Abstract
Body fluid regulation, or osmoregulation, continues to be a major topic in comparative physiology, and teleost fishes have been the subject of intensive research. Great progress has been made in understanding the osmoregulatory mechanisms including drinking behavior in teleosts and mammals. Mudskipper gobies can bridge the gap from aquatic to terrestrial habitats by their amphibious behavior, but the studies are yet emerging. In this review, we introduce this unique teleost as a model to study osmoregulatory behaviors, particularly amphibious behaviors regulated by the central action of hormones. Regarding drinking behavior of mammals, a thirst sensation is aroused by angiotensin II (Ang II) through direct actions on the forebrain circumventricular structures, which predominantly motivates them to search for water and take it into the mouth for drinking. By contrast, aquatic teleosts can drink water that is constantly present in their mouth only by reflex swallowing, and Ang II induces swallowing by acting on the hindbrain circumventricular organ without inducing thirst. In mudskippers, however, through the loss of buccal water by swallowing, which appears to induce buccal drying on land, Ang II motivates these fishes to move to water for drinking. Thus, mudskippers revealed a unique thirst regulation by sensory detection in the buccal cavity. In addition, the neurohypophysial hormones, isotocin (IT) and vasotocin (VT), promote migration to water via IT receptors in mudskippers. VT is also dipsogenic and the neurons in the forebrain may mediate their thirst. VT regulates social behaviors as well as osmoregulation. The VT-induced migration appears to be a submissive response of subordinate mudskippers to escape from competitive and dehydrating land. Together with implications of VT in aggression, mudskippers may bridge the multiple functions of neurohypophysial hormones. Interestingly, cortisol, an important hormone for seawater adaptation and stress response in teleosts, also stimulates the migration toward water, mediated possibly via the mineralocorticoid receptor. The corticosteroid system that is responsive to external stressors can accelerate emergence of migration to alternative habitats. In this review, we suggest this unique teleost as an important model to deepen insights into the behavioral roles of these hormones in relation to osmoregulation.
Highlights
Portugal Steffen Madsen, University of Southern Denmark, Denmark Hon Jung Liew, Universiti Malaysia Terengganu, Malaysia Fernando Diaz, Centro de Investigación Científica y de Educación Superior de Ensenada, Mexico
The ventromedial telencephalic area was the site of high density expression for both of these receptors (Loveland and Fernald, 2017). These findings suggest that VT neurons projecting to the ventromedial telencephalic area and/or preoptic area act via V1a2 in the dominant mudskipper to elicit general aggressive behavior, and that the VT neurons act via V1a1 in the subordinate to inhibit general aggressive behavior (Figure 3C)
We summarized the role of Ang angiotensin II (II), neurohypophysial hormones, and corticosteroids in the regulation of amphibious behavior in mudskippers
Summary
Osmolality, and volume of body fluids are important internal parameters that are tightly controlled in vertebrates by the ingestion and excretion of water and ions (Bourque, 2008) As vertebrates expanded their habitats from aquatic to terrestrial environments, terrestrial adaptation requires critical changes in the osmoregulatory and cardiovascular systems to counter both dehydration and gravity (Leow, 2015). The osmoregulatory mechanisms are flexible in euryhaline or migratory species such as eels and salmonids, which experience drastic salinity changes during their life cycle and have to switch ion and water regulation to opposite directions via active transport (Figure 1A) Studies on these teleosts have highlighted pivotal roles of various hormones in adaptation to fluctuating environmental salinities (McCormick, 2001; Takei and McCormick, 2012). As we often found differences in the response to osmoregulatory hormones among teleost species (Kobayashi et al, 1983), a comparative approach may benefit deeper understanding on the function of osmoregulatory hormones, which will not be readily available when studying mammals exclusively
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