close

Вход

Забыли?

вход по аккаунту

?

Demography range use and behavior in black lemurs (Eulemur macaco macaco) at Ampasikely northwest Madagascar.

код для вставкиСкачать
American Journal of Primatology 67:299–312 (2005)
RESEARCH ARTICLE
Demography, Range Use, and Behavior in Black Lemurs
(Eulemur macaco macaco) at Ampasikely,
Northwest Madagascar
FRANÇOISE BAYART1n and BRUNO SIMMEN2
1
Département Écologie et Gestion de la Biodiversite´, CNRS-UMR5176,
Musée National d’Histoire Naturelle, Brunoy, France
2
Département Hommes, Natures et Sociéte´s, CNRS-UMR5145,
Muséum National d’Histoire Naturelle, Brunoy, France
We studied a black lemur population over a 2-year period (1992–1993)
and 8 years later (2000) in a 50-ha secondary forest in northwest
Madagascar. All of the animals were marked to investigate population
dynamics and seasonal variation in ranging and behavior, and new data
on black lemurs were obtained. Our data on demographic characteristics
were expanded to include other forest sites and contrasted with those
collected in other Eulemur macaco macaco field studies, in relation to
human activity and the presence of introduced and cultivated plant
species. Density is affected by deforestation and hunting. Group size and
home range depend on the composition of the forest and probably food
patches. Sex ratio at birth varies according to the number of females per
group, a result that fits the local resource competition model. Groups are
multimale-multifemale, and adult females form the core of the groups.
Reproductive parameters indicate sharply defined seasonal breeding, a
high female reproductive rate, and birth synchrony. Changes in group
composition reveal male and female juvenile dispersal, male transfer
between groups at the time of mating, and adult female transfer and
group fission when groups exceed a critical size. At mating and birth,
intergroup agonistic encounters occurred at home-range boundaries, and
larger groups were dominant over smaller groups. Patterns of intragroup
interactions suggest that males compete for access to groups of females
during the mating season, and that females may compete for food
resources during the birth season. Our study also reports female social
dominance and lack of sexual weight dimorphism in this species. Am. J.
Primatol. 67:299–312, 2005.
r 2005 Wiley-Liss, Inc.
Contract grant sponsor: CNRS; Contract grant sponsor: Institute of Embryology of the University
Louis Pasteur; Contract grant sponsor: French Ministry of the Environment (ECOFOR/MNHN);
Contract grant number: 2000.18.
n
Correspondence to: Françoise Bayart, CNRS-UMR 5176, Laboratoire d’Écologie Générale, Musée
National d’Histoire Naturelle, 4 Avenue du Petit Château, 91800 Brunoy, France.
E-mail: Fbayart@mnhn.fr
Received 11 July 2002; revised 22 March 2005; revision accepted 22 March 2005
DOI: 10.1002/ajp.20186
Published online in Wiley InterScience (www.interscience.wiley.com).
r
2005 Wiley-Liss, Inc.
300 / Bayart and Simmen
Key words: Eulemur macaco; demography; ranging patterns; social
structure; seasonal variation
INTRODUCTION
The life history traits of group-living lemurs are now recognized to be very
different from those of most other group-living primates. Such traits include
fewer females per group on average, equal adult sex ratios, male and female
transfer between groups, sharply seasonal breeding, lack of sexual size
dimorphism, female aggression, strong male–female bonds, and female feeding
priority over males [Jolly, 1998; Kappeler, 1997, 1999, 2000; Kappeler &
Ganzhorn, 1994]. After the ‘‘female need hypothesis’’ was proposed by Jolly
[1984], the ‘‘energy conservation hypothesis’’ [Pereira, 1993; Pereira et al., 1999]
and ‘‘energy frugality hypothesis’’ [Wright, 1999] emphasized how the ecological
constraints of a harsh and unpredictable environment in Madagascar have
shaped the evolution of major lemur traits. Elsewhere, van Schaik and Kappeler
[1993, 1996] focused on the role of the Holocene extinction of large diurnal
raptors in the emergence of lemur cathemerality (i.e., the transition from a
nocturnal to a diurnal lifestyle), as well as small group size in non-nocturnalliving species (i.e., evolving from pair-living).
To understand lemur adaptations, it is useful to compare different
populations of the same species [Sussman, 2002]. As regards the Lemuridae,
studies on demography, ranging, social behavior, and seasonality have focused on
Lemur catta [Gould et al., 2003; Jolly et al., 2002] and Varecia [Vasey, 2003], but
data are sparse for most Eulemur species [Overdorff & Johnson, 2003], except for
Eulemur fulvus [Overdorff et al., 1999; Tattersall, 1977]. In this study we
investigated the socioecological mechanisms by which the demography of black
lemur populations (Eulemur macaco macaco) is regulated by comparing data
collected in three locations in northwestern Madagascar in 1992–1993 and 2000
with those collected by other researchers in other northwestern forests in recent
years. Toward that end we sought to determine the limits of variation in density,
home range, group size, and group composition in populations inhabiting
different habitats. Long-term data on a population of black lemurs in northwest
Madagascar allowed us to analyze demographic changes along with major
ecological and reproductive correlates. Our main study site (Ampasikely, 131250 131260 S, 481280 -481290 E; Fig. 1) was a secondary forest (50 ha) with old plantations
and introduced plant species. Additionally, in 1992 we assessed population
densities from group censuses at two other study sites, Ampangorina (north shore
of Nosy Komba; 131260 3000 S, 481210 E) and Ambalahonko (south shore of Nosy Be,
131240 S, 481210 E, just outside the boundaries of Lokobe Reserve). Ampangorina is
a village surrounded by various crop fields and degraded secondary forest (50 ha),
where black lemurs are protected by the villagers and are fed bananas on a
regular basis. Ambalahonko and its surroundings (200 ha) are secondary forest
composed of mangroves, extensive bare ground areas due to deforestation, and
relics of primary forest where hunting is prohibited. Other black lemur
populations living nearby have also been studied, at Ambato Massif in ‘‘well
established secondary forest’’ [Colquhoun, 1993, 1998a], and in the primary
forest of Lokobe Reserve on Nosy Be [Andrews & Birkinshaw, 1998; Birkinshaw,
1999]. Since those studies and ours were conducted simultaneously, it is feasible
to compare these sites in terms of black lemur demography, range use, and
behavior.
Am. J. Primatol. DOI 10.1002/ajp
Black Lemur Demography and Behavior / 301
Main roads
Reserve boundaries
Scale
N
NOSY BE
10 km
0
NOSY FALY
LOKOBE
NATURE
RESERVE
HELL-VILLE
NOSY FALY
PENINSULA
Ambalahonko
Ampangorina
Ampasikely
NOSY KOMBA
Antsatsaka
AMBATO
MASSIF
Ambaliha
ANKIFY
PENINSULA
AMBANJA
AMPASINDAVA
PENINSULA
Beraty
MANONGARIVO
SPECIAL
RESERVE
MAROMANDIA
Fig. 1. Black lemur study-site locations in the northwest of Madagascar (map derived from Andrews
(unpublished results)). Ambalahonko: fragmented secondary forest. Ampangorina: cultivated
secondary forest with provisioning of the lemurs. Ampasikely: secondary forest with cultivated
and introduced plant species.
MATERIALS AND METHODS
Study Site
The main study site (Ampasikely) is a private landholding located along the
west coast of the Nosy Faly Peninsula. In addition to mangroves, the area is
Am. J. Primatol. DOI 10.1002/ajp
302 / Bayart and Simmen
composed of relics of primary forest and of dense, low-canopy, seasonally moist,
semideciduous secondary forest. The flora [Simmen et al., in press] include many
species that differ from those found in the Lokobe rain forest [Birkinshaw, 1999]
or Ambato Massif secondary forest [Colquhoun, 1993]. Cultivated plants are
particularly important since they form large clumps of food for the lemurs, and
include cashew (Anacardium occidentale; 3 ha), mango (Mangifera indica; 2 ha),
Albizia lebbeck and Piper sp. (2 ha), Coffea sp. (1 ha), and Carica papaya (1 ha).
Annona spp., Artocarpus spp., Musa spp., Citrus spp., Ceiba pentandra, Cananga
odorata, and Albizia saman are grown near local houses. The rainfall and
temperatures that were observed during our study [see Colquhoun, 1993] are
typical of the Sambirano climate, with an austral summer from November to
April (rainy season) and an austral winter from May to October (dry season). The
population has suffered from sporadic hunting. Since 1992 an effort to prevent
hunting has been made, concomitant with the construction of a hotel on the
seashore. The nearest black lemur population was found 5 km to the southeast of
our study site. The only other resident prosimian species is the nocturnal Mirza
cocquereli (Cheirogaleidae). Potential predators were raptors, whose sighting was
responded to with alarm calls by the lemurs (see also Colquhoun [1993]). There
were no constrictor snakes or large carnivores (except dogs).
Captures and Behavioral Observations
At this site, the black lemur population was censused in May 1987 by Meier
and Rumpler [1992], who earmarked the individuals in 1988 by Andrews
(unpublished results), and in 1992–1993 by Bayart et al. [1993] and Rabarivola
et al. [1998]. In January 1992, 29 out of 30 individuals were captured (with the
use of a blowpipe and ketalar anesthetic (0.3 ml/kg)), weighed, measured, bloodsampled, and marked with collars. They were then released at the site of capture.
We put collars on adults (eight males and eight females) and juveniles (three
males and three females). Infants (five males and two females) were simply
earmarked and tail-marked for identification. Infants born in 1991 and juveniles
born in 1990 were recaptured in May 1992 so that they could be collared. Infants
born in 1992 (four males and four females) were captured in April 1993, when
individuals born in 1990 were recaptured. In 1992–1993, the population was
studied for a total of 7 months 3 weeks across different seasons (Table I). In 2000,
we returned to the site for 3 weeks to assess survival and gather additional data to
complement our 1992–1993 data set.
We used ad libitum observations to map group locations, using trails with
trees marked at 15-m intervals, and to record group composition and the
TABLE I. Observation Protocol
Reproductive phase
1992
1992
1992
1993
2000
a
Season
Dates
weaning season Middle rainy
Jan 17 to Feb 23
mating season
Middle dry
May 24 to Aug 3
birth season
Late dry
Sept 4 to Oct 6
mating season
Early dry March 26 to June 23
birth season
Late dry
Sept 24 to Oct 15
Daysa Scan-days
30
42
21
76
21
10
15
18
28
15
2
Including scanned and ad libitum observations; (D): daytime; (N): nighttime observations.
Am. J. Primatol. DOI 10.1002/ajp
5-min scans
(hours)
240 (20, D)
540 (45, D)
324 (27, D)
1020 (85, D)
543 (45, D)
129 (11, N)
Black Lemur Demography and Behavior / 303
exclusion of individuals (i.e., animals seen alone at the same location for several
days). A 5-min scan sampling method [Altmann, 1974; Crook & Aldrich-Blake,
1968] was used to record diurnal activity on focal animals from 5 a.m. until 7 p.m.
In 2000, we also made observations throughout two nights of full moon. Morning
and afternoon observation sessions were alternated among groups and distributed across different times of the day. The behavioral categories included travel
(locomotion from one place to another); rest (alone or in contact); feed (or forage);
affiliative intragroup interactions (allogrooming, allomarking, courtship, and
mating); agonistic intragroup interactions (displacement, threat, slapping, and
targeted aggression, as defined by Vick and Pereira [1989]); long-distance
intergroup interactions (loud calls exchanged at a distance between groups);
pacific intergroup interactions (at a short distance with affiliative calls);
intergroup displays (marking, tail swishing, and leaping back and forth
accompanied by loud calls); and intergroup chases (pursuing targeted individuals
with loud calls and staccato grunts). For each period, all activities were analyzed
as a percentage of scans. Pearson chi-square tests were performed to compare
behavioral activities across the different reproductive periods. For inter- and
intragroup interaction analyses, the two mating seasons (which did not differ
from each other) were lumped together.
RESULTS
Population Demography
At the onset of the study (January 1992), only seven individuals (five adult
males and two adult females) of the 50 captured in May 1987 were still present,
and the population had been reduced to 30 individuals. The villagers explained
this 40% decrease in the population within a 5-year period as the result of
sporadic hunting.
Between 1992 and 1993, the total population size fluctuated between 29 and
40 individuals (Table II). The population comprised three social groups (GP, GV,
and GT) in February 1992, and four in June 1993. Overall, group size ranged
between four and 14 individuals. The mean group size varied from 9.1 individuals
(SD=1.6) during the two mating seasons to 12.7 individuals (SD=1.8) following
the 1992 birth season. On average, the groups contained 3.2 adult males and
females (SD=0.8) at weaning, 3.4 adult females (SD=0.5) and 3.6 (SD=0.9) adult
males at mating, and 3.7 adult males and females (SD=0.4) following the 1992
birth season. All groups were multimale-multifemale except one that consisted of
one adult pair with a juvenile and an infant. In February 1992, this small group
(GP) separated from GT and established a new home range at the west corner of
the site. Three months later, this small group had incorporated two adult males
and two juvenile females from groups GV and GT.
Throughout all phases of the reproductive cycle, mature females formed the
core of their groups. In contrast, adult males moved between groups, especially
during the mating season (two in 1992 and five in 1993). We also observed the
exclusion of some individuals: a young female and an old male in 1992, and two
old males and one young male that died from pulmonary edema in 1993. Juvenile
males and females dispersed from their natal group as early as 1 year of age,
during the birth season (three cases), at 112 years of age, during the mating season
(five cases), or later at 2 years of age (five cases).
During the 1992 and 1993 mating seasons, the operational sex ratio (i.e.,
potentially reproducing individuals) varied from one to 1.08 male/female. There
were twice as many old males as old females (born before 1987) and only half as
Am. J. Primatol. DOI 10.1002/ajp
Am. J. Primatol. DOI 10.1002/ajp
Adult males
Adult females
Juvenile males
Juvenile females
Infant males
Infant females
Group size GT
GV
GT
29
1
1
2.5
7
2
3
1
0
2
0
8
3
4
2
0
2
2
13
3
1
0
3
1
0
8
May–July 92
40
1
2.5
1.2
4
4
4
2
1
3(2)
1
15
4
4
3
0
0
4(1)
15
3
3
0
1
3
0
10
Sept–Oct 92
GP, new group issued from GTA=GT+GP; (n), individual found dead or disapeared; ND, not determined.
30
1
1
1.67
4
GT/GP
3
3
2
1
2
1(1)
12
Adult males
Adult females
Juvenile males
Juvenile females
Infant males
Infant females
Group size GV
GP
Population size
Adult M/F ratio
Juvenile M/F ratio
Infant M/F ratio
Individual transfer
Group fission
4
4
1
1
2
2
14
Adult males
Adult females
Juvenile males
Juvenile females
Infant males
Infant females
Group size GP
Population
1
1
0
1
1
0
4
Age-sex classes
Group identity
Jan–Feb 92
37
1
2.5
1
2
4
4
2
1
1
1
13
4
4
3
0
0
3
14
3
3
0
1
3
0
10
March–Apr 93
TABLE II. Group Composition and Demographic Characteristics of the Population Across Seasons and Years
35
0.91
2
1
5
GV1/GV2
3
4
2
0
1
1
11
5(1)
4
3(1)
2
0
3
8þ7
3
3
0
0
3
0
9
May–June 93
50
1.23
2.67
ND
ND
GP1/GP2
5
4
3
1
2
2
17
4
4
2
1
1
1
13
7
5
3
1
2
2
11 þ 9
Sept–Oct 2000
304 / Bayart and Simmen
Black Lemur Demography and Behavior / 305
TABLE III. Mean Weights (in g) of Males and Females From Infancy to Adulthoodn
Age (in months)
Male
Female
4
8
933756 (3) 13117141 (7)
950750 (2) 13637138 (6)
16
20
18007100 (3)
16927144 (3)
32
2017778 (3) 2283722 (3)
20677122 (3) 2283744 (3)
n
Figures in parenthesis indicate the number of individuals sampled.
many young males as young females (born in 1987 or after). In 1992, mating
occurred from 24 May until 3 August. In 1993, mating started as early as 7 April
and lasted until 23 June. Thus, the mating season may span 4 months, from early
April to early August. All females gave birth in 1991 and 1992. In 1992, eight
females (73%) gave birth within a 3-week period (4–26 September), and three
young females were still pregnant on 6 October. Considering that gestation lasts
4 months for this species, this means that conception occurred mainly in May and
was probably delayed for the juveniles whose first reproductive activity and first
parturition occurred at ~20 months and 2 years of age, respectively.
The infant sex ratio at birth showed a male bias (1.67 in 1991, and 1.2 in
1992). A 4-month-old infant died in February 1992, and three infants less than
6 months old disappeared after the 1992 birth season. Thus the female
reproductive rate was high (100%), but infant mortality ranged from 12.5% to
27.3%. Despite the small sample of infants born in 1991, survival into adulthood
was estimated at about 75%. Between 1992 and 1993, the juvenile sex ratio varied
from one to two males/female. No sex differences in the weight of young
individuals could be detected (Table III). The mean adult weights of males (n=8)
and females (n=8) in the middle of the 1992 wet season were 2,197 g (SD=98;
range=1,975–2,400 g) and 2,148 g (SD=116; range=1780–2350 g), respectively.
Although the population had increased (to 50 individuals) by 2000, the group
size had not (four groups of nine to 17 individuals, mean=12.5, SD=2.5). There
was an imbalance in adult and juvenile sex ratios (1.23 and 2.66 males/female,
respectively). The sex ratio at birth was not determined, because not all females
(77%) gave birth before the end of the study. Overall, between 1993 and 2000 the
survival rate was significantly greater for males (64%) than for females (33%). In
2000, at least two 10-year-old males and two 12-year-old females were still alive.
By that time, five males and two females that were captured as adults in 1987 had
disappeared, which suggests that longevity for this species is about 15 years. The
population comprised three to four social groups after the splitting of group GP.
All observed cases of group fission occurred when group size exceeded 16
individuals (i.e., GT before separation in 1992, GV before the deaths of two males
in 1993, and GP before the birth of four infants in 2000). If we compare female
core areas between 1992–1993 and 2000, two adult females were still in their
original home range, whereas one female had transferred from GT to GP, as did a
female in the past. These latter cases indicate that during their lifespan, adult
females are able to join another group or establish a new home range.
Seasonal Variation in Ranging Patterns, Activity Budgets, and Social
Behavior
Data accumulated from the three groups in different seasons (92 hr) in 1992
indicated that the population ranged over 33.5 ha, and the mean home range area
was 18.2 ha (range=14.4–23.8 ha; convex polygon excluding sea areas; Fig. 2). The
core areas of GV (24 ha), GT (16 ha), and GP (14 ha) were in the south, north, and
Am. J. Primatol. DOI 10.1002/ajp
306 / Bayart and Simmen
N
N
Sea
N
Sea
Sea
GT
Mangroves
GT
Mangroves
GP
GT
Mangroves
GP
GP
Sea
100m
GV
GV
1992 all seasons
Sea
100m
1993 mating season
Sea
100m
GV
2000 birth season
Fig. 2. Group home ranges at different periods.
west, respectively. With the exception of the mangroves used only by group GT,
home ranges showed considerable overlap between groups: 18% of the total area
was shared by the three groups (GT and GV shared 21%, GT and GP shared 25%,
and GP and GV shared up to 52%). The mean home range size was smaller during
the 1993 mating season (85 hr): 11.3 ha (range=7.3–16.2 ha), and during the 2000
birth season (56 hr): 9 ha (range=5.1–13.1 ha). In 1993, the total population range
was only 20 ha, but 25% of the area was still shared by the three groups. In 2000,
of a total range of 24 ha, only 8% of the area was common to the three groups,
suggesting group avoidance during the birth season.
The proportions of traveling (32%) and resting (30–33%) during the daytime
were fairly stable across seasons, but day range and speed of travel were reduced
during the dry season (from 1,000 m at 20 m/min at weaning, to 500 m at 4 m/min
at mating, down to 250 m at 2 m/min at birth). At mating and birth, there were
also more intragroup interactions (14% and 19%, respectively) and less feeding
behavior (16% and 15%, respectively) than at weaning (4% social interactions and
23% feeding behavior; Pearson w2=35.94, df=4, P=0.001). At birth, during two
nights of full moon, we found more resting (55%) and intergroup interactions
(10%) and less traveling (20%), feeding (10%), and intragroup interactions (5%)
than during the day (Pearson w2=75.8, df=8, P=0.001). Intergroup interactions
diminished from the rainy season (8%) to the dry season (4%), but their patterns
varied according to the reproductive cycle (w2=18.84, df=3, P=0.001; Fig. 3). At
weaning, the intergroup interactions were long-distance (53%) or pacific (47%)
with groups foraging together on fruits of Dypsis spp. and Grewia spp. (both of
which are nonlimiting resources during the rainy season). At mating, the animals
engaged in intergroup displays (47%) or agonistic chases (11%) rather than longdistance calls (36%). These encounters were not associated with preferred food,
such as the fruits of Coffea sp., Carica papaya, Dypsis spp., or Anacardium
occidentale. At birth, intergroup agonistic interactions occurred at short distances
(55%, of which 38% involved chases over patches of preferred plant species (fruits
of Sorindeia madagascariensis and Albizia saman) at home-range boundaries).
Based on group-chasing directions, GV (five chases) was dominant over GP and
GT (two chases each) in 1992–1993, whereas GP (eight chases) was dominant over
GV and GT (three chases each) in 2000. Intragroup interactions also showed
significant differences between the mating and birth seasons (Pearson w2=12.67,
df=3, P=0.005; Fig. 4). Male–male agonistic interactions occurred at mating
Am. J. Primatol. DOI 10.1002/ajp
Black Lemur Demography and Behavior / 307
weaning 1992
0%
0%
long distance
pacific encounter
47%
53%
agonistic display
agonistic chase
mating 1992-93
11%
36%
long distance
pacific encounter
agonistic display
47%
6%
agonistic chase
birth 2000
31%
38%
long distance
pacific encounter
agonistic display
17%
14%
agonistic chase
Fig. 3. Distribution of intergroup interactions across the reproductive cycle (in percentage of scans).
(13%, n=209) and at birth (6%, n=108), while female–female targeted aggression
was observed at birth (10%, n=108). In all seasons, females were dominant over
males (displacement during foraging bouts, threats, or slapping of males, 9.5%,
n=327). Male agonistic behaviors against females were never observed.
DISCUSSION
Densities, Group Sizes, and Home Ranges
As with other Eulemur species, black lemur population densities vary with
the level of forest disturbance [Mittermeier et al., 1994]. Overall, in 1992,
densities ranged between 40 individuals/km2 in Ambalahonko ‘‘fragmented
forest’’ to 200/km2 in Ambato Massif ‘‘well established secondary forest’’
[Colquhoun, 1993], with intermediate values for Ampasikely (60/km2) and
Ampangorina (132/km2), two anthropogenically disturbed forests. At Ampasikely,
the population declined from 100 individuals/km2 in 1987 to 88/km2 in 1988, and
to 60/km2 in 1992, but rose again to 100 individuals/km2 in 2000, after the site
became protected. Despite the protected status of the lemurs in northwest
Am. J. Primatol. DOI 10.1002/ajp
308 / Bayart and Simmen
weaning 1992
10%
30%
60%
0%
mating 1992-93
2%
8%
13%
77%
birth 2000
10%
10%
6%
74%
Fig. 4. Distribution of intragroup interactions across the reproductive cycle (in percentage of scans).
Pacific=affiliative interaction between two individuals; other categories=agonistic interaction
between two individuals (M4M (male against male), F4M (female against male), and F4F (female
against female)).
Madagascar [Harpet et al., 2000], these results indicate how vulnerable the
species is in areas where deforestation and occasional hunting persist.
The distribution of food resources is of paramount importance in terms of
foraging and ranging behavior, and consequently the group size of primates
[Oates, 1987]. In black lemurs, group size and home range appear to vary
depending on the floral composition of the forest, the abundance of cultivated and
introduced plant species, and provisioning. Overall, in 1992, the average group
sizes were 7.4 individuals (n=11; SD=1.4) at Ambalahonko (before birth), 7.7
(n=53) in Lokobe primary forest [Andrews & Birkinshaw, 1998), 10.25 (n=4;
SD=1.25) at Ambato Massif (after birth [Colquhoun, 1993]), 12.7 (n=3; SD=1.8)
at Ampasikely (after birth), and 22 (n=3; SD=7.3) at Ampangorina (before birth).
The protection and feeding of the lemurs at Ampangorina undoubtedly account
for the largest group size observed. The floral richness of the forest at Ambato
[Colquhoun, 1998a], and the year-round availability of large clumps of fruits at
Am. J. Primatol. DOI 10.1002/ajp
Black Lemur Demography and Behavior / 309
Ampasikely may be responsible for the larger group sizes in these two sites
compared to those observed in the Lokobe primary forest or the Ambalahonko
fragmented forest. Groups may be smaller in Lokobe because food resources are
more randomly distributed (Andrews, unpublished results), and in Ambalahonko
because of food scarcity. Also probably linked to food patches, the composition of
black lemur study populations varied between two to five groups (two to four this
study; three to four at Ampangorina and in the metapopulation of 11 groups at
Ambalahonko, and four to five at Ambato). Group fissions occurred when the
groups reached a critical size (n=16–17, this study; n=12 in Colquhoun [1993]).
At Ampasikely, the patches of cultivated plants may also be responsible for the
large home range size: 18.2 ha/group (range=14.4–23.8 ha) compared to 5.25 ha/
group (range=3.5–7 ha) at Ambato (n=4 [Colquhoun, 1993]), and just 3.25 ha/
group at Lokobe (Birkinshaw, personal communication). In our study, home
range size decreased during the dry season, but even with fewer hours of
observation, the home ranges were still larger than in primary or well-established
secondary forests.
Group Composition and Sex Ratio Regulation
The groups contained on average the same number of adult females and
males (respectively 2.4 and 2.3 in Andrews (unpublished results), 2.6 and 2.8 in
Colquhoun [1993], and 3.4 and 3.6 this study). However, in 2000, when the
Ampasikely population reached 50 individuals, we observed more adult males
than adult females per group on average (4 and 3.25, respectively), and a strongly
male-biased sex ratio in juveniles (2.7). To a lesser extent, in 1992 and 1993,
infant and juvenile sex ratios were also male-biased. Thus, contrary to the
conclusions of Andrews (unpublished results) and Colquhoun [1993], our results
indicate the presence of a male-biased sex ratio in E. m. macaco, as reported
earlier by Petter [1962] and Jolly [1966]. Since the latter studies (like ours) were
conducted in more degraded forest habitats compared to those studied by
Colquhoun and Andrews, it is possible that the type of habitat has an indirect
impact on sex ratio regulation in this species. Indeed, according to Andrews
(unpublished results), there is a strong infant male bias (3.5) in the five groups
located on Nosy Faly Peninsula (anthropogenically disturbed forests), and a
strong infant female bias (3.5) in seven groups in Manongarivo (primary forests).
The local resource competition model for facultative sex ratio adjustment
[Clark, 1978; Jolly, 1984; Perret, 1990; Nunn & Pereira, 2000] may explain these
discrepancies. Lack of resources may have more drastic effects on maternal
investment in lemurs than in other primates [Pereira et al., 1999]. In the context
of secondary forests, despite potential food richness [Ganzhorn, 1995], local
female–female competition may occur because of a larger group size and higher
number of females per group, as observed for black lemurs. Considering that the
optimal number of females per group is the result of an evolutionary adjustment
of group size to food availability in undisturbed forests, a higher number of
females would enhance local female–female competition. This would lead to
higher mortality rates in females, as detected in the present study. Resource
competition between females would be lowered with a high production of males.
Consequently, if the average number of females per group is below 3, as in Lokobe
(2.4), Manongarivo (2.4), and Ambato (2.6), we observe a female-biased sex ratio
at birth. If it is over 3, as in Ampasikely (3.4), Nosy Faly Peninsula (3.4), and Nosy
Komba (6), we observe a male-biased sex ratio at birth. Moreover, this model
agrees with observations made in captive lemur populations. In zoos where
Am. J. Primatol. DOI 10.1002/ajp
310 / Bayart and Simmen
females were grouped, the sex ratio was often male-biased, whereas in a semifree-ranging group of black lemurs, targeted aggression and exclusion between
females occurred whenever the number of adult females in the group rose above 3
(Roeder, personal communication). In captive brown lemurs as well, targeted
aggression has been linked to group size and adult sex ratio [Vick & Pereira,
1989].
Seasonal Variation in Behavior
Our data on reproductive parameters confirm both seasonal breeding and
birth synchrony for this species [Rasmussen, 1985]. Moreover, the patterns of
intergroup encounters varied across seasons (pacific during the rainy season, and
agonistic with dominance of larger groups over smaller groups during the dry
season). Dry-season observations indicate that the black lemurs did not suffer
from food scarcity, because numerous fruiting or flowering cultivated species
were available (Simmen et al., unpublished results). At mating, intergroup
agonistic encounters were not linked to the principal food, and probably reflect
male–male competition for mates, whereas at birth, disputes over preferred fruit
species indicate possible female–female competition for resources during
lactation. In the future, social competition must be studied more extensively
along with the distribution and productivity of food resources. In our study, black
lemurs behaved during the dry season as if they were minimizing foraging costs
in order to allocate more energy for reproductive purposes [Pereira et al., 1999].
However, more data are needed regarding nocturnal activity [Andrews &
Birkinshaw, 1998; Colquhoun, 1998b] and reproductive tactics in this species to
confirm this hypothesis.
ACKNOWLEDGMENTS
We are grateful to the Ministère des Eaux et Forêts in Madagascar, and to R.
and H. D’Ambelle for permission to conduct this research. We thank Y. Rumpler
and B. Krafft for supporting the project. We appreciate the help and advice of J.J.
Petter, R.D. Martin, B. Meier, S. Crovella, D. Montagnon, B. Rakotosamimanana,
C. Rabarivola, the technicians from Tsimbazaza (Antananarivo) and CNRO (Nosy
Be), the students, the forest guides, and the villagers. We thank the anonymous
reviewers who commented on earlier drafts of the manuscript.
REFERENCES
Altmann J. 1974. Observational study of
behavior: sampling methods. Behaviour 49:
227–267.
Andrews JR, Birkinshaw CR. 1998. A comparison between the daytime and nighttime diet, activity and feeding height of the
black lemur, Eulemur macaco (Primates,
Lemuridae), in Lokobe Forest, Madagascar.
Folia Primatol 69(suppl 1):175–182.
Bayart F, Rabarivola C, Ludes B, Krafft B,
Rumpler Y. 1993. Eco-ethological, demographic and genetic survey of three populations of Eulemur macaco macaco in
northwestern Madagascar. In: Proceedings
of the 23rd International Ethological Conference, Torremolinos, Spain. 49p.
Am. J. Primatol. DOI 10.1002/ajp
Birkinshaw CR. 1999. The importance of the
black lemur (Eulemur macaco) for seed
dispersal in Lokobe Forest, Nosy Be. In:
Rakotosamimanana B, Rasamimanana H,
Ganzhorn JU, Goodman SM, editors. New
directions in lemur studies. New York: Kluwer
Academic/Plenum Publishers. p 189–199.
Clark AB. 1978. Sex ratio and local competition resource in a prosimian primate.
Science 201:165–168.
Colquhoun IC. 1993. The socioecology
of Eulemur macaco: a preliminary report.
In:
Kappeler
PM,
Ganzhorn
JU,
editors. Lemur social systems and their
ecological basis. New York: Plenum Press.
p 11–23.
Black Lemur Demography and Behavior / 311
Colquhoun IC. 1998a. The lemur community
of Ambato Massif: an example of the species
richness of Madagascar’s classified forests.
Lemur News 3:11–14.
Colquhoun IC. 1998b. Cathemeral behavior
of Eulemur macaco macaco at Ambato
Massif,
Madagascar.
Folia
Primatol
69(suppl 1):22–34.
Crook JH, Aldrich-Blake P. 1968. Ecological
and behavioral contrasts between sympatric ground dwelling primates in Ethiopia.
Folia Primatol 8:192–227.
Ganzhorn JU. 1995. Low-level forest disturbance effects on primary production, leaf
chemistry, and lemur populations. Ecology
76:2048–2096.
Gould L, Sussman RW, Sauther ML. 2003.
Demographic and life-history patterns in a
population of ring-tailed lemurs (Lemur
catta) at Beza Mahafaly Reserve, Madagascar: a 15-year perspective. Am J Phys
Anthropol 120:182–194.
Harpet C, Jeannoda V, Hladik CM. 2000. Sites
à lémuriens sacrés en pays Sakalava, au
nord-ouest de Madagascar: réactualisation
des données et implications dans les programmes de développement et de conservation. Rev Ecol (Terre Vie) 55:291–295.
Jolly A. 1966. Lemur behavior: a Madagascar
field study. Chicago: University of Chicago
Press. 187p.
Jolly A. 1984. The puzzle of female feeding
priority. In: Small MF, editor. Female
primates: studies by women primatologists.
Monographs in primatology. Vol. IV. New
York: Alan R. Liss. p 197–215.
Jolly A. 1998. Pair bonding, female aggression
and the evolution of lemur societies. Folia
Primatol 69(suppl 1):1–13.
Jolly A, Dobson A, Rasamimanana HM,
Walker J, O’Connor S, Solberg M, Perel
V. 2002. Demography of Lemur catta at
Berenty Reserve, Madagascar: effects of
troop size, habitat and rainfall. Int J
Primatol 23:327–353.
Kappeler PM, Ganzhorn JU. 1994. The
evolution of primate communities and
societies in Madagascar. Evol Anthropol
2:159–171.
Kappeler PM. 1997. Determinants of primate
social organization: comparative evidence
and new insights from Malagasy lemurs.
Biol Rev 72:111–151.
Kappeler PM. 1999. Lemur social structure
and convergence in primate socioecology.
In: Lee PC, editor. Comparative primate
socioecology. Cambridge: Cambridge University Press. p 273–299.
Kappeler PM. 2000. Causes and consequences
of unusual sex ratios among lemurs. In:
Kappeler PM, editor. Primate males.
Cambridge: Cambridge University Press.
p 55–63.
Meier B, Rumpler Y. 1992. Enzyme variability
in island and mainland populations of black
lemur (Eulemur macaco): a contribution
to conservation biology. Karger Gazette
54:10–12.
Mittermeier RA, Tattersall I, Konstant WR,
Meyers DM, Mast RB. 1994. Lemurs of
Madagascar. Conservation international
tropical field guide series 1. Washington,
DC: Conservation International. 356p.
Nunn CL, Pereira ME. 2000. Group histories
and offspring sex ratios in ringtailed lemurs
(Lemur catta). Behav Ecol Sociobiol 48:
18–28.
Oates JF. 1987. Food distribution and foraging behaviour. In: Smuts BB, Cheney DL,
Seyfarth RM, Wrangham R, Struhsaker
TT, editors. Primate societies. Chicago:
Chicago University Press. p 197–209.
Overdorff DJ, Merenlender AM, Talata P,
Telo A, Forward ZA. 1999. Life history of
Eulemur fulvus rufus from 1988–1998 in
southeastern Madagascar. Am J Phys
Anthropol 108:295–310.
Overdorff DJ, Johnson S. 2003. Eulemur, true
lemurs. In: Goodman SM, Benstead JP,
editors. The natural history of Madagascar.
Chicago: University of Chicago Press.
p 1320–1324.
Pereira ME. 1993. Seasonal adjustment of
growth rate and adult body weight in ringtailed lemurs. In: Kappeler PM, Ganzhorn
JU, editors. Lemur social systems and their
ecological basis. New York: Plenum Press.
p 205–221.
Pereira ME, Strohecker RA, Cavigelli SA,
Hughes CL, Pearson DD. 1999. Metabolic
strategy and social behavior in Lemuridae.
In: Rakotosamimanana B, Rasamimanana
H, Ganzhorn JU, Goodman SM, editors.
New directions in lemur studies. New York:
Kluwer
Academic/Plenum
Publishers.
p 93–117.
Perret M. 1990. Influence of social factors on
sex ratio at birth, maternal investment and
young survival in a prosimian primate.
Behav Ecol Sociobiol 27:447–454.
Petter JJ. 1962. Recherches sur l’écologie
et l’éthologie des lémuriens malgaches.
Mém Mus Natl Hist Nat Paris Sér A Zool
XXVII:1–146.
Rabarivola C, Meier B, Langer C, Bayart F,
Ludes B, Rumpler Y. 1998. Comparison of
genetic variability in wild insular and
mainland populations of Eulemur macaco:
implications for conservation strategy.
Folia Primatol 69(suppl 1):136–146.
Rasmussen DT. 1985. A comparative study
of breeding seasonality and litter size in
eleven taxa of captive lemurs (Lemur and
Varecia). Int J Primatol 6:501–517.
Simmen B, Tarnaud L, Bayart F, Hladik A,
Thiberge A-L, Jaspart S, Jeanson M, Marez
Am. J. Primatol. DOI 10.1002/ajp
312 / Bayart and Simmen
A. Richesse en métabolites secondaires des
forêts de Mayotte et de Madagascar et
incidence sur la consommation de feuillage
chez deux espèces de lémurs (Eulemur
spp.). Rev Ecol (Terre Vie) (in press).
Sussman RW. 2002. Adaptive array of lemurs
of Madagascar revisited. Evol Anthropol
Issues News Rev 11(Suppl 1):75–78.
Tattersall I. 1977. Ecology and behavior of
Lemur fulvus mayottensis (Primates, Lemuriformes). Anthropol Pap Am Mus Nat
Hist 54:422–482.
van Schaik CP, Kappeler PM. 1993. Life
history, activity period and lemur social
systems. In: Kappeler PM, Ganzhorn JU,
editors. Lemur social systems and their
ecological basis. New York: Plenum Press. p
241–260.
Am. J. Primatol. DOI 10.1002/ajp
van Schaik CP, Kappeler PM. 1996. The social
systems of gregarious lemurs: lack of convergence with anthropoids due to evolutionary disequilibrium? Ethology 102:
915–941.
Vasey N. 2003. Varecia, ruffed lemurs. In:
Goodman SM, Benstead JP, editors.
The natural history of Madagascar.
Chicago: University of Chicago Press.
p 1332–1336.
Vick LG, Pereira ME. 1989. Episodic targeting aggression and the histories of Lemur
social groups. Behav Ecol Sociobiol 24:
265–276.
Wright PC. 1999. Lemur traits and Madagascar ecology: coping with an island environment. Yearb Phys Anthropol 42:
31–72.
Документ
Категория
Без категории
Просмотров
0
Размер файла
262 Кб
Теги
black, behavior, northwest, lemur, ranger, eulemur, madagascar, macaca, ampasikely, use, demographic
1/--страниц
Пожаловаться на содержимое документа