Behavioral Neuroscience 2003, Vol. 117, No. 6, 1142–1149
Copyright 2003 by the American Psychological Association, Inc. 0735-7044/03/$12.00 DOI: 10.1037/0735-7044.117.6.1142
Olfactory Sensitivity for Aliphatic Esters in Spider Monkeys (Ateles geoffroyi) Laura Teresa Hernandez Salazar
Matthias Laska
Universidad Veracruzana
University of Munich Medical School
Ernesto Rodriguez Luna Universidad Veracruzana
Using a conditioning paradigm, the authors investigated the olfactory sensitivity of 3 spider monkeys (Ateles geoffroyi) for a homologous series of aliphatic esters (ethyl acetate to n-octyl acetate) and isomeric forms of some of these substances. With all odorants, the monkeys significantly discriminated concentrations below 1 ppm from the odorless solvent, and in several cases, individual monkeys even demonstrated thresholds below 1 ppb. The results showed spider monkeys to have a high olfactory sensitivity for aliphatic esters, which for the majority of substances matches or even is better than that of species such as the rat, the mouse, or the dog. These findings support the assumption that betweenspecies comparisons of neuroanatomical features are poor predictors of olfactory performance.
to members of this order of mammals (Heymann, 1998; Kappeler, 1998; Smith & Abbott, 1998). Laska and coworkers introduced a new behavioral test that, for the first time, allowed the assessment of olfactory performance in two species of nonhuman primates, the squirrel monkey (Saimiri sciureus) and the pigtail macaque (Macaca nemestrina), using psychophysical methods (Hu¨bener & Laska, 2001; Laska & Hudson, 1993a). Subsequent studies demonstrated that both species possess highly developed olfactory discrimination abilities (Laska & Freyer, 1997; Laska & Hudson, 1993b, 1995; Laska, Liesen, & Teubner, 1999; Laska & Teubner, 1998; Laska, Trolp, & Teubner, 1999), as well as an excellent long-term memory for odors (Hu¨bener & Laska, 1998; Laska, Alicke, & Hudson, 1996). Further, these studies showed that Saimiri sciureus and Macaca nemestrina have a well-developed olfactory sensitivity for aliphatic carboxylic acids (Laska, Seibt, & Weber, 2000), esters (Laska & Seibt, 2002b), alcohols (Laska & Seibt, 2002b), and aldehydes (Laska, Hofmann, & Simon, 2003) that is not generally inferior to, and in some cases is even better than, that of species traditionally regarded as being macrosmatic. In order to get an indication of whether squirrel monkeys and pigtail macaques are special in their olfactory performance or whether a more general reevaluation of the efficiency of the sense of smell in simian primates should be considered, we believe that it is worthwhile to conduct corresponding investigations of olfactory capacity using other primate species. This should also allow us to further assess the suitability of allometric comparisons of neuroanatomical features to predict olfactory performance, and thus the validity of the concept of microsmatic and macrosmatic species. A comparison of olfactory capabilities between different primate species might also help to reveal evolutionary adaptations of this sensory system among this order of mammals (Barton, Purvis, & Harvey, 1995).
There is a long-standing tradition in olfactory research of assigning animal species or even whole orders of animals as being “macrosmatic,” that is, having a keen sense of smell, or as being “microsmatic,” that is, having a poor sense of smell. This dichotomy is mainly, if not exclusively, based on an interpretation of neuroanatomical features such as the relative size of olfactory brain structures or the absolute size of olfactory epithelia (Farbman, 1992; Stephan, Baron, & Frahm, 1988). However, physiological evidence supporting a positive correlation between allometric measures of neuroanatomical structures and olfactory performance is largely lacking (Brown, 2001; De Winter & Oxnard, 2001; Schoenemann, 2001). Primates, for example, are invariably regarded as microsmatic animals (e.g., King & Fobes, 1974; Walker & Jennings, 1991), at least partly as a result of the fact that the massive increase in their neocortex volume during evolution led to a decrease in the relative size (although not necessarily the absolute size) of their olfactory bulbs, that is, the first neuropil of the olfactory pathway (Barton, 1996). In recent years, however, an increasing number of behavioral observations call into question the still widely held belief that primates have generally only poor olfactory capabilities and that this sensory modality is of only little, if any, behavioral relevance
Laura Teresa Hernandez Salazar and Ernesto Rodriguez Luna, Instituto de Neuro-Etologia, Universidad Veracruzana, Xalapa, Mexico; Matthias Laska, Department of Medical Psychology, University of Munich Medical School, Munich, Germany. Financial support provided by the Volkswagen Foundation (I/77 391) is gratefully acknowledged. Laura Teresa Hernandez Salazar was awarded Grant 124786 by Conacyt Mexico. Correspondence concerning this article should be addressed to Matthias Laska, Department of Medical Psychology, University of Munich Medical School, Goethestrasse 31, D-80336 Munich, Germany. E-mail:
[email protected] 1142
OLFACTORY SENSITIVITY IN SPIDER MONKEYS
Recently, the authors of the present study successfully introduced the behavioral test used with squirrel monkeys and pigtail macaques to another primate species, the spider monkey (Ateles geoffroyi; Laska, Hernandez Salazar, & Rodriguez Luna, 2003). It was therefore the aim of the present study to assess the olfactory sensitivity of Ateles geoffroyi by determining olfactory detection thresholds for an array of monomolecular odorants. We chose aliphatic esters as odor stimuli because this class of substances comprises the quantitatively and qualitatively dominant components in a wide variety of fruit odors (Nursten, 1970; Rouseff & Leahy, 1995) and thus is presumed to be behaviorally relevant for these primates, and because comparative data from humans and, at least for the majority of odorants, from other mammals including two species of nonhuman primates are at hand.
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increasing dilutions of an odorant used as S⫹, and the alternative paper strip scented with the odorless solvent alone used as S⫺. Starting with a dilution of 1:100, each odorant was successively presented in 10-fold dilution steps for three sessions each until a monkey failed to significantly discriminate the odorant from the solvent. Subsequently, this descending staircase procedure was repeated for three more sessions per dilution step. Finally, intermediate dilutions were tested in order to determine the threshold value more exactly. If, for example, a monkey significantly discriminated a 1:10,000 dilution from the solvent but failed to do so with a 1:100,000 dilution, then the monkey was presented with a 1:30,000 dilution. To prevent the more challenging conditions leading to extinction or to a decline in the monkey’s motivation, these were always followed by a return to an easy control task. This consisted of the discrimination between a 100-fold dilution of the S⫹ and the odorless solvent as S⫺.
Odorants Method Subjects Testing was performed with 3 adult female spider monkeys (Ateles geoffroyi) maintained as part of a breeding colony at the Parque de la Flora y Fauna Silvestre Tropical, Catemaco, Veracruz, Mexico. All monkeys had served as subjects in previous olfactory experiments (Laska, Hernandez Salazar, & Rodriguez Luna, 2003) and were completely familiar with the basic test procedure. The group was housed under seminatural conditions in an enclosure of 72 m3 with three adjacent single cages that could be closed by sliding doors, thus allowing the temporary separation of monkeys for individual testing. The monkeys were trained to enter their test cage voluntarily and remained in visual and auditory contact with the rest of their social group during testing. Monkeys were fed fresh fruit and vegetables, with ad-lib access to water. The experiments reported here comply with the Guide for the Care and Use of Laboratory Animals (National Institutes of Health Publication No. 86 –23, revised 1985) and with current German and Mexican laws.
Behavioral Test The spider monkeys were tested in a two-choice instrumental conditioning paradigm (Hu¨ bener & Laska, 2001; Laska, Hernandez Salazar, & Rodriguez Luna, 2003). Two cube-shaped open PVC containers (side length, 5.5 cm) were attached to a metal bar (50 cm long and 6 cm wide) at a distance of 22 cm. Each container was equipped with a hinged metallic lid, hanging 2 cm down the front of the container. From the center of the front part of the lid, a pin of 3 cm length extended toward the monkey and served as a lever to open the lid. A clip on top of each lid held an absorbent paper strip (70 ⫻ 10 mm) impregnated with 10 l of an odorant, signaling either that the container held a Kellogg’s Honey Loop food reward (S⫹) or that it did not (S⫺). The odorized paper strips extended 5 cm into the test cage when the apparatus was attached to the front of the cage. When a monkey tried to open a container without prior sniffing, the experimenter held a chain connected to the lid tight so that the monkey could not move the lid. After the olfactory investigation had taken place, the chain was loosened and the monkey could open the container. In each test trial, each monkey sniffed at both options for as often as it liked and then decided to open one of the two boxes. After each decision, the experimenter removed the apparatus from the mesh and— out of sight of the test monkey—prepared it for the next trial by again baiting the container bearing the S⫹. A pseudorandomized sequence of presentations of the S⫹ on the left or on the right side was adopted. Ten such trials were conducted per monkey and session, and, usually, three sessions were conducted per day. Olfactory detection thresholds were determined by testing the monkey’s ability to discriminate between an absorbent paper strip scented with
A set of 10 odorants was used: ethyl acetate, n-propyl acetate, n-butyl acetate, n-pentyl acetate, n-hexyl acetate, n-heptyl acetate, n-octyl acetate, isopropyl acetate, isobutyl acetate, and isopentyl acetate. The rationale for choosing these substances was to assess the monkeys’ sensitivity for odorants representing members of a homologous series of aliphatic compounds, that is, substances sharing the same functional group but differing in carbon chain length, as well as isomeric forms of some of these compounds, that is, substances sharing the same sum formula and functional group but differing in the branching of their carbon chains, allowing us to assess the impact of both structural features on detectability. All substances were obtained from Merck (Darmstadt, Germany) and had a nominal purity of at least 99%. They were diluted with odorless diethyl phthalate (Merck) as the solvent. The order of presentation of odorants did not follow the sequence mentioned above but was pseudorandomized between monkeys.
Data Analysis In the method described here, the monkey had two options: to correctly open the container that contained the positive stimulus (hit), or to incorrectly open the container that contained the negative stimulus (false alarm). For each individual spider monkey, the percentage of hits from the best three consecutive sessions per dilution step, comprising a total of 30 decisions, was calculated and taken as the measure of performance. Significance levels were determined by calculating binomial z-scores corrected for continuity (Siegel & Castellan, 1988) from the number of correct and false responses for each individual monkey and condition. All tests were two-tailed, and the alpha level was set at 0.05. Correlations between olfactory threshold values and carbon chain length of the substances tested were calculated by using both the Spearman rank-correlation test and second order polynomial regression analysis.
Results Figure 1 shows the performance of the spider monkeys in discriminating between various dilutions of a given odorant and the odorless solvent. All 3 monkeys significantly distinguished dilutions as low as 1:1 million ethyl acetate, 1:100,000 n-propyl acetate, 1:30 million n-butyl acetate, 1:30 million n-pentyl acetate, 1:1 million n-hexyl acetate, 1:300,000 n-heptyl acetate, 1:100,000 n-octyl acetate, 1:10 million isopropyl acetate, 1:30,000 isobutyl acetate, and 1:30 million isopentyl acetate from the solvent (binomial test, p ⬍ .05), with single individuals even scoring better. The individual spider monkeys demonstrated very similar threshold values, and with 8 of the 10 odorants, they differed only by a dilution factor of 3 or 10 between the highest- and the
OLFACTORY SENSITIVITY IN SPIDER MONKEYS
lowest-scoring monkey. The largest difference in sensitivity for a given odorant between individual monkeys represented a dilution factor of 33 and was found with n-hexyl acetate and n-heptyl acetate. Figure 2 shows the olfactory detection threshold values (expressed as vapor phase concentrations) of the spider monkeys as a function of carbon chain length of the aliphatic esters tested. When linear correlational statistics were applied to the data, no significant correlation between perceptibility in terms of olfactory detection thresholds and carbon chain length of the n-acetic esters was found (Spearman, rs ⫽ ⫺.37, p ⬎ .05). However, when the threshold values for the two substances with the longest carbon chains tested, that is, n-heptyl acetate and n-octyl acetate, were removed from the calculations, a statistically significant negative correlation was found (Spearman, rs ⫽ ⫺.63, p ⬍ .02). Similarly, when the threshold values for the two substances with the shortest carbon chains tested, that is, ethyl acetate and n-propyl acetate, were removed from the calculations, a statistically significant positive correlation was found (Spearman, rs ⫽ .67, p ⬍ .02). Thus, the correlation between olfactory detection thresholds of the spider monkeys and carbon chain length of the n-aliphatic esters tested can best be described as a U-shaped function (second-order polynomial regression, r ⫽ .75, p ⬍ .01). With the three isoforms of the acetic esters tested, linear correlational analysis also failed to find a statistically significant correlation between threshold values and carbon chain length (Spearman, rs ⫽ ⫺.29, p ⬎ .05). However, when applying second-order polynomial regression analysis to the data, the correlation was found to follow an inverted U-shaped function (r ⫽ .97, p ⬍ .01). A comparison of detection threshold values for n- and isoforms of acetic esters sharing the same number of carbons shows the following: Whereas the isoform of propyl acetate is detected at markedly lower concentrations compared with the n-form by all 3 monkeys, the reverse is true for the two butyl acetates tested. The two isomers of pentyl acetate were detected at similar concentrations (cf. Figure 2). Table 1 summarizes the threshold dilutions for both the best and the poorest performing spider monkeys, and shows various measures of corresponding vapor phase concentrations (Weast, 1987) allowing readers to easily compare the data obtained in the present study to those reported by other authors using one of these convertible measures. All threshold dilutions correspond to vapor phase concentrations below 1 ppm, and in several cases, the monkeys were even able to detect concentrations below 1 ppb.
Discussion The results of this study demonstrate, for the first time, that spider monkeys have a high olfactory sensitivity for monomolecular odorants belonging to the class of aliphatic esters. Further, they show a nonlinear correlation between perceptibility in terms of olfactory detection thresholds and carbon chain length of the substances tested.
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Figure 2. Olfactory detection threshold values (expressed as vapor phase concentrations) of the 3 spider monkeys (Nanny, circles; Suki, squares, Piolina, triangles) as a function of carbon chain length of the aliphatic esters tested. ppm ⫽ parts per million.
Although only 3 monkeys were tested, the results appear robust, as interindividual variability was remarkably low and generally smaller than the range reported in studies on human olfactory sensitivity, that is, within three orders of magnitude (Stevens, Cain, & Burke, 1988). In fact, for the majority of substances tested, there was a factor of only 3 or 10 between the threshold values of the highest and the lowest scoring monkey. Further, with all substances tested, the monkeys’ performance with the lowest concentrations presented dropped to chance level, suggesting that the statistically significant discrimination between higher concentrations of an odorant and the odorless diluent was indeed based on olfactory perception and not on other cues. Figure 3 compares the olfactory detection threshold values obtained with the spider monkeys for the substances tested to those from other mammalian species. Although such across-species comparisons should be considered with caution, as different methods may lead to widely differing results—as can be seen with the threshold values depicted for n-butyl acetate, n-pentyl acetate, and n-hexyl acetate in the rat—it seems admissible to state that Ateles geoffroyi is far from being considered a microsmat, that is, a species with a poorly developed sense of smell. With all n-acetic esters, the spider monkeys demonstrated olfactory threshold values that are at least two orders of magnitude lower than those of the rat (Moulton, 1960) and the dog (Passe & Walker, 1985), both of which are traditionally regarded as macrosmatic animals, that is, species with a highly developed sense of smell. Similarly, the sensitivity of the spider monkey for n-pentyl acetate was found to be markedly higher than that of the rabbit (Passe & Walker, 1985), and for ethyl acetate to be as good as that of the mouse (Bodyak & Slotnick, 1999), two other species usually considered to be macrosmats. It should be mentioned that all animal data shown in
Figure 1 (opposite). Performance of 3 spider monkeys in discriminating between various dilutions of a given odorant and the odorless solvent. Each data point represents the percentage of correct choices from 30 decisions. Filled symbols indicate dilutions that were not discriminated above chance level (binomial test, p ⬎ .05).
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Table 1 Olfactory Detection Threshold Values in Ateles geoffroyi Expressed in Various Measures of Vapor Phase Concentrations Odorant ethyl acetate n-propyl acetate n-butyl acetate n-pentyl acetate n-hexyl acetate n-heptyl acetate n-octyl acetate iso-propyl acetate iso-butyl acetate iso-pentyl acetate
Dilution
Molec./cm3
1:1 million 1:3 million 1:100,000 1:1 million 1:30 million 1:300 million 1:30 million 1:300 million 1:1 million 1:30 million 1:300,000 1:10 million 1:100,000 1:300,000 1:10 million 1:30 million 1:30,000 1:100,000 1:30 million 1:100 million
3.0 ⫻ 10 1.0 ⫻ 1012 1.2 ⫻ 1013 1.2 ⫻ 1012 1.6 ⫻ 1010 1.6 ⫻ 109 7.3 ⫻ 109 7.3 ⫻ 108 1.1 ⫻ 1011 3.5 ⫻ 109 1.6 ⫻ 1011 4.8 ⫻ 109 2.7 ⫻ 1011 8.9 ⫻ 1010 1.9 ⫻ 1011 6.4 ⫻ 1010 2.3 ⫻ 1013 7.0 ⫻ 1012 9.8 ⫻ 109 2.9 ⫻ 109 12
ppm 0.11 0.036 0.45 0.045 0.0006 0.00006 0.00027 0.000027 0.0039 0.00013 0.0059 0.00018 0.0099 0.0033 0.0072 0.0024 0.85 0.26 0.00036 0.00012
log ppm ⫺0.96 ⫺1.43 ⫺0.34 ⫺1.35 ⫺3.22 ⫺4.22 ⫺3.57 ⫺4.57 ⫺2.40 ⫺3.88 ⫺2.23 ⫺3.75 ⫺2.01 ⫺2.48 ⫺2.15 ⫺2.63 ⫺0.07 ⫺0.58 ⫺3.44 ⫺3.96
Mol/L ⫺9
5.0 ⫻ 10 1.7 ⫻ 10⫺9 2.0 ⫻ 10⫺8 2.0 ⫻ 10⫺9 2.7 ⫻ 10⫺11 2.7 ⫻ 10⫺12 1.2 ⫻ 10⫺11 1.2 ⫻ 10⫺12 1.8 ⫻ 10⫺10 5.9 ⫻ 10⫺12 2.7 ⫻ 10⫺10 7.9 ⫻ 10⫺12 4.4 ⫻ 10⫺10 1.5 ⫻ 10⫺10 3.2 ⫻ 10⫺10 1.1 ⫻ 10⫺10 3.9 ⫻ 10⫺8 1.2 ⫻ 10⫺8 1.6 ⫻ 10⫺11 4.9 ⫻ 10⫺12
log mol/L ⫺8.30 ⫺8.78 ⫺7.69 ⫺8.69 ⫺10.57 ⫺11.57 ⫺10.92 ⫺11.92 ⫺9.75 ⫺11.23 ⫺9.58 ⫺11.10 ⫺9.35 ⫺9.83 ⫺9.49 ⫺9.97 ⫺7.41 ⫺7.93 ⫺10.79 ⫺11.31
Note. With each stimulus, the upper line represents the lowest concentration that all 3 monkeys were able to detect, and the lower line represents the lowest concentration that the best performing monkey was able to detect. molec. ⫽ molecules; ppm ⫽ parts per million.
Figure 3 are taken from studies that used instrumental conditioning paradigms (and not spontaneous preference or habituation/dishabituation paradigms), and it is commonly agreed that such methods provide the best approximation of an animal’s sensory capabilities (Hastings, 2003). A comparison of the spider monkeys’ performance with that of two other species of nonhuman primates tested in an earlier study (Laska & Seibt, 2002b) using exactly the same (pigtail macaques) or a very similar (squirrel monkeys) method as that of the present study reveals that, with the exception of n-heptyl acetate, spider monkeys and squirrel monkeys display very similar or even identical olfactory detection thresholds for acetic esters, and that, with the exception of isobutyl acetate, both New World primate species perform better than the pigtail macaque, an Old World primate species. All three species of nonhuman primates generally show lower threshold values compared with human subjects, which nevertheless appear to be more sensitive for most of the n-acetic esters tested than the rat (cf. Figure 5). It should be mentioned that the threshold values of the human subjects as depicted in Figure 3 are taken from the study by Cometto-Muniz and Cain (1991). Although some other studies reported slightly lower values for some of the substances (e.g., for ethyl acetate [Hellman & Small, 1974] and for n-butyl acetate [Dravnieks & Laffort, 1972]), these other studies had tested only one or a few members of the homologous series of esters, and none of them had used signal detection methods and a comparably sophisticated mode of stimulus presentation as had ComettoMuniz and Cain. Across-species comparisons of olfactory performance raise the question as to possible reasons for the observed similarities and— sometimes marked— differences in olfactory sensitivity for a given substance. Likewise, within-species comparisons of olfac-
tory performance should be discussed with regard to possible explanations for differences in sensitivity between substances. Our finding of a high olfactory sensitivity for aliphatic esters in spider monkeys is yet another example showing that allometric comparisons of olfactory brain structure volumes or of the absolute size of olfactory epithelia are poor predictors of chemosensory performance. There is no doubt that the relative size of the rat’s or the dog’s brain structures devoted to processing olfactory information and the total area of the dog’s olfactory epithelium (and concomitantly its total number of olfactory receptors) are both considerably larger than those of the spider monkey or of other human or nonhuman primates (Farbman, 1992; Stephan et al., 1988). The present data as well as those from other studies that reported olfactory detection threshold values for aliphatic alcohols, aldehydes, and carboxylic acids in squirrel monkeys and pigtail macaques (Laska et al., 2000; Laska, Hofmann, & Simon, 2003; Laska & Seibt, 2002a), however, clearly show that such comparisons of neuroanatomical structures do not allow generalizable conclusions as to olfactory sensitivity of any two species. Considering that even for the most intensively studied species of nonhuman mammals, measurements of olfactory sensitivity or discrimination abilities have so far usually been restricted to little more than a handful of substances (Walker & Jennings, 1991), it is obvious that the assignment of general labels such as microsmat or macrosmat to any species is at least premature and does not take into account the vast complexity of our natural odor world (Laing, Cain, McBride, & Ache, 1989) and the diversity of contexts in which the sense of smell may be crucial for an animal (Doty, 1986). Therefore, we argue that these terms should no longer be used. In order to explain similarities or differences in olfactory performance between or within species, it might be more promising to
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Figure 3. Comparison of the olfactory detection threshold values (expressed as vapor phase concentrations) of the spider monkeys for aliphatic esters with those of other mammalian species (human data: Cometto-Muniz & Cain, 1991; animal data: Bodyak & Slotnick, 1999; Laska, 1990; Laska & Seibt, 2002b; Moulton, 1960; Passe & Walker, 1985). ppm ⫽ parts per million.
consider whether given odorants or classes of odorants might differ in their degree of behavioral relevance for a species. Spider monkeys, as well as squirrel monkeys and pigtail macaques, have been reported to include a considerable proportion of fruits in their diets, with the two first-mentioned species usually scoring higher values regarding this dietary specialization compared with the last-mentioned species (Clutton-Brock & Harvey, 1977; Ross, 1992). Our finding that both spider monkeys and squirrel monkeys are generally—and in some cases even markedly—more sensitive to aliphatic esters than rats or dogs appears to make sense in terms of an evolutionary adaptation to optimal foraging (Stephens & Krebs, 1986), as these substances are known to be major components of a wide variety of fruit odors (Nursten, 1970; Rouseff & Leahy, 1995) and thus are likely to be more relevant for species feeding on fruit than for a carnivorous species such as the dog or a granivorous species such as the rat (Chivers & Hladik, 1980). This idea is also supported by the finding that the short-tailed fruit bat, Carollia perspicillata, a frugivorous species also belonging to an order of mammals traditionally considered as microsmatic, has been reported to show olfactory detection thresholds for aliphatic esters that are markedly lower than those of rats and at least as low as those of dogs (Laska, 1990; cf. Figure 3). Carnivorous, insectivorous, or sanguivorous species such as the dog, the hedgehog, or the vampire bat, in turn, have been found to be more sensitive to short-chained carboxylic acids compared with squirrel monkeys or pigtail macaques (Hu¨ bener & Laska, 2001; Laska et al., 2000). This class of odorants comprises the main components of body-borne prey odors (Flood, 1985) and thus is
believed to be highly relevant for species feeding on animal prey but presumably less important for mainly frugivorous primates. Despite the obvious role that the sense of smell plays in finding and selecting food in many species, it should be emphasized that dietary specialization is only one of presumably numerous factors that make up the ecological niche of a species and that are likely to affect its pattern of olfactory sensitivity and discrimination ability (Barton et al., 1995). Identifying such factors and their impact on measures of olfactory performance warrants further studies that include as many animal species and odor stimuli as possible. A final aspect of the present study is our finding of a nonlinear (i.e., U-shaped) correlation between olfactory detection threshold values obtained in the spider monkeys and carbon chain length of the n-aliphatic esters tested. Although squirrel monkeys and pigtail macaques have been reported to show a significant linear negative correlation between these two measures (Laska & Seibt, 2002b), second order polynomial regression analysis, which was not performed in the original study, reveals that in these two nonhuman primate species, too, the distribution of sensitivity across the homologous series of esters can best be described by a U-shaped function. This finding lends further support to the notion that olfactory sensitivity for structurally related substances is not a simple function of vapor pressure, as the latter decreases monotonically with increasing carbon chain length of the esters tested. Interestingly, with the three isoforms of the acetic esters tested, the squirrel monkeys, but not the pigtail macaques, showed the
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HERNANDEZ SALAZAR, LASKA, AND RODRIGUEZ LUNA
same inverted U-shaped correlation between sensitivity and molecular length as the spider monkeys (Laska & Seibt, 2002b). Both linear and U-shaped correlations between sensitivity and carbon chain length of acetic esters have also been found in humans (Cometto-Muniz & Cain, 1991) and in rats (Moulton, 1960). For other homologous series of aliphatic substances such as alcohols, aldehydes, or carboxylic acids, corresponding correlations have been reported both in squirrel monkeys and in humans (Cometto-Muniz, Cain, & Abraham, 1998; Laska et al., 2000; Laska & Seibt, 2002a; Laska, Hofmann, & Simon, 2003). This suggests that regular connections between perceptibility and this molecular structural feature might not be restricted to the class of odorants tested here but instead may represent a more general phenomenon. This may not be surprising, considering that carbon chain length of odorant molecules has been shown to be an important determinant of the specificity of interaction between stimulus and receptor (Kaluza & Breer, 2000) as well as of the chemotopic organization and thus of odor quality coding within the olfactory bulb (Johnson & Leon, 2000). However, with regard to differences in sensitivity for members of a homologous series of substances at the organismal level, it should be considered that the quantitative distribution of individual receptor types, each responding selectively to a limited range of carbon chain lengths and functional groups, may differ between species. This may explain why one species may show a regular connection between sensitivity and carbon chain length of a given class of substances, whereas another species does not or displays a different type of correlation. A heightened expression of a given receptor type with a specific molecular receptive range may also explain phenomena such as the markedly higher sensitivity of the spider monkey for n-butyl acetate compared with its neighbor in the homologous series, n-propyl acetate (cf. Figure 2). A possible reason underlying such phenomena is that repeated exposure to a given odorant—perhaps due to its high abundance in the odorous environment of or its biological significance for an animal—may induce an increased expression of a corresponding receptor type (Yee & Wysocki, 2001). In conclusion, the results of the present study provide first evidence of a well-developed olfactory sensitivity in the spider monkey. This finding supports the assumption that olfaction may play an important role in the regulation of behavior in this species. Further, the results lend additional support to the suggestions that between-species comparisons of neuroanatomical features are a poor predictor of olfactory performance and that general labels such as microsmat or macrosmat—which usually are based on allometric comparisons of olfactory brain structures—are inadequate to describe a species’ olfactory capabilities. An ecological view of such capabilities that attempts to correlate sensory performance with behavioral relevance of odor stimuli might offer a promising approach in appraising the significance of the sense of smell for a particular species.
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Received May 5, 2003 Revision received May 21, 2003 Accepted June 5, 2003 䡲
