Chem. Senses 28: 381-388,
2003
© Oxford University Press 2003
Possible Coding for Recognition of Sexes, Individuals and Species in Anal Gland Volatiles of Mustela eversmanni and M. sibirica
1 State Key Laboratory of Integrated Management of Pest Insects and Rodents in Agriculture, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080 2 Department of Biology, Capital Normal University, Beijing 100083, China 3 Department of Biological Sciences, Central Washington University, Ellensburg, Washington, WA 98926-7537, USA 4 Present address: Department of Chemistry, Institute for Pheromone Research, Indiana University, Bloomington, IN 47405, USA
Correspondence to be sent to: Zhi-Bin Zhang, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China. e-mail: zhangzb{at}panda.ioz.ac.cn
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Abstract |
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With a combination of solvent extraction and gas chromatography—mass spectrometry, we found eight new compounds in the two sympatric Mustela species, M. eversmanni and M. sibirica. These compounds had not been detected by headspace sampling with solvent desorption. Two of the newly detected compounds are nitrogen-containing compounds, indole and o-aminoacetophenone and the remaining are sulfur-containing volatiles. By comparing same and opposite sexes between the two Mustela species, we found that qualitative differences in the anal gland secretion are most likely to be used to code for information about species, corresponding to the idea of digital coding. In the Siberian weasel (M. sibirica), both presence or absence of sex-specific compounds (Z-2-ethyl-3-methylthietane only in females) and relative abundance of some compounds between males and females could be used to code for information about sex, corresponding to the idea of digital and analog coding, respectively. In the steppe polecat (M. eversmanni), only quantitative differences provided the possibility for inter-sexual communication. Thus coding for information about sex appeared to be digital. Coding for individual information could also be either digital or analog or both through the presence or absence of certain compounds and/or the difference in the relative abundances of certain compounds among individuals. Comparing with other Mustela spp., we failed to find a congruence between the chemical composition of anal gland secretions and the phylogenetic relationship among the species in this genus.
Key words: anal gland secretion, volatile compounds, Siberian weasel, Mustela sibirica, steppe polecat, Mustela eversmanni
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Introduction |
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How information is coded is one of the main questions in the study of animal chemical communication. This question is normally answered through two ways, behavioral and chemical (Sun and Müller-Schwarze, 1998a
,b).
In mammals, where chemical signals are characteristically complex with
multiple components, the chemical analysis approach is particularly desirable
and often the first step in deciphering a complex chemical signal (Sun and
Müller-Schwarze,
1998a,b).
Small carnivores, especially the genus Mustela, are amongst the
most intensively studied groups in mammals with respect to chemical
communication. Chemical secretions from the anal gland have been chemically
analyzed in seven species of Mustela
(Albone, 1984;
Brown and Macdonald, 1985;
Zhang et al., 2002b).
Because of this, a wealth of information in these species has been accumulated
for comparison and, thus, these species are valuable model systems in the
study of mammalian chemical communication.
Anal gland volatiles of the following species in the genus Mustela
have been chemically analyzed: the American mink, M. vison (Brinck
et al., 1978,
1983;
Sokolov et al.,
1980); the stoat, M. erminea and the domestic ferret,
M. putorius furo, in New Zealand (Crump,
1980a,1980b;
Crump and Moore, 1985); the
mountain weasel (M. nivalis); the European polecat, M.
putorius (Brinck et al.,
1983); the steppe polecat, M. eversmanni; and the
Siberian weasel, M. sibirica (Zhang et al.,
2002a,2002b).
Most of the 18 major volatiles detected in their anal glands are unique to the
genus Mustela and have not been found in other genera of the family
Mustelidae (Gorman et al.,
1978; Brinck et al.,
1983; Crump and Moors,
1985). Among them are two nitrogen-containing compounds, indole
(in all Mustela species) and o-aminoacetophenone (in M.
erminea only), with the remainder all being sulfur-containing
compounds.
The main function of anal glands in mustelids is widely believed to be
intraspecific communication. It is also possibly used for interspecific
communication as well, because there are qualitative and quantitative
differences between species in the chemical composition of anal gland
secretions (Brinck et al.,
1983). However, few studies are available that compare anal gland
volatiles within and between sympatric Mustela species and
investigate their ecological and evolutionary significance associated with
communication (Zhang et al.,
2002b). Additionally, the widely used, labor-intensive procedure
of headspace sampling with solvent desorption and concentration by liquid gas
blow may raise the question of reliability, because proportional distortion
and escape of anal gland volatiles are likely (Zhang et al.,
2002a,2002b).
For example, using this method we were unable to find indole in the secretions
of the American mink (Zhang et
al., 2002a), the steppe polecat, or the Siberian weasel
(Zhang et al.,
2002b). This nitrogen-containing compound is common to
Mustela species and has also been identified in the anal gland
secretion of the American mink (Brinck
et al., 1983; Sokolov
et al., 1980). It was therefore necessary to conduct a
further investigation of anal gland volatiles using a more sensitive sampling
method.
Sun and Müller-Schwarze (Sun and Müller-Schwarze,
1998a,
1999) postulate two general
forms of information coding—digital and analog—corresponding to
information coding by presence/absence of chemicals used for communication
versus coding by varying amounts of these substances. In the genus
Mustela, it has been reported
(Crump, 1980a) that
2-ethylthietane and 3-ethyl-1,2-dithiacyclopentane are female-specific in
stoats and inferred from gas chromatography (GC) profiles that
3-propyl-1,2-dithiacyclopentane seems more abundant in females. Thus, coding
for sex information in stoats can be either digital or analog or both. There
have also been several valuable attempts to determine how individuality is
coded by chemically analyzing anal gland secretions in the mink and stoat
(Brinck et al., 1978;
Erlinge, et al.,
1982; Clapperton et
al., 1988). The forms of coding and the generality of these
findings might be substantiated by comparing situations in other mustelids,
which are yet to be investigated.
In this study, we investigated the chemical composition and coding
form—digital or analog or a combination of the two—in two closely
related, sympatric species, the Siberian weasel (M. sibirica
fortanieri) and the steppe polecat (M. eversmanni admirata). The
two species overlap in ecological niches in North China
(Gao, 1987). Specifically, we
intended to achieve two research goals in this study. The first was to find
previously undetected compounds and to quantify the proportions of anal gland
volatiles in the two species by the solvent extract sampling method. The
second was to explore the likely forms—digital or analog or
both—of coding for information about species, sex and individuality in
the two species.
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Materials and methods |
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Collection and extraction
Anal glands along with anuses were removed fresh from steppe polecats (11
males and 10 females) and Siberian weasels (11 males and 11 females) within 12
h of their being captured by legal fur trappers in several farmland areas in
central North China in midwinter (January) 2001. They were immediately frozen
and then transferred to the laboratory and stored at -20°C until use. For
both species, males with a baculum weight >350 mg and females with body wt
>500 g were classified as adults and their anal glands were used
(Sheng and Lu, 1976;
Gao, 1987).
After thawing, we thoroughly cleaned every collected specimen using a 75% solution of ethyl alcohol, squeezed the anal gland sacs and collected the yellowish secretion around the two gland duct openings using a clear glass capillary pipette. We weighed the collected secretion and then immersed the pipette in redistilled dichloromethane in a glass vial in the proportion of 8 mg secretion in 1 ml dichloromethane. After 5 min, we removed the pipette and stored the sealed vials at -20°C for gas chromatography and mass spectrometry (GC—MS) analysis within 1 week.
GC—MS analysis
Analytical GC—MS was performed on a Finnigan GC—MS (Trace 2000 series) instrument. Xcalibur (Windows 2000) was used for data acquisition and processing. The initial area reject threshold was 20 000. The GC was equipped with a 30 m glass capillary column (internal diameter 0.25 mm) coated with DB5. Helium was used as the carrier gas at a flow rate of 1.0 ml/min. The temperature of the injector was set at 250°C and the split ratio was set at 1:10. The oven temperature was programmed as follows: 50°C for 5 min initially, increased by 5°C/min up to 200°C and held at 220°C for 5 min and then increased again at 10°C/min up to 290°C and finally held at 290°C for 15 min. Electron impact ionization was used at 70 eV. Transfer line temperature was 250°C. The amount of sample injected was 1 µl every time.
We used parallel GC—MS analyses to compare GC retention times and MS
spectra between previous (prepared by headspace trap and solvent desorption)
and present samples (solvent extraction) of anal gland secretions from male
steppe polecats. We identified the following compounds: (1)
2,2-dimethylthietane; (2) Z- or E-2,4-dimethylthietane; (3)
E-2,3-dimethylthietane; (4) 2-ethylthietane; (5)
E-2-ethyl-3-methylthietane; (7) Z-2-ethyl-3-methylthietane;
(8) 2-propylthietane; (9) 3,3-dimethyl-1,2-dithiacyclopentane; and (12)
Z-3,4-dimethyl-2,2-dithiacyclopentane. These compounds have
previously been identified in headspace samples of anal gland secretions in
steppe polecats (Zhang et al.,
2002b).
Similarly, indole has been identified in the American mink (Brinck et
al., 1978,
1983;
Sokolov et al.,
1980). The parallel analysis of solvent-extracted samples of anal
gland secretion in American minks led to the identification of (16) indole in
steppe polecats and Siberian weasels.
We used the mass spectra available in the literature to aid the
identification of the following compounds: (6) 2-isopropylthietane, (10)
3-ethyl-1,2-dithiacyclopentane, (11)
E-3,4-dimethyl-1,2-dithiacyclopentane, (13) 2-pentylthietane, (14) 3-
and (15) 4-propyl-1,2-dithiacyclopentane and (17) o-aminoacetophenone
(Crump, 1980b;
Sokolov et al., 1980;
Brinck et al., 1983;
Crump and Moors, 1985).
We used the method developed previously
(Sun and Müller-Schwarze,
1998b) to quantify the relative abundance of relevant compounds.
That is, we converted the peak area of a particular compound into the
percentage of the summed peak areas of all 17 compounds in steppe polecats and
14 compounds in female and 13 in male Siberian weasels in a sample,
respectively. The statistical comparisons of the levels of excreted volatiles
among two species and two sexes were made using one-way analysis of variance
(ANOVA) with the post hoc Bonferoni t-test. The level of
significance was set at P < 0.05 for all tests. The statistical
analysis was conducted in SPSS v. 6.0.
To determine the variability of the volatile compositions between
individuals, relative standard deviation (RSD) was used and calculated using
the following formula:
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Results |
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Anal gland volatiles
GC—MS analysis of individual samples revealed 17 total ion chromatogram (TIC) peaks in both sexes of steppe polecats. Fourteen TIC peaks (absence of peaks 11, 13 and 14) in females and 13 TIC peaks (one more absent peak: 7) in males of Siberian weasels were detected within 25 min (Fig. 1 and Table 1).
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Using parallel GC—MS analysis of previous samples (prepared by
headspace trap and solvent desorption) of male steppe polecats and comparing
their retention times and MS data with the previous results
(Zhang et al.,
2002b), we identified nine compounds: (1) 2,2-dimethylthietane;
(2) Z-or E-2,4-dimethylthietane; (3)
E-2,3-dimethylthietane; (4) 2-ethylthietane; (5)
E-2-ethyl-3-methylthietane; (7) Z-2-ethyl-3-methylthietane;
(8) 2-propylthietane; (10) 3,3-dimethyl-1,2-dithiacyclopentane; and (12)
Z-3,4-dimethyl-2,2-dithiacyclopentane. Comparing their retention
times and MS data with the GC—MS data from the solvent-extracted samples
of polecats and the weasels, we identified these nine compounds in the two
Mustela species (Table
1 and Fig. 2).
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Through parallel analysis of the anal gland secretion from the American
mink with the same sample preparation method as used in this study, we
identified peak 16 as indole in M. eversmanni and M.
sibirica, since the retention time and MS data were the same as those of
indole in American minks (Sokolov et
al., 1980; Brinck, et
al., 1983) (Table
1 and Fig. 2)
Analysis of the mass spectrum implied that peak 6 is the fourth isomer of
2-propylthietane. The loss of m/z 101 and
m/z 74 suggested the presence of methyl and propyl,
respectively; in addition, the absence of m/z 87, 88 implied
the absence of ethylene. This suggested that the compound was
2-isopropylthietane, which has been identified in ferrets, M.
putorius forma furo (Crump
and Moors, 1985) (Table
1 and Fig. 2).
In peak 9, the loss of m/z 101, m/z 69
and m/z 55 implied the presence of HS, HS2 and
CH3S2, respectively, which implied a
dithiacyclopentane ring. In addition, the loss of m/z 105
implied an ethyl. These data suggested 3-ethyl-1,2-dithiacyclopentane
(Crump, 1980a)
(Table 1 and
Fig. 2).
Peak 11 had a similar MS spectrum to peak 12 and a shorter retention time
than Z-3,4-dimethyl-1,2-dithiacyclopentane. This led us to identify
peak 11 as E-3,4-dimethyl-1,2-dithiacyclopentane, as was identified
by Crump (Crump, 1980b) in the
ferret (Figs 1
2 and
Table 1).
In peak 13, the loss of m/z 115, m/z
101, m/z 87 and m/z 73 implied ethyl,
propyl, butyl and pentyl. These data implied an n-pentyl. Comparison
of the mass spectrum with that of peak 8 (2-propylthietane) revealed a
thietane structure with a pentyl side-chain. Peak 13 was identified as
2-pentylthietane (Crump, 1980a)
(Table 1 and
Fig. 2).
The GC and MS data for the peaks 14 and 15 showed that they both had a mol.
wt of 148 and were similar to those of 3-propyl-1,2-dithiacyclopentane, as
identified by Crump (Crump,
1980a) in stoats. The loss of m/z 115,
m/z 83 and m/z 69 implied HS,
HS2 and CH3S2, which implied a
dithiacyclopentane ring. In addition, the loss of m/z 106
implied a propyl. These data suggested that the two peaks were 4- or
3-propyl-1,2-dithiacyclopentane (Crump,
1980a) (Table 1 and
Fig. 2).
The MS data for peak 17 were identical with o-aminoacetophenone,
which was found only in the stoat (Crump,
1980a; Brinck et al.,
1983) (Table 1 and
Fig. 2).
Intraspecific differences
Sex differences
In the steppe polecat, seven compounds showed quantitative differences
between the two sexes. Compounds 1, 9 and 17 were all higher in females,
whereas compounds 2, 3, 12 and 13 were all higher in males. However, no
sex-specific compounds were observed (Table
2). In the Siberian weasel, compound 4 was detected in 7 out of 11
females, but not in any males. Also, the relative abundances of compounds 9,
10, 15 and 16 were significantly higher in females than in males. Furthermore,
peak 17 was more abundant in males than in females
(Table 2).
Individual differences
First, the presence or absence of some compounds in different combinations
may qualitatively characterize different individuals. In the steppe polecat,
some males did not have compounds 6, 7, 13, 14, 15, 16 or 17 and some females
did not have compounds 6, 7, 8, 14 or 15
(Table 3). In the Siberian
weasel, some males lacked compounds 3, 4, 5, 6, 7, 12, 15, 16 or 17 and some
females lacked compounds 3, 4, 5, 6, 7, 8, 12, 15, 16, 17 or 18
(Table 3).
Secondly, most compounds had extremely high RSDs. Generally, RSDs between duplicate GC—MC experiments are <10. With the exception of RSDs of compounds 2, 3 and 15, which in male steppe polecats were 16.91, 18.42 and 16.27, respectively, the RSDs of the remaining compounds ranged from 33.45 to 207.89 (Table 2, n = 10 or 11). This implied that some volatiles of anal gland secretions in both Mustela species may be quantitatively different among different individuals (Table 3).
Interspecific differences
In males, four compounds (7, 11, 13 and 14) were present only in the polecat and were absent in the weasel. For the remaining 11 compounds found in both species, nine differed significantly in quantity. Compounds 1, 9 and 17 were significantly lower and compounds 2, 3, 4, 5, 10, 12, 15 and 16 higher in male polecats than in male weasels. Compounds 6 and 8 showed no significant differences between males of the two species (Table 2)
In females, three compounds (peaks 11, 13 and 14) were present only in the polecat and were absent in the weasel. However, only compound 9 was lower in female polecats than in female weasels and other compounds common to the two species (1, 2, 3, 4, 5, 6, 7, 8, 10, 12, 15, 16 and 17) showed no significant differences in quantity (Table 2).
Between male polecats and female weasels, compounds 11, 13 and 14 were unique to the polecat. Compounds 1, 9 and 17, though present in both, were less abundant and compounds 2 and 3 were more abundant in the polecat than in the weasel (Table 2).
Between female polecats and male weasels, compounds 7, 11, 13 and 14 were not found in male weasels. Female steppe polecats had a higher quantity in peaks 3, 4, 5, 10 and 16, and a lower quantity in peaks 1 and 17 (Table 2).
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Discussion |
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Besides the previously identified nine volatiles in the two Mustela species, which were 2,2-dimethylthietane (1), Z-or E-2,4-dimethylthietane (2), E-2,3-dimethylthietane (3), 2-ethylthietane (4), E-2-ethyl-3-methylthietane (5), Z-2-ethyl-3-methylthietane (7), 2-propylthietane (8), 3,3-dimethyl-1, 2-dithiacyclopentane (9) and Z-3,4-dimethyl-2,2-dithiacyclopentane (12) (Zhang et al., 2002b
), eight new compounds were detected: 2-isopropylthietane
(6), 3-ethyl-1,2-dithiacyclopentane (10),
E-3,4-dimethyl-1,2-dithiacyclopentane (11), 2-pentylthietane (13), 3-
(14) or 4-propyl-1,2-dithiacyclopentane (15), indole (16) and
o-aminoacetophenone (17). These compounds have been previously
identified in other Mustela species, but not in the steppe polecat
and the Siberian weasel, with the exception of 4-propyl-1,2-dithiacyclopentane
(Crump, 1980b;
Sokolov et al., 1980;
Brinck et al., 1983;
Crump and Moors, 1985;
Zhang et al., 2002b).
It appears that most of the newly detected compounds in this study are
relatively low in concentration or volatility. For example, the two
nitrogen-containing compounds, indole (16) and o-aminoacetophenone
(17), both have a high mol. wt despite their high abundance. Also, the
concentrations in male Siberian weasels of 2-isopropylthietane (6) and
2-ethylthietane (4) are low, despite their higher volatility. This indicates
that the failure to detect these compounds could be ascribed to the
insensitivity of headspace sampling with solvent-desorption.
In a chemical information coding study, Sun and Müller-Schwarze (Sun
and Müller-Schwarze,
1998a,
1999) first proposed the idea
of digital and analog coding to distinguish the two forms of information
coding: presence/absence of chemicals versus varying amounts of shared
chemicals. This distinction has greatly clarified and simplified our
discussion on information coding in mammals. The presence in steppe polecats
and absence in Siberian weasels of peaks 11, 13 and 14 could be used as cues
for species discrimination. These differences might be sufficient for
discrimination between the two species and, thus, the coding for species
information could be most likely digital. Besides digital coding, analog
coding by varying the amounts of some shared compounds might also be used for
interspecific communication in some Mustela species
(Brinck et al., 1983),
but we did not find the common differences in quantity amongst opposite-
and/or same-sexes of the two Mustela species. Only the compounds with
stable and common differences might code for the difference between
species.
Volatiles from the anal gland among species of Mustela are similar
and most of the compounds, especially the sulfur-containing compounds, are
genus-specific. These compounds have not been found in other genera of family
Mustelidae and other families in the order Carnivora
(Brinck et al., 1983;
Albone, 1984;
Raymer, 1984;
Brown and Macdonald, 1985;
Buesching et al.,
2002a,b).
There is a substantial amount of evidence for the positive correlation between
relatedness and similarity in the chemical composition in the anal gland
secretions between conspecific individuals in beavers (Castor
canadensis) (Sun and Müller-Schwarze,
1998a,1998b),
lions (Panthera leo) (Anderson and Vulpius, 1999) and badgers
(Meles meles) (Buesching et
al., 2002a). One would expect that this relationship might
also occur above the species level. That is, the closer the two species are
related phylogenetically, the more similar the composition of the anal gland
secretion might be. This, however, turns out not to be the case in
Mustela and other related genera. For example, ferrets (M.
purorius forma furo) are closely related to and can interbreed
with the European and steppe polecats, but we cannot determine their
phylogentic relationship with stoats and weasels by comparing the volatiles in
the anal gland secretion (Brinck et
al., 1983; Crump and
Moors, 1985). The steppe polecat shares 14 volatile compounds with
the Siberian weasel and 11 with the stoat, but only eight with ferrets and
three or four with the European polecat
(Brinck et al., 1983;
Schildknecht and Birkner,
1983; Crump and Moors,
1985). Two other factors will have to be considered before we can
determine whether there is a correlation between phylogenetic relationship and
similarity in the anal gland secretion in mustelids. One is the effect of
microbial community (Zhang et
al., 2002b) and the other is the role of high mol.-wt
compounds and odor-binding proteins.
Our results also demonstrate that the anal gland secretion contains a
wealth of information characteristic of sexes and individuals in the two
Mustela species. In the Siberian weasel, both the presence or absence
of sex-specific compounds (Z-2-ethyl-3-methylthietane only in
females) and relative abundance of some compounds between males and females
could be used to code for information about sex. Thus, the coding for
information about sex could be either digital or analog or both. In steppe
polecats, however, only quantitative differences provide the possibility of
analog coding for inter-sexual communication. Some studies have also shown
that other carnivores use either or both of the two forms to code for sex
information. For example, in red foxes (Vulpes vulpes), quinaldine is
male-specific in the urine (Jorgenson
et al., 1978). In stoats, inter-sexual communication
might be based on the qualitative differences (digital) in 2-ethylthietane and
3-ethyl-1,2-dithiacyclopentane and quantitative differences (analog) in
3-propyl-1,2-dithiacyclopentane (Crump,
1980a). Female ferrets have high concentrations of
2,3-dimethylthietane and/or 3,4-dimethyl-1,2-dithiacyclopentane, while males
have high concentrations of indole
(Clapperton et al.,
1988). In lions, there are no sex-specific compounds, but
2-butanone is higher and acetone is lower in the urine of males versus females
(Andersen and Vulpius,
1999).
Coding for individual information may take either or both of these two
forms: presence or absence of some compounds (digital) and/or difference in
the relative abundance of some compounds (analog) among individuals. The two
Mustela species in this study might take both forms, analog and
digital coding, to code for individual information. In ferrets, Clapperton
et al. (Clapperton et al.
1988) identified an inter-individual variation in the combination
of five compounds of anal gland secretions (analog) and also noted consistent
qualitative differences (digital) in the color of anal gland secretions of
different individuals, but without supporting GC—MS data. In lions, no
two individuals had an identical compound composition in urine; therefore, it
is possible that the compound composition of a scent mark alone could provide
information about individuality (Andersen
and Vulpius, 1999), corresponding to the digital coding. In female
marmoset monkeys (Callithrix jacchus), there are few qualitative
differences in the chemical composition of circumgenital scent marks among
individuals. Instead, quantitative differences might be the key for
distinguishing individuals (Smith et
al., 2001) and such coding for individuality would be
digital.
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Acknowledgments |
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We express our gratitude to Mengxia Xie and Fang Xie of Beijing Normal University for their help in GC—MS analysis. Dr Helena Soini provided critical comments for the improvement of our paper. Dr Tony Tegeler read an earlier version of the manuscript. The work was supported by grants from the Chinese NSF (39970110, 39730090 and 39825105), the Chinese Academy of Sciences (KSCX2-1-03, STZ-01-06, KSCX2-SW-103 and KSCX2-SW-105) and the Ministry of Science and Technology (FS2000-009).
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References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Albone, E.S. (1984) Mammalian Semiochemistry: The Investigation of Chemical Signals Between Mammals. John Wiley, Chichester.
Andersen, K.F. and Vulpius, T. (1999)
Urinary Volatile Constituents of the Lion, Panthera leo. Chem.
Senses, 24,179
–189.
Brinck, C., Gerell, R. and Odham, G. (1978) Anal pouch secretion in mink, Mustela vison.Oikos , 38,68 –75.[CrossRef]
Brinck, C., Erlinge, S. and Sandell, M. (1983) Anal sac secretion in mustelids: a comparison.J. Chem. Ecol. , 9,727 –745.[CrossRef][Web of Science]
Brown, R.E., and Macdonald, D.W. (1985)Social Odours in Mammals . Oxford University Press, Oxford.
Buesching, C.D., Waterhouse, J.S. and Macdonald, D.W. (2002a) Gas-chromatographic analyses of the subcaudal gland secretion of the European badger (Meles meles) Part I: chemical differences related to individual parameters. J. Chem. Ecol., 28,41 –56.[CrossRef][Web of Science][Medline]
Buesching, C.D., Waterhouse, J.S. and Macdonald, D.W. (2002b) Gas-chromatographic analyses of the subcaudal gland secretion of the European badger (Meles meles) Part II: time-related variation in the individual-specific composition. J. Chem. Ecol., 28,57 –69.[CrossRef][Web of Science][Medline]
Clapperton, B.K., Minot, E.O. and Crump, D.R. (1988) An olfactory recognition system in the ferret Mustela furo L. (Carnivora: Mustelidae). Anim. Behav.,36 , 541–553.[CrossRef]
Crump, D.R. (1980a) Thietanes and dithiolanes from the anal gland of the stoat (Mustela erminea).J. Chem. Ecol. , 6,341 –347.[CrossRef][Web of Science]
Crump, D.R. (1980b) Anal gland secretion of the ferret (Mustela putorius furo). J. Chem. Ecol. 6,837 –844.[CrossRef]
Crump, D.R. and Moors, P.J. (1985) Anal gland secretions of the stoat (Mustela erminea) and the ferret (Mustela putorius furo): some additional thietane components. J. Chem. Ecol., 8,1037 –1043[CrossRef]
Erlinge, S., Sandwell, M. and Brinck, C. (1982) Scent marking and its territorial significance in stoat, Mustela erminea. Anim. Behav.,30 , 811–818.[CrossRef]
Gao, Y. (1987) Fauna Sinica: Mammalia. Vol. 8. Carnivora. Science Press, Beijing [in Chinese].
Gorman, M.L., Jenkins, D. and Harper, R.J. (1978) The anal scent sacs of the otter (Lutra lutra). J. Zool., 186,463 –474.
Jorgenson, J.W., Novotny, M., Carmack, M., Copland, G.B.,
Wilson, S.R., Whitten, W.K. and Katona, S. (1978)
Chemical scent constituents in the urine of the red fox (Vulpes
vulpes L.) during the winter season. Science,199
,:796
–798.
Raymer, J.H. (1984) Investigations into the chemical nature of chemo-olfactory communication in the wolf (Canis lupus). PhD thesis, Indiana University, Bloomington, IN.
Schildknecht, H. and Birkner, C. (1983) Analyse der analbeutelsekrete mitteleuropäischer Musteliden.Chemische Ztitung , 108,1 –5.
Sheng, H. and Lu., H. (1976) Identification of adult-juvenile weasels (Mustela sibirica) and its productive significance during the hunting season. Acta Zoologica Sinica, 22,329 –335 [in Chinese].
Smith, T.E., Tomlinson, A.J., Mlotkiewicz, J.A. and
Abbott, D.H. (2001) Female marmoset monkeys
(Callithrix jacchus) can be identified from the chemical composition
of their scent marks. Chem. Senses,26
, 449–458.
Sokolov, V.E., Albone, E.S., Flood, P.F., Heap, P.E, Kagan, M.Z., Vasilieva, V.S., Roznov, V.V. and Zinkevich, E.P. (1980) Secretion and secretory tissues of the anal sac of the mink, Mustela vison: chemical and histological studies.J. Chem. Ecol. , 6,805 –825.[CrossRef]
Sun, L. and Müller-Schwarze, D. (1998a) Anal gland secretion codes for family membership in the beavers. Behav. Ecol. Sociol.,44 , 199–208.[CrossRef][Web of Science]
Sun, L. and Müller-Schwarze, D. (1998b) Anal gland secretion codes for relatedness in the beaver, Castor canadensis. Ethology,104 ,917 –927.[Web of Science]
Sun, L. and Müller-Schwarze, D. (1999) Chemical signals in the beaver. In Johnson, R.E., Müller-Schwarze, D. and Sorensen, P. (eds), Advances in Chemical Signals in Vertebrates. Kluwer Academic/Plenum, New York, pp.281 –288.
Zhang, J., Zhang, Z., Wang, R., Chen, Y. and Wang, Z. (2002a) A headspace sampling method and its application in analysis of volatiles of anal glands of the American mink (Mustela vison). Acta Zool Sinica, 48,137 –141 [in Chinese].
Zhang, J., Sun, L., Zhang, Z., Wang, Z., Chen, Y. and Wang, R. (2002b) Volatile compounds in the anal gland of Siberian weasels (Mustela sibirica) and steppe polecats (M. eversmanni). J. Chem. Ecol.,28 ,1287 –1297.[CrossRef][Web of Science][Medline]
Accepted April 14, 2003
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