The Complementarity of Chemosensory Systems in Mediating the Searching Behavioral Response to Food Chemical Signals in Stone Loach Barbatula barbatula

Abstract

The olfactory system is responsible for the searching behavioral response to food odor in most species of fish. Fish deprived on olfactory sensitivity leads to a complete loss of the ability to search for food after the stimulation with food extract [1‐3]. However, representatives of some species of fish, including catfish of the genus Ictalurus , with experimental anosmia retain this ability due to the well-developed external (extraoral) taste receptors fulfilling the function of a distant sensory system [4]. More than 90% of all taste buds in these catfishes are located outside the oral cavity and cover the entire external surface of the body [5]. The presence or absence of external taste buds, as well as their distribution and density on the body surface, depends on the way of life and the role of sense organs, mainly organs of sight, in searching and detecting the prey in each specific case. The density of external taste buds is the highest on the body parts that are most likely to touch a food object when the fish is searching for food: the feelers, lips, lower surface of the head, etc. [6]. External taste buds are especially numerous in bottom-dwelling fishes and in fishes with dusk and night feeding maximums. The stone loach Barbatula barbatula is a typical representative of these species. In this study, we estimated the contributions of the olfactory and extraoral taste systems to the searching response of stone loach to food extract. Experiments with chemosensory deprived fish demonstrated the combined involvement of both main chemosensory systems in the search for the source of food odor, which indicates that olfactory and taste receptor systems are complementary in the formation of important behaviors in fish. We used mature fish with body lengths between 55‐ 65 and 70‐90 mm caught in the Tarusa River (Kaluga oblast). Before the experiments, anosmia was caused in some of the fish by bilateral cauterization of the olfactory organs (the destruction of the olfactory rosettes was controlled under a binocular microscope). In another group of fish, the feelers were ablated by cauterization. The surgery was performed under cold anesthesia. We used a total of 12 intact and 8 anosmic fish and 8 fish with the feelers ablated. The fish from the latter two groups were used in experiments 20 days after the deprivation. The fish were fed live wrigglers (larvae of Chironomidae) daily after the experiments. Water was partly renewed every day. The experiments were performed in 3.5-l tanks ( 24 × 14 × 14 cm); the olfactory stimulus was applied locally (point application). The fish were kept in the tanks (one fish per tank) for two to three weeks before the experiments. There were no ground in the tanks. Water was conveyed (0.06 l/min) from a biological filter by a pipe that was fixed 6 cm above the bottom and directed downwards. Water flew along the tank and then was transferred back to the biological filter by means of an airlift. The stimulus solutions were conveyed at a rate of 0.01 l/min for 3 min from a reservoir by a special pipe to the same zone as purified water was. Solutions of a water extract of wrigglers was used as food chemical stimuli. To prepare the solutions, we used the water that had passed through the biological filter. The same water without extracts was used as a control stimulus. The experiments were performed no later than 3 h after all stimulus solutions were prepared. Experiments with the same fish were performed at intervals of at least 2 h. The intensity of the behavioral response was estimated by the total time when the fish displayed characteristic elements of food-searching behavior near the source of the chemical stimulus (one-third of the tank area). The duration of the response was recorded by means of a summing hand stopwatch. Student’s t test was used for statistical treatment. A