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Behavioral study in the gray mouse lemur (Microcebus murinus) using compounds considered sweet by humans.

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American Journal of Primatology 62:43–48 (2004)
BRIEF REPORT
Behavioral Study in the Gray Mouse Lemur (Microcebus
murinus) Using Compounds Considered Sweet by
Humans
ALAIN SCHILLING1, VICKTORIA DANILOVA2, and GORAN HELLEKANT2n
1
Département d’Écologie et Gestion de la Biodiversite´, CNRS-MNHN UMR, Brunoy,
France
2
Department of Animal Health and Biomedical Sciences, University of Wisconsin–
Madison, Madison, Wisconsin
This study presents the results from two-bottle preference (TBP) tests
performed on the gray mouse lemur (Microcebus murinus), a small
Malagasy primate. We found that of 18 compounds considered sweet by
humans, M. murinus preferred only six: D-tryptophan, dulcin, fructose,
sucrose, SC45647, and xylitol. The animals neither preferred nor rejected
acesulfame-K, alitame, aspartame, N-4-cyanophenyl-N0 -cyanoguanidineacetate (CCGA), cyanosuosan, cyclamate, monellin, saccharin, suosan,
super-aspartame, N-trifluoroacetyl-L-glutamyl-4-aminophenylcarbonitrile (TGC), and thaumatin. Together with previously recorded tastenerve responses in M. murinus to acesulfame-K, alitame, aspartame,
cyclamate, monellin, saccharin, and suosan [Hellekant et al., Chem
Senses 18:307–320, 1993b], the current results suggest that these
compounds either do not taste sweet to M. murinus or they have an
aversive taste component. In this work we also relate these findings to
phylogeny. Am. J. Primatol. 62:43–48, 2004. r 2004 Wiley-Liss, Inc.
Key words: sweet taste; mouse lemur; two-bottle preference; taste
coding; taste qualities; receptors
INTRODUCTION
Although many studies have demonstrated anatomical or morphological
differences among primates that can be related to phylogeny, few investigators
have systematically explored the influence of phylogenetic factors in taste.
One reason for this may be that species differences were not evident because
‘‘taste primaries,’’ such as NaCl, sucrose, and quinine, were used as the taste
stimuli. However, with the introduction of new compounds, such as the potent
sweetener aspartame and the extremely bitter compound denatonium benzoate,
n
Correspondence to: Goran Hellekant, Department of Animal Health and Biomedical Sciences,
University of Wisconsin–Madison, 1656 Linden Dr., Madison, WI 53706.
E-mail: hellekant@svm.vetmed.wisc.edu
Received 7 August 2003; revision accepted 8 October 2003
DOI 10.1002/ajp.20004
Published online in Wiley InterScience (www.interscience.wiley.com).
r
2004 Wiley-Liss, Inc.
44 / Schilling et al.
phylogenetic factors became important. For example, of some 30 compounds
distinctly sweet taste to humans, more than one-third do not taste sweet to the
South American primate Callithrix jacchus jacchus, as judged by its behavior and
recordings from its taste nerves [Danilova et al., 1998b, 2002].
The nocturnal Malagasy primate (Microcebus murinus) is phylogenetically
more distant from humans than C. jacchus. Consequently, its sense of taste
probably differs more from that of humans compared to C. jacchus. M. murinus
belongs to the Lemuridae family, which is part of the prosimii infraorder and is
one of the smallest extant primates [Nowak, 1991]. As a result of about 54 million
years of isolation on Madagascar, it has developed some remarkable features. One
is a seasonal change of body weight of up to 100% [Petter-Rousseaux, 1980].
These weight changes have been shown to correlate with variations of
‘‘preference thresholds’’ for sucrose [Simmen and Hladik, 1988]. This correlation
led us to investigate the relationship between weight changes and taste in two
groups of M. murinus (heavy and light). We found no relationship between
seasonal weight and taste-nerve response to sucrose [Hellekant et al., 1993a].
However, in a second study we recorded the taste-nerve responses to a number of
other compounds considered sweet by humans and found that some produced no
taste response, while others, such as acesulfame-K, dulcin, saccharin, stevioside,
suosan, and xylitol elicited strong responses [Hellekant et al., 1993b].
We sought to determine how the above sweeteners taste to M. murinus. One
way to assess this is with behavioral observations. In the current study we used
another approachFthe two-bottle preference (TBP) test.
MATERIALS AND METHODS
Five female gray mouse lemurs (M. murinus) were used in this study. The
animals were born in the laboratory breeding colony of Brunoy (MNHN, France;
European Institutions Agreement 962773) and raised from birth under controlled
conditions of temperature (24–261), relative humidity (55%), and an artificial
photoperiodic regimen of 5 months of long days/short nights and 3 months of
short days/long nights [Perret, 1992].
The experiments were carried out during the long-days/short-nights phase.
Under such a regimen, increased physiological and behavioral activity is
associated with a seasonal activation of reproductive function in this highly
photoperiod-dependent species. The animals were housed individually and fed ad
libitum.
The animals had uninterrupted access to water before and after the tests.
During the TBP tests, each animal was offered 10 ml of water and 10 ml of one of
the compounds listed in Table I. Their concentrations (see Table I) were chosen to
be equisweet to 0.3 M sucrose in terms of human taste. The intake of water and
the compound in question was recorded during two consecutive TBP test sessions
of 10-hr night periods, and the position of the bottles was switched between
measurements.
The preference ratio was calculated for each animal and session as the amount
of sweetener consumed, divided by the total amount of liquid consumed. The mean
preference ratios were then calculated for each animal and the results were
averaged for five animals. Thus equal consumption of both water and sweetener
yields a preference ratio of 0.5; complete preference yields a preference ratio of 1.
The results were first assessed by analysis of variance (ANOVA). Then a twotailed t-test was used to compare mean preference ratios to 0.5. A P-value o0.05
was considered significant.
Sweet Taste in Mouse Lemur / 45
TABLE I. List of Compounds Used in TBP Experiments With M. murinus
Compounds
Acesulfame-K
Alitame
Aspartame
CCGA (N-4-cyanophrnyl-N’-cyanoguanidineacetate)
Cyanosuosan
Cyclamate
D-tryptophan
Dulcin
Fructose
Monellin
Saccharin
SC-45647
Sucrose
Suosan
Super-aspartame
TGC (N-trifluoroacetyl-L-glutamyl-4-aminophenylcarbonitrile)
Thaumatin
Xylitol
Concentration
7.3 mM
0.21mM
3.6 mM
0.21 mM
2.5 mM
33.5 mM
19.5 mM
1.67 mM
0.45 M
3 uM
2 mM
0.04 mM
0.3 M
2.17 mM
0.11 mM
0.17 mM
1.5 uM
820 mM
Potencies of sweeteners in human compared with sucrose were presented in Danilova et al. [2002].
RESULTS
Figure 1 presents the average intake of water and each compound, and Fig. 2
shows the average preference ratios for each sweetener. In the figures, the
compounds are arranged in order of decreasing preference ratio, and fall into two
groups.
The first group of sweeteners consisted of D-tryptophan, dulcin, fructose,
sucrose, SC45647, and xylitol. The consumption of these sweeteners was
significantly higher than the consumption of water.
The second group (acesulfame-K, alitame, aspartame, N-4-cyanophenyl-N0 cyanoguanidineacetate (CCGA), cyanosuosan, cyclamate, monellin, saccharin,
suosan, super-aspartame, N-trifluoroacetyl-L-glutamyl-4-aminophenylcarbonitrile (TGC), and thaumatin) was neither rejected nor preferred over water. The
preference ratios for these compounds did not significantly differ from 0.5.
DISCUSSION
Although M. murinus has a ‘‘sweet tooth’’ and likes many solutions
considered sweet by humans [Hellekant et al., 1993a; Simmen and Hladik,
1988], the results described above show that only one-third of 18 compounds that
taste distinctly sweet to humans elicited a significant preference in the TBP tests.
As mentioned above, we used concentrations equisweet to humans. It is possible,
and perhaps likely, that some of the compounds in the second group might have
induced significant behavioral effects at higher concentrations. However, because
the major emphasis of this study was to compare the sense of taste in M. murinus
with that in humans, we used only concentrations that clearly tasted sweet to
humans. Furthermore, when these concentrations were applied to Old World
monkeys, they elicited taste responses. This indicates that the results from the
compounds in the second group reflected phylogenetic differences, and were
unrelated to the concentrations of the compounds.
46 / Schilling et al.
10
*
*
8
water
*
sweetener
*
*
6
*
4
2
0
Fig. 1. Consumption of sweeteners and water in TBP tests. Data were averaged for five animals.
Stimuli concentrations are listed in Table I. Error bars are SE. Asterisks indicate significant
difference between sweetener and water consumption (Po0.05).
1
0.9
0.8
0.7
*
*
*
*
*
*
0.6
0.5
0.4
0.3
0.2
0.1
0
Fig. 2. Preference ratios from TBP tests. Data were averaged for five animals. Stimuli
concentrations are listed in Table I. Error bars are SE. Asterisks indicate significant difference
from preference ratio 0.5 (P o0.05).
Sweet Taste in Mouse Lemur / 47
In the following, we relate these results with those from earlier studies in M.
murinus and other mammals. We then discuss the results in the context of the
recent identification of a sweet taste receptor family (T1Rs).
With regard to the preferred compounds, we know from our earlier
electrophysiological work [Hellekant et al., 1993a, b] that xylitol, sucrose, and
dulcin elicit CT responses in M. murinus. Consequently, they have a taste to
M. murinus. Although we have no electrophysiological data for M. murinus
regarding fructose, D-tryptophan, or SC45647, it is likely that these compounds
also would have evoked a taste-nerve response, because they elicit taste-nerve
responses in all other species studied, from rodents to primates.
Of the 12 nonpreferred compounds, acesulfame-K, alitame, aspartame,
cyclamate, monellin, saccharin, and suosan elicited a CT response in our earlier
study of M. murinus. Since they produced a taste-nerve response at the same
concentrations as used here, lack of taste cannot explain the behavioral results.
Therefore, the taste sensation they evoked was either not attractive or was a
combination of an aversive taste with an attractive one.
Of the five remaining nonpreferred compounds, super-aspartame and
thaumatin elicited no CT response. Although it is possible that they
could stimulate some other taste nerves, this indicates that they do not
taste to M. murinus. Since we lacked electrophysiological data for CCGA,
cyanosuosan, and TGC, we were unable to draw any conclusions regarding those
compounds.
Of the preferred compounds, the mouse lemur shares a preference for xylitol,
fructose, sucrose, dulcin, D-tryptophan, and SC45647 with nonprimates, such as
hamsters [Danilova, 1998a] and mice [Bachmanov et al., 2001; Inoue et al., 2001;
Ninomiya et al., 1992], and higher primates, such as chimpanzees, rhesus
monkeys, and marmosets [Danilova et al., 1998a; Hellekant et al., 1997a,b; Hobi
and Glaser, 1983; Nofre et al., 1996; Plata-Salaman et al., 1992, 1993].
Furthermore, some of the compounds that were not preferred by M. murinus
are preferred by higher primates. For example, marmosets, rhesus monkeys, and
chimpanzees, all of which are more closely related to humans than M. murinus,
prefer alitame, super-aspartame, acesulfame-K, and cyanosuosan–compounds
that taste pleasantly sweet to humans. This points to phylogenetic differences in
the sense of taste, not only between primates and nonprimates, but also among
primates.
This conclusion is supported by a recent finding that the members of a
recently identified sweet receptor family, T1R, vary among primates. Li et al.
[2003] found eight sequence variant sites in T1R3, and 19 in T1R2 that were
different between primates tasting and not tasting aspartame. This may also
explain observed differences in the ability of New and Old World primates to taste
other compounds, such as thaumatin or monellin [Brouwer et al., 1973;
Hellekant, 1976; Glaser et al., 1978]. The genetical differences in T1Rs between
species show that the presence or absence of a taste-nerve response or behavioral
response is not determined by dietary factors. It is true that in the case of a
compound that has a taste, dietary factors may lead to shifts in intake or
preference, but diet does not abolish or produce taste-nerve response to a
compound. The only exceptions to this are the compounds known as taste
modifiers; however, their effects do not last long.
In summary, we have presented behavioral data showing that the sense of
taste in M. murinus differs from that in humans. Only six of 18 compounds
considered sweet by humans were preferred over water by M. murinus. These
differences are phylogenetically related. Thus, with increasing distance on the
48 / Schilling et al.
evolutionary tree, the number of compounds that elicit the same behavioral
response in two primate species decreases.
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