Taste Responsiveness to Food-Associated Acids in the Squirrel Monkey (Saimiri sciureus)

The taste responsiveness of six adult squirrel monkeys to five food-associated acids was assessed in two-bottle preference tests of brief duration (5 min). In experiment 1 the monkeys were given the choice between tap water and defined concentrations of citric acid, ascorbic acid, malic acid, acetic acid, or tannic acid dissolved in tap water. In experiment 2 the animals were given the choice between a 50 mM sucrose solution and defined concentrations of the same acids dissolved in a 50 mM sucrose solution. With both procedures Saimiri sciureus significantly discriminated concentrations as low as 10 mM ascorbic acid and acetic acid, 5 mM citric acid and malic acid, and 0.2 mM tannic acid from the alternative stimulus. The results showed: (1) that squirrel monkeys respond to the same range of acid concentrations as other nonhuman primate species tested so far, (2) that Saimiri sciureus detects food-associated acids at concentrations well below those present in most fruits, and (3) that the responsiveness of this New World primate to acidic tastants was largely unaffected by the addition of a sweet-tasting substance. The results support the assumption that squirrel monkeys may use sourness and/or astringency of food-associated acids as a criterion for food selection.     

Gustatory Responsiveness to Six Bitter Tastants in Three Species of Nonhuman Primates

Gustatory responsiveness of six adult squirrel monkeys, four spider monkeys, and five pigtail macaques to six bitter tastants was assessed in two-bottle preference tests of brief duration (2 min). Animals were given the choice between a 30-mM sucrose solution and defined concentrations of a bitter tastant dissolved in a 30-mM sucrose solution. With this procedure, Saimiri sciureus, Ateles geoffroyi, and Macaca nemestrina were found to significantly discriminate concentrations as low as 0.2, 0.05, and 0.1 mM quinine hydrochloride; 1, 1, and 0.05 mM caffeine; 20, 5, and 1 mM naringin; 5, 2, and 1 mM salicin; 0.01, 0.001, and 0.02 mM sucrose octaacetate; and 0.05, 0.01, and 0.5 mM denatonium benzoate, from the alternative stimulus. With the exception of naringin in the pigtail macaques, all three species rejected all suprathreshold concentrations of all bitter tastants tested. The spider monkeys and the pigtail macaques displayed the lowest taste avoidance thresholds with three of the six tastants each; in contrast, the squirrel monkeys displayed the highest taste avoidance thresholds with four of the six tastants. The across-tastant patterns of taste avoidance thresholds were identical in spider monkeys and squirrel monkeys; both species displayed the following order of sensitivity: sucrose octaacetate > denatonium benzoate > quinine hydrochloride > caffeine > salicin > naringin. All three primate species were more sensitive to the two artificial tastants (sucrose octaacetate and denatonium benzoate) compared to the four naturally occurring tastants. However, the concentrations detected by all three primate species with the four naturally occurring tastants are well below those reported in plants or arthropods consumed by these species suggesting that they may use bitterness as a criterion for food selection.     

A Blend of Ethanol and (−)-α-Pinene were Highly Attractive to Native Siricid Woodwasps (Siricidae,Siricinae) Infesting Conifers of the Sierra Nevada and the Allegheny Mountains

Woodwasps in Sirex and related genera are well-represented in North American conifer forests, but the chemical ecology of native woodwasps is limited to a few studies demonstrating their attraction to volatile host tree compounds, primarily monoterpene hydrocarbons and monoterpene alcohols. Thus, we systematically investigated woodwasp-host chemical interactions in California’s Sierra Nevada and West Virginia’s Allegheny Mountains. We first tested common conifer monoterpene hydrocarbons and found that (?)-α-pinene, (+)-3-carene, and (?)-β-pinene were the three most attractive compounds. Based on these results and those of earlier studies, we further tested three monoterpene hydrocarbons and four monoterpene alcohols along with ethanol in California: monoterpene hydrocarbons caught 72.3% of all woodwasps. Among monoterpene hydrocarbons, (+)-3-carene was the most attractive followed by (?)-β-pinene and (?)-α-pinene. Among alcohols, ethanol was the most attractive, catching 41.4% of woodwasps trapped. Subsequent tests were done with fewer selected compounds, including ethanol, 3-carene, and ethanol plus (?)-α-pinene in both Sierra Nevada and Allegheny Mountains. In both locations, ethanol plus (?)-α-pinene caught more woodwasps than other treatments. We discussed the implications of these results for understanding the chemical ecology of native woodwasps and invasive Sirex noctilio in North America. In California, 749 woodwasps were caught, representing five species: Sirex areolatus Cresson, Sirex behrensii Cresson, Sirex cyaneus Fabricius, Sirex longicauda Middlekauff, and Urocerus californicus Norton. In West Virginia 411 woodwasps were caught representing four species: Sirex edwardsii Brullé, Tremex columba Linnaeus, Sirex nigricornis F., and Urocerus cressoni Norton.     

Taste Preferences for Five Food-Associated Sugars in the Squirrel Monkey (Saimiri sciureus)

The taste preferences of six adult squirrel monkeys for sucrose, fructose, glucose, lactose, and maltose were assessed in two-solution choice tests of brief duration (5 min). In experiment 1 the monkeys were given the choice between all binary combinations of the saccharides presented in equimolar concentrations of 50, 100, 200, and 400 mM, respectively. Preferences for individual sugars were stable across the concentrations tested and indicate an order of relative effectiveness (sucrose > fructose > glucose ≥ maltose ≥ lactose), which is identical to the order of sensitivity found in this species and similar to findings on relative sweetness in man. In experiment 2 the squirrel monkeys were given the choice between a standard sucrose solution of 50 mM and ascending series of concentrations of the other saccharides in order to determine concentrations that were consumed in equal amounts compared to the standard. Solutions of 100 mM fructose, 300 mM glucose, and 200 mM lactose and maltose were found to be equally effective to the 50 mM sucrose, whereas other concentrations led to marked preferences for one of the alternatives. The finding of concentrations of equal effectiveness are consistent with findings on concentration-dependent loss of discrimination ability in man and support the hypothesis that for squirrel monkeys sucrose may indeed be indiscriminate from fructose, glucose, lactose and maltose when concentrations are suitably adjusted. The results suggest that squirrel monkeys and man share important features of sweet-taste perception.     

Olfaction in the boll weevil,Anthonomus grandis Boh. (Coleoptera: Curculionidae): Electroantennogram studies

Electroantennogram (EAG) techniques were utilized to measure the antennal olfactory responsiveness of adult boll weevils,Anthonomus grandis Boh. (Coleoptera: Curculionidae), to 38 odorants, including both insect and host plant (Gossypium hirsutum L.) volatiles. EAGs of both sexes were indicative of at least two receptor populations: one receptor population primarily responsive to pheromone components and related compounds, the other receptor population primarily responsive to plant odors. Similar responses to male aggregation pheromone components (i.e., compounds I, II, and III + IV) were obtained from both sexes, but females were slightly more sensitive to I. Both sexes were highly responsive to components of the “green leaf volatile complex,” especially the six-carbon saturated and monounsaturated primary alcohols. Heptanal was the most active aldehyde tested. More acceptors responded to oxygenated monoterpenes than to monoterpene hydrocarbons. β-Bisabolol, the major volatile of cotton, was the most active sesquiterpene. In general, males, which are responsible for host selection and pheromone production, were more sensitive to plant odors than were females. In fact, males were as sensitive to β-bisabolol and heptanal as to aggregation pheromone components. Electrophysiological data are discussed with regard to the role of insect and host plant volatiles in host selection and aggregation behavior of the boll weevil.     

Use of Chemical Communication by the Subterranean Rodent Ctenomys talarum (Tuco-Tuco) During the Breeding Season

Solitary subterranean rodents with a low frequency of direct contact between conspecifics are expected to use chemical communication to coordinate social and reproductive behavior. We examined whether reproductive tuco-tucos (Ctenomys talarum) were able to discriminate the reproductive condition, sex, and source population of conspecifics by means of chemical cues contained in urine, feces, soiled shavings, or anogenital secretions. During preference tests in which animals had direct contact with these chemical cues, tuco-tucos were able to determine the reproductive condition of opposite sex conspecifics independent of the source of odor. When only olfactory cues were available, both sexes discriminated reproductive condition of opposite sex individuals using urine. Females were also able to discriminate the reproductive condition of males using soiled shavings. Females spent more time investigating male odors than female odors; except in the case of feces, breeding males spent similar amounts of time investigating male and female odors. No preferences were detected for opposite sex urine from members of an animal's own versus another population. The role of chemical cues in territory defense and breeding performance by this highly territorial subterranean rodent is discussed.     

Gustatory Responsiveness to Polycose in Four Species of Nonhuman Primates

The taste responsiveness of six squirrel monkeys, five pigtail macaques, four olive baboons, and four spider monkeys to polycose, a starch-derived polysaccharide, was assessed in two-bottle preference tests of brief duration (2 min). In experiment 1, the monkeys were given the choice between tap water and defined concentrations of polycose dissolved in tap water. In experiment 2, the animals were given the choice between polycose and sucrose, fructose, glucose, lactose, and maltose presented in equimolar concentrations of 100 and 200 mM, respectively. The animals were found to prefer concentrations of polycose as low as 10 mM (pigtail macaques), 30 mM (olive baboons and spider monkeys), and 60 mM (squirrel monkeys) over tap water. Relative taste preferences were stable across the concentrations tested and indicate an order of relative effectiveness (sucrose > polycose maltose) in squirrel monkeys, spider monkeys, and olive baboons that is similar to the order of relative sweetness in humans. Pigtail macaques, however, displayed an order of relative effectiveness (maltose > polycose sucrose) that differs markedly from that found in the other primate species tested and is similar to relative taste preferences found in rodents such as rats. Both the high sensitivity of the pigtail macaques to polycose and their vivid predilection for this polysaccharide and its disaccharide constituent maltose suggest that Macaca nemestrina, unlike other primates, but like rodents, may have specialized taste receptors for starch.     

Chemical Ecology of Fruit Bat Foraging Behavior in Relation to the Fruit Odors of Two Species of Paleotropical Bat-Dispersed Figs (<Emphasis Type="Italic">Ficus hispida</Emphasis> and <Emphasis Type="Italic">Ficus scortechinii</Emphasis>)

We investigated the fruit odors of two bat-dispersed fig species in the Paleotropics, in relation to the foraging behavior of fruit bats, to test the following hypotheses: 1) fruit odor plays a critical role for detection and selection of ripe figs by fruit bats; 2) bat-dispersed fig species are characterized by the same, or similar, chemical compounds; and 3) total scent production, in bat-dispersed figs, increases when fruits ripen. We performed bioassays to test the effect of both natural and synthetic fig fruit odors on the foraging behavior of the short-nosed fruit bat (Cynopterus brachyotis)—an important disperser of figs within the study area. Fruit bats responded to both visual and chemical (olfactory) cues when foraging for figs. However, the strongest foraging reaction that resulted in a landing or feeding attempt was almost exclusively associated with the presence of a ripe fruit odor—either in combination with visual cues or when presented alone. Fruit bats also used fruit odors to distinguish between ripe and unripe fruits. By using gas chromatography (GC) and GC/mass spectrometry (MS), a total of 16 main compounds were identified in the ripe fruit odor of Ficus hispida and 13 in the ripe fruit odor of Ficus scortechinii—including alcohols, ketones, esters, and two terpenes. Additional compounds were also recorded in F. hispida, but not identified—four of which also occurred in F. scortechinii. Total scent production increased in both species when fruits ripened. Both natural and synthetic fruit odors resulted in feeding attempts by bats, with no feeding attempts elicited by unscented controls. Reaction rates to natural fruit odors were higher than those to synthetic blends.     

Olfactory Mechanisms for Discovery of Odorants to Reduce Insect-Host Contact

Insects have developed highly sophisticated and sensitive olfactory systems to find animal or plant hosts for feeding. Some insects vector pathogens that cause diseases in hundreds of millions of people and destroy billions of dollars of food products every year. There is great interest, therefore, in understanding how the insect olfactory system can be manipulated to reduce their contact with hosts. Here, we review recent advances in our understanding of insect olfactory detection mechanisms, which may serve as a foundation for designing insect control programs based on manipulation of their behaviors by using odorants. Because every insect species has a unique set of olfactory receptors and olfactory-mediated behaviors, we focus primarily on general principles of odor detection that potentially apply to most insects. While these mechanisms have emerged from studies on model systems for study of insect olfaction, such as Drosophila melanogaster, they provide a foundation for discovery of odorants to repel vector insects or reduce their host-seeking behavior.     

Antennal olfactory responsiveness ofMicroplitis croceipes (Hymenoptera: Braconidae) to cotton plant volatiles

Antennal olfactory responses of the parasitoid,Microplitis croceipes (Cresson) (Hymenoptera: Braconidae), to 29 cotton volatile compounds were measured by electroantennogram (EAG) techniques. No significant sexual differences were found in EAGs of males and females to volatiles emanating from 100-μg stimulus loads of the 29 cotton compounds. Green leaf volatiles (saturated and monounsaturated six-carbon alcohols, aldehydes, and their acetate derivatives), heptanal, and the benzene derivatives, benzaldehyde and acetophenone, elicited the largest EAGs. Monoterpenes elicited moderate EAGs withβ-ocimene being the most effective monoterpene tested. Among the sesquiterpenes tested,β-bisabolol was the most effective stimulus at the 100-μg dose. Dose-response curves constructed from EAGs of females revealed a low threshold for (Z)-3-hexenyl acetate, a compound previously shown to be an effective attractant in wind-tunnel bioassays. Comparison of relative volatilities of the various odorants indicated differential selectivity and sensitivity ofM. croceipes antennal receptors to them. The roles of cotton plant volatiles in host habitat location ofM. croceipes are discussed.     

Olfactory Preferences of the Parasitic Nematode <Emphasis Type="Italic">Howardula aoronymphium</Emphasis> and its Insect Host <Emphasis Type="Italic">Drosophila falleni</Emphasis>

Many parasitic nematodes have an environmental infective stage that searches for hosts. Olfaction plays an important role in this process, with nematodes navigating their environment using host-emitted and environmental olfactory cues. The interactions between parasitic nematodes and their hosts are also influenced by the olfactory behaviors of the host, since host olfactory preferences drive behaviors that may facilitate or impede parasitic infection. However, how olfaction shapes parasite-host interactions is poorly understood. Here we investigated this question using the insect-parasitic nematode Howardula aoronymphium and its host, the mushroom fly Drosophila falleni. We found that both H. aoronymphium and D. falleni are attracted to mushroom odor and a subset of mushroom-derived odorants, but they have divergent olfactory preferences that are tuned to different mushroom odorants despite their shared mushroom environment. H. aoronymphium and D. falleni respond more narrowly to odorants than Caenorhabditis elegans and Drosophila melanogaster, consistent with their more specialized niches. Infection of D. falleni with H. aoronymphium alters its olfactory preferences, rendering it more narrowly tuned to mushroom odor. Our results establish H. aoronymphium-D. falleni as a model system for studying olfaction in the context of parasite-host interactions.     

Olfactory Sensitivity of the Gilthead Seabream (Sparus auratus L) to Conspecific Body Fluids

The potential for intraspecific chemical communication in the gilthead seabream (a marine perciform) was investigated by assessing the olfactory sensitivity to conspecific body-fluids (water occupied by conspecifics, intestinal fluid, urine, semen, egg fluid) by multiunit electrophysiological recording from the olfactory nerve. The olfactory system was responsive to water previously occupied by conspecifics, and the active compound(s) could be extracted by solid-phase extraction. The olfactory system was extremely sensitive to body fluids of sexually mature conspecifics: thresholds of detection were 1:10^7.4 (intestinal fluid), 1:10^6.1 (gametes), and 1:10^4.2 (urine). The olfactory system was also sensitive to amino acids with thresholds of detection from 10^–8.1 M (l-leucine) to 10^–6.1 M (l-phenylalanine). However, a range of other known fish odorants (steroids, bile acids, and prostaglandins) failed to evoke significant responses. Given the high olfactory sensitivity to intestinal fluid and the low urine release rates of marine compared with freshwater fish, we suggest that chemical communication is likely to be mediated via compounds present in the intestinal fluid rather than urine. Furthermore, the types of chemicals involved are likely to be different from those of freshwater fish. Their exact chemical identity and biological roles remain to be established.     

Odor Detection in Insects: Volatile Codes

Insect olfactory systems present models to study interactions between animal genomes and the environment. They have evolved for fast processing of specific odorant blends and for general chemical monitoring. Here, we review molecular and physiological mechanisms in the context of the ecology of chemical signals. Different classes of olfactory receptor neurons (ORNs) detect volatile chemicals with various degrees of specialization. Their sensitivities are determined by an insect-specific family of receptor genes along with other accessory proteins. Whereas moth pheromones are detected by highly specialized neurons, many insects share sensitivities to chemical signals from microbial processes and plant secondary metabolism. We promote a more integrated research approach that links molecular physiology of receptor neurons to the ecology of odorants.     

Cell-Based Odorant Sensor Array for Odor Discrimination Based on Insect Odorant Receptors

The olfactory system of living organisms can accurately discriminate numerous odors by recognizing the pattern of activation of several odorant receptors (ORs). Thus, development of an odorant sensor array based on multiple ORs presents the possibility of mimicking biological odor discrimination mechanisms. Recently, we developed novel odorant sensor elements with high sensitivity and selectivity based on insect OR-expressing Sf21 cells that respond to target odorants by displaying increased fluorescence intensity. Here we introduce the development of an odorant sensor array composed of several Sf21 cell lines expressing different ORs. In this study, an array pattern of four cell lines expressing Or13a, Or56a, BmOR1, and BmOR3 was successfully created using a patterned polydimethylsiloxane film template and cell-immobilizing reagents, termed biocompatible anchor for membrane (BAM). We demonstrated that BAM could create a clear pattern of Sf21 sensor cells without impacting their odorant-sensing performance. Our sensor array showed odorant-specific response patterns toward both odorant mixtures and single odorant stimuli, allowing us to visualize the presence of 1-octen-3-ol, geosmin, bombykol, and bombykal as an increased fluorescence intensity in the region of Or13a, Or56a, BmOR1, and BmOR3 cell lines, respectively. Therefore, we successfully developed a new methodology for creating a cell-based odorant sensor array that enables us to discriminate multiple target odorants. Our method might be expanded into the development of an odorant sensor capable of detecting a large range of environmental odorants that might become a promising tool used in various applications including the study of insect semiochemicals and food contamination.     

Odor and Structure

In contrast to previous hypotheses that there are a few primary odors, recent results show the existence of an extremely large number of receptors each capable of recognizing a small number of odorants. Although in principle enantiomers have different odors, in many cases the size of the difference is small or even zero. Minor structural change often has a major effect on the odor perceived. Detailed results of structure-odor relationship have been obtained with several classes of odorants. Most investigated are the classes of fatty aldehydes, degraded carotenoids, sandalwood odorants, ambergris and musk compounds. Various rules and correlations have been established. Despite numerous excellent studies during the last 30 years the area of structure-odor relationship remains rather confusing.     

Serum α-lipoprotein responses to variations in dietary cholesterol,protein and carbohydrate in different non-human primate species

Serum α-lipoprotein responses to variations in dietary cholesterol, protein, and carbohydrate were studied in different nonhuman primate species. Chimpanzee, rhesus, green, patas, squirrel and spider monkeys all showed significant interspecies differences in serum total cholesterol responses to 1.84 mg/kcal exogenous cholesterol. Dietary cholesterol significantly increased the α-lipoprotein cholesterol in all species except rhesus and chimpanzee. Among these species, there was no relationship between the basal serum lipoprotein profile and subsequent lipoprotein responses to dietary cholesterol. Although the level of dietary protein at 6%, 12%, and 37% of calories had no appreciable main effect on serum total cholesterol in spider monkeys, very low protein diet (6% of calories) produced a significant elevation in α-lipoprotein cholesterol. Serum α-lipoprotein responses to exogenous cholesterol (1.84 mg/kcal) was highest for the very low protein diet and lowest for low protein diet (12% of calories). Diets with high sucrose (76.5% of calories) and low saturated fat (12.5% of calories) containing no added cholesterol were tested in squirrel and spider monkeys and produced a consistent serum total cholesterol response; the α-lipoprotein response was significantly higher in squirrel monkeys than in spider monkeys. The above findings have implications in experimentally induced and comparative atherogenesis. Presented at the Lipoprotein Symposium AOCS meeting, St. Louis, Missouri, May 1978.     

Sour-Taste Tolerance in Four Species of Nonhuman Primates

The taste of most fruits is characterized by a mixture of sensations termed sweet and sour by humans, and the food selection behavior of primates suggests that they may use the relative salience of sweetness and sourness to assess palatability of potential food items. Therefore, taste responses of six squirrel monkeys, five pigtail macaques, four olive baboons, and four spider monkeys to sweet-sour taste mixtures were assessed in two-bottle preference tests of brief duration (2 min). Monkeys were given the choice between a reference solution of 50 mM sucrose and mixtures containing 10, 30, or 50 mM citric acid plus 10, 20, 50, 100, 200, 400, 800, or 1000 mM sucrose. We found that the four species differed markedly in their acceptance of physiological concentrations of sour-tasting citric acid. Whereas olive baboons showed the highest degree of sour-taste tolerance and actually preferred most of the sweet-sour taste mixtures over sweet-tasting reference solutions, squirrel monkeys showed the lowest degree of sour-taste tolerance and rejected most of the sweet-sour taste mixtures even when they contained considerably more sucrose than the reference solutions. Additional tests demonstrated that the preference for sweet-sour taste mixtures was not based on masking effects. Rather, the animals perceived both the sweetness and the sourness of the taste mixtures and made a trade-off between the attractive and aversive properties of the two taste qualities. The results of this study suggest that the proximate reason for the marked differences in acceptance of sweet-sour taste mixtures are differences among species in the hedonic evaluation of the sour taste of citric acid. Possible ultimate reasons, which do not necessarily exclude, but may complement each other, include evolutionary adaptation to dietary specialization, avoidance of competition pressure, and phylogenetic relatedness.     

Effects of monoterpene odors on food selection by red deer calves (Cervus elaphus)

The response of red deer calves (Cervus elaphus) to the odors of Sitka spruce (Picea sitchensis) and lodgepole pine (Pinus conforta) needles and five monoterpene constituents of their essential oils was measured by simple two-choice feeding trials. All odors were significantly rejected (P < 0.05) except Sitka spruce and lodgepole pine by females and Sitka spruce and alpha-terpineol by males. Females had a stronger dislike of all odors except lodgepole pine than males. Rejection of monoterpene odors weakened slightly with time. A strong logarithmic relationship between the strength of the rejection response and vapor pressure of the compounds tested suggested that the odors were rejected on the basis of concentration rather than quality.Research supported by the Natural Environment Research Council and the Forestry Commission.     

The use of Odors at Different Spatial Scales: Comparing Birds with Fish

Salmon travel hundreds of kilometers of open ocean and meandering rivers to return to their natal stream to spawn; procellariiform seabirds soar over thousands of kilometers of the ocean's surface searching for foraging opportunities and accurately return to their nesting islands. These large-scale olfactory-guided behaviors are among the most dramatic examples of animal navigation ever described. At much closer ranges, the sense of smell can be used for behaviors as diverse as tracking prey, nest location, and mate selection. Both fish and birds face similar problems interpreting olfactory information in fluid mediums where odors are dispersed as filamentous patches. Similar to insects, which have served as model organisms for investigating olfactory related behaviors, the few fish and bird species that have been studied tend to use olfactory information in conjunction with other sensory modalities. Similar to insects, fish and birds also employ oscillatory or cross-stream movement as sampling mechanisms. This review compares and contrasts the use of odors by fish and birds over a range of spatial scales that span from thousands of kilometers to less than a meter. In so doing, we identify behavioral similarities and new questions that need to be addressed regarding the olfactory ecology of these diverse groups of organisms.