gastrointestinal tract as compared to when in freshwater. These cardiovascular alterations are associated with distinct reductions in systemic and gastrointestinal vascular resistance (RSys and RGI, respectively). Although increased gastrointestinal blood flow (GBF) is likely essential for osmoregulation in seawater, the sensory functions and mechanisms driving the vascular resistance changes and other associated cardiovascular changes in euryhaline fishes remain poorly understood. Here, we examined whether internal gastrointestinal mechanisms responsive to osmotic changes mediate the cardiovascular changes typically observed in seawater, by comparing the cardiovascular responses of freshwater-acclimated rainbow trout receiving continuous (for 4 days) gastric perfusion with half-strength seawater (½ SW, ~ 17 ppt) to control fish (i.e., no perfusion). We show that perfusion with ½ SW causes significantly larger increases in CO, SV and GBF, as well as reductions in RSys and RGI, compared with the control, whilst there were no significant differences in blood composition between treatments. Taken together, our data suggest that increased gastrointestinal luminal osmolality is sensed directly in the gut, and at least partly, mediates cardiovascular responses previously observed in SW acclimated rainbow trout. Even though a potential role of mechano-receptor stimulation from gastrointestinal volume loading in eliciting these cardiovascular responses cannot be excluded, our study indicates the presence of internal gastrointestinal milieu-sensing mechanisms that affect cardiovascular responses when environmental salinity changes.

Highlights

  • Successful transitions from freshwater (FW) to seawater (SW) by euryhaline fishes rely on a series of behavioural and physiological adjustments to switch from hyper- to hypo-osmoregulation, respectively (Zydlewski and Wilkie 2013)

  • The increases in gastrointestinal blood flow (GBF) observed in both treatments were associated with general reductions in RGI (Fig. 3c), and, no treatment effect was identified, a trend for an interaction between treatment and time was found as reductions in RGI were larger between day 0 and day 4 in the 1⁄2 SW treatment (% Δ from baseline, t(13) = 2.514, P = 0.026; Fig. 4)

  • This points to the existence of internal gastrointestinal sensory mechanisms that respond to changes in luminal osmolality and/or ion concentration, eliciting cardiovascular responses

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Summary

Introduction

Successful transitions from freshwater (FW) to seawater (SW) by euryhaline fishes rely on a series of behavioural and physiological adjustments to switch from hyper- to hypo-osmoregulation, respectively (Zydlewski and Wilkie 2013). These adjustments compensate for the passive fluxes of water and ions across permeable biological membranes, Communicated by B. SW-acclimated rainbow trout have a reduced dorsal aortic blood pressure (PDA) compared with FW conspecifics (Sundell et al 2018; Morgenroth et al 2019; Olson and Hoagland 2008). Olson and Hoagland (2008) showed that SW-acclimated rainbow trout were unable to fully compensate for the dehydrating effect of the hyperosmotic milieu and were in a state of chronic hypovolemia, which could contribute to reduce arterial blood pressure in SW

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