Chemosensory function of amphibian skin: integrating epithelial transport, capillary blood flow and behaviour

Abstract

Terrestrial anuran amphibians absorb water across specialized regions of skin on the posterioventral region of their bodies. Rapid water absorption is mediated by the insertion of aquaporins into the apical membrane of the outermost cell layer. Water moves out of the epithelium via aquaglyceroporins in the basolateral membrane and into the circulation in conjunction with increased capillary blood flow to the skin and aquaporins in the capillary endothelial cells. These physiological responses are activated by intrinsic stimuli relating to the animals' hydration status and extrinsic stimuli relating to the detection of osmotically available water. The integration of these processes has been studied using behavioural observations in conjunction with neurophysiological recordings and studies of epithelial transport. These studies have identified plasma volume and urinary bladder stores as intrinsic stimuli that activate the formation of angiotensin II (AII) to stimulate water absorption behaviour. The coordinated increase in water permeability and capillary blood flow appears to be mediated primarily by sympathetic stimulation of beta adrenergic receptors, although the neurohypopyseal hormone arginine vasotocin (AVT) may also play a role. Extrinsic stimuli relate primarily to the ionic and osmotic properties of hydration sources. Toads avoid NaCl solutions that have been shown to be harmful in acute exposure, approx. 200-250 mm. The avoidance is partially attenuated by amiloride raising the hypothesis that the mechanism for salt detection by toads resembles that for salt taste in mammals that take in water by mouth. In this model, depolarization of the basolateral membrane of taste cells is coupled to afferent neural stimulation. In toad skin we have identified innervation of skin epithelial cells by branches of spinal nerves and measured neural responses to NaCl solutions that elicit behavioural avoidance. These same concentrations produce depolarization of the basolateral membrane in isolated epithelial preparations. As with salt taste in mammals, the neural responses and depolarization of basolateral membrane potential are partially inhibited by amiloride. In addition, toads are more tolerant of sodium gluconate solution which is consistent with the phenomenon in mammalian taste physiology termed the anion paradox in which sodium salts with larger molecular weight anions produce a reduced intensity of salt taste. Finally, toads also avoid concentrated solutions of a non-electrolyte, mannitol, which differs from NaCl solutions in not affecting transepithelial conductance and requires a longer time to depolarize the basolateral membrane. Osmotic stimuli may mediate sensory processes for longer term detection of conditions with low water potential while ionic stimuli are more important for shorter term analysis of rehydration sources.

Novel Vasotocin-Regulated Aquaporins Expressed in the Ventral Skin of Semiaquatic Anuran Amphibians: Evolution of Cutaneous Water-Absorbing Mechanisms

“…A physiological study using the pelvic skin of B. bufo showed that perfusion of the skin with a Ringer solution sustained the elevated high water flux by AVT, but stopping the perfusion resulted in a dramatic drop in the water flux (43). It was also reported that dehydrated bufonids responded to water contact with a rapid increase in blood flow, as well as water uptake, in the pelvic skin (38,39,44). Furthermore, IP injection to B. bufo facilitates not only cutaneous water uptake but also capillary perfusion, suggesting an important role of sympathetic nervous system in the regulation of cutaneous blood flow and water absorption in vivo (38).…”

Amphibian species vary in their learned avoidance response to the deadly fungal pathogen Batrachochytrium dendrobatidis

“…More research is needed to understand the mechanisms underlying the behavioural response demonstrated by the toads. Amphibians may be able to detect these chemical metabolites through the chemo-or pain receptors in their skin (Hillyard & Willumsen, 2011), which could facilitate the detection and avoidance of external stimuli through epidermal contact (for example see Kiesecker et al, 1999). Pavlovian conditioning predicts that chemicals that induce negative stimuli, for example pain or itching, or are associated with allelochemicals, for example odours, would produce a strong behavioural avoidance response.…”

Amphibian species vary in their learned avoidance response to the deadly fungal pathogen Batrachochytrium dendrobatidis

“…Bd metabolites triggered the associational behavioral avoidance in southern toads, which is not surprising given that many vertebrate species are capable learning to avoid a cue that is accompanied by a painful stimulus (Dunlop et al 2006 , and thus exposure to metabolites might indeed be painful. Amphibians may be able to detect these chemical metabolites through the chemo-or pain receptors in their skin (Hillyard & Willumsen 2011), which could facilitate the detection and avoidance of external stimuli through epidermal contact (for example see Kiesecker et al 1999). Pavlovian conditioning predicts that pain inducing chemicals would produce a strong behavioral avoidance response.…”