Adaptive variability of the gustatory system receptor part of the carp Cyprinus carpio (Cyprinidae, Teleostei) after chronic anosmia

To confirm the existence in fish of the olfactogustatory interactions of adaptive significance, the study was performed of reactions of the receptor part of the carp gustatory system to the complete olfactory deafferentation with use of the method of scanning electron microscopy. Peculiarities of morphological changes of the taste receptor apparatus of the external and oral localization were revealed, and the dynamic of development of the taste receptor adaptive changes was traced for 1–9 months after production of anosmia. Receptors of the intraoral gustatory system had reactions of low statistical significance which were delayed in time by 5–6 months. The receptor apparatus of the external gustatory system receptors of the intraoral taste system showed pronounced hypertrophic changes that appeared since 2–3 months after the beginning of anosmia. The changes consisted in an increase of the area of the taste bud (TB) sensory field and of their number in the sensory zones of the maxillary and mandibular parts. The taste receptors located in the maxillary barbels and in the mandible gular zone had the most expressed reactions to the olfactory deafferentation. In the fish with anosmia, formation of the additional structures of the “external taste” was detected in the form of epidermal processes under the lower lip, which were covered with taste papillae. Thus, it has been shown that the fish olfactory and gustatory systems are functionally interrelated; under conditions of olfactory deprivation the external gustatory system is able to undergo compensatory morphofunctional changes aimed at vicariation of the lost distant chemical reception.     

Effects of the long-term anosmia combined with vision deprivation on the taste sensitivity and feeding behavior of the rainbow trout <Emphasis Type="Italic">Parasalmo</Emphasis> (=<Emphasis Type="Italic">Oncorhynchus</Emphasis>) <Emphasis Type="Italic">mykiss</Emphasis>

We compared taste preferences, taste sensitivity, and behavior in testing food objects in the group of intact and two groups of sensory deprived rainbow trout Oncorhynchus mykiss yearlings. We demonstrated that long-term anosmia (for 9 months), as well as anosmia (for 9 months) combined with enucleation (object vision deprivation for 4 months), does not change the taste preference of fish for the agar pellets containing amino acids (L-alanine, L-proline, L-histidine, or glycine; 0.1 M). For all groups of fish, the threshold L-alanine concentration in pellets that caused a significant increase in consumption is 0.01 M. We showed that sensory deprived fish change their behavior of gustatory testing, namely, the rate of repeated snaps decreases as well as the pellet retention time in the mouth cavity. These results demonstrate that long-term anosmia combined with a partial vision deprivation does not significantly change the taste preferences and sensitivity in the fish that have no external taste buds. However, the observed reduction in the testing time of food objects and other changes in fish feeding behavior may suggest some functional alterations in the intraoral sensory systems (gustatory and/or tactile).     

The effect of olfactory deprivation on the thresholds of sensitivity of skin chemoreceptors of carp <Emphasis Type="Italic">Cyprinus carpio</Emphasis>

Using method of registration of electrical potentials caused by chemical stimulation of the skin surface of the head of the carp Cyprinus carpio, the effect of prolonged olfactory deprivation (3, 9, and 12 months after operation) and partial blinding of anosmiated fish (9 months) on the sensitivity thresholds of external chemoreceptors was studied. It was found that, 3 months following anosmiation, the thresholds decreased by orders of 0.1–0.5, and, after 9 and 12 months, they decreased by orders of 0.1–0.8 depending on the kind of the chemical stimulus and the zone of registration. The highest increase in the sensitivity of skin chemoreceptors was recorded in anosmiated fish deprived also of object vision, by orders of 0.3–1.5. The results obtained indicate the existence of a close functional relationship between the olfactory and visual systems, on the one hand, and the skin chemosensory system, on the other hand. The compensatory processes taking place in these systems in the case of the loss of one of them have an adaptive pattern and are directed at provision of reliability of behavioral contacts and survival of fish in the environment.     

Chemosensory mediation of food searching in the Buenos Aires tetra <Emphasis Type="Italic">Hyphessobrycon anisitsi</Emphasis> (Characidae)

Food searching behavior of the Buenos Aires tetra Hyphessobrycon anisitsi has been investigated before and after experimentally induced anosmia combined with visual deprivation. The threshold concentration of a water extract of familiar food (chironomid larvae) for fish with intact olfaction was 10^–6 g/L. Induced anosmia led to complete loss of the search reaction to food odor. The chemosensory behavioral response to the water extract of food used at high concentrations (10^-1-10^-2 g/L) was not restored in fish after 1.5, 5, or 13.5 months of anosmia. The obtained results show that the external sense of taste is absent or extremely poorly developed in the Buenos Aires tetra.     

Effect of chronic anosmia on morphofunctional parameters of the gustatory system primary centers of the carp <Emphasis Type="Italic">Cyprinus carpio</Emphasis>

Morphofunctional state of neurons in primary centers of olfactory, external and intraoral gustatory systems in carp yearlings was studied at different time after bilateral anosmia, with use of methods of morphometrical, biochemical, and histochemical analyses. The olfactory deafferentation produces centripetal translocation of olfactory bulbs and development of their degenerative changes. Chronic elimination of olfactory reception in carps leads to activation of neurons in the facial lobe of medulla—the primary center of the outer gustatory system. The neuronal complexes of the vagal lobe representing the primary center of the intraoral taste did not have a similar reaction to elimination of the olfactory reception. The high level of central interaction of the fish olfactory and gustatory systems and its role in providing reliability of alimentary behavior are discussed.     

Feeding behavior and responsivity to food odors in Nile tilapia <Emphasis Type="Italic">Oreochromis niloticus</Emphasis> (Cichlidae) after chronic polisensory deprivation

The paper reports the study of the food searching behavior in the Nile tilapia Oreochromis niloticus before and after the experimental anosmia combined with visual deprivation. The threshold concentration of the water extract of the common food organisms (Chironomidae larvae) was found for the tilapia with intact olfaction to be 10^–4 g/L, which allows this fish to search for food under the restriction of visual reception. The food searching behavior in response to food odors is completely lost as a result of irreversible anosmia and do not be restored after a 4.5-month period even for the high concentrations of the extract (10^–1–10^–2 g/L). These findings point to the absence of external taste buds on the head, body, and fins, or to their extremely low numbers. It is assumed that tactile sense also plays a significant role in the food search and prey location in the Nile tilapia.     

Taste preferences and feeding behavior of the stone loach <Emphasis Type="Italic">Barbatula barbatula</Emphasis> (Balitoridae,Cypriniformes) after partial deprivation of circum-mouth external gustatory and tactile receptors

Comparative study of the feeding behavior and gustatory preferences mediated by extraoral and intraoral gustatory reception in the stone loach Barbatula barbatula in the norm and 1–6 months after extirpation of all three pairs of barbels was performed. It was found that partial loss of external gustatory receptors and the sensory deficit caused by it do not lead to any noticeable disturbances of the ability of fish to evaluate taste properties of food objects (artificial agar-agar pellets containing L-isomers of alanine, lysine, cysteine or an water extract of chironomid larvae) and make an adequate decision of their grasping or ignoring and swallowing or refusing. The extirpation of the barbels does not influence feeding behavior related to determination by fish of the taste properties of pellets and completely retains in its ritual an obligatory preliminary examination of the food object using external gustatory reception. It is suggested that external taste buds having different localization are equally capable of providing for fish a preliminary evaluation of the taste properties of the object. After extirpation of the barbels, the efficiency of grasping pellets decreases in fish, which indicates an important role of tactile reception in the determination of the site of location of the food object and in providing of the accuracy of the hunter’s dart in fish with a weak vision development.     

Assessing the impact of anosmia: review of a questionnaire's findings

The inability to detect odours, anosmia, can cause profound psychological effects resulting in feelings of physical and social vulnerability and victimization. In addition, there may be unhappiness related to the loss of the ability to detect pleasurable food smells and, as a consequence, anosmics may develop problems relating to eating. These profound effects arise from a condition which can have a rapid onset and a very poor prognosis for recovery, and are largely treated with a lack of sympathy and indifference by people with normal olfactory ability. In an attempt to educate, inform and help sufferers, a questionnaire was developed in the early 1980s and sent to those who contacted the Warwick Olfaction Research Group. The responses from this questionnaire form the basis of this review. Feelings of personal isolation, lack of interest in eating and emotional blunting were common responses from these sufferers and it seems that we still have some way to go before an adequate recognition of problems associated with anosmia is gained by the general population and, more importantly, within the medical profession.     

High correlation between microvillous olfactory receptor cell abundance and sensitivity to pheromones in olfactory nerve-sectioned goldfish

1. To determine whether microvillous olfactory receptor cells mediate responses to pheromonal cues, the olfactory nerves of mature male goldfish were axotomized and both the olfactory and behavioral sensitivity of these animals to olfactory stimuli investigated after which the histological condition of their olfactory epithelia was determined. 2. Behavioral responsiveness to food odor returned within 2 weeks but responsiveness to sexually-active females (pheromones) took 4–10 weeks to return. 3. Electro-olfactogram recordings from the olfactory epithelium of axotomized fish found that olfactory responsiveness to amino acids and pheromones changed little during the first week subsequent to axotomy. However, olfactory sensitivity decreased rapidly during the second week. During the course of the third week, electro-olfactogram sensitivity to amino acids remained while exposure to pheromones evoked no recordable electro-olfactogram. During week 4, sensitivity to amino acids increased further, and weak sensitivity to some pheromones became evident. Further recovery of electro-olfactogram sensitivity to all odorants was slow and erratic over the next 6 months, particularly to the pheromones. 4. Histological examination of the olfactory epithelia of axotomized fish demonstrated that while ciliated receptor cells were present within 2 weeks, microvillous receptor cells took approximately 4 weeks to regenerate. 5. Together these data suggest that microvillous receptor cells mediate responsiveness to pheromones in this species. Accepted: 22 August 1996     

The effect of food odor background on gustatory preferences and gustatory behavior of carp <Emphasis Type="Italic">Cyprinus carpio</Emphasis> and cod <Emphasis Type="Italic">Gadus morhua</Emphasis>

It was shown that stimulation by food odor (aquatic extract of food organisms, 10^?2 and 10^?3 g/l) does not cause shifts in gustatory preferences in carp Cyprinus carpio and cod Gadus morhua but modifies gustatory behavior. The level of consumption by carp of control granules and granules with attractive, by taste, L-proline (0.1 M) or deterrent L-lysine (0.1 M) (item by item presentation of granules) and by cod of control granules and granules with indifferent, to it, L-asparagine (0.1 M) (presentation of 10 granules simultaneously) is similar prior to and during olfactory stimulation. In the presence of food odor, the duration of taste testing for most types of granules, as well as the number of repeated graspings of granules with an attractive taste do not change in fish. At the same time, granules with indifferent or repulsive gustatory properties are rejected and repeatedly grasped by fish against the background of food odor more frequently than in water without odor. Olfactory stimulation leads to a considerable increase in the average number of graspings per one grasped granule with an indifferent or repulsive taste. Such behavior manifested by fish in the presence of food odor in response to granules with unattractive gustatory properties is apparently caused by the contradiction between the information coming via different chemosensory canals—olfactory and gustatory. The obtained results indicate that food stimulation caused by food odor in nature can lead to an increase in the actual consumption of only those accessible food items that have an attractive taste for fish.     

Risk-taking behavior in weight-compensating coho salmon, Oncorhynchus kisutch

The effects of food restriction on predation risk-taking behaviorwere studied in juvenile coho salmon, Oncorhyndtus kisutch,during the period before seawater migration in the spring. Aradiographic technique enabled the study of individual foodintake in a safe and risky food patch before and after exposureto a piscivorous predator. The study revealed a significantincrease in food intake and specific growth rate in the weeksfollowing deprivation, resulting in compensatory growth anda recovery of the weight loss caused by dietary restriction.The increase in food intake resulted from a change in risk-takingbehavior. Following a period of diet restriction, the fish habituatedfalter after predator exposure, and the proportion of fish inthe risky patch was significantly higher than before deprivation.Deprived fish took greater shares of the group meal comparedwith control fish, and the pattern of the individual share ofthe group meal after food restriction indicated a change inthe social hierarchy. This study indicates that risk-takingbehavior is state dependent and changes temporarily to compensatefor a period of food restriction. The results are discussedin terms of tradeoffs between food and risk in a period leadingup to an ontogenetic habitat shift.     

Different olfactory system deficits affect the antigonadal action of light deprivation differently in male rats

Twenty-eight day-old male rats were subjected to: Blinding-olfactory bulbectomy, Blinding-peripheral anosmia, Blinding-accessory olfactory bulbectomy and Blinding-sham olfactory operation. A set of rats remained intact. Six weeks later, their pituitary-gonads-accessory sex organs were studied. Bulbectomy as well as peripheral anosmia exaggerated the antigonadal effects of blindness, while the accessory olfactory system impairment did not. It is suggested that olfactory bulbectomy potentiation of the antigonadal effects of light deprivation is due to a lack of sensory function rather than to bulbectomy itself and that the accessory olfactory system which is involved in the priming pheromonal effects does not play any role in the inhibition of the antigonadal effects of blindness.     

Behavior of food objects testing by taste in the carp <Emphasis Type="Italic">Cyprinus carpio</Emphasis> in the norm and at chronic anosmia

Comparative study of behavior of testing artificial food objects (agar-agar pellets containing L-proline 0.1 M, L-alanine 0.1 M, L-glutamine 0.1 M, or L-glutamic acid 0.01 M and control pellets) by intact and olfactorily deprived (16 months) two-year-olds of the carp Cyprinus carpio (TL 8.5 cm) was performed. It was found that chronic anosmia causes in fish an increase in the latent time of response to food objects (period from pellet falling in water up to the moment of its being grasped by fish); however, the main characteristics of behavior related to sensory testing (intraoral gustatory reception) of suitability of food objects for consumption do not change in fish. Intact and deprived carps retain the pellet in the oral cavity at the first grasp for a maximum time and reduce this time with each subsequent retention, whereas the duration of intervals between the grasps do not obey this regularity. In experiments that terminate with pellet consumption, fish perform considerably less repeated acts of testing and retain the pellet at each grasping several times longer than in experiments terminating with the rejection by fish from its consumption. It is suggested that the sensory properties of the food object are evaluated by fish at the moment of its first grasping and that the results of such assessment are the basis for the subsequent behavior whose development can proceed according to two different stereotypes.     

Partial compensatory growth in hybrid tilapia Oreochromis mossambicus × O. niloticus following food deprivation

The capacity of hybrid tilapia Oreochromis mossambicus × O. niloticus [23.2 ± 0.2 g (mean ± SE)] to show compensatory growth was assessed in an 8‐week experiment. Fish were deprived of feed for 1, 2 and 4 weeks, and then fed to satiation for 4 weeks; fish fed to satiation during the experiment served as control. Water temperature gradually declined from 28.1 to 25.5°C throughout the experiment. Specific growth rate (SGR) decreased with progressive food deprivation. At the end of deprivation, body weight was lower in the deprived fish than in the control. Fish deprived for 4 weeks exhibited lower contents of lipids and energy in whole body, and higher moisture content and ratio of protein to energy (P/E) than those of the control; they also consumed feed faster than the control when normal feeding was resumed. All deprived fish showed higher food intake (FI) than that of the control during re‐alimentation; however, enhanced SGR was only observed in the fish deprived for 4 weeks. There were no significant differences in digestibility of protein and energy, food efficiency (FE) or energy retention efficiency between the control and deprived fish. At the end of re‐alimentation, deprived fish failed to catch up in body weight with the control, while content of moisture, lipids and energy, and P/E in whole body of the deprived fish did not significantly differ from that of the control. The results of the experiment revealed that the hybrid tilapia reared in freshwater showed partial capacity for compensatory growth following food deprivation of 4 weeks, and that growth compensation was due mainly to increased FI, rather than to improved FE.     

Functional development of chemosensory systems in the fish ontogeny

Regularities of the functional development of chemosensory systems in the ontogeny of fish has been studied, i.e., the olfactory system, the taste system, and the common chemical sense. The olfactory system begins to function and provides response of juveniles to chemical signals before the taste system. Embryos that have hatched from eggs but that do not yet take food exhibit nonspecialized motor responses to olfactory stimuli already. Immediately after the transition to exogenous feeding, olfactory sensitivity to signals which elicit defensive and feeding behavioral responses begins to form and the ability to differentiate between similar odors develops. The reception of a limited number of taste stimuli occurs in the larvae during the transition to exogenous feeding. With age, the spectrum of effective taste substances expands and the time spent on the definition of palatability by juvenile fishes reduces. Functional development of individual components of the taste system arises heterochronously, i.e., the external (extraoral) form of taste reception arises earlier and more rapidly, and the oral (intraoral) form of taste reception arises slower. No information is available about the functional development of the common chemical sense in the ontogeny of fish. It is assumed that the function of the chemosensory system arises in fish in early larval stages.     

Compensatory growth in juvenile roach Rutilus caspicus: effect of starvation and re‐feeding on growth and digestive surface area

The aim of this study was to investigate compensatory growth in juvenile Rutilus caspicus during starvation and re‐feeding periods. The results confirmed the existence of compensatory growth in R. caspicus which depended on the duration of food deprivation. Complete compensatory growth occurred in the fish that were food deprived for at least 3 weeks. Starvation and re‐feeding had no significant effect on the digestive somatic index and intestinal surface areas in the fish that were food deprived for 1 week, while they showed a significant decrease and increase, during starvation and re‐feeding in the fish that were food deprived for 2 and 3 weeks. This knowledge may have application in aquaculture, as appropriate exploitation of compensatory growth can give increased growth rate and feeding efficiency.     

On the trigeminal percept of androstenone and its implications on the rate of specific anosmia

Specific anosmia is a term that describes an inability to perceive a particular odorant in the context of an otherwise normal olfactory acuity. The most common example, for the odor of androstenone, has been ascribed a prevalence ranging from 2 to 45%. In two experiments we sought to determine whether this wide range could be explained by the difference in steroid concentrations used, and by the degree to which the trigeminal system contributes to perception of androstenone. Experiment 1 demonstrated that high concentrations of androstenone stimulated the trigeminal system, as indicated by electrophysiological recordings. Experiment 2 demonstrated that conscious detection of androstenone is possible based solely on the trigeminal system. Interestingly, detection seems to interact with olfactory acuity in that subjects with a low olfactory sensitivity to androstenone were better able to detect its trigeminal component. The agreement between conscious experience and behavioral discrimination was not well calibrated, in that subjects demonstrated a clear overconfidence in their abilities. Altogether, the current study suggests that androstenone is an odorant that produces a concentration-dependent degree of trigeminal stimulation. This trigeminal component explains the diversity of the reported prevalence of specific anosmia for androstenone and might have implications on future use of specific anosmia as a tool to understand odor processing.     

Effect of cycles of feed deprivation on growth and food consumption of immature three-spined sticklebacks and European minnows

Individual juvenile three-spined sticklebacks Gasterosteus aculeatus and European minnow Phoxinus phoxinus , from sympatric populations, were subjected to four cycles of 1 week of food deprivation and 2 weeks of ad libitum feeding. Mean specific growth rate during the weeks of deprivation was negative and did not differ between species. The three-spined stickleback showed sufficient growth compensation to recover to the growth trajectory shown by control fish daily fed ad libitum . The compensation was generated by hyperphagia during the re-feeding periods, and in the last two periods of re-feeding, the gross growth efficiencies of deprived three-spined sticklebacks were greater than in control fish. The expression of the compensatory changes in growth and food consumption became clearer over the successive periods of re-feeding. The European minnow developed only a weak compensatory growth response and the mass trajectory of the deprived fish deviated more and more from the control trajectory. During re-feeding periods, there were no significant differences in food consumption or gross growth efficiency between control and deprived European minnows. The differences between the two species are discussed in terms of the possible costs of compensatory growth, the control of growth and differences in feeding biology.     

Growth and feeding of juvenile sterlet Acipenser ruthenus L. (Acipenseridae) in a pond after various durations of being preliminarily kept in tanks

It is shown that the level of information richness of the environment in which the juvenile fish were raised at early stages of ontogenesis is one of the determining factors for the development of the most important adaptive patterns of behavior. Minimal values of fullness index, lower body weight, and shorter length, along with a feeding spectrum strongly differing from that in natural conditions, are characteristics of juvenile fish kept preliminarily in the hatchery. The food of this group of fish is dominated by organisms of epibenthos, which may have been detected by the fish using gustatory and tactile receptors. At the same time, the proportion of infaunal invertebrates, the detection of which is only possible using olfaction and electric reception, is minimal. The prolonged development of juvenile fish under conditions of sensory deprivations leads to inadequate behavioral skills, making the process of conventionally reflective “switching” upon the release of such juvenile fish in the wild more difficult.