The Amphibious Mudskipper: A Unique Model Bridging the Gap of Central Actions of Osmoregulatory Hormones Between Terrestrial and Aquatic Vertebrates

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.

Introducing the Amphibious Mudskipper Goby as a Unique Model to Evaluate Neuro/Endocrine Regulation of Behaviors Mediated by Buccal Sensation and Corticosteroids

“…On land, mudskippers continually search for water (Supplementary Video S1), in much the same way as tetrapods [16]. Indeed, we recently demonstrated that artificial removal (e.g., by piercing holes in the opercula) of buccal water stored on land by the mudskipper resulted in a strong behavioral preference for a water environment, suggesting the presence of thirst (defined as a conscious sensation of a need for water and a desire to drink, which is followed by a search for water in terrestrial animals such as mammals [29,30]) in fish [17].…”

“…The factors such as stressors driving many amphibious fish to water have been reviewed, and these factors can also be triggered in cyprinodontiforms, including in model species (e.g., Kryptolebias marmoratus) [105,106]. The mode of action can be assessed through neurohistological methods of labeling of Fos and neuro/endocrine transmitter systems in the less complicated fish brain [16], since these species have sequenced genomes [7,[107][108][109].…”

“…Periophthalmus modestus spend a significant amount (70–90%) of time out of water (0–40 parts per thousand) [ 16 , 17 ], as a means of predator avoidance and to forage ( Supplementary Video S1 ), which appears to be ecologically diverse across the families [ 1 ]. They have evolved numerous physiological and behavioral traits of locomotion, gas exchange, nitrogen excretion, ionoregulation and osmoregulation associated with amphibious lives [ 7 , 8 , 18 , 19 , 20 , 21 , 22 ].…”

“…The aquatic preference and rolling behavior on wet land are also notable for moistening the dorsal skin [ 23 ]. The emersion is very easy to score as an individual is either in or out of water, which makes the mudskipper an interesting model to examine the effects of external stressors such as ammonia and dehydration ( Figure 2 ), and may provide novel avenues for investigations of the neuro/endocrine systems, since some of these have recently been analyzed [ 16 ].…”

Neural populations for maintaining body fluid balance

“…Interestingly, studies in aquatic amphibious fishes revealed a unique system of Ang II-related thirst regulation. In mudskipper, Ang II stimulates the area postrema (AP), a hindbrain nucleus, to induce swallowing action [17,18]. Recent studies with contemporary neural manipulation tools have expanded our knowledge of thirst circuits at a finer resolution.…”