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Anogenital gland secretions of Lemur catta and Propithecus verreauxi coquereli A preliminary chemical examination.

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American Journal of Primatology 63:49–62 (2004)
RESEARCH ARTICLE
Anogenital Gland Secretions of Lemur catta and
Propithecus verreauxi coquereli : A Preliminary Chemical
Examination
R.A. HAYES1n, T.L. MORELLI2, and P.C. WRIGHT3
1
School of Natural Resource Sciences, Queensland University of Technology, Brisbane,
Australia
2
Department of Ecology and Evolution, State University of New York at Stony Brook,
Stony Brook, New York
3
Department of Anthropology, State University of New York at Stony Brook, Stony Brook,
New York
Although prosimians are greatly olfaction-oriented, little is known about
the specifics of how they use scent to communicate. In this preliminary
study we attempted to delineate intra- and interspecific differences
among the anogenital gland secretions of two lemur species (Lemur catta
and Propithecus verreauxi coquereli) using gas chromatography-mass
spectrometry (GC-MS). The results indicate that the two species are
discernible through scent. Furthermore, we were able to identify
reproductive status using this technique. The anogenital secretions of
the different sexes in L. catta, though perhaps not P. v. coquereli,
are chemically distinguishable. Given this information, it appears that
at least some lemur species can use scent marks to determine species,
sex, and reproductive status. Am J Primatol 63:49–62, 2004.
r 2004 Wiley-Liss, Inc.
Key words: lemur; scent marking; chemical fingerprint; olfaction; gas
chromatography-mass spectrometry; prosimian primate
INTRODUCTION
Although olfactory communication is known to be important in many
mammalian species, researchers rarely study its use, not to mention its evolution,
in primates. Sensory faculties in general, with the exception of vision, have been
largely overlooked in primate species [Epple, 1986]. Although most primates are
believed to have a visual and auditory focus, prosimians, along with many New
Contract grant sponsor: DUPC; Contract grant sponsor: Wenner Gren Foundation; Contract grant
sponsor: Sokal/Slobodkin.
n
Correspondence to: R.A. Hayes, School of Natural Resource Sciences, Queensland University of
Technology, Brisbane, QLD 4001 Australia. E-mail: a.hayes@qut.edu.au
Received 3 March 2003; revision accepted 1 April 2004
DOI 10.1002/ajp.20038
Published online in Wiley InterScience (www.interscience.wiley.com).
r
2004 Wiley-Liss, Inc.
50 / Hayes et al.
World monkeys, have retained olfactory complexity in addition to developing
other sensory modalities [Jolly, 1966]. Olfactory messages (particularly scent
marks) offer a relatively prolonged signal for communicating dominance status,
sexual condition, and territorial ownership [Epple, 1986]. An animal may use odor
to advertise key information about itself, including its species, group, or family
membership; long- or short-term breeding or social status; and sex [Albone,
1984]. In addition, the scent mark can potentially communicate genetic
information for use in decisions regarding mate choice or nepotism [Jordan &
Bruford, 1998; Penn & Potts, 1999; Zavazava & Eggert, 1997].
Previous investigations of olfaction in prosimians concentrated on the
animals’ response to scent, or the role of tradition in scent placement in the
wild, but did not attempt to explore the chemical nature of the scent itself, or to
distinguish chemical differences between individuals [e.g., Epple et al., 1987;
Evans, 1980; Harrington, 1974, 1977; Mertl-Millhollen, 2000; Price & Feistner,
1994; Ramsay & Giller, 1996; Vick & Conley, 1976]. With this preliminary study
we begin to fill that gap by investigating olfactory communication in prosimians,
using the ring-tailed lemur (Lemur catta) and Coquerel’s sifaka (Propithecus
verreauxi coquereli) as models. By analyzing the chemistry of scent through
coupled gas chromatography-mass spectrometry (GC-MS), we hope to learn more
about the information contained in the scent mark, as well as to begin to discover
how disparate life histories may affect the kind of information communicated.
Since a comparable investigation has not been conducted in prosimians, this
study also aims to test the predictive power of this methodology.
Both of the species studied here are classified in the IUCN Red List of
Threatened Species as ‘‘Vulnerable’’ (L. catta: VU A1c; P. v. coquereli: VU A2cd).
Coquerel’s sifaka (Propithecus verreauxi coquereli) is a diurnal, primarily
folivorous primate. The ring-tailed lemur (Lemur catta) is also diurnal, but it
feeds mainly on fruit, is not quite as large as P. v. coquereli, and is much more
terrestrial than other lemurs. Neither species displays significant sexual
dimorphism in their appearance [Kappeler, 1990b], and both are considered to
live in female-dominated groups [Jolly, 1966; Kubzdela et al., 1992; Pereira et al.,
1990]. Both species live in multi-male, multi-female groups; however, P. v.
coquereli has a smaller mean group size than L. catta [Richard et al., 2002]. The
two taxa studied here are allopatric: Coquerel’s sifakas inhabit the forests of
northwestern Madagascar, while ring-tailed lemurs are found in the forests and
arid, open areas of southern and southwestern Madagascar. Social groups of both
species have overlapping home ranges [Gould & Overdorff, 2002; Richard et al.,
2001]. However, while ring-tailed lemur females in the wild at Berenty have been
observed to aggressively defend their territory, with some groups having frequent
intergroup encounters, intergroup encounters between sifakas appeared to be
rare and nonconfrontational [Jolly, 1966; Kubzdela et al., 1992; Richard, 1974;
Richard et al., 2002]. In another sifaka field site, where intertroop interactions
were more common, these interactions consisted of threat displays, such as
chasing and rushing at opponents, but no biting [Mertl-Millhollen, 1979]. Both
species are strongly seasonal breeders [Rasmussen, 1985; Wright, 1999].
Both L. catta and P. verreauxi, like most prosimians, have specialized glands
for scent-marking their surroundings. Ring-tailed lemur males have antebrachial
organs, located on the flexor surface of each forearm near a keratinized spur, and
brachial organs just above each clavicle. In addition, there are glands on the
surface of the scrotum and perianal region [Montagna & Soonyun, 1962]. The
spur is used to gouge the surface of a tree, to deposit scent. Often the male mixes
the secretion from the antebrachial organ with that of the brachial organ, and
Chemistry of Gland Secretions of Two Lemurs / 51
then scent-marks [Evans & Guy, 1968]. During ‘‘stinkfights,’’ males rub their
tails with these two secretions and wave them at other males [Jolly, 1966; Mertl,
1976]. Both males and females scent-mark by rubbing the surface of their genital
and/or anal region against a tree [Mertl, 1977]. Similarly, male sifakas possess
specialized throat glands that they use to mark surrounding branches and tree
trunks. Both males and females also mark anogenitally [Mertl-Millhollen, 1979].
Although little is known about the olfactory behavior of P. v. coquereli
[Brockman & Whitten, 1996; Mertl-Millhollen, 1979], more data have been
published concerning the other subject of this study, L. catta–especially with
respect to the glands of the anogenital region. The relationship between
the anogenital marking rate and social status in males is ambiguous: two
studies reported finding no difference between high- and low-ranking males
[Gould & Overdorff, 2002; Oda, 1999], whereas another study showed that
higher-ranking males scent-mark more often than lower-ranking males [Ramsay
& Giller, 1996]. However, the social status of females does not appear to have any
effect on their rate of scent-marking [Kappeler, 1990a; Oda, 1999]. Moreover, Oda
[1999] found no significant effect of age (subadult vs. adult) on the marking rate
for either sex.
It is likely that the female L. catta anogenital mark conveys information
about reproductive status, since the marking rate increases as females approach
estrus, with a high peak during and after estrus [Jolly, 1972; Kappeler, 1990a,
1998]. In addition, male ring-tailed lemurs mark more frequently [Gould &
Overdorff, 2002] and are more interested in female secretion in the breeding
season than in the nonbreeding season [Dugmore et al., 1984]. On the other hand,
the marks placed by males may be deposited for the information of other males,
rather than females [Kappeler, 1990a, 1998; Oda, 1999]. However, the anogenital
gland is used by both male (in addition to other glands) and female L. catta to
mark the borders of group territories [Mertl-Millhollen, 1988, 2000]. Male ringtailed lemurs respond differently to scent marks from male and female donors
[Dugmore et al., 1984; Ramsay & Giller, 1996], although there is no difference in
the frequency with which males and females scent-mark with the anogenital
region [Oda, 1999].
In an interesting study, Mertl [1975] performed a series of habituation
experiments on L. catta, in which a male lemur was exposed to the scent of
another lemur’s glandular secretion until it became habituated to the new
animal. The male was then exposed to the secretion of a new animal, and any
difference in response between the two scents was measured. These experiments
showed that male L. catta can distinguish between the secretions of different
individuals.
If olfaction, and thus scent-marking behavior, is an important part of a
species’ behavior and ecology, what is it about this secretion that functions to
communicate so much information? What are the components of the secretion,
and how do they vary among individuals? Does each individual possess a unique
‘‘chemical fingerprint’’ that allows the animals to distinguish between the
glandular secretions? Furthermore, what, if any, are the interspecific differences
of the secretion?
MATERIALS AND METHODS
Samples were collected in February 2002 from two species of lemur that were
held in captivity at the Duke University Primate Center (DUPC), Durham, NC
(Table I). All of the animals were captive-born, with the exception of the oldest
52 / Hayes et al.
TABLE I. Details of the Species, Sex and Age of Each of the Animals Sampled
Name
Species
Sex
Cleis
Cleomenis
Dorieus
Dory
Katina
Hector
Licinius
Selacius
Teres
Thrasun
Alexianus
Antonia
Drusilla
Livia II
Paulina
Brutus
Nero
Philip
Trajan
Zeno
Lemur catta
Lemur catta
Lemur catta
Lemur catta
Lemur catta
Lemur catta
Lemur catta
Lemur catta
Lemur catta
Lemur catta
Propithecus verreauxi
Propithecus verreauxi
Propithecus verreauxi
Propithecus verreauxi
Propithecus verreauxi
Propithecus verreauxi
Propithecus verreauxi
Propithecus verreauxi
Propithecus verreauxi
Propithecus verreauxi
F
F
F
F
F
M
M
M
M
M
F
F
F
F
F
M
M
M
M
M
coquereli
coquereli
coquereli
coquereli
coquereli
coquereli
coquereli
coquereli
coquereli
coquereli
Age
17
15
2
13
15
13
9
17
7
6
5
4
9
5
11
1
7
3
22
2
P. v. coquereli, Trajan. The L. catta at DUPC, including the test subjects, were
allowed to range in semi-free-range enclosures (9.1 ha) during the warmer
months (approximately April–October). During the winter they were housed in
indoor/outdoor enclosures with other L. catta, separated from the P. v. coquereli.
The P. v. coquereli were housed in open-air enclosures that still admitted natural
light when the animals were closed in for the winter months. The L. catta were
fed vegetables and commercial primate pellets (Lab Diet Product 5038 Monkey
Diet; PMI Feeds Inc., Purina, Richmond, IN), whereas the P. v. coquereli were fed
vegetables, nuts, leaves, and a different type of commercial primate pellet (Leaf
Eater Primate Diet Mini-Biscuit #5672, Mazuri, Richmond, IN). The analysis
included sexually mature and immature animals of both species. Although the age
of sexual maturity is variable, it is considered to be 2 years for L. catta and 3–5
years for P. v. coquereli (Hess, personal communication) [Richard et al., 2001].
In analyses of skin gland secretion in mammals, purity is important, volumes
are generally small, and high volatility is common. Given these concerns, we
chose to use gas-chromatography-mass spectrometry, since it is considered by
many researchers in the field to be the most practical analytical method [e.g.,
Buesching et al., 2002a, b; Gassett et al., 1997; Hayes et al., 2001, 2002a, b].
Duplicate swabs were taken of the anogenital region of 10 individuals of
each species (five males and five females). Swabs were also collected from the
other scent glands of the male, the results of which are discussed elsewhere [Hayes et al., in press]. We collected secretions by rubbing the area of
the scent gland of a hand-captured lemur with 1 cm 4 cm glass filter paper
[Salamon, 1994]. The swabs were then sealed in an airtight vial and stored in
the laboratory at a reduced temperature (approximately –751C). The samples
were air-freighted at ambient temperature to Australia, and then immediately returned to –751C before they were analyzed at the University of
Western Sydney.
Chemistry of Gland Secretions of Two Lemurs / 53
In the laboratory, the vial containing the swab was opened and the filter
paper was inserted into the liner of the cooled injector port (451C) of a gas
chromatograph (GC; 5890 Series II; Hewlett Packard) coupled to a mass
spectrometer (MS; model 5971A; Hewlett Packard) and fitted with a silica
capillary column (model DB5-HT, no. 122-5731; J&W; 30 m long 0.25 mm ID
0.1 mm film thickness). We cryofocused the sample onto the front of the GC
column by maintaining the column at low temperature (21C) and ramping up the
injector to 1501C at 271C/min.
Data were acquired under the following GC conditions: inlet temperature: 1501C; carrier gas: helium at 1.1 mL/min; split ratio = 1:2; detector
temperature = 2801C; temperature program: initial temperature = 21C; initial
time = 4 min; rate = 201C/min to 501C and then 51C/min; final temperature =
2501C; final time = 2 min. The MS was held at 1901C in the ion source with an
ionization energy of 70 eV and a scan rate of 0.9 scans/sec. The two swabs
collected from each animal were analyzed and compared. Tentative identities
were assigned to peaks with respect to the Wiley mass spectral library. Mass
spectra of peaks from different samples with the same retention time were
compared to ensure that the compounds were indeed the same. An arbitrary
threshold of peak size of an abundance of 100,000 relative to background was
used to define the presence or absence of a peak. We used this figure in an attempt
to reduce the number of analyzed peaks to a manageable level without excluding
important components.
We statistically assessed the presence of peaks in the chromatograms,
and their relative areas by nonparametric methods (Bray-Curtis cluster
analysis and multidimensional scaling (MDS) ordination) to ascertain
whether any differences could be detected between the animals. It can
be difficult to analyze chromatographic data statistically, because they
typically show high levels of variation and very right-skewed distributions. In
this way they are similar to ecological data regarding species composition
[Clarke & Warwick, 1994a, b]. The use of informal display methods, such
as clustering and MDS, may be a more valid approach for such data compared
to other commonly used techniques, such as principal components analysis
(PCA) [Hayes et al., 2002b]. MDS works on a sample dissimilarity matrix
rather than the original data array, makes fewer assumptions about the nature
and quality of the data, and does not assume normality of the data [Clarke &
Warwick, 1994a, b].
MDS uses the dissimilarity matrix of the data to produce a graphical
representation. Each point in the MDS represents an individual lemur, and points
that are close together (clumped) correspond to individuals with similar peak
composition (presence and abundance). Since they represent relative differences
between samples, the axes of an MDS plot are dimensionless. MDS has been used
successfully in previous studies to analyze chromatographic data [Hayes et al.,
2002a, b, 2003].
To determine whether clusters of individual lemurs were significantly
different from each other, we used an analysis of similarity (ANOSIM). The
ANOSIM tests are a range of Mantel-type permutations of randomization
procedures, which make no distributional assumptions. These tests depend only
upon rank similarities, and thus are appropriate for this type of data. We used a
similarity percentages (SIMPER) analysis to determine which peaks were the
most important in contributing to any differences between groups, and to assess
similarity between individuals within each group. The software used for the
multivariate analysis was Primer 5 for Windows (V 5.2.4, 2001).
54 / Hayes et al.
RESULTS
Several compounds found in the secretion of the lemurs were identified by
MS (Table II). These compounds were primarily identified as straight and
branched long-chain hydrocarbons with alcohol and aldehyde components. In
addition, several of the components were oxygenated compounds, particularly
esters. The percentage of individuals in each group from which the component
was identified is shown in Table II. It should be noted that there is a contaminant
peak at approximately 51 min that appears in all chromatograms, including blank
samples of paper without secretion. This peak acted as an internal standard, and
was thus invaluable in allowing comparisons of retention times to be made
between chromatograms.
The chromatograms produced by the two species of lemurs are distinctly
different from each other. Swabs from the anogenital region of L. catta
demonstrate many more peaks compared to those from P. v. coquereli (Figs. 1
and 2). In addition to looking different, the samples from the two species are
statistically distinguishable (ANOSIM: global R = 0.492, P = 0.001); in other
words, it is possible to determine from which species an unknown sample was
collected.
In the case of L. catta, it is also possible to determine the sex of the animal
from which a swab was obtained (ANOSIM: R = 0.248, P = 0.032). In contrast,
however, swabs from male and female P. v. coquereli are statistically
indistinguishable (ANOSIM: R = 0.14, P = 0.135). There is more variability in
the P. v. coquereli samples compared to the L. catta samples, with larger distances
between individuals. This larger variability may account for the lack of
statistically significant difference between the sexes in P. v. coquereli.
The SIMPER analysis shown in Table III is a measure of the similarities and
differences of samples within a defined grouping, in this case based on species and
sex. One can see from a comparison of the within-group similarities (Table IIIa)
that samples from P. v. coquereli females are much less similar to each other than
are samples from the other three groups. In addition, one can see that the average
dissimilarity between all of the groupings is very high (Table IIIb), which suggests
that each group is distinct from the others, as described above.
The MDS output is shown in Fig. 3, which gives a visual representation of the
data described by the ANOSIM (above). Each point on the figure represents an
individual lemur. Points that are close together are more similar, and those
farther away are more different. One can see that individuals from each of the two
species clump together, that male and female L. catta are different from each
other, and that the sexes of P. v. coquereli are not well differentiated.
DISCUSSION
The objective of this pilot study was to investigate the use of GC-MS to reveal
specific information encoded in prosimian scent marks, and to compare this
information intra- and interspecifically. We collected swabs from the surface of
the skin directly overlying scent glands in the anogenital region of manually
restrained lemurs, and equated this with the scent mark. This is most likely an
oversimplification of a natural scent mark, which may be chemically more
complex than that found on a collected swab. For example, when a scent mark is
placed by a free-ranging animal, the glandular secretion may be mixed with
materials from other sources, such as urine. Although the results presented here
should be interpreted with caution, it is likely that the observed patterns in the
collected anogenital gland secretions are important and worthy of note.
Chemistry of Gland Secretions of Two Lemurs / 55
TABLE II. Tentative Identity of Compounds Identified From Swabs of the Glandular Regions
of the Two Species of Lemurn
Name
Cyclooctane
1-dodecanol
Methyl-cyclodecane
(Z)-2-decene
4-decene
1-butyl-1-methyl2-propyl-cyclopropane
6-tridecene
Hydrocarbon
Cyclododecane
3-methyl-6-octen-1-ol
Hydrocarbon
Long chain alcohol
1-tridecene
1-pentadecanol
1-hexadecanol
Long chain alcohol
Long chain alcohol
1-heptadecanol
(Z)-7-hexadecene
Long chain ester
1-octadecanol
Long chain alcohol
Long chain alcohol
Long chain alcohol
Hydrocarbon
Long chain ester
Long chain alkene
Hydrocarbon
(E)-b-farnesene
Long chain ester
Long chain ester
Long chain ester
Octanoic acid,
hexadecyl ester
Hydrocarbon
Decanoic acid, decyl ester
Long chain ester
Long chain ester
1-hexadecanal, acetate
Long chain alcohol
Long chain alcohol
Long chain alcohol
Long chain alcohol
Long chain alcohol
Long chain alcohol
Long chain alcohol
L. catta,
f. anogenital
L. catta,
m. anogenital
P. v. coquereli,
f. anogenital
P. v. coquereli,
m. anogenital
0
60
60
60
80
80
0
60
60
60
60
60
20
0
0
0
40
0
60
0
0
0
100
20
80
100
100
100
100
80
80
80
80
100
100
100
60
100
100
80
100
40
60
60
80
80
80
80
100
60
80
60
60
60
60
60
60
60
60
60
60
60
20
40
40
60
20
40
40
40
40
60
60
40
40
40
80
40
0
0
40
0
0
0
0
0
0
20
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
80
0
0
0
60
0
20
80
80
0
80
60
0
80
80
0
0
0
0
0
0
80
0
0
0
60
20
60
20
40
40
40
40
40
20
40
40
60
80
60
80
80
100
100
100
80
40
80
80
40
0
0
0
20
40
0
20
0
60
0
0
80
0
0
0
60
20
20
20
20
20
20
20
n
The number indicates the percentage of individuals sampled in which the given compound was identified in
retention time order.
56 / Hayes et al.
L. catta female (Cleomenis) - anogenital gland
7500000
7000000
6500000
6000000
Abundance
5500000
5000000
4500000
4000000
3500000
3000000
2500000
2000000
1500000
1000000
500000
0
10.00
20.00
30.00
(a)
40.00
50.00
60.00
Time (min)
L. catta male (Thrason) - anogenital gland
6000000
5500000
5000000
Abundance
4500000
4000000
3500000
3000000
2500000
2000000
1500000
1000000
500000
0
10.00
(b)
20.00
30.00
40.00
50.00
60.00
Time (min)
Fig. 1. Chromatograms produced by swabs from the anogenital region of L. catta. A typical female
swab is shown on top (a), and a typical male swab is shown below (b). These two animals were
selected at random. The peak at approximately 51 min is a contaminant that appears in all of the
chromatograms, including blanks.
The collected anogenital gland secretions appear to reveal specifics regarding
species, sex, age, and reproductive status. Other information indicating group and
family membership may also be communicated, but this is ambiguous because of
the small sample size. The observed differences between the anogenital gland
secretions of the two study species may reflect how these scent marks are used in
the wild. Behavioral observations suggest that these scent marks are used to
mark the boundaries of the territory defended by the social group. Since the
major use of these secretions may be for intraspecific communication [Kappeler,
1998], an animal should be able to distinguish a mark placed by a member of its
own species from a less relevant mark derived from a different species. Where the
Chemistry of Gland Secretions of Two Lemurs / 57
Abundance
P. v. coquereli female (Drusilla) - anogenital gland
3.4e+07
3.2e+07
3e+07
2.8e+07
2.6e+07
2.4e+07
2.2e+07
2e+07
1.8e+07
1.6e+07
1.4e+07
1.2e+07
1e+07
8000000
6000000
4000000
2000000
0
10.00
20.00
30.00
(a)
40.00
50.00
60.00
Time (min)
P. v. coquereli male (Zeno) - anogenital gland
4500000
4000000
Abundance
3500000
3000000
2500000
2000000
1500000
1000000
500000
0
10.00
20.00
30.00
(b)
40.00
50.00
60.00
50.00
60.00
Time (min)
P. v. coquereli male (Nero) - anogenital gland
6e+07
5.5e+07
5e+07
Abundance
4.5e+07
4e+07
3.5e+07
3e+07
2.5e+07
2e+07
1.5e+07
1e+07
5000000
0
10.00
(c)
20.00
30.00
40.00
Time (min)
Fig. 2. Chromatograms produced by swabs from the anogenital region of P. v. coquereli. A typical
female swab selected at random is shown at the top (a), with two different types of male swab below
(b and c). The peak at approximately 51 min is a contaminant that appears in all of the
chromatograms, including blanks.
58 / Hayes et al.
TABLE III. Results of the SIMPER Analysis, a Measure of the Average Similarity/
Dissimilarities Between the Anogenital Swabs From Lemursn
Group/s
Similarity/dissimilarity (%)
a. Similarity within group
L. catta female
L. catta male
P. v. coquereli female
P. v. coquereli male
49.6
34.5
5.7
25.8
b. Dissimilarity between groups
L. catta female/L. catta male
L. catta female/P. v. coquereli female
L. catta female/P. v. coquereli male
L. catta male/P. v. coquereli female
L. catta male/P. v. coquereli male
P. v. coquereli female/P. v. coquereli male
69.0
92.5
77.5
92.6
83.3
87.7
n
Comparisons are made with samples grouped according to species and sex. The results shown are: a) the
average percentage similarity within groups, and b) the average percentage dissimilarity of samples between
groups. One can see that the swabs from the P. v. coquereli females are much less similar than are the swabs from
the other groups. It can also be seen that the average percentage dissimilarity between groupings is very high,
demonstrating that the groups are discrete.
Stress: 0.12
Fig. 3. Two-dimensional MDS ordination of the 20 lemur anogenital samples. The plot is based on
square root-transformed abundances and a Bray-Curtis similarity matrix. Note that the two species
are separate, and the sexes are separate for L. catta. SymbolsFm: L. catta females (n = 5); n: L.
catta males (n = 5); ’: P. v. coquereli females (n = 5); &: P. v. coquereli males (n = 5).
distribution of L. catta overlaps with that of another P. verreauxi subspecies (P.
verreauxi verreauxi), although there is some vertical zonation of marking location,
the vertical distribution of marks overlap extensively [Millhollen, 1986].
Chemistry of Gland Secretions of Two Lemurs / 59
In addition to being used to mark the boundaries of social group territory (an
action performed by all individuals in the group [Mertl-Millhollen, 1988, 2000]),
the secretions of the anogenital gland are used to determine sexual condition in
female L. catta [Jolly, 1972; Kappeler, 1990a, 1998].
The results from the present study indicate that L. catta scent marks may
communicate detailed information to the recipient, including the sex of the
marker. However, male and female sifaka anogenital gland secretions were not
distinguishable by our tests. There are several possible explanations for this. P.v.
coquereli may not use scent marks in the same way as the ring-tailed lemurs. On
the other hand, it may be that sex is encoded by some information other than that
found in the volatile chemicals of the anogenital mark. For example, the secretion
from other scent glands (such as the throat gland in the P. v. coquereli males) may
be used in contexts in which sex differentiation is important, since they are not
present in females [Hayes et al., in press]. We will soon be conducting habituation
tests and behavioral bioassays to determine whether P. v. coquereli can in practice
differentiate between the scent marks of males and females from the different
glands [after Mertl, 1975; Epple, 1986].
There are some complicating factors that arise when one attempts to
interpret the results of this preliminary study. The two species were fed similar,
but not identical, diets. The animals were also housed differently. Although the
housing at the time of the study was very similar, L. catta may exhibit long-term
effects from their semi-free-range allowances during the warmer months. This,
rather than genetic causes, may explain the differences observed between the two
species. However, it would not explain the differences observed between
individuals or between the sexes within species, and thus we suspect that these
interspecific differences are real.
The handling procedures were stressful for most of the animals; however,
since there was only a short period of time between the capture of the animal and
the collection of the secretion, it is difficult to imagine how handling could have
affected the results. In addition, because of the comparative nature of the study, it
is likely that stress had little effect on the results. Similarly, although manual
expression of the secretion may have affected the results [Belcher et al., 1988],
such manipulation does not easily explain the observed differences, since both
species were treated similarly.
The shipping process may have caused a decrease in variation through a
potential loss of some of the more volatile constituents from the airtight vials in
which the samples were transported, or as a result of bacterial activity.
Consequently, samples that were actually different may have become indistinguishable. However, since differences were still apparent between samples, the
conclusions drawn in the current study are likely to be correct, or to err on the
conservative side. A similar issue is that concerning loss of information
throughout the collection and analysis. It may be that although the animals
themselves are able to gain information from the anogenital gland secretions, the
analytical technique employed in this study may not be sensitive enough to detect
the subtle nuances that are used as cues. As in all such studies, one cannot
assume that absence in the results means absence in nature.
Although it was originally believed that semiochemical messages could only
be composed of highly volatile compounds, this is no longer thought to be the case.
Research has shown that proteins are vital components of the scent-mark
secretions of a variety of organisms, including the golden hamster (Mesocricetus
auratus) [Singer et al., 1986], meadow vole (Microtus pennsylvanicus) [Ferkin
et al., 1997], cotton-top tamarin (Saguinus fuscicolis) [Belcher et al., 1990], and
60 / Hayes et al.
house mouse (Mus domesticus) [Hurst et al., 1998]. It is possible that there are
other important components to the scent mark, such as high-molecular-weight,
nonvolatile compounds (e.g., proteins) that are not detected by GC-MS, and thus
were not examined in this study. Given that prosimians possess a functioning
vomeronasal system, it may be worthwhile in future studies to examine these
compounds to determine whether there is other information that is not being
captured by the present analytical technique. However, using GC-MS to analyze
the information found in the glandular secretions of prosimians appears to be a
meaningful and efficient way to better understand this important sensory
modality.
This research demonstrates that the lemur anogenital gland secretions
encode information on sex, reproductive status, and individuality, as well as
species. The methodological complications in this work may cause differences to
be underestimated; however, the evidence of categorical distinctions indicates
that important information can be gleaned from the technique used. Forthcoming
habituation experiments and behavioral bioassays, such as those described above,
will help to clarify the context in which these scent marks are used by these
species, and the importance of the differences between these and other lemur
species. It is hoped they will also lead to a better understanding of the evolution of
olfactory communication in prosimians.
ACKNOWLEDGMENTS
The authors thank Associate Professor S. Grant Wylie and Dr. Sonia Claus
for assistance with technical aspects of this paper, and Bill Hess and David Haring
for their advice and help with the sample collections. This research was carried
out under SUNY Stony Brook University IACUC registry no. A026-02-01, and
Duke University IACUC registry no. A026-02-01. The samples were imported into
Australia under AQIS permit no. 200205460. This research was supported in part
by a grant from the Wenner Gren Foundation to P.C.W., and a Sokal/Slobodkin
travel award to T.L.M. This is DUPC publication #767.
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