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First published online July 20, 2007
Journal of Experimental Biology 210, 2700-2705 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.002121
Females do it better. Individual recognition experiments reveal sexual dimorphism in Lemur catta (Linnaeus 1758) olfactory motivation and territorial defence
1 Centro Interdipartimentale Museo di Storia Naturale e del Territorio,
Università di Pisa, Via Roma 79, 56011, Calci, Pisa, Italy
2 Istituto Comprensivo Materna Elementare Media Convenevole da Prato via
1° Maggio 40, 59100, Prato, Italy
* Author for correspondence (e-mail: betta.palagi{at}museo.unipi.it)
Accepted 1 May 2007
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Summary |
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Key words: female genital secretions, gas chromatography, scent tests, individual recognition, sexual dimorphism, Lemur catta
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Introduction |
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;
Wrangham, 1980). Consequently,
costs and benefits of territorial defence should vary as a function of the sex
of resident and foreign individuals, which meet inside a territory
(Boydston et al., 2001).
Generally, mammals defend their own territories most vigorously against
same-sex intruders (King,
1954; Rood, 1983;
Heinsohn and Packer, 1985). By contrast, it is difficult to predict the
outcome of the encounters between conspecifics of the opposite sex. In that
case, additional factors, such as reproductive opportunities, may interact
with territoriality and force animals to evaluate costs and benefits of a
potential response (Cant et al.,
2002). The relative amount of costs and benefits may be determined
by the social and biological characteristics of the species (social and kin
structure, male or female dominance, male or female philopatry, seasonal
reproduction, group size) and by the particular social context during which
the encounter takes place (number of animals engaging in the conflict, their
ages and social status) (Krebs and Davies,
1991).
During the inter-group encounters, animals have to categorize conspecifics
as males or females, group-mates or aliens on the basis of several cues before
modulating the possible response. This information may also be present when
functional cues (even those decoupled from the sender, as in the case of some
chemical cues) are perceived by the resident animal
(Bradbury and Veherencamp,
1998; Hebets and Papaj,
2005). Consequently, the response given in the absence of the cue
bearer often matches the response given when the bearer is present
(Palagi and Dapporto, 2006;
Scordato and Drea, 2007). For
this reason, when a cue carries messages involved both in reproductive
strategies and in inter-group competition (i.e. genital secretions of alien
females), the reaction of the receiver to such a cue should also predict the
outcome of the encounters between conspecifics of different sexes and groups.
To clarify this issue, we selected Lemur catta as a model species
since its social life history and communication systems are well known.
Ring-tailed lemur communication is strongly scent oriented, with chemical
signals playing a pivotal role both in reproductive strategies and in
territorial competition (Kappeler,
1998; Gould and Overdorff,
2002; Palagi et al.,
2005).
In a recent paper, we demonstrated that both male and female ring-tailed
lemurs are able to recognize male conspecifics on the basis of their highly
specialized brachial secretions (Palagi
and Dapporto, 2006). In that paper, we verified the occurrence of
the three components of recognition systems: (1) the expression component (the
presence of diversification of some cues), (2) the perception component (the
perception and discrimination of such cues) and (3) the action component (the
functional response to the perception of such cues). This last component is
crucial to demonstrate that recognition goes beyond odour discrimination and
that animals are able to form a mental image of the sender by perceiving its
scent (Johnston and Bullock,
2001; Thom and Hurst,
2004; Palagi and Dapporto,
2006). We demonstrated the occurrence of the action component on
Lemur catta male secretions by designing an experiment based on the
hypothesis that male scent should be involved in territorial competition.
Ring-tailed lemurs of both sexes usually prefer to smell unfamiliar odours
compared with familiar ones, but when a well-known odour belonging to a
competitor is proposed this is preferred
(Palagi and Dapporto,
2006).
Individual recognition of female scent marks has not yet been demonstrated.
Lemur catta females exclusively use genital secretions to mark the
environment (Jolly, 1966;
Sauther et al., 1999). Female
marking is widely used in inter-group (between competing groups) and
intra-group communication (communication of reproductive status and
maintenance of linear hierarchical relationships among females which always
dominate over males) (Mertl-Millhollen,
2006; Palagi et al.,
2003; Palagi et al.,
2004). Due to the short receptive period of females (a few hours
per year) (Van Horn, 1975;
Van Horn and Resko, 1977;
Van Horn and Eaton, 1979;
Sauther, 1991) and to qualify
seasonal variations in their genital markings, it is crucial for males to
focus their investigation of female odours during the reproductive period
(Hayes et al., 2004;
Hayes et al., 2006;
Palagi et al., 2004;
Scordato and Drea, 2007).
To search for individual recognition of female genital marking, we applied
the same approach described in Palagi and Dapporto
(Palagi and Dapporto, 2006).
The occurrence of individual recognition of female secretions is not obvious
due to theoretical complications and confounding empirical observations
regarding the three components: (1) the vaginal secretion, a non-specialized
scent, may vary as a function of physiological and environmental factors,
which may make the expression component unstable
(Thom and Hurst, 2004); (2)
habituation/dishabituation tests on female secretions have failed to
demonstrate the occurrence of the perception component
(Mertl-Millhollen, 2006) and
(3) unlike the response to alien males, which are competitors for both sexes,
alien females may be considered by resident males not as competitors but as
possible sexual partners. In this case, the action component may remain
undetected by experiments based on territorial defence. Therefore, the outcome
of individual recognition experiments on female odours may also open
interesting scenarios to evaluate the territorial defence investment within
and between sexes.
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Materials and methods |
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)].
In particular, the P1 and P2 groups utilized the same outside grassy enclosure
alternately for 4–6 h per day; the groups were always in olfactory and
visual contact. P3 and P1/P2 groups were always separated from each other and
were, consequently, unfamiliar.
Collection of genital secretions
We collected female genital secretions from seven females of P1, P2 and P3
groups from November 2003 to June 2006 during both reproductive and birth
seasons. The secretions were collected by placing sheets of filter paper
(50x50 cm2) on the branches usually marked by lemurs. Prior
to use, we washed the paper in organic solvents (methanol:pentane 1:1) to
remove any volatile compounds occurring naturally in the paper. As a female
marked the paper, we removed the area (
5x5 mm2) soaked
with genital secretions. In order to prevent chemical contamination, the
samples were wrapped in an aluminium sheet. Each sample was labelled with the
date and the name of the donor subject and was immediately frozen at
–20°C (Hayes et al.,
2002; Hayes et al.,
2004). We used some of these secretions for scent trials (see
below) and others for gas chromatography/flame ionization detection (GC/FID)
analyses.
Experiment 1 – GC/FID analyses
Pieces of filter paper soaked with genital secretions were extracted in 300
µl of extraction solvent (1:3 v/v methanol:dichloromethane) for 20 min. The
solution was then dried and re-suspended in 25 µl of solvent. We injected 2
µl of solution into a Varian 3900 gas chromatograph (Middelburg, The
Netherlands) fitted with a Flame Ionization Detector (FID) and a fused silica
capillary column coated with 5% diphenyl/95% dimethyl polysiloxane (Varian
FactorFour VF-5ms; 30 mx0.25 mmx0.5 µm). Injector temperature
was 280°C and detector temperature was 300°C. The carrier gas was
hydrogen (at 12 psi; 1 psi=6.9 kPa). The temperature protocol was as follows:
70–150°C at a rate of 30 deg. min–1 (held for 5
min), and then 150–310°C at a rate of 5 deg. min–1
(held for 11.3 min).
Scent tests
Two pieces of filter paper soaked with genital secretions were fixed to the
gates of the enclosure at a distance of 50 cm from each other using forceps.
One of the two authors numbered the two pieces of paper. The other author
performed a blind trial, presenting the filter paper to animals and
registering olfactory responses without knowing the meaning of the two
numbers. The observer waited until the animals spontaneously approached the
samples. The experimental trials were considered valid only if the animal
spent more than 10 s inspecting both samples and if both pieces of filter
paper were detected by the subject. Each trial lasted three minutes for each
animal; when two animals simultaneously approached the stimuli, the first
author timed the three-minute trial of the two different animals (no more than
two animals approached the stimuli simultaneously). Time spent investigating
was tape-recorded, starting when the animal was about 2 cm from the scent
stimuli and ending when the individual moved away. Since trials were performed
on the whole group, we frequently changed the relative position (left/right)
of the two samples during the trials so that previous experience and copying
behaviours did not bias the scent tests. Moreover, if a subject countermarked
one of the two samples, we changed both samples at the end of the trial
performed by that subject. During each trial, the names of individuals
interacting and time spent sniffing and/or licking the samples were recorded.
Since the animals showed a high variability in their motivation to
investigate, we obtained different sample sizes for the different experiments
performed. We performed one trial per animal.
Experiment 2 – scent discrimination
In the first experiment we compared the olfactory response elicited by the
genital secretion and clean paper to verify whether animals actually perceived
the scents (Experiment 2a).
To verify the occurrence of the perception component we performed
habituation/discrimination tests as suggested by Johnston and Jernigan
(Johnston and Jernigan, 1994)
and Thom and Hurst (Thom and Hurst,
2004) (Experiment 2b). During four habituation trials, subjects
were presented with two pieces of filter paper, both containing the secretions
from an individual (individual A). The habituation response is usually
observed in the form of a decrease in the inspection time. In the final trial,
we presented two different odours, one belonging to the same individual (A)
and one belonging to another individual (B). If the subject perceives the
difference between the new scent (B) and the habituated scent (A),
investigation of the former is expected to be higher when compared with the
latter (Thom and Hurst, 2004).
The habituation trials were followed by 1 min-intervals.
Experiment 3 – individual recognition by scent
To verify the occurrence of the functional component we performed a
bioassay based on two experiments on the two groups competing for the same
outside enclosure (P1 and P2). In the first experiment we presented the
familiar odour of the female belonging to the competing group and the
unfamiliar female from the P3 group (Experiment 3a). In the second experiment,
we presented the familiar scent belonging to a group-mate and another one
belonging to the unfamiliar subject from the P3 group (Experiment 3b). The
scent tests were performed in the outdoor enclosure, which represents the
overlapping area for P1 and P2 groups.
Statistical analysis
The peak areas of the FID gas chromatograms of each sample were processed
and analyzed using Varian Star GC Workstation 6.0. Each peak was identified on
the basis of the relative retention time in the 35 analyses; peak areas were
transformed into percentages for each sample. All peaks with a percentage area
less than 0.01% of the total compound content (considering all the samples)
were excluded from the analyses because of unreliable quantification at such
low relative amounts, as suggested by Smith et al.
(Smith et al., 2001).
We performed Discriminant Analysis (DA) on 28 samples collected from five donors in different years (from 2003 to 2006) and periods (mating and birth seasons) to determine whether the samples from each animal could be distinguished according to their chemical composition. We performed Principal Component Analysis (PCA) to reduce the number of variables into a smaller number of uncorrelated principal components. We extracted 13 factors with eigenvalues greater than 1, which together explained 100% of the total variance. As no peak showed communalities of <0.8, we did not remove any peak from the PCA. The 13 principal components were used as independent variables for the DA. Wilks' lambda and the number of cases assigned to their original group were used as indexes of correct DA.
We used the Wilcoxon matched-pairs signed-rank test to evaluate differences
in time spent investigating during scent tests (blank paper vs
genital secretion), habituation/discrimination tests (habituated vs
non-habituated scent) and functional tests (familiar vs unfamiliar
scent). We used exact tests as suggested by Mundry and Fischer
(Mundry and Fischer,
1998).
We used randomization tests when males and females were tested separately. All analyses were two-tailed, and the level of significance was set at 5%.
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Results |
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DA performed on the 28 samples using the 13 PCs obtained by PCA extracted four functions explaining 100% of variance and correctly assigned 100% of cases to their own group (Fig. 1). In particular, on the basis of function 1 (explained variance 50.1%, Wilks' lambda=0.003, P<0.001) and function 2 only (explained variance 38.1%, Wilks' lambda=0.030, P=0.003) we obtained a good separation of the samples belonging to the five females (Fig. 1).
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Individual recognition by scent (Experiment 3)
As a whole, P1 and P2 lemurs showed no preference towards unfamiliar
genital markings compared with group-mate ones (Exact Wilcoxon signed-ranks
test, T=29, ties=0, N=12, P=0.458). Moreover,
subjects from both groups did not prefer to investigate the familiar odour
belonging to the competing female (P1 female for P2 group; P2 female for P1
group; Exact Wilcoxon signed-ranks test, T=15.5, ties=0,
N=12, P=0.068). However, when males and females were tested
separately in Experiment 3a, the analysis revealed that all the females
preferred unfamiliar odours to familiar ones (randomization paired test,
t=4.32, N=5, P<0.001;
Fig. 2A) while males did not
show any preference (randomization paired test, t=–0.42,
N=7, P=0.702; Fig.
2B). Conversely, in Experiment 3b, all the females preferentially
investigated the familiar-competitor odours compared with the unfamiliar ones
(randomization paired test, t=–3.47, N=6,
P<0.001; Fig. 2C)
and males showed no preference again (randomization paired test,
t=1.372, N=6, P=0.244).
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Discussion |
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Olfactory behaviour plays a fundamental role in territorial defence
(Gould and Overdorff, 2002);
owners extensively mark their territories (mainly at boundaries) and spend a
lot of time seeking and investigating conspecific depositions [e.g.
Eulemur mongoz (Curtis and
Zaramody, 1999), L. catta
(Jolly, 1966;
Mertl-Millhollen, 1986;
Mertl-Millhollen, 2006;
Kappeler, 1998),
Propithecus spp. (Lewis,
2005; Pochron et al.,
2005a; Pochron et al.,
2005b)]. Generally, an odour belonging to a novel unfamiliar
individual (a potential competitor) elicits more intense olfactory responses
compared with a scent belonging to a group mate
(Ramsay and Giller, 1996;
Palagi et al., 2005). The
clear response of L. catta females during Experiment 3 can be
explained by their strong intrasexual competition over resources and by their
strong activity in territorial defence, as might be expected in a
female-dominant species. Scordato and Drea also found that the strongest
response during olfactory trials was that of females towards genital odour
from female `intruders' (Scordato and
Drea, 2007). Both in wild and semi-free-ranging ring-tailed
lemurs, during intertroop agonistic interactions, females of opposing groups
often run toward each other and genital mark concurrently
(Nakamichi and Koyama, 1997;
Nunn and Deaner, 2004;
Mertl-Millhollen, 2006).
Moreover, Mertl-Millhollen
(Mertl-Millhollen, 2006)
observed that when females travelled out of their defended range, they
significantly increased their rate of sniffing behaviour. In this view, the
capability to recognize the individual ownership, other than to simply
perceive the spatial and temporal pattern of scent depositions, may provide
considerable advantages both to the sender and the receiver, especially when
animals can remember and use information from previous encounters to moderate
future responses (Gosling,
1982; Bradbury and Vehrencamp,
1998; Hurst and Beynon,
2004). In particular, Gosling proposed the Scent Matching
Hypothesis, which predicts that territory marking provides an olfactory
association between the resident and the defended area that allows intruders
to identify the resident when they meet and thus reduce the frequency of
escalating agonistic encounters (Gosling,
1982).
Demonstrating the action component (the last component of recognition systems) requires (1) a hypothesis about the function of the signal and (2) a functional experiment designed on the basis of such a hypothesis (Fig. 3). The occurrence of the action component not only demonstrates definitively the occurrence of the recognition but also confirms the hypothesis about the function of the signal as well. Conversely, the failure of the experiment does not necessarily imply the lack of the recognition skill, since it may be due to a wrong functional hypothesis (Fig. 3).
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During our trials, males were more active than females in olfactory
investigation, spending more time in sniffing and licking the scent
depositions than did females (Fig.
2). As these sex differences are generally consistent with
previous observations of olfactory investigation and scent marking in the wild
(Gould and Overdorff, 2002) and
in semi-free-ranging ring-tailed lemurs
(Kappeler, 1998) it is
unlikely that our testing environment significantly altered the natural
response pattern. The absence of a territorial functional response by
ring-tailed males to female secretions in Experiment 3 may be explained by
male-peculiar life histories and reproductive events such as mating and male
dispersal. Unlike females, the response of male ring-tailed lemurs is
consistent with patterns of olfactory signalling in other mammals
(Thiessen and Rice, 1976;
Johnston, 2003); males are
mainly attentive to the physiological state of potential female mates
independently from their familiarity [this evidence is supported also by
Heymann (Heymann, 1998) and
Scordato and Drea (Scordato and Drea,
2007)], probably because alien females are considered not as
competitors but as possible sexual partners. This hypothesis matches the
observation in the field, where it has been demonstrated that fights between
males and females are rare (4% of the aggressions between groups)
(Nakamichi and Koyama, 1997).
Moreover, in the wild, male transfer is well documented and females were
observed to mate not only with group males or transfer males but also with
`temporary visitors' from adjacent groups
(Jolly, 1966;
Sauther, 1991;
Sussman, 1992). Similarly,
Gould (Gould, 1997) documented
male migration between November and January, and these foreign males were
later able to mate with females, even though they were usually the last to do
so (Sussman, 1992). Therefore,
in the wild, genital marking by females may also serve to advertise to
extra-troop males, thus increasing mate choice opportunities. Since it has
been demonstrated that female secretions contain information on their
reproductive status (Hayes et al.,
2004; Scordato and Drea,
2007), migrating males could use such female scent-marking to
gauge into which groups to attempt to immigrate. However, this follow-up on
female odours is useless in a multi-female group when a male is not able to
recognize the owner of the scent deposition. From this perspective, it is hard
to think that, within a species, females are able to individually recognize
both males and females, but males are able to individually recognize only
males. In a more parsimonious hypothesis we suggest that males did not show
the action component toward female genital odours as the territorial defence
functional hypothesis is not suitable for resident males toward alien females,
which are considered as potential partners more than territorial
competitors.
In conclusion, in designing a functional bioassay, a scientist should carefully consider the social and biological characteristics of the species under study in order to avoid type II errors. In L. catta, both sexes are probably able to identify females by their unique odour signatures. The absence of preference showed by males towards unfamiliar and familiar-competitor females (Experiment 3) may be due to the sexual dimorphism in territorial defence and/or a high motivation for males in investigating both group-mate and alien females. Both factors could have made the functional bioassay ineffective. Further observational and experimental studies are required to elucidate the role of odour cues in intra- and extra-group dynamics.
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Acknowledgments |
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