Abstract
The large-scale migrations of anadromous fish species from freshwater to seawater have long been considered particularly enigmatic, as this life history necessitates potentially energetically costly changes in behaviour and physiology. A significant knowledge gap concerns the integral role of cardiovascular responses, which directly link many of the well-documented adaptations (i.e. through oxygen delivery, water and ion transport) allowing fish to maintain osmotic homeostasis in the sea. Using long-term recordings of cardiorespiratory variables and a novel method for examining drinking dynamics, we show that euryhaline rainbow trout (Oncorhynchus mykiss) initiate drinking long before the surrounding environment reaches full seawater salinity (30–33 ppt), suggesting the presence of an external osmo-sensing mechanism. Onset of drinking was followed by a delayed, yet substantial increase in gastrointestinal blood flow through increased pulse volume exclusively, as heart rate remained unchanged. While seawater entry did not affect whole animal energy expenditure, enhanced gastrointestinal perfusion represents a mechanism crucial for ion and water absorption, as well as possibly increasing local gastrointestinal oxygen supply. Collectively, these modifications are essential for anadromous fish to maintain homeostasis at sea, whilst conserving cardiac and metabolic scope for activities directly contributing to fitness and reproductive success.
Highlights
Flows, while minimizing drinking rate and renal salt loss[6]
gastrointestinal blood flow (GBF) was significantly affected by a transition to seawater (F = 26.48, P < 0 .001), time (F = 7.19, P = 0 .008) and their interaction (F = 50.48, P < 0.001, Fig. 1a)
The pulse volume showed a response profile that closely mirrored that of GBF, increasing after 36 h in seawater and reaching a relative pulse volume of 193 ± 1 7% at 96 h
Summary
Flows, while minimizing drinking rate and renal salt loss[6]. in marine environments, fish hypo-osmoregulate to counter the osmotic loss of water and diffusional gain of salts[7]. Seawater entering the gut during drinking likely requires increased gastrointestinal processing (e.g. water and ion absorption). This would potentially entail an increased gastrointestinal blood flow (GBF) in order to transport absorbed ions and increase oxygen supply as metabolic demands increase in the active gastrointestinal tissues[16,17]. Despite the previously suggested benefits of gastrointestinal hyperemia during seawater transfer[16,18], gut blood flow responses in fish exposed to different salinities remain completely unexplored. We hypothesized that upon a transition to seawater, rainbow trout would exhibit an increase in GBF and SMR to transport absorbed ions and water, as well as supply oxygen and nutrients to a more metabolically active gastrointestinal tract. The knowledge gained from this study is essential for understanding physiological and energetic processes operating in fish migrating from freshwater to seawater, and the environmental selection pressures and physiological constraints that have shaped the evolution and ecology of anadromy in fishes
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