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First published online November 19, 2007
Journal of Experimental Biology 210, 4169-4178 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.012237
Olfactory sensitivity for putrefaction-associated thiols and indols in three species of non-human primate
1 IFM Biology, Linköping University, 581 83 Linköping,
Sweden
2 Instituto de Neuro-Etologia, Universidad Veracruzana, 91000 Xalapa,
Veracruz, Mexico
3 Department of Medical Psychology, University of Munich, 80336 Munich,
Germany
* Author for correspondence (e-mail: malas{at}ifm.liu.se)
Accepted 20 September 2007
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Summary |
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Key words: olfactory sensitivity, detection thresholds, non-human primates, thiols, indols, putrefaction
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Walker and Jennings, 1991). A
more recent version of this view states that the number of functional
olfactory receptor (OR) genes – which some authors believe to co-vary
with olfactory brain size (Gilad et al.,
2004) – may allow predictions as to the efficiency of a
species' sense of smell (Rouquier et al.,
2000). Both views, however, have recently been called into
question (Shepherd, 2004;
Smith and Bhatnagar, 2004). An
increasing number of studies now suggest that the behavioural relevance of
odour stimuli rather than neuroanatomical features or the size of the
repertoire of olfactory receptors may determine both a species' olfactory
sensitivity and its discrimination performance
(Laska et al., 2000;
Laska et al., 2003a;
Laska et al., 2006a).
In contrast to the widely held belief that primates are `microsmatic', for
example, several studies have demonstrated that their olfactory detection
thresholds for certain odorants such as fruit-associated acetic esters are at
least as low as, and in some cases even markedly lower than, those of the rat
or dog, both species being commonly regarded as `macrosmatic' based on the
relative size of their olfactory bulbs and cortices
(Hernandez Salazar et al.,
2003; Laska and Seibt,
2002a). Similarly, honeybees have been shown to be better at
discriminating between structurally related odorants such as flower-associated
enantiomers compared with species having markedly larger numbers of functional
OR genes (Laska and Galizia,
2001). Both findings can be plausibly explained by assuming that
the odour stimuli in question differ in their behavioural relevance among the
species mentioned, an assumption that is supported by reports on their ecology
and behaviour.
Differences in the behavioural relevance of odorants may also explain
within-species differences in olfactory performance. In rats, for example, the
lowest olfactory detection threshold determined so far has been reported for
2,4,5-trimethylthiazoline (TMT), a volatile compound characteristic of fox
faecal odour: the odour of a natural predator of the rat
(Laska et al., 2005b).
In addition to predator avoidance, two of the main functions of the sense
of smell are food selection and social communication. Avoidance of spoiled
food should be of particular importance to primates as they generally lack
specific physiological detoxification mechanisms. Sulphur- and
nitrogen-containing odorants such as thiols and indols have been found to be
characteristic of putrefaction – that is, of the microbial degradation
of proteins (Janzen, 1977;
Barker, 1981;
Kamiya and Ose, 1984).
Interestingly, the same groups of odorants have also been described in the
body-borne odours of primates, raising the possibility that they may also play
a role in olfactory social communication
(Tonzetich et al., 1978;
Moore et al., 1987).
The three primate species employed here, spider monkeys, squirrel monkeys
and pigtail macaques, are known to differ – at least to some degree
– in their dietary habits, with the first-mentioned species showing the
highest degree of frugivory and the last-mentioned species the lowest degree
of fruit consumption (Caldecott,
1986; Clutton-Brock and Harvey,
1977; Ross, 1992).
They also differ in their degree of phylogenetic relatedness to each other,
with spider monkeys and squirrel monkeys representing New World primates and
pigtail macaques being an Old World primate species, and in their use of
olfactory cues for social communication
(Caldecott, 1986;
Epple, 1985;
Kinzey, 1997). These
between-species differences allowed us to assess whether such ecological
factors might affect olfactory sensitivity to the odorants under
investigation.
It was therefore the aim of the present study to determine olfactory detection thresholds for members of the chemical classes of thiols and indols in these three species of non-human primate. By comparing these threshold values with those obtained in earlier studies using the same methods and animals but with other classes of odorants, we aimed at further testing the hypothesis that within-species differences in olfactory sensitivity may reflect differences in the behavioural relevance of odorants. Employing odorants that share certain molecular features such as the type of sulphur- or nitrogen-containing functional group or structure of the carbon chain backbone, and differ from each other in others such as carbon chain length or presence vs absence of a methyl group, allowed us to additionally address the question of the impact of these features on the detectability of odorants.
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Materials and methods |
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Conditions of the animals' maintenance have been described in detail
elsewhere (Hernandez Salazar et al.,
2003; Laska and Seibt,
2002a). They were fed fresh fruit and vegetables ad
libitum. The amount of food offered daily to the animals was such that
left-overs were still present the next morning and thus it was unlikely that
ravenous appetite affected the animals' choice behaviour in the tests. The
experiments reported here comply with the `Principles of animal care',
publication no. 86-23, revised 1985, of the National Institutes of Health, and
also with current laws in Germany and Mexico, the countries in which the study
was performed.
Behavioural test
The experimental procedures for assessing olfactory detection thresholds in
the three primate species have been described in detail elsewhere
(Laska and Hudson, 1993;
Hübener and Laska, 2001;
Laska et al., 2003a). Briefly,
the animals were tested using a food-rewarded instrumental conditioning
paradigm. Olfactory detection thresholds were determined by testing the
animals' ability to discriminate between increasing dilutions of an odorant
used as the rewarded stimulus (S+), and the odourless solvent diethyl
phthalate alone used as the unrewarded stimulus (S–). In each test
trial, each monkey sniffed at both options and then decided on one of the
alternatives by performing an operant response which, in the case of a correct
decision, was food rewarded. Ten such trials were conducted per animal and
session, and at least three sessions per experimental condition were
performed. To minimize the possibility of adaptation, inter-trial intervals
were at least 30 s and only one concentration step was tested per animal per
day. Starting with a dilution of 1:10 000 with the thiols, 0.5 g
l–1 with indol and 0.1 g l–1 with 3-methyl
indol, each stimulus was successively presented in 10-fold dilution steps
until an animal failed to significantly discriminate the odorant from the
solvent. Subsequently, an intermediate concentration (0.5 log units between
the lowest concentration that was detected above chance and the first
concentration that was not) was tested in order to determine the threshold
value more exactly.
Odorants
A set of six odorants belonging to the chemical classes of thiols
(ethanethiol, 1-propanethiol, 1-butanethiol, and 1-pentanethiol) and indols
(indol and 3-methyl indol) was used. The rationale for choosing these
substances was to assess the monkeys' sensitivity to odorants that have been
shown to be associated with putrefaction
(Janzen, 1977;
Barker, 1981;
Kamiya and Ose, 1984).
Additionally, the thiols used here are structurally similar to each other;
that is, they share molecular properties such as type and position of the
sulphur-containing functional group, and only differ from each other in carbon
chain length (Fig. 1).
Similarly, the indols used here share type and position of the
nitrogen-containing functional group and only differ from each other in the
presence vs absence of a methyl group, allowing us to assess the
impact of these structural features on detectability. All substances were
obtained from Fluka (Taufkirchen, Germany) and had a nominal purity of at
least 99%. They were diluted using odourless diethyl phthalate as the
solvent.
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Correlations between olfactory threshold values of a given species (individual scores per stimulus were used) and carbon chain length of the thiols tested were calculated using the Spearman rank-correlation test and tested for significance by computing t values. Across-species comparisons of performance were conducted using Mann-Whitney U tests for independent samples. All tests were two-tailed and, if not otherwise mentioned, the alpha level was set at 0.05.
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Results |
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Table 1 summarizes the
threshold dilutions for the four spider monkeys and shows various measurements
of corresponding vapour phase concentrations
(Weast, 1987), to enable easy
comparison of the data obtained in the present study with those reported by
other authors. In all cases, threshold dilutions correspond to vapour phase
concentrations below 0.1 p.p.m.; in about half of the cases the animals were
even able to detect concentrations below 1 p.p.b.; and with ethanethiol two of
the animals detected concentrations below 1 p.p.t.
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A significant positive correlation between detection threshold values for the spider monkeys and carbon chain length of the thiols tested was found (Spearman, rs=+0.55, P=0.0338). This means that the sensitivity of the animals for the thiols decreased with increasing carbon chain length (see Fig. 5, upper panel).
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Table 2 summarizes the
threshold dilutions for the three squirrel monkeys and shows various
measurements of corresponding vapour phase concentrations
(Weast, 1987). In all cases,
threshold dilutions correspond to vapour phase concentrations below 1 p.p.m.;
in about half of the cases the animals were even able to detect concentrations
below 1 p.p.b.; and with indol two of the animals detected concentrations
below 1 p.p.t.
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A significant negative correlation between detection threshold values for the squirrel monkeys and carbon chain length of the thiols tested was found (Spearman, rs=–0.85, P=0.0051). This means that the sensitivity of the animals for the thiols increased with increasing carbon chain length (see Fig. 5, middle panel).
Pigtail macaques
Fig. 4 shows the performance
of the pigtail macaques in discriminating between various dilutions of a given
thiol or indol and the odourless solvent. All three animals significantly
distinguished dilutions as low as 1:3 million ethanethiol, 1:30 million
1-propanethiol, 1:300 million 1-butanethiol, 1:10 million 1-pentanethiol,
0.0005 mg l–1 indol and 3 mg l–1 3-methyl
indol from the solvent (binomial test, P<0.05), with single
individuals even scoring better.
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Table 3 summarizes the
threshold dilutions for the three pigtail macaques and shows various
measurements of corresponding vapour phase concentrations
(Weast, 1987). In all cases,
threshold dilutions correspond to vapour phase concentrations below 0.1
p.p.m., in about half of the cases the animals were even able to detect
concentrations below 1 p.p.b., and with indol all animals detected
concentrations below 1 p.p.t.
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No significant negative correlation between detection threshold values of the pigtail macaques and carbon chain length of the thiols tested was found (Spearman, rs=–0.40, P=0.19). This means that the sensitivity of the animals for the thiols did not systematically vary as a function of carbon chain length (see Fig. 5, lower panel).
Across-species comparison of performance
Considering all six odorants combined, none of the three species performed
significantly better – that is, showed lower detection thresholds
– than any of the other two species (Mann-Whitney, P>0.05,
for all comparisons). The same is true when comparing the performance between
species for the thiols and the indols separately (Mann-Whitney,
P>0.05, for all comparisons). Nevertheless, all four spider
monkeys were more sensitive to ethanethiol than all three squirrel monkeys,
whereas all three squirrel monkeys and all three pigtail macaques were more
sensitive to indol than all four spider monkeys (see
Fig. 6).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Although only three or, in the case of the spider monkeys, four animals per
species were tested, the results appear robust as interindividual variability
was low and generally smaller than the range reported in studies on human
olfactory sensitivity; that is, within three orders of magnitude
(Stevens et al., 1988). In
fact, for the majority of substances tested there was only a factor of 33 or
smaller between the threshold values of the highest- and the lowest-scoring
animal of a species. Further, with all substances tested, the animals'
performance with the lowest concentrations presented dropped to chance level,
suggesting that the statistically significant discrimination between higher
concentrations of an odorant and the odourless diluent was indeed based on
olfactory perception and not on other cues.
Fig. 6 compares the
olfactory detection threshold values obtained with spider monkeys, squirrel
monkeys and pigtail macaques for the thiols and indols tested with those from
human subjects. Although such across-species comparisons should be considered
with caution as different methods may lead to widely differing results, it
seems admissible to state that human subjects do not generally perform poorer
than the non-human primates tested – despite the fact that the relative
size of the human brain structures devoted to processing olfactory information
is markedly smaller than that of the non-human primates
(Stephan et al., 1988), and
despite the fact that the number of functional olfactory receptor genes in
Homo sapiens (
350) is considerably smaller than that of
Macaca nemestrina (700) and of Saimiri sciureus and
Ateles geoffroyi (900)
(Rouquier et al., 2000;
Glusman et al., 2001;
Gilad et al., 2004).
Similarly, the pigtail macaques did not generally perform poorer with the
odorants tested here compared with the spider monkeys and the squirrel
monkeys, again despite the fact that the relative size of the olfactory brain
and the size of the repertoire of functional OR types in this Old World
primate species is smaller compared with the two other species, which are New
World primates. These findings lend additional support to the notion that
between-species differences in neuroanatomical or genetic features may not be
indicative of olfactory sensitivity – at least within the order of
primates. Unfortunately, only very few studies so far have tested some of the
thiols and indols used here with other species. Snyder and Peterson
(Snyder and Peterson, 1979)
reported olfactory detection thresholds of blackbilled magpies (Pica
pica) and pigeons (Columba livia) for ethanethiol to be 6 and 8
p.p.m., respectively, and for 1-butanethiol to be 2 p.p.m. in both species.
Smith and Paselk (Smith and Paselk,
1986) reported the turkey vulture (Cathartes aura) to
respond to concentrations of ethanethiol as low as 22 p.p.m. It should be
mentioned, however, that these studies employed changes in respiration
frequency and heart rate, respectively, to determine olfactory detection
thresholds, and both methods are known to be less sensitive than operant
conditioning procedures (Hastings,
2003).
A within-species comparison between the detection threshold values of the
present study with those obtained in earlier studies using the same methods
and animals but with other classes of odorants such as aliphatic esters
(Hernandez Salazar et al.,
2003; Laska and Seibt,
2002a), alcohols (Laska and
Seibt, 2002b; Laska et al.,
2006a), aldehydes (Laska et
al., 2003b; Laska et al.,
2006a), ketones (Laska et al.,
2005a), carboxylic acids
(Laska et al., 2000;
Laska et al., 2004), terpenes
(Laska et al., 2006c),
thiazoles (Laska et al.,
2005b), or steroids (Laska et
al., 2005c; Laska et al.,
2006b) reveals that in all three species of primate at least one
of the putrefaction-associated odorants employed here (indol with squirrel
monkeys and pigtail macaques, ethanethiol and 3-methyl indol with the spider
monkeys) yielded the lowest detection thresholds among the more than 50
odorants tested so far. This finding is in line with reports showing that
human subjects are particularly sensitive to thiols and indols
(van Gemert, 2003). It should
be emphasized that the 0.03 p.p.t. indol that both Saimiri sciureus
and Macaca nemestrina were able to perceive and the 0.96 p.p.t.
ethanethiol that Ateles geoffroyi was able to detect are in the same
order of magnitude as the lowest detection thresholds determined so far in the
rat (0.04 p.p.t. 2,4,5-trimethylthiazoline)
(Laska et al., 2005b) and in
the mouse (4.8 p.p.t. pentyl acetate)
(Walker and O'Connell, 1986),
both species presumed to be macrosmatic.
The most plausible explanation for the high sensitivity to thiols and
indols found with all three species of non-human primate tested here is that
members of these chemical classes may play an important role in controlling
their behaviour. Goff and Klee (Goff and
Klee, 2006) demonstrated that food-associated volatiles may
provide important information about the nutritional makeup and health value of
foods. As thiols and indols, in turn, have been found to be major products of
the microbial degradation of proteins
(Barker, 1981;
Kamiya and Ose, 1984) and thus
of putrefaction processes, which are usually accompanied by the production of
toxins (Janzen, 1977), it
seems reasonable to assume that primates should be highly sensitive to such
compounds in order to avoid intoxication. Indeed, the food selection behaviour
of primates suggests that they use their sense of smell for the evaluation of
potential food items (Laska et al.,
2007; Visalberghi and Addessi,
2000) and thus supports this assumption.
Indols and thiols have also been found to be major compounds of primate
faecal odours (Dehnhard et al.,
1991; Moore et al.,
1987) and breath odour (Ochiai
et al., 2001; Phillips et al.,
1999). In both human subjects and non-human mammals, oral breath
odour has been demonstrated to be indicative of health status
(Eubanks, 2006;
Kostelc et al., 1981;
Sanz et al., 2001), and in
humans the concentrations of volatile sulphur compounds of mouth air have been
shown to vary as a function of the menstrual cycle in females
(Tonzetich et al., 1978). This
raises the possibility that oral breath odour may convey olfactory social
information about the health and oestrus status in female primates. Similarly,
the composition of human faecal odours is known to vary with health status
(Garner et al., 2007) and the
obvious interest that a variety of non-human primate species display in their
faeces raises the possibility that faecal odour, too, may convey information
about the health status and dietary composition of conspecifics. Additionally,
it has been hypothesized that the sulphurous metabolites of meat digestion are
important for the repellency of predator urine and faecal odours to potential
prey (Nolte et al., 1994), and
primates have been shown to actively avoid such odours
(Sündermann et al.,
2005). Taken together, these findings strongly support the notion
that indols and thiols should be of high behavioural relevance for non-human
primates.
Differences in dietary habits have repeatedly been shown to plausibly
explain differences in chemosensory performance between species
(Spector, 2000). Among New
World primates, for example, the degree of frugivory has been found to
correlate positively with sensitivity for food-associated mono- and
disaccharides (Laska, 2000).
Similarly, the proportion of animal protein in the diet of primates appears to
correlate negatively with their sensitivity for monosodium glutamate
(Laska and Hernandez Salazar,
2004). In the olfactory domain with its countless types of stimuli
and perceptual qualities, however, such correlations are less easy to
establish. The three primate species studied here have been reported to differ
markedly in the proportion of animal matter in their diet, with up to 72% of
total intake in the squirrel monkey compared with only 1% in the spider
monkey, with pigtail macaques (13% of total intake) taking an intermediate
position. The spider monkeys' diet, in turn, is known to be composed of up to
90% fruit and seeds whereas the corresponding percentages for pigtail macaques
(70%) and squirrel monkeys (26%) are markedly lower
(Caldecott, 1986;
Clutton-Brock and Harvey, 1977;
Ross, 1992). Unfortunately,
there is only very little information available on whether the microbial
degradation of animal and plant protein leads to different proportions or
frequencies of occurrence of the thiols and indols tested here, which might
explain the between-species differences in sensitivity for individual odorants
found in the present study.
All three species of primate tested here have been reported to display
anogenital sniffing (Hopf,
1974; Klein, 1971;
Reite and Short, 1980) and
thus exposure to conspecific faecal odours that may convey behaviourally
relevant information. However, in this context, too, there is too little
quantitative information available with regard to both the frequency of such
behaviours and possible differences in the composition of faecal odours among
the three primate species to draw conclusions that might explain the observed
odorant-specific differences in sensitivity. Future studies should therefore
aim at analysing the chemical environment of non-human primate species, with
particular emphasis on differences in the frequency of occurrence of odorants
presumed to play a role in controlling their behaviour.
A second aspect of the present study is our finding of a significant
correlation between olfactory detection thresholds and carbon chain length of
the thiols in the spider monkeys and the squirrel monkeys (see
Fig. 5), and a marked effect of
the presence vs absence of a methyl group on the detectability of
indols in the squirrel monkeys and pigtail macaques (see
Fig. 6). Corresponding
correlations between olfactory sensitivity and length of the carbon chain
backbone have also been found in all three species of non-human primate as
well as in human subjects for homologous series of esters, alcohols,
aldehydes, ketones and carboxylic acids
(Laska and Seibt, 2002a;
Laska and Seibt, 2002b;
Laska et al., 2000;
Laska et al., 2003b;
Laska et al., 2004;
Laska et al., 2005a;
Laska et al., 2006a;
Cometto-Muniz and Cain, 1994).
This suggests that this type of correlation might not be restricted to classes
of odorants with oxygen-containing functional groups but may represent a more
general phenomenon. This should not be surprising, considering that the carbon
chain length of odorant molecules has been shown to be an important
determinant of the specificity of interaction between stimulus and receptor
(Gaillard et al., 2002), as
well as of the chemotopic organization, and thus odour quality coding within
the olfactory bulb (Johnson et al.,
2004).
A marked effect of the presence vs absence of a methyl group on
the detectability of odorants has also been reported in all three species of
primate for terpenes (Laska et al.,
2006c). Here, too, the present findings suggest that this
phenomenon may not be restricted to odorants with oxygen moieties.
Our finding of a lack of correlation between olfactory detection thresholds and carbon chain length of the thiols in the pigtail macaques (see Fig. 5), and between detectability and the presence vs absence of a methyl group in the spider monkeys (see Fig. 6) may at first seem difficult to explain. However, with regard to differences in across-odorant patterns of olfactory sensitivity 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, in turn, may plausibly explain why one species may show a regular connection between sensitivity and a given molecular structural feature whereas another species does not.
Taken together, the results of the present study support the hypotheses that (a) between-species differences in neuroanatomical or genetic features may not be indicative of olfactory sensitivity, and (b) within-species differences in olfactory sensitivity may reflect differences in the behavioural relevance of odorants.
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Acknowledgments |
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