Marine mammals such as cetaceans and pinnipeds are known to have largely lost their sense of taste, probably due to their transition from a mixed to a strictly carnivorous diet and from masticating plant-based food to swallowing their animal prey whole. In contrast, nothing is known so far about the functionality of the sense of taste in sirenians, the only extant herbivorous marine mammals. Using two-bottle preference tests of short duration (2 min), we therefore assessed the gustatory responsiveness of three adult male Greater Caribbean manatees (Trichechus manatus manatus) to food-associated substances representing the five canonical taste qualities. Further, we assessed if the manatees display a preference for the taste of freshwater over that of seawater. We found that the manatees showed no significant preference for or significant avoidance of any of the taste stimuli when presented at concentrations that are detectable for most mammal species tested so far. This was true both when using seawater or freshwater as the solvent and as the alternative stimulus. The manatees also showed no significant preference for freshwater over seawater. These results are not consistent with anatomical findings that reported manatees to possess a high number of taste buds and with genetic findings suggesting the taste receptor genes of manatees to be intact. Further, they do not align with the notion that access to freshwater sources is an important feature of their habitat. Our results suggest that the herbivorous dietary specialization of manatees may not have prevented a reduction in their sense of taste. However, at this point we cannot decide whether the manatees can't taste or don't care about taste.

Environmental enrichment is used to enhance the well-being of zoo-housed animals by providing a variety of stimuli and to encourage the expression of species-specific natural behaviours. This study assessed the effects of different types of environmental enrichment on the behaviour of 13 cinereous vultures Aegypius monachus in a zoo setting. Six enrichment items were used: large carcasses, forage boxes, twig balls, a wooden box with tubes, mirrors, and basketballs. Vulture behaviour was observed and compared between a baseline period and an enrichment period. The vultures only interacted with the large carcass and mirror enrichments, likely due to neophobia toward novel stimuli. However, we found a significant decrease in abnormal repetitive behaviours during the enrichment period, even with enrichment items that the vultures did not directly interact with. Finally, the presentation of large carcasses allowed the zoo-housed vultures to behave more naturally as they would in the wild, significantly increasing their social and locomotive behaviours. Overall, this study highlights the importance of providing optimal conditions for zoo-housed vultures, particularly given the endangered status of many species and their involvement in breeding programs aimed to boost wild populations.

Field studies suggest that the size of potential food items plays an important role in the food selection behavior of nonhuman primates. However, there is only limited knowledge about how good primates are at visually discriminating between the size of three-dimensional objects of the same kind and shape. We therefore conducted two experiments on ten adult spider monkeys: a two-choice test based on spontaneous preferences with differently-sized pieces of food of the same kind and shape, and a two-choice test based on an operant conditioning procedure in which the animals were trained to choose the larger one of two cube-shaped wooden blocks. We found that the spider monkeys displayed a robust and spontaneous preference for the larger one of two simultaneously presented pieces of food of the same kind when the size difference was 11% or larger. This was true with cube-shaped food pieces as well as with ball-shaped and hemisphere-shaped food pieces. Considering that the normal size variation among fully ripe fruits of a given plant species is at least 10% this suggests that spider monkeys are as picky as necessary to make size-based food choices in line with optimal foraging theory. We also found that the spider monkeys successfully discriminated between two simultaneously presented wooden cubes when their edge length differed by only 2 mm which was the smallest size difference tested. Thus, they displayed a well-developed ability to visually discriminate between three-dimensional non-edible objects of the same kind and shape which is at least as good as that of other nonhuman primate species tested previously on similar tasks. Our findings support the notion that frugivory may have favored the evolution of cognitive abilities in the physical domain which may, possibly, include the ability to perform fine visual size discriminations.

Food selection in primates is guided by a sensory evaluation of the physical and chemical properties of the foods. These properties vary with plant species, plant part, and plant maturity. Spider monkeys generally consume ripe fruits, but their diet also includes unripe fruits and young and mature leaves from a wide variety of plant species. We evaluated food selection in ten adult black-handed spider monkeys (Ateles geoffroyi) living in a controlled environment in Catemaco (Veracruz, Mexico). We used six plant species which are part of their natural diet and compared selection between ripe and unripe fruits and young and mature leaves, respectively, for the same plant species. We also analyzed the sucrose content, pH, size, and color of fruits and the color and size of leaves of each plant species. For fruit selection, our model showed that 75% of choices depended on an association between the plant species and the stage of maturity. In contrast, our model predicted 52% of the leaf selection, and monkeys considered both the stage of maturity and the plant species. Our results suggest that Ateles geoffroyi exhibit a more specific food selection for fruits than leaves, resulting in different food choices based on the physical and chemical properties of these food items.

Geoffroy’s spider monkeys (Ateles geoffroyi) can modulate the acidity-alkalinity (pH) and salivary expression of total proteins (TP) and proline-rich proteins (PRPs) depending on the concentration of tannins in their diet, helping to counteract negative post-ingestive effects. Besides tannins, plants produce a wide variety of secondary metabolites like flavonoids and alkaloids that elicit a bitter taste. Geoffroy’s spider monkeys feed on various plant species and consume different concentrations of secondary metabolites. However, it is unclear whether there is salivary modulation of pH, TP, and PRPs to secondary metabolites other than tannins, or whether this effect also occurs towards bitter substances not associated with secondary metabolites. Therefore, we assessed if there are changes in salivary pH, TP, and PRPs expression towards bitter substances or if spider monkeys display a specific response to secondary metabolites present in their diet and substances not associated with secondary metabolites. We determined the concentration of tannic acid, caffeine and rutin in fruits and leaves in different maturity stages reported as a part of the diet of Geoffroy’s spider monkeys. We presented six adults Geoffroy’s spider monkeys with different concentrations of tannic acid, caffeine, and rutin (0.1, 0.3, 0.6 and one mM) and denatonium benzoate (0.001, 0.003, 0.006 and 0.01 mM) dissolved in a 30 mM sucrose solution. We administered each concentration and collected saliva using swabs (SalivaBio). We used test paper strips to measure the pH and determined the TP concentration using the Bradford method at 595 nm. We also determined the percentage of PRPs using sodium dodecyl sulfate–polyacrylamide gel electrophoresis (SDS-PAGE). The results showed marked differences in tannic acid, caffeine and rutin concentration depending on the plant part and species. We found an increase in salivary pH in response to consumption of secondary metabolites, no variations in TP concentration, variations in the percentage of PRPs associated with tannic acid concentrations, and no significant changes when the animals consumed denatonium benzoate. Our results showed that spider monkeys specifically modulate acidity-alkalinity towards secondary metabolites and salivary PRPs expression towards tannic acid in their diet, and that they do not have a generalized salivary response to bitter compounds that are typically considered as toxic substances.

Geosmin, a ubiquitous volatile sesquiterpenoid of microbiological origin, is causative for deteriorating the quality of many foods, beverages, and drinking water, by eliciting an undesirable "earthy/musty" off-flavor. Moreover, and across species from worm to human, geosmin is a volatile, chemosensory trigger of both avoidance and attraction behaviors, suggesting its role as semiochemical. Volatiles typically are detected by chemosensory receptors of the nose, which have evolved to best detect ecologically relevant food-related odorants and semiochemicals. An insect receptor for geosmin was recently identified in flies. A human geosmin-selective receptor, however, has been elusive. Here, we report on the identification and characterization of a human odorant receptor for geosmin, with its function being conserved in orthologs across six mammalian species. Notably, the receptor from the desert-dwelling kangaroo rat showed a more than 100-fold higher sensitivity compared to its human ortholog and detected geosmin at low nmol/L concentrations in extracts from geosmin-producing actinomycetes.

The number of functional genes coding for olfactory receptors differs markedly between species and has repeatedly been suggested to be predictive of a species' olfactory capabilities. To test this assumption, we compiled a database of all published olfactory detection threshold values in mammals and used three sets of data on olfactory discrimination performance that employed the same structurally related monomolecular odour pairs with different mammal species. We extracted the number of functional olfactory receptor genes of the 20 mammal species for which we found data on olfactory sensitivity and/or olfactory discrimination performance from the Chordata Olfactory Receptor Database. We found that the overall olfactory detection thresholds significantly correlate with the number of functional olfactory receptor genes. Similarly, the overall proportion of successfully discriminated monomolecular odour pairs significantly correlates with the number of functional olfactory receptor genes. These results provide the first statistically robust evidence for the relationship between olfactory capabilities and their genomics correlates. However, when analysed individually, of the 44 monomolecular odourants for which data on olfactory sensitivity from at least five mammal species are available, only five yielded a significant correlation between olfactory detection thresholds and the number of functional olfactory receptors genes. Also, for the olfactory discrimination performance, no significant correlation was found for any of the 74 relationships between the proportion of successfully discriminated monomolecular odour pairs and the number of functional olfactory receptor genes. While only a rather limited amount of data on olfactory detection thresholds and olfactory discrimination scores in a rather limited number of mammal species is available so far, we conclude that the number of functional olfactory receptor genes may be a predictor of olfactory sensitivity and discrimination performance in mammals.

White-faced sakis (Pithecia pithecia) are commonly considered as frugivores but are unusual among primates as they do not specialize on ripe fruits but rather include a high proportion of unripe fruits into their diet, even during seasons when ripe fruits are available. Using a two-bottle preference test of short duration we therefore assessed whether this dietary specialization affects the taste responsiveness and sour-taste tolerance of four adult white-faced sakis for five food-associated acids. We found taste preference thresholds of the sakis to be 1-10 mM for citric acid, 0.5-20 mM for ascorbic acid, 2-10 mM for malic acid, 0.1-1 mM for tannic acid, and 2-20 mM for acetic acid, respectively. When given the choice between a reference solution of 50 mM sucrose and mixtures containing varying concentrations of sucrose plus citric acid, the sakis displayed a high sour-taste tolerance and required only 100 mM of sucrose (when mixed with 10 mM citric acid) or 200 mM of sucrose (when mixed with 30 or 50 mM citric acid), respectively, to prefer the sweet-sour mixture over the purely sweet 50 mM sucrose reference solution. These results demonstrate that white-faced sakis have a well-developed taste sensitivity for food-associated acids which is not inferior to that of primates specializing on ripe fruits. Compared to other platyrrhine primates, the sakis displayed a markedly higher sour-taste tolerance. These results may therefore reflect an evolutionary adaptation to the dietary specialization of the white-faced sakis to sour-tasting unripe fruits.

Recent research suggests that socio-ecological factors such as dietary specialization and social complexity may be drivers of advanced cognitive skills among primates. Therefore, we assessed the ability of 12 black-handed spider monkeys (Ateles geoffroyi), a highly frugivorous platyrrhine primate with strong fission-fusion dynamics, to succeed in a serial visual reversal learning task. Using a two-alternative choice paradigm we first trained the animals to reliably choose a rewarded visual stimulus over a non-rewarded one. Upon reaching a pre-set learning criterion we then switched the reward values of the two stimuli and assessed if and how quickly the animals learned to reverse their choices, again to a pre-set learning criterion. This stimulus reversal procedure was then continued for a total of 80 sessions of 10 trials each. We found that the spider monkeys quickly learned to reliably discriminate between two simultaneously presented visual stimuli, that they succeeded in a visual reversal learning task, and that they displayed an increase in learning speed across consecutive reversals, suggesting that they are capable of serial reversal learning-set formation with visual cues. The fastest-learning individual completed five reversals within the 80 sessions. The spider monkeys outperformed most other primate and nonprimate mammal species tested so far on this type of cognitive task, including chimpanzees, with regard to their learning speed in both the initial learning task and in the first reversal task, suggesting a high degree of behavioral flexibility and inhibitory control. Our findings support the notion that socio-ecological factors such as dietary specialization and social complexity foster advanced cognitive skills in primates.

Studies of food preferences in captive primates have so far mainly been restricted to frugivorous species. It was therefore the aim of the present study to assess the occurrence of spontaneous food preferences in a mainly folivorous primate, the captive Southern brown howler monkey, and to analyze whether these preferences correlate with nutrient composition. Using a two-alternative choice test, we presented ten male and five female adult Alouatta guariba clamitans with all possible binary combinations of ten types of food that are part of their diet in captivity and recorded their choice behavior. We found the howler monkeys to display the following rank order of preference: banana > mango > watermelon > papaya > beetroot > apple > pear > orange > cucumber > tomato. This preference ranking significantly and positively correlated with the total carbohydrate content and with the sucrose content of the food items. We also found significant positive correlations between the food preference ranking and the content of the minerals copper and magnesium. Male and female howler monkeys did not differ significantly in their food preference rankings. These results suggest this howler monkeys under human care are not opportunistic, but selective feeders with regard to maximizing their net gain of energy as only the content of carbohydrates, but not the contents of total energy, proteins, or lipids significantly correlated with the displayed food preferences. Thus, the food preferences of this primate are similar to those reported in several species of frugivorous primates tested with cultivated fruits and vegetables.

Differences in taste perception between species are thought to reflect evolutionary adaptations to dietary specialization. White-faced sakis (Pithecia pithecia) are commonly considered as frugivores but are unusual among primates as they do not serve as seed dispersers but rather prey upon the seeds of the fruits they consume and are thought to exploit the lipids and proteins that these seeds contain in high amounts. Using a two-bottle preference test of short duration we therefore assessed whether this dietary specialization affects the taste responsiveness of four adult white-faced sakis for five food-associated carbohydrates. We found that the sakis significantly preferred concentrations as low as 10 mM sucrose, 10-40 mM fructose, 20-30 mM glucose and maltose, and 30-40 mM lactose over tap water. When given the choice between all binary combinations of these five saccharides presented at equimolar concentrations of 100, 200, and 300 mM, respectively, the sakis displayed significant preferences for individual saccharides in the following order: sucrose > fructose > glucose ≥ maltose = lactose. These results demonstrate that seed-predating white-faced sakis have a well-developed taste sensitivity for food-associated carbohydrates which is not inferior to that of most other primates including seed-dispersing frugivores, but rather ranks among the more sweet-taste sensitive species. Further, they show that their pattern of relative preference for the five carbohydrates is similar to that found in other frugivorous primate species. These findings may represent an example of Liem's paradox as the sakis' morphological adaptations to efficiently predate on and exploit the lipid- and protein-rich hard-shelled seeds of fruits does not compromise their ability to detect the carbohydrates found in the pulp of fruits at low concentrations.

Horses (Equus ferus caballus) engage their sense of smell in numerous behaviors. However, only few studies so far evaluated responses of horses to olfactory stimuli presumed to be either attractive or aversive and rather focused on presenting horses with only one type of odor. Therefore, we assessed behavioral responses of horses towards seven natural odors that are either potentially threatening, or socially attractive, or socially aversive. To this end, we presented a total of 10 horses with the following odors: same-sex and opposite-sex horse feces; same-sex and opposite-sex horse urine; tiger (Panthera tigris) feces and urine; and horse blood attached to one of two simul-taneously presented food buckets and recorded their behavior. We found that the horses displayed clear behavioral reactions towards potentially threatening odors (tiger feces and urine; horse blood) compared to socially attractive (opposite-sex feces and urine) and, in some cases, socially aversive (same-sex feces and urine) odors. More precisely, the horses put their ears back significantly more frequently and tended to do it for longer in the potentially threatening odor condition compared to the socially attractive one. In the potentially threat-ening odor condition, the horses ate from the control bucket significantly more frequently compared to the other two conditions. Detailed analyses showed that the horses' behavioral responses were particularly pronounced following exposure to tiger feces and urine. Furthermore, we found that, in some situations, socially aversive odor stimuli caused higher vigilance and more cautious approach, as reflected in increased time of sniffing the odor-bearing bucket and decreased frequency of eating from it in the socially aversive compared to the poten-tially threatening odor condition. These findings suggest that horses, which are known as prey and social ani-mals, are sensitive to social odors and even more so to odors from predators.

We assessed two aspects of numerical cognition in a group of nine captive spider monkeys (Ateles geoffroyi). Petri dishes with varying amounts of food were used to assess relative quantity discrimination, and boxes fitted with dotted cards were used to assess discrete number discrimination with equally-sized dots and various-sized dots, respectively. We found that all animals succeeded in all three tasks and, as a group, reached the learning criterion of 70% correct responses within 110 trials in the quantity discrimination task, 160 trials in the numerosity task with equally-sized dots, and 30 trials in the numerosity task with various-sized dots. In all three tasks, the animals displayed a significant correlation between performance in terms of success rate and task difficulty in terms of numerical similarity of the stimuli and thus a ratio effect. The spider monkeys performed clearly better compared to strepsirrhine, catarrhine, and other platyrrhine primates tested previously on both types of numerical cognition tasks and at the same level as chimpanzees, bonobos, and orangutans. Our results support the notion that ecological traits such as a high degree of frugivory and/or social traits such as a high degree of fission-fusion dynamics may underlie between-species differences in cognitive abilities.

Tannins are a chemical defense mechanism of plants consumed by herbivores. Variations in salivary physicochemical characteristics such as pH, total protein concentration (TP), and presence of proline-rich proteins (PRPs) in animals have been reported as a mechanism to protect the oral cavity when consuming food with variations in pH and tannins. Variations in salivary physiochemistry as adaptations for consuming tannin-rich foods have been found in omnivorous and folivorous primates, but have not yet been reported in frugivorous species such as spider monkeys. We therefore assessed changes in pH using test strips, TP concentration by measuring absorbance at 595 nm in a spectrophotometer and salivary PRPs using the SDS-PAGE electrophoresis technique in the saliva of nine captive spider monkeys in response to the consumption of solutions with different concentrations of tannic acid. The results showed variations in pH, TP concentration and the presence and variation of possible salivary PRPs associated with tannic acid concentration. These findings suggest that spider monkeys may tailor their salivary physicochemical characteristics in response to the ingestion of potentially toxic compounds.

There is extensive knowledge about the visual system and the implications of the evolution of trichromatic color vision in howler monkeys (genus Alouatta ) related to food selection; however, information about the other sensory systems is limited. In this study we assessed the use of touch, sniffing, and taste in fruit evaluation by 20 adult mantled howler monkeys ( Alouatta palliata ) on Agaltepec Island, Mexico. During 9 months of observation, we recorded the frequency that each monkey used touch, sniffing, and taste in evaluating cryptic fruits (that remain green during their ripening process) and conspicuous fruits (with red, yellow, or orange colorations when they are ripe). Sucrose content and hardness measurements were made to establish the degree of ripeness of the fruits. We found that mantled howler monkeys used long behavioral sequences during conspicuous fruit investigations. Sniffing was used infrequently, but significantly more often in the evaluation of conspicuous-ripe and unripe fruits compared to cryptic-ripe and unripe fruits. During the evaluation of cryptic-ripe fruits, mantled howler monkeys increased the use of touch compared to evaluating cryptic-unripe fruits. We did not find significant differences in the use of taste in the evaluation of cryptic and conspicuous fruits (both ripe and unripe). Our results suggest that the non-visual senses play an essential role in fruit selection by howler monkeys, with differences in the behavioral strategy according to the fruit's conspicuity. The multimodal signals of ripe and unripe fruits allow the howler monkeys to assess their palatability before being consumed.

The role that single nutrients may play for food choices in nonhuman primates is not fully understood. White-faced sakis ( Pithecia pithecia ) are unusual among frugivorous primates as they do not serve as seed dispersers but rather exploit the seeds they consume, presumably for their high contents of lipids and proteins. Therefore, we assessed the occurrence of spontaneous food preferences in zoo-housed white-faced sakis and analyzed whether these preferences correlate with nutrient composition. Using a two-alternative choice test, we repeatedly presented three female and two male sakis with all possible binary combinations of 15 types of food that are part of their diet under human care, and found them to display the following rank order of preference: peanut > hazelnut > avocado > melon > egg > apple > mealworms > beetroot > carrot > cucumber > cabbage > tomato > sweet potato > broccoli > eggplant. This preference ranking significantly and positively correlated with the total energy content of the food items. However, we found the strongest positive correlation among the three macronutrients providing metabolic energy between the sakis’ food preferences and lipid content. This is remarkable as all other primate species tested so far using this method displayed the strongest correlation with carbohydrates instead. Together with our finding that the sakis significantly preferred foods high in mono-unsaturated fatty acids, the building blocks of lipids, these results support the notion that white-faced sakis exploit the lipids contained in seeds to meet their requirements of metabolic energy.

Taste-induced facial expressions are thought to reflect the hedonic valence of an animal's gustatory experience. We therefore assessed taste-induced facial responses in six black-handed spider monkeys (Ateles geoffroyi) to water, sucrose, caffeine, citric acid and aspartame, representing the taste qualities sweet, bitter, and sour, respectively. We decided not to include salty-tasting substances as the concentrations of such tastants found in the fruits consumed by spider monkeys are below their taste preference threshold. We found that the monkeys displayed significant differences in their facial responses between substances, with significantly higher frequencies of licking, sucking, closed eyes, tongue protruding, mouth gaping and lip smacking in response to sucrose, a presumably pleasant stimulus. The response to caffeine and citric acid, in contrast, yielded the lowest frequencies of these behaviors, but the highest frequency of withdrawals from the stimulus, suggesting these substances are perceived as unpleasant. Lip stretching, a newly described behavior, was performed significantly more often in response to caffeine than to any other substance, suggesting an association with the response to bitter taste. The facial response to the artificial sweetener aspartame was generally similar to the response to water, corroborating the notion that Platyrrhines may be unable to detect its sweetness. Overall, the present study supports the idea of similarity of taste-induced facial responses in non-hominoid primates and humans, suggesting these displays to be evolutionarily conserved across the primate order.