Introducing the Amphibious Mudskipper Goby As a Unique Model to Evaluate Neuro/Endocrine Regulation of Behaviors Mediated by Buccal Sensation and Corticosteroids
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Okayama University Scientific Achievement Repository International Journal of Molecular Sciences Review Introducing the Amphibious Mudskipper Goby as a Unique Model to Evaluate Neuro/Endocrine Regulation of Behaviors Mediated by Buccal Sensation and Corticosteroids Yukitoshi Katayama *, Kazuhiro Saito and Tatsuya Sakamoto Ushimado Marine Institute, Faculty of Science, Okayama University, Kashino 130-17, Setouchi, Okayama 701-4303, Japan; [email protected] (K.S.); [email protected] (T.S.) * Correspondence: [email protected]; Tel.: +81-869-34-5210 Received: 9 July 2020; Accepted: 8 September 2020; Published: 14 September 2020 Abstract: Some fish have acquired the ability to breathe air, but these fish can no longer flush their gills effectively when out of water. Hence, they have developed characteristic means for defense against external stressors, including thirst (osmolarity/ions) and toxicity. Amphibious fish, extant air-breathing fish emerged from water, may serve as models to examine physiological responses to these stressors. Some of these fish, including mudskipper gobies such as Periophthalmodon schlosseri, Boleophthalmus boddarti and our Periophthalmus modestus, display distinct adaptational behaviors to these factors compared with fully aquatic fish. In this review, we introduce the mudskipper goby as a unique model to study the behaviors and the neuro/endocrine mechanisms of behavioral responses to the stressors. Our studies have shown that a local sensation of thirst in the buccal cavity—this being induced by dipsogenic hormones—motivates these fish to move to water through a forebrain response. The corticosteroid system, which is responsive to various stressors, also stimulates migration, possibly via the receptors in the brain. We suggest that such fish are an important model to deepen insights into the stress-related neuro/endocrine-behavioral effects. Keywords: stressors; thirst; angiotensin II; corticosteroids; amphibious fish 1. Introduction Water–land transition necessitates many important physiological and biochemical adaptations to the terrestrial environment. In particular, fish that routinely emerge from water, such as mudskippers (class Actinopterygii, order Perciformes, family Gobiidae; e.g., Periophthalmodon schlosseri, Boleophthalmus boddarti and our Periophthalmus modestus) commonly found in estuaries of the Indo-Pacific and evolutionarily many other fish taxa [1], cannot effectively flush their body surfaces (primarily gills) due to a lack of water. Hence, these fishes are amphibious and have developed ways to ameliorate terrestrial stress (e.g., endogenous ammonia) during emersion. They are equipped with strategies on land, such as modified nitrogen metabolism (Figure1), and amphibious behavior to defend against ammonia toxicity, whereas most aquatic animals excrete ammonia in water. Therefore, these fish, as well as ammonia-tolerant nonamphibious fish such as the Gulf toadfish and a gobiid fish (Mugilogobius abei)[2–6], may serve as unique models to examine the effects of stressors such as ammonia, but their characteristic adaptational behaviors and neuro/endocrine mechanisms have only been minimally studied [7–13]. Int. J. Mol. Sci. 2020, 21, 6748; doi:10.3390/ijms21186748 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 13 Int. J. Mol. Sci. 2020, 21, 6748 2 of 13 Figure 1. Glutamine synthesis adopted by amphibious fish to defend against ammonia toxicity. Level of Figureglutamine 1. Glutamine synthetase synthesis mRNA in adopted mudskippers by amphibious exposed for fish 1 dayto defend (n = 6). against Bars represent ammonia the toxicity. mean LevelSEM. ± of* p glutamine< 0.05 vs control.synthetase This mRNA strategy in mudskippers involves the detoxification exposed for 1 ofday ammonia (n = 6). Bars to glutamine, represent whereasthe mean the ± SEM.glutamine * p < 0.05 synthetase vs control. activity This isstrategy generally involves undetectable the detoxification or low in nonureosmoticof ammonia to fishesglutamine, [14,15 whereas]. the glutamine synthetase activity is generally undetectable or low in nonureosmotic fishes [14,15]. Periophthalmus modestus spend a significant amount (70–90%) of time out of water (0–40 parts per thousand)Periophthalmus [16,17 modestus], as a means spend ofa significant predator avoidance amount (70–90%) and to forage of time (Supplementary out of water (0–40 Video parts S1), perwhich thousand) appears [16,17], to be ecologicallyas a means of diverse predator across avoidance the families and to [ 1forage]. They (Supplementary have evolved Video numerous S1), whichphysiological appears and to behavioralbe ecologically traits diverse of locomotion, across the gas exchange,families [1]. nitrogen They have excretion, evolved ionoregulation numerous physiologicaland osmoregulation and behavioral associated traits with of amphibious locomotion, lives gas [7 exchange,,8,18–22]. Fornitrogen example, excretion, they can ionoregulation store water in andthe buccalosmoregulation and opercular associated cavities with when amphibious they are lives on land, [7,8,18–22]. because For their example, opercula they are can closed store without water inventilation the buccal of and the opercular gills [17]. Thecavities aquatic when preference they are andon land, rolling because behavior their on opercula wet land are are closed also notable without for ventilationmoistening of the the dorsal gills [17]. skin The [23]. aq Theuatic emersion preference is very and easy rolling to score behavi asor an on individual wet land is are either also innotable or out forof water,moistening which the makes dorsal the skin mudskipper [23]. The an emersion interesting is very model easy to to examine score as the an e ffindividualects of external is either stressors in or outsuch of as water, ammonia which and makes dehydration the mudskipper (Figure2), an and inte mayresting provide model novel to avenuesexamine for the investigations effects of external of the stressorsneuro/endocrine such as systems, ammonia since and some dehydration of these have (Figure recently 2), beenand analyzedmay provide [16]. novel avenues for investigations of the neuro/endocrine systems, since some of these have recently been analyzed [16]. Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 3 of 13 Int. J. Mol. Sci. 2020, 21, 6748 3 of 13 Figure 2. Schematic of the experimental setup used to examine amphibious behavior in mudskippers. FigureThe hashed 2. Schematic area represents of the experimental land and issetup easily used accessible to examine to the amphibious mudskipper behavior placed in in mudskippers. the water area. TheTreatment hashed witharea represents stressors and land hormones and is easily allows accessible the observation to the mudskipper of the period placed of time in inthe water water and area. the Treatmentfrequency with of migration. stressors and Plastic hormon meshes on allows the land the area observation facilitates of drainage the period of water.of time Water in water in the and tank the is frequencyconstantly of aerated migration. [17, 24Plastic–26]. mesh on the land area facilitates drainage of water. Water in the tank is constantly aerated [17,24–26]. In this review, we focus on two topics relevant to the neuro/endocrine regulations of stress-related behavioralIn this changes.review, we First, focus we discusson two thetopics behavior releva motivatednt to the byneuro/endocrine dipsogenic hormones regulations via a buccalof stress- local relatedsensation behavioral of thirst changes. and external First, factors we discuss such asthe eating. behavior Then, motivated we introduce by dipsogenic the roles ofhormones corticosteroids via a buccalthat are local responsive sensation to of various thirst externaland external stressors factors [27 ,28such] in as the eating. amphibious Then, behavior.we introduce We hopethe roles that thisof corticosteroidsreview will create that furtherare responsive interest into thevarious neuro external/endocrine stressors regulation [27,28] of in this the behavior amphibious not only behavior. among Wefish hope endocrinologists, that this review but alsowill for create those further working interest on other in animals.the neuro/endocrine regulation of this behavior not only among fish endocrinologists, but also for those working on other animals. 2. Migration to Water Motivated by Local Sensation in the Buccal/Opercular Cavity 2. Migration to Water Motivated by Local Sensation in the Buccal/Opercular Cavity On land, mudskippers continually search for water (Supplementary Video S1), in much the same wayOn as land, tetrapods mudskippers [16]. Indeed, continually we recently search demonstrated for water (Supplementary that artificial removal Video S1), (e.g., in bymuch piercing the same holes wayin the as tetrapods opercula) [16]. of buccal Indeed, water we recently stored ondemonstrated land by the that mudskipper artificial removal resulted (e.g., in a by strong piercing behavioral holes inpreference the opercula) for a of water buccal environment, water stored suggesting on land theby presencethe mudskipper of thirst resulted (defined in as a consciousstrong behavioral sensation preferenceof a need forfor water a water and aenvironment, desire to drink, suggesting which is followedthe presence by a searchof thirst for water(defined in terrestrialas a conscious animals sensationsuch as mammalsof a need [29for,30 water]) in fishand