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Does nonnutritive tree gouging in a rainforest-dwelling lemur convey resource ownership as does loud calling in a dry forest-dwelling lemur.

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American Journal of Primatology 72:1062–1072 (2010)
RESEARCH ARTICLE
Does Nonnutritive Tree Gouging in a Rainforest-Dwelling Lemur Convey
Resource Ownership as Does Loud Calling in a Dry Forest-Dwelling Lemur?
SOLOFONIRINA RASOLOHARIJAONA1, BLANCHARD RANDRIANAMBININA1, AND MARINE JOLY-RADKO2
1
Faculty of Sciences, University of Mahajanga, Mahajanga, Madagascar
2
Institute of Zoology, University of Veterinary Medicine Hannover, Hannover, Germany
Nonhuman primates may defend crucial resources using acoustic or chemical signals. When essential
resources are limited, ownership display for a resource may be enhanced. Defending resources may
depend on population density and habitat characteristics. Using the Milne Edwards’ sportive lemurs
(Lepilemur edwardsi) and weasel sportive lemurs (L. mustelinus) as models, we tested whether two
cryptic nocturnal lemur species differing in population density and habitat show differences in their
vocal and chemical communication for signaling ownership of resources. L. edwardsi inhabits a western
dry deciduous forest in a high-density population, whereas L. mustelinus is found in an eastern
rainforest in low density. We followed ten L. edwardsi (six males and four females) and nine
L. mustelinus (four males and five females) for 215 hr during the early evening (06:00–10:00 p.m.) and
the early morning (02:00–05:00 a.m.) and recorded their behavior using focal animal sampling. We found
that both species differed in their vocal and chemical communication. L. edwardsi was highly vocal and
displayed loud calling in the mornings and evenings while feeding or in the vicinity of resting places. In
contrast, L. mustelinus never vocalized during observations, but displayed tree-gouging behavior that
was never observed in L. edwardsi. Tree gouging occurred more often during early evening sessions than
early morning sessions. Subjects gouged trees after leaving their sleeping hole and before moving
around. We suggest that, in weasel sportive lemurs, non-nutritive tree gouging is used as a scentmarking behavior in order to display ownership of sleeping sites. Altogether, our findings provide first
empirical evidence on the evolution of different communication systems in two cryptic nocturnal primate
species contrasting in habitat quality and population density. Further investigations are needed
to provide more insight into the underlying mechanisms. Am. J. Primatol. 72:1062–1072, 2010.
r 2010
Wiley-Liss, Inc.
Key words: nonnutritive tree gouging; resource defense; scent marking; vocal communication;
nocturnal lemur
INTRODUCTION
In nonhuman primates, rich repertoires of
signals may be used for communication [see Hauser,
1996]. Vocalizations, as acoustic signals, and scent
marking, as chemical signals, were described in
contexts, such as intergroup communication [e.g.
Braune et al., 2005; Irwin et al., 2004; Lazaro-Perea
et al., 1999; Méndez-Cárdenas & Zimmermann,
2009; Rasoloharijaona et al., 2006], social and
reproductive advertisement [e.g. Di Fiore et al.,
2006; Heymann, 2006; Miller et al., 2003], territorial
defense and resource usage [e.g. Braune et al., 2005;
Lewis, 2006; Mertl-Millhollen, 2006; Palagi & Norscia,
2009; Pochron et al., 2005; Rasoloharijaona et al.,
2006]. Nonhuman primates may defend crucial
resources, such as feeding areas or safe sleeping
sites, by loud calling or scent marking. Territorial
r 2010 Wiley-Liss, Inc.
defense or display of a resource ownership is costly
and should be linked to the defendability of limited
resources [Mitani & Rodman, 1979]. If crucial
resources are limited, ownership display for a resource
may evolve [Horiuchi, 2008]. Defending resources
may thus be shaped by population density and
habitat quality: Animals living in a poor habitat in
a high population density should demonstrate more
ownership display behavior when resources are
Correspondence to: Marine Joly-Radko, Institute of Zoology,
University of Veterinary Medicine Hannover, Buenteweg 17, D-30559
Hannover, Germany. E-mail: marine.joly@tiho-hannover.de
Received 13 January 2010; revised 16 June 2010; revision
accepted 17 June 2010
DOI 10.1002/ajp.20865
Published online 7 July 2010 in Wiley Online Library (wiley
onlinelibrary.com).
Tree Gouging in Sportive Lemurs / 1063
limited than animals living in a rich habitat in a low
population density. Sound and scent may both be
used for long-distance communication in mammals
[Brown & Macdonald, 1985]. However, Although
scent may provide long-term cues, sound provides
short-term cues. The use of acoustic or chemical cues
may depend on the need to defend resources and on
the presence of potential receivers of the signal.
Short-term reaction, i.e. use of acoustic cues for
signaling ownership, should prevail when the availability of resources is limited and when the presence
of potential competitors in the vicinity increases. On
the other hand, the use of chemical cues may be
useful to leave long-lasting messages for competitors,
which may access limited resources at a later time.
Nocturnal prosimians are an interesting model
to investigate the plasticity in vocal and chemical
communication. Although an enhanced visual system and reduced olfactory system are generally
considered to be a specific trait in primate evolution,
most of the nocturnal prosimians possess a still
functional accessory olfaction system in addition to
the main olfactory system [see Barton, 2006; Schilling,
1979]. This may reflect an enhanced chemical
sensitivity. Although the major role of the main
olfactory system is to detect volatile molecules, the
accessory olfaction system is mainly involved in
the reception of large nonvolatile molecules, e.g. the
sampling of fluids, such as urine or saliva [see Evans,
2006]. Besides acoustic communication, which has
been thoroughly investigated [see Braune et al., 2005;
Méndez-Cárdenas et al., 2008; Rasoloharijaona et al.,
2006], information on the function of olfactory communication in wild nocturnal prosimians remains sparse
[Braune et al., 2005]. Earlier field investigations on
golden brown mouse lemurs demonstrated that olfactory signals, such as urine washing at sleeping sites,
could represent an important mechanism to regulate
the distribution of different groups in space, whereas
acoustic signals control intragroup cohesion and coordination [Braune et al., 2005]. However, to date,
olfactory communication remains poorly investigated in
other families of nocturnal lemurs.
The sportive lemurs (Lepilemuridae) may represent an excellent model to gain more insight into the
plasticity of communication modalities of nocturnal
prosimians. Twenty-five different species are currently recognized [see Mittermeier et al., 2008].
Comparative data on their socioecology and communication are still rare, because only a few species
have been studied so far.
The Milne Edwards’ sportive lemur (Lepilemur
edwardsi) and the weasel sportive lemur (L. mustelinus) have a limited distribution in Madagascar.
Although L. edwardsi inhabits the western dry
deciduous forest, L. mustelinus is found in the eastern
rainforest [Mittermeier et al., 2006]. Both species are
mainly folivorous and show similar feeding habits, but
differ in morphology [Rasoloharijaona et al., 2003,
2008], genetics [Andriaholinirina et al., 2006; Craul
et al., 2007], and behavioral aspects [Rasoloharijaona,
2001].
The Milne Edwards’ sportive lemur (L. edwardsi)
lives in dispersed male–female pairs [Rasoloharijaona
et al., 2000, 2003, 2006; Thalmann, 2006; Thalmann
& Ganzhorn, 2003]. Individuals usually forage alone
at night, but establish long-term pairs and sleep
together during the day [Rasoloharijaona et al.,
2003]. Pair partners share a home range with
suitable sleeping and feeding sites, usually sleeping
together in the same sleeping site and using home
ranges exclusively [Rasoloharijaona et al., 2003,
2006]. Pairs are highly vocal. They possess an
elaborate vocal repertoire consisting of nine structurally different call types [Rasoloharijaona, 2001;
Rasoloharijaona et al., 2006]. Vocalizations are
shown to carry signatures for sex, individual and
pair identity [Méndez-Cárdenas & Zimmermann,
2009; Rasoloharijaona et al., 2006]. Pairs use duetting as a vocal display for signaling territory ownership, and thus limit direct aggressive encounters
between neighbors and strangers [Méndez-Cárdenas
& Zimmermann, 2009; Rasoloharijaona et al., 2006].
Milne Edwards’ sportive lemurs emit loud calls
mostly during feeding events and in the vicinity of
their sleeping sites [Rasoloharijaona et al., 2006].
The weasel sportive lemur (L. mustelinus) is a
rainforest-dwelling lemur and is distributed in eastern Madagascar [Mittermeier et al., 2008]. Compared
with the sportive lemurs of the northwestern and
southwestern part of Madagascar, they have not
been well studied in the wild. Weasel sportive lemurs
were observed to forage solitarily [Ganzhorn, 1988].
Sexes show a sexual dimorphism; although males
and females do not differ in their body length,
females are heavier than males [Rasoloharijaona
et al., 2008]. Both sex use dense vegetation and
tree holes for sleeping during the day. Each animal
has its own preferred sleeping sites and uses them
alone. Only four types of vocalizations were described in L. mustelinus [Rasoloharijaona, 2001].
However, those vocalizations occurred rarely and
were only recorded in one male of six focal
individuals [Rasoloharijaona, 2001]. Interestingly,
we earlier witnessed that L. mustelinus gouge trees
[Rasoloharijaona et al., 2008]. Tree gouging has
already been described in other strepsirrhines [Patel
& Girard-Buttoz, 2008; Petter et al., 1971; Tan &
Drake, 2000]. Tree gouging may be used in a
nutritive context; fork-marked lemurs and pygmy
slow lorises stimulate exudate flow by gouging
trees [Petter et al., 1971; Tan & Drake, 2000].
However, recently Patel and Girard-Buttoz [2008]
reported the use of tree gouging in a nonnutritive
context; wild male Milne-Edwards’ sifakas combine
tree gouging with scent marks for overmarking. The
function of this behavior in L. mustelinus is so far
not clear.
Am. J. Primatol.
1064 / Rasoloharijaona et al.
The sportive lemur’s density may vary according to
the Malagasy study areas. Although Rasoloharijaona
[2001] found that the density of L. mustelinus was 1–2
individuals/hectare in the eastern rainforest, the
population density of L. edwardsi in the northwestern
dry deciduous forest was about five individuals/hectare
[Rasoloharijaona et al., 2000]. The home-range size also
varied with about 2.3 ha for males [no data available for
females; Rasoloharijaona, 2001] in weasel sportive
lemurs in Andasibe and about 1 ha for Milne-Edwards’
sportive lemurs in the forest of Ampijoroa [0.9870.4 ha
females and 1.0170.25 ha for males; Rasoloharijaona
et al., 2006].
The aim of this study was to provide new insight
into the resource ownership display behavior, and
especially to assess the presence and significance of
specific vocal and tree-marking behaviors of two
cryptic sportive lemur species. We hypothesize that
specific vocal and marking behaviors are shaped by
socioecological factors, such as habitat quality and
population density. On the one hand, we expect
animals living in a poor habitat in a high-density
population to display more vocalizations than animals living in a rich habitat in a low-density
population. We, therefore, hypothesize that L. edwardsi
living in the dry deciduous forest will demonstrate
more frequent loud calls to defend crucial resources,
such as sleeping and feeding sites, than L. mustelinus,
which lives in the rainforest in a low-density
population. Moreover, we hypothesized that
L. mustelinus use tree gouging as an alternative
communication strategy to leave long-lasting cues in
the rainforest. We hypothesize that tree gouging is
used to signal resource ownership by L. mustelinus,
as L. edwardsi use loud calling and we will describe
its behavioral context.
METHODS
Study Sites and Climatic Conditions
The study was conducted both in eastern and
northwestern Madagascar using comparable methods. In the eastern Malagasy rainforest, we worked
at two different study sites close to Andasibe: The
Mantadia National Park (S18147.50 , E48126.60 , altitude: 900 m) and the Maromizà private reserve
(S181580 , E481280 , altitude: 1,020 m). The direct
distance between Mantadia and Maromizà is about
12 km and both sites belong to the district of
Andasibe. In the western Malagasy dry deciduous
forest, we worked in the Réserve Forestière d’Ampijoroa (S160 190 , E461490 ), located about 115 km
southeast of the town Mahajanga in northwest
Madagascar. The study was performed at two
geographically different study sites, the so-called
‘‘Jardin Botanique A’’ and the so-called ‘‘Jardin
Botanique B.’’
In the eastern rainforest, the climate conditions,
such as daily minimum and maximum temperatures
Am. J. Primatol.
and rainfall, were provided by the Service de la
Métérologie Nationale [Rasoloharijaona, 2001]. The
climate is seasonal with strong temperature fluctuations during the year; the maximum daily temperature was recorded in December (351C), the minimum
daily temperature in July (0.21C). Rainfall was
highest from December to April with a monthly
maximum rainfall of 380 mm, and lowest from May
to November with a monthly minimum rainfall of
20 mm. In the western dry deciduous forest in
Ampijoroa climate conditions, such as daily minimum and maximum temperatures and rainfall, were
measured by the staff of the Durrell Wildlife
Conservation Trust. The climate is highly seasonal
and characterized by a hot and humid rainy season
from November to April, with heavy rains in January
and February and a cool dry season from May to
October [Rasoloharijaona, 2001]. In 1998, the maximum daily temperature was recorded in November
(39.51C) and the minimum in June (10.51C). Rainfall
was highest from December to March with a monthly
maximum rainfall of 532 mm in February, and no
rainfall at all between June and September.
Animals and Their Identification
We studied weasel sportive lemurs (L. mustelinus) in eastern Madagascar from May to December
1999, from May to July 2005, and in November and
December 2005. In 1999, six adult animals (four
males and two females) were captured, measured,
and radiocollared with TW-3 button cell tags (Biotrack, Dorset, UK; see Table I). In May 2005, three
females were captured, measured, and radiocollared
(see Table I).
We studied sportive lemurs (L. edwardsi) in
northwestern Madagascar from May to December in
1998. Ten adult animals (six males and four females;
see Table I) were captured, measured, and radiocollared with TW-3 button cell tags (Biotrack; see
Table I). The same capture procedures were used at
both study areas [see Rasoloharijaona et al., 2003,
2006].
Research conducted in this study adhered to the
legal requirements of Madagascar and permission
was obtained from the appropriate agencies. Capture
procedures, animal handling, and radio-tracking
techniques followed standard protocols and were
authorized by the appropriate institutional or government bodies. The research complied with the American
Society of Primatologists Principles for the Ethical
Treatment of Non-Human Primates.
Data Collection and Analysis
Direct focal observations were carried out on
radio-collared individuals by one observer, using
focal animal sampling with continuous recording
[Altmann, 1974; Martin & Bateson, 1993] for two
sessions: 4 hr after the individuals left their sleeping
Tree Gouging in Sportive Lemurs / 1065
TABLE I. List of Focal Animals
Site
Lepilemur edwardsi
in Ampijoroa
Lepilemur mustelinus
in Andasibe
Sex
Animal
number
F
F
F
F
M
M
F-01-97
F-01-98
F-05-97
F-07-98
M-08-98
M-09-98
M
M
M
M
M-13-98
M-15-98
M-18-98
M-19-98
F
F
F
F
F
M
F-04-99
F-05-99
F-01-05
F-02-05
F-03-05
M-02-99
M
M
M
M-03-99
M-06-99
M-08-99
Total focal
time (hours)
Total contact
time (hours)
% contact
time
June, August
October
July, September
June
June
June, August, September,
November
October
July, November
September
September
14.06
6.54
12.09
6.48
6.35
33.20
10.15
4.43
9.38
5.85
5.73
25.94
72.19
67.67
77.61
90.34
90.25
78.13
7.63
12.40
6.39
12.17
5.49
8.3
4.99
11.07
71.96
66.98
78.08
90.97
August, October
June
July
June
June
August, September, October,
November
August, November
August, September
August, September
16.69
4.91
2.99
11.45
9.80
21.8
5.29
2.34
0.5
2.83
2.95
11.7
31.69
47.71
16.68
24.71
30.1
53.67
8.73
16.27
6.75
1.36
8.49
1.36
15.62
52.17
20.09
Months of observations
sites (from 06:00 to 10:00 p.m.), and for 3 hr before
they returned in the early morning (from 02:00 to
05:00 a.m.). The total focal time (i.e. total duration
an animal was followed and observed) and the total
contact time (i.e. total duration an animal was seen
during the observation) per individual and site are
shown in Table I. In the eastern rainforest, it was
more difficult to maintain a long-lasting visual
contact with the focal animals because the trees are
relatively tall and the ground is very uneven and
sloping.
Lemurs were observed by dimmed light using
white headlamps. Behavior and additional information related to spatial and ecological factors were
recorded on a dictaphone and subsequently transferred to data sheets. We continuously recorded the
behavior and differentiated among the following
categories: resting (REST), feeding (FEED), in the
sleeping hole (HOLE), scanning (SCAN 5 the animal
looked to the left and right side), moving (LOC), selfgrooming (SG), social activity (SOC 5 encounter with
one or more conspecifics within 5 m range of the focal
animal), vocalizing (VOC 5 loud calling), tree gouging (GOUG 5 the animal gouges the bark of a tree
using its tooth comb), and unknown behavior
(UNKN).
We determined the activity budget for each
individual by calculating the percentage of time an
animal spent in each behavioral category in relation
to the total contact time. We counted all vocalization
bouts and all tree-gouging bouts for each individual.
A bout was defined as a sequence of vocalizations or
tree gouging occurring successively. The bout was
stopped as soon as the animal displayed another
behavior without vocalization or tree gouging. We
then divided the total number of vocalization or treegouging bouts for an individual by the contact time
to express it as a rate per hour of contact time. The
behavioral rate was calculated for both the early
evening (from 06:00 to 12:00 p.m.) and the early
morning (from 02:00 to 05:00 a.m.) observation
sessions separately in order to compare the two
periods. Finally, we assessed the behavioral context
in which the vocalization and tree-gouging bouts
occurred by analyzing the behavioral sequence 5 min
before and 5 min after the occurrence of each bout.
We thus, analyzed what the animal was doing just
before and after vocalizing or tree gouging. For each
5 min interval range and each individual, we determined and compared the relative duration of each
behavior occurring 5 min before and after the
vocalization and tree-gouging bouts. Medians and
range were calculated for all variables. We analyzed
the data using the program Statistica 6.0 (Statsoft
Inc., Tulsa, OK) and SPSS 17.0 (SPSS Inc., Chicago,
IL) and applying nonparametric exact two-tailed
tests. The statistical significance was P 5 0.05 for
all tests. To control for multiple testing, the
sequential Bonferroni procedure was used [Holm,
1979]. For that purpose, P-values were ordered and
the smallest P-value was compared with 0.005
( 5 0.05/10 when the same question was asked
Am. J. Primatol.
1066 / Rasoloharijaona et al.
repeatedly for the ten behaviors). If the smallest
value was less than 0.005, we rejected the null
hypothesis. The procedure was repeated until the
smallest P-value could not be rejected. All hypotheses that had not been rejected in the earlier steps
were then accepted.
RESULTS
Activity Budget
Both species showed very similar patterns in
their activity budget (Fig. 1). Most of the time,
animals were seen resting, feeding, in the sleeping
hole, and scanning (representing more than 90%
of the activity budget for L. edwardsi and more
than 80% of the activity budget for L. mustelinus;
see Fig. 1). However, both species differed in their
feeding duration, loud calling, and tree gouging
(same results, Mann–Whitney U test, NL. edwardsi 5 10,
NL. mustelinus 5 9, U 5 5, Z 5 3.27, P 5 0.0001; see
Fig. 1). L. edwardsi in Ampijoroa spent more time
feeding than L. mustelinus in Andasibe (L. edwardsi:
median 5 33.81%; range 5 14.78–37.16%; L. mustelinus:
median 5 7.16%; range 5 3.75–29.93% of the contact
time). L. edwardsi also spent more time making loud
calls (Mann–Whitney U test, NL. edwardsi 5 10,
NL. mustelinus 5 9, U 5 5, Z 5 3.35, P 5 0.0001; see
Fig. 1), whereas L. mustelinus displayed a longer
tree-gouging activity (Mann–Whitney U test,
NL. edwardsi 5 10, NL. mustelinus 5 9, U 5 5, Z 5 3.64,
P 5 0.0001; see Fig. 1). There was no sex difference
in activities in both study areas (Mann–Whitney U
test, P40.05).
Loud Calls and Tree-Gouging Bouts
During our focal observations, 124 bouts of loud
calls were recorded. They were restricted exclusively
to L. edwardsi (Fig. 2A). Both males and females
emitted loud calls at a rate of 1.31 calls
(range 5 0.4–3.49) per hour. Fifty tree-gouging bouts
were recorded. They were exclusively observed in
L. mustelinus (Fig. 2B). Both male and female
L. mustelinus were seen gouging and there was no
sex difference in the gouging rate (Mann–Whitney U
Test, Nmales 5 4, Nfemales 5 5, U 5 5, P40.05). The
focal animals gouged on the trunks using their tooth
comb, making transverse lines about 2 cm in length,
Fig. 1. Behavioral activity budgets of L. edwardsi (in white) in the northwestern dry deciduous forest and L. mustelinus (in gray) in the
eastern rainforest. Line 5 median, box 5 25–75%, and whisker 5 nonoutlier range. Outliers and extremes are not represented.
Abbreviations of the behavioral categories: REST, resting; FEED, feeding; HOLE, in the sleeping hole; SCAN, scanning; LOC, moving;
SG, self-grooming; SOC, social activity; VOC, vocalizing; GOUG, tree gouging; UNKN, unknown behavior; see Material and Methods for
the definition of each behavior. Mann–Whitney test, Po0.0001.
Am. J. Primatol.
Tree Gouging in Sportive Lemurs / 1067
Fig. 2. (A) Rate of vocalizations made by both sexes in Lepilemur sp. (B) Rate of tree-gouging bouts made by both sexes in Lepilemur sp.
Fig. 3. (A) Tree-gouging marks in the neighborhood of a sleeping hole. (B) Close-up photograph of tree-gouging marks. Photos by
Randrianarison [2009]; white arrows indicate some of the visible tree-gouging marks.
two to six times in each sequence of gouging (see
Fig. 3A and B). We never observed the focal animals
eating the wood or licking the bark while gouging or
after gouging. Such a gouging behavior was never
observed in Ampijoroa.
Behavioral Context of Loud Calling
Focal individuals emitted loud calls during early
evening as well as early morning sessions. There was
no difference in the vocalization frequency between
both sessions in both sexes combined (Wilcoxon
matched-pairs test, N 5 10, Z 5 0.36, P 5 0.72; males
only: N 5 6, P 5 0.465; no analysis was possible for
the females owing to the sample size being too small;
N 5 4). There were no sex differences in the overall
vocalization frequency (Mann–Whitney U test,
Nmales 5 6, Nfemales 5 4, U 5 10, P40.05).
We determined the behavioral context of 124
vocalization bouts. Figure 4A illustrates the behaviors
before and after vocalizing. Three behavioral categories prevailed before vocalization: FEED (median 5
32.74%; range 5 0.00–53.35%), SCAN (median 5 30.13%;
range 5 0.00–51.98%), and REST (median 5 14.10%;
Am. J. Primatol.
1068 / Rasoloharijaona et al.
Fig. 4. (A) Behavioral context of loud calling in L. edwardsi. Behaviors which occurred during the 5 min before (in white) and 5 min after
(in gray) are expressed in percentage of duration. Line 5 median, box 5 25–75%, and whisker 5 nonoutlier range. Outliers and extremes
are not represented. REST, resting; FEED, feeding; HOLE, in the sleeping hole; SCAN, scanning; LOC, moving; SG, self-grooming;
SOC, social activity; VOC, vocalizing; GOUG, tree gouging; UNKN, unknown behavior; see Material and Methods for the definition of
each behavior. Wilcoxon matched pairs test, 0.05oPo0.07. (B) Behavioral context of a tree-gouging bout in L. mustelinus. Behaviors
which occurred during the 5 min before (in white) and 5 min after (in gray) are expressed in percentage of duration. Line 5 median,
box 5 25–75%, and whisker 5 nonoutlier range. Outliers and extremes are not represented. REST, resting; FEED, feeding; HOLE, in the
sleeping hole; SCAN, scanning; LOC, moving; SG, self-grooming; SOC, social activity; VOC, vocalizing; GOUG, tree gouging; UNKN,
unknown behavior; see Material and Methods for the definition of each behavior. Wilcoxon matched pairs test, Po0.01.
range 5 0.00–64.46%). After vocalizing (see Fig. 4A),
animals were mostly seen feeding (median 5 42.10%;
range 5 15.79–69.33%), resting (median 5 28.36%;
range 5 11.51–64.58%), and scanning (median 5
16.74%; range 5 0.00–26.04%). After a loud call,
L. edwardsi tend to increase their feeding activity
(Wilcoxon matched-pairs test, N 5 10, Z 5 0.059,
P 5 0.064) and decrease their time spent moving
(Wilcoxon matched-pairs test, N 5 10, Z 5 0.059,
P 5 0.064) and in the hole (Wilcoxon matched-pairs
test, N 5 10, Z 5 0.046, P 5 0.063). However, we
could not reject the null hypotheses according to
the sequential Bonferroni procedure, and thus these
results could have been explained by chance.
Behavioral Context of a Tree-Gouging Bout
Focal individuals displayed tree gouging during
the early evening as well as the early morning
sessions. They gouged more at the beginning of
their activity (N 5 8; median 5 2.1 tree-gouging bouts
per hour; range 5 1.2–2.9) than at the end (N 5 8;
median 5 0.0 tree-gouging bout per hour; range 5
0.0–0.7; Wilcoxon matched-pairs test, N 5 8,
Z 5 2.52, P 5 0.008). No analysis was possible for
either sex owing to the small sample size (Nmales 5
Nfemales 5 4).
Am. J. Primatol.
We determined the behavioral context of 50 treegouging bouts. Figure 4B illustrates the behaviors
and their relative duration before and after gouging.
Three categories of behavior prevailed within
5 min before a tree-gouging bout: HOLE (median 5 41.04%; range 5 28.64–93.53%), SCAN (median 5
29.47%; range 5 1.16–68.3%), and REST (median 5 5.53%; range 5 0.00–37.74%). After gouging
(see Fig. 4B), animals were mostly seen scanning
(median 5 61.87%; range 5 45.98–81.47%), feeding
(median 5 11.98%; range 5 0.00–25.46%), and in
locomotion (median 5 11.90%; range 5 6.09–27.94%).
L. mustelinus spent more time in the hole before
than after a tree-gouging bout (Wilcoxon matched
pairs test, N 5 9, Z 5 2.66, P 5 0.004; null hypothesis rejected by the sequential Bonferroni procedure). Conversely, the subjects were more in
locomotion, scanning (same results, Wilcoxon
matched pairs test, N 5 9, Z 5 2.66, P 5 0.004; null
hypothesis rejected by the sequential Bonferroni
procedure) after than before a tree-gouging bout.
DISCUSSION
We report here differences in the vocal behavior
of two cryptic sportive lemurs differing in habitat
and population density. In agreement with our
Tree Gouging in Sportive Lemurs / 1069
hypothesis, L. edwardsi, living in a high population
density in the dry deciduous forest of Ampijoroa,
displayed loud calls, whereas L. mustelinus, living in
a low population density, did not display loud calls.
Most of the loud calls were produced while feeding or
resting, which corroborate earlier results showing
that L. edwardsi produce loud calls for signaling ownership of sleeping and feeding sites [Rasoloharijaona
et al., 2006]. L. mustelinus did not vocalize but
displayed tree-gouging behavior mostly after leaving
its sleeping site and moving around. The meaning
and function of this behavior is not yet clear. Tree
gouging has been reported in primates [see CoimbraFilho & Mittermeier, 1976; Fonseca & Lacher, 1984;
Lacher et al., 1981; Lazaro-Perea et al., 1999; Nash,
1986; Rylands, 1985; Smith, 2006]. Two behavioral
contexts have been described for gouging a tree:
Either a nutritive or a nonnutritive context. Tree
gouging for feeding was observed in gum-feeding or
insectivorous animals, which used this technique to
scratch the bark and access the tree fluid or the
insect larvae under the bark in order to eat it [see
Nash, 1986]. Nonnutritive tree gouging has been
observed in strepsirrhines and New World monkeys
for scent marking a site. Wild male Milne-Edwardś
sifakas combine tree gouging with chest-anogenital
scent marking for overmarking [Patel & GirardButtoz, 2008]. Callithrix may urinate in holes in both
dry and fresh wood and perform genital rubbing in
their vicinity [Coimbra-Filho & Mittermeier, 1976].
Similarly, marmosets deposit a high number of scent
marks at gouging sites where they have previously
fed [Lacher et al., 1981]. It has been suggested that
these gouging sites function as ‘‘bulletinboards’’ for
the intragroup communication of information specific to an individual [e.g. Lazaro-Perea et al., 1999;
Rylands, 1985; Smith, 2006]. In this study, Lepilemur
never ate the wood or licked the bark while gouging
and we, therefore, hypothesize that tree gouging in
L. mustelinus was not a feeding behavior but had
more a non-nutritive function. Tree gouging leaves
long-lasting visible marks which, for instance, may
be used either for signaling the presence of an owner
of a specific shelter to other individuals or by the
owner itself in order to return to a safe shelter.
Because the visual acuity of prosimians is low
[Pereira, 1995] and sportive lemurs are furthermore
nocturnal, an alternative explanation would be that
tree gouging in sportive lemurs is not only used for
visual marking but for scent marking. As reported
for wild Milne-Edwards’ sifakas [Patel & GirardButtoz, 2008], Lepilemur could use a combination of
tree gouging and scent marking. Lepilemur have no
scent glands, except a scrotal gland in males [Petter
et al., 1977; p 289]. Because we did not observe
Lepilemur urinating on or close to the gouged sites
and males never performed a genital rubbing
behavior, we hypothesize that by gouging the tree
bark, animals may scent mark by depositing saliva
on the substrate. Indeed, saliva can contain hormone
molecules which play a role in social behavior in
mammals [see Gröschl, 2009]. For instance, mice and
pigs use salivary steroids to mark their territory or
attract potential mates [see Gröschl, 2009]. In
nonhuman primates, the presence of pheromones
in saliva has not been properly investigated yet. In
fact, relatively little is known about pheromones
in primates, but they seem to play a great role
in strepsirrhines and platyrrhines [Aujard, 1997;
Barrett et al., 1993]. Strepsirrhines and platyrrhines
are actually the only primates owning both functional main olfactory and accessory olfactory systems
[see Swaney & Keverne, 2009]. We already know that
in mouse lemurs the accessory olfactory system is
critical for pheromonal communication [Aujard,
1997]. To date, nothing is known regarding potential
pheromonal communication in other strepsirrhines.
Behavioral Differences Between L. edwardsi
and L. mustelinus
Our observations showed that tree gouging was
observed only in one of the two studied populations,
i.e. only in L. mustelinus from Andasibe and not in
L. edwardsi from Ampijoroa. Such a difference in the
behavioral repertoire may have been shaped by
socioecological constraints related to the habitat
quality and the population density. Earlier studies
showed that in both study sites, sportive lemurs
preferred tree holes and that they used only a few
sleeping sites [Rasoloharijaona, 2001; Rasoloharijaona
et al., 2008]. Since the distribution of lemurs using
tree holes is suggested to be associated with the
availability of suitable shelters [Lutermann, 2001;
Rasoloharijaona et al., 2003], we propose that both
study areas have a limited number of safe shelters
for sportive lemurs. In both study sites, sportive
lemurs should thus defend such an essential
resource. However, both study sites differ qualitatively in their food resource availability. Although
the rainforest of Andasibe is characterized by dense
vegetation and large evergreen trees, Ampijoroa is
covered by a dry deciduous forest that is influenced
by a higher seasonality. Food resources (mainly
leaves, fruits, and seeds for Lepilemur) are thus
more accessible in Andasibe than in Ampijoroa,
especially during the austral winter during which
we conducted the observations. Both study sites
differed in sportive lemur’s density. In Ampijoroa,
the population density is higher than in Andasibe.
Competition for food is thus higher for Lepilemur in
Ampijoroa than in Andasibe. We thus suggest that
during our study in the dry season Lepilemur in
Ampijoroa needed to compete for both feeding and
sleeping sites while Lepilemur in Andasibe primarily
needed to compete for sleeping sites. Milne-Edwards’
sportive lemurs defend sleeping and feeding sites
mainly by loud call displays, which represent a direct
Am. J. Primatol.
1070 / Rasoloharijaona et al.
and short-time information transmission for neighbors situated less than 200 m apart [Rasoloharijaona
et al., 2006]. Weasel sportive lemurs from Andasibe
rarely vocalized, but population density is also lower,
which limits the probability for a vocalizing animal
to be heard by neighbors. In order to optimize social
communication, an alternative strategy would be to
deposit longer lasting information by using visual
or/and scent marking instead of using short-term
signals, such as vocalizations. In the case of treegouging animals, they may thus transmit information on not only the ownership of their sleeping site
but also potentially on their reproductive status
during the mating season.
Earlier investigations showed that the vocal
activity of L. edwardsi from ten different local
populations was not affected by the population
density [Rabesandratana, 2006]. However, because
the populations were geographically close (all belonging to the Ankarafantsika National Park in northwestern Madagascar), they could still belong to the
same metapopulation. Resulting from our findings,
we suggest that differences in the vocal and chemical
communication between L. edwardsi and L. mustelinus may have actually evolved as a long-term
adaptation to the use of short-term signals in high
population density areas and to long-lasting signals
in low-density population areas. Intra- and interspecific variability in the vocal and chemical communication needs to be investigated further.
Possible Costs of the Tree Gouging—
Implications for Conservation
Scent marking may be costly for animals if
predators are able to use the marks to locate a
sleeping site. For instance, Franklin et al. [2007]
reported on a large population of golden lion tamarins
(Leonpithecus rosalia) in Brazil decreasing from
approximately 330 to 220 individuals in a time span
of 5 years, owing to a dramatic increase in predation at
sleeping sites. Natural predators used the scent
marking of these cavity-nesting primates in order to
localize them. During our observations, gouge marks
were not directly present on the sleeping trees, but
sportive lemurs were observed to leave the marks on
trees surrounding the sleeping sites. Further investigations would be needed to determine which surrounding trees are marked, i.e. whether sportive
lemurs use particular tree species and whether there
is a marking pattern in relation to the distance from
the sleeping tree. Indeed, with the help of these gouge
marks, we were able to easily localize a sleeping hole
or nest of a sportive lemur in the forest. These
observations imply two statements: First, gouge
marking could be costly for L. mustelinus if natural
diurnal predators could use the marks in the vicinity
of the sleeping site. Diurnal predators in Andasibe are
the fosa (Cryptoprocta ferox) which can be active both
Am. J. Primatol.
day and night and other birds of prey [mainly eagles,
such as Accipiter sp.; see Goodman et al., 2003].
Second, sportive lemurs are among those species
which are frequently poached in Malagasy forests
[Garcia & Goodman, 2003; Golden, 2009]. They are
usually easy to capture during the day while sleeping
in tree holes. Indeed, poachers were reported to have
followed the gouge marks in order to track down the
sleeping holes of sportive lemurs. Particular conservation and protection efforts in areas where sportive
lemurs signal their presence by marking trees are thus
essential to shield the local populations from poaching.
CONCLUSION
Altogether, we demonstrate in this article that
two cryptic species of nocturnal lemurs display
differences in the use of vocal and chemical communication to signal the use or ownership of resources.
According to our hypothesis, L. edwardsi, which lives
in a high-density population in the dry deciduous
forest, displayed loud calls, whereas L. mustelinus,
which lives in a low-density population in the
rainforest, did not emit loud calls. Most of the loud
calls were produced while feeding or in the vicinity of
resting places, which corroborate with our earlier
investigations that L. edwardsi produce loud calls for
signaling territory ownership. For the first time,
here we describe tree-gouging behavior, which
occurred outside a feeding context in a nocturnal
lemur species. We suggest that tree gouging is used
by individuals for signaling sleeping site ownership.
Further investigations are needed in order to provide
more insights into the mechanisms driving the
evolution of social communication.
ACKNOWLEDGMENTS
We thank the Malagasy authorities and, in
particular, the Ministère de l’Environnement et des
Forêts and the Madagascar National Parks for their
permission to conduct this study in the National Park
of Ankarafantsika, Andasibe—Mantadia and the
private Maromizà Reserve and for their logistic
support. For the help we received in Ankarafantsika,
we thank Jaofetra Randrianarivony, Michel Bisoa, and
Romain Rajaonirinaharison. For the help given in
Andasibe, we thank Alexandre Rasolofonirina (MNP
Andasibe), Jaofetra Randrianarivony, Pafo Velontiana,
and Hermano Raveloarisoa (NAT Foundation). We are
indebted to Rose Marie Randrianarison for the photograph of a marked tree. We thank Elke Zimmermann,
Ute Radespiel, and two anonymous reviewers for
valuable comments on an earlier version of the article.
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