Behavioral Neuroscience Copyright 2003 by the American Psychological Association, Inc.

2003, Vol. 117, No. 6, 1142–1149 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 between-
species comparisons of neuroanatomical features are poor predictors of olfactory performance.

There is a long-standing tradition in olfactory research of as-
signing 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 dichot-
omy 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 (Farb-
man, 1992; Stephan, Baron, & Frahm, 1988). However, physio-
logical evidence supporting a positive correlation between allo-
metric measures of neuroanatomical structures and olfactory
performance is largely lacking (Brown, 2001; De Winter & Ox-
nard, 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 behav-
ioral 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:
laska@imp.med.uni-muenchen.de
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 (Hübener & Laska, 2001; Laska & Hud-
son, 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
(Hübener & Laska, 1998; Laska, Alicke, & Hudson, 1996). Fur-
ther, these studies showed that Saimiri sciureus and Macaca nem-
estrina 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 olfac-
tory 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).

1142
 OLFACTORY SENSITIVITY IN SPIDER MONKEYS
Recently, the authors of the present study successfully intro-
duced 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 sub-
stances 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.
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 vege-
tables, 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 condition-
ing paradigm (Hübener & 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
1143
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 thresh-
old value more exactly. If, for example, a monkey significantly discrimi-
nated 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 dilu-
tion. 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
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 com-
pounds, 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 func-
tional 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 incor-
rectly 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 (bino-
mial 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 (ex-
pressed 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 signifi-
cant correlation between perceptibility in terms of olfactory detec-
tion 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 corre-
lational analysis also failed to find a statistically significant cor-
relation between threshold values and carbon chain length (Spear-
man, 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 concentra-
tions (cf. Figure 2).
Table 1 summarizes the threshold dilutions for both the best and
the poorest performing spider monkeys, and shows various mea-
sures 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 con-
vertible 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 monomolec-
ular 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.
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).
1145
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 con-
centrations presented dropped to chance level, suggesting that the
statistically significant discrimination between higher concentra-
tions 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 meth-
ods 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
1146 HERNANDEZ SALAZAR, LASKA, AND RODRIGUEZ LUNA

Table 1
Olfactory Detection Threshold Values in Ateles geoffroyi Expressed in Various Measures of
Vapor Phase Concentrations

Odorant Dilution Molec./cm3 ppm log ppm Mol/L log mol/L

⫺9
ethyl acetate 1:1 million 3.0 ⫻ 10 12
0.11 ⫺0.96 5.0 ⫻ 10 ⫺8.30
1:3 million 1.0 ⫻ 1012 0.036 ⫺1.43 1.7 ⫻ 10⫺9 ⫺8.78
n-propyl acetate 1:100,000 1.2 ⫻ 1013 0.45 ⫺0.34 2.0 ⫻ 10⫺8 ⫺7.69
1:1 million 1.2 ⫻ 1012 0.045 ⫺1.35 2.0 ⫻ 10⫺9 ⫺8.69
n-butyl acetate 1:30 million 1.6 ⫻ 1010 0.0006 ⫺3.22 2.7 ⫻ 10⫺11 ⫺10.57
1:300 million 1.6 ⫻ 109 0.00006 ⫺4.22 2.7 ⫻ 10⫺12 ⫺11.57
n-pentyl acetate 1:30 million 7.3 ⫻ 109 0.00027 ⫺3.57 1.2 ⫻ 10⫺11 ⫺10.92
1:300 million 7.3 ⫻ 108 0.000027 ⫺4.57 1.2 ⫻ 10⫺12 ⫺11.92
n-hexyl acetate 1:1 million 1.1 ⫻ 1011 0.0039 ⫺2.40 1.8 ⫻ 10⫺10 ⫺9.75
1:30 million 3.5 ⫻ 109 0.00013 ⫺3.88 5.9 ⫻ 10⫺12 ⫺11.23
n-heptyl acetate 1:300,000 1.6 ⫻ 1011 0.0059 ⫺2.23 2.7 ⫻ 10⫺10 ⫺9.58
1:10 million 4.8 ⫻ 109 0.00018 ⫺3.75 7.9 ⫻ 10⫺12 ⫺11.10
n-octyl acetate 1:100,000 2.7 ⫻ 1011 0.0099 ⫺2.01 4.4 ⫻ 10⫺10 ⫺9.35
1:300,000 8.9 ⫻ 1010 0.0033 ⫺2.48 1.5 ⫻ 10⫺10 ⫺9.83
iso-propyl acetate 1:10 million 1.9 ⫻ 1011 0.0072 ⫺2.15 3.2 ⫻ 10⫺10 ⫺9.49
1:30 million 6.4 ⫻ 1010 0.0024 ⫺2.63 1.1 ⫻ 10⫺10 ⫺9.97
iso-butyl acetate 1:30,000 2.3 ⫻ 1013 0.85 ⫺0.07 3.9 ⫻ 10⫺8 ⫺7.41
1:100,000 7.0 ⫻ 1012 0.26 ⫺0.58 1.2 ⫻ 10⫺8 ⫺7.93
iso-pentyl acetate 1:30 million 9.8 ⫻ 109 0.00036 ⫺3.44 1.6 ⫻ 10⫺11 ⫺10.79
1:100 million 2.9 ⫻ 109 0.00012 ⫺3.96 4.9 ⫻ 10⫺12 ⫺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/disha-
bituation 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 iden-
tical 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 Cometto-
Muniz 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 infor-
mation 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 compar-
isons 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 per-
formance between or within species, it might be more promising to
 OLFACTORY SENSITIVITY IN SPIDER MONKEYS 1147

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 ma-
caques, 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 com-
pared 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 mark-
edly—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 thresh-
olds 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 (Hübener & 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 per-
formed 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 mono-
tonically 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
1148 HERNANDEZ SALAZAR, LASKA, AND RODRIGUEZ LUNA
same inverted U-shaped correlation between sensitivity and mo-
lecular 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 correla-
tions 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 determi-
nant 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 organis-
mal 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 inade-
quate 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