Download Female Coordination of Group Travel in Wild Propithecus Elizabeth M. Erhart

International Journal of Primatology, Vol. 20, No. 6, 1999
Female Coordination of Group Travel in Wild
Propithecus and Eulemur
Elizabeth M. Erhart1 and Deborah J. Overdorff'1,2
Received November 11, 1998; revised May 24, 1999; accepted July 21, 1999
Coordination of primate group movements by individual group members is
generally categorized as leadership behavior, which entails several steps:
deciding where to move next, initiating travel, and leading a group between
food, water sources, and rest sites. Presumably, leaders are able to influence
their daily foraging efficiency and nutritional intake, which could influence
an individual's feeding ecology and long-term reproductive success. Within
anthropoid species, females lead group movements in most female-bonded
groups, while males lead groups in most nonfemale-bonded groups. Group
leadership has not been described for social prosimians, which are typically
not female-bonded. We describe group movements in two nonfemale-bonded,
lemurid species living in southeastern Madagascar, Propithecus diadema
edwardsi and Eulemur fulvus rufus. Although several social lemurids exhibit
female dominance, Eulemur fulvus rufus does not, and evidence for female
dominance is equivocal in Propithecus diadema edwardsi. Given the ecological stresses that females face during reproduction, we predict that females in
these two species will implement alternative behavioral strategies such as
group leadership in conjunction with, or in the absence of, dominance interactions to improve access to food. We found that females in both species
initiated and led group movements significantly more often than males did.
In groups with multiple females, one female was primarily responsible for
initiating and leading group movements. We conclude that female nutritional
needs may determine ranging behavior to a large extent in these prosimian
species, at least during months of gestation and lactation.
KEY WORDS: prosimian; leadership; group movements; female-bonded species; nonfemalebonded species; female dominance.
1
Department of Anthropology, University of Texas at Austin, Austin, Texas.
To whom correspondence should be addressed, at Department of Anthropology C3200,
University of Texas, Austin, Texas 78712-1086; e-mail: [email protected].
2
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0164-0291/99/1200-0927$16.00/0 © 1999 Plenum Publishing Corporation
Erhart and Overdorff
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aNTRODUCTION
Most primatologists agree that the distribution of food plays an important role in determining nonhuman primate group size and social organization (Wrangham, 1980; Janson, 1988). Van Schaik (1989) demonstrated
that most of the variation in female social relationships within groups could
be explained by the degree of scramble or contest competition experienced
by females when they feed (Sterck et al., 1997). Groups tend to be organized
in an egalitarian and individualistic way under scramble conditions when
food is evenly distributed so that each group member's food intake is
affected equally. With little intra- and intergroup feeding competition, there
is low incentive for females to establish close bonds or be philopatric:
nonfemale-bonded groups (Wrangham, 1980). In contrast, despotic and
nepotistic dominance hierarchies develop in groups that experience contest
competition when food is clumped and easily defendable so that each group
member's food intake varies. Females in these groups are philopatric and
often establish close ties to enhance their access to resources during competitive encounters: female-bonded groups (Wrangham, 1980).
In general, van Schaik's (1989) hypothesis adequately explains the
variation in social organization among anthropoid primates. Most folivorous
primates are nonfemale-bonded, while most frugivorous and omnivorous
primates are female-bonded. However, his hypothesis does not fit the behavioral patterns observed among prosimian primates. For example, female
Lemur catta have a clear, linear dominance hierarchy but seasonally incorporate leaves into the diet (Sussman, 1974; Sauther, 1994). Other species
such as Eulemur fulvus are primarily frugivorous in southeastern Madagascar and have no clear linear dominance hierarchy (Pereira et al., 1990).
In addition, many prosimians exhibit low rates of aggression in feeding
contexts (Hemingway, 1995; Overdorff, 1998) compared to polygynous
anthropoids in which male dominance over females in feeding contexts is
common (Hrdy, 1981; Jolly, 1984). Male dominance has not been reported
for the lemurids. Instead, female dominance, or female agonistic superiority
over males, occurs in several social species (L. catta, Varecia spp., and
some Eulemur spp.: van Schaik and Kappeler, 1993). However, other social
lemurids do not exhibit female dominance, e.g., E. fulvus rufus (Pereira et
al., 1990), and for some species there are conflicting reports, e.g., Propithecus
(Richard, 1987; Wright, 1995; van Schaik and Kappeler, 1996; Hemingway, 1995).
Further, the relationship between female dominance and feeding priority remains unclear, as several lemurids may have female feeding priority
without female dominance, e.g., Indri, Propithecus, Phaner (van Schaik and
Kappeler, 1996; Pereira et al., 1990). Female feeding priority may be the
Group Movements
929
result of male deference (Hrdy, 1981), which implies that females have
consistent access to food but not other resources. However, the male deference hypothesis does not seem adequate in its current form for prosimians.
Jolly (1984) predicted that if male prosimians are deferential, then variance
in male reproductive success should be lower, male-male competition
should be reduced, and males may have an equal opportunity to mate
whether they are deferential or not. Recent captive and wild studies imply
that male reproductive success can be quite variable and males compete
for access to reproductive females (White et al., 1996; Overdorff, 1998;
Overdorff et al., 1999; Sauther, 1992, 1993).
What alternative behavioral strategies could primate females implement
in conjunction with or in the absence of dominance interactions to improve
access to food? Sex differences in food intake occur in many anthropoid species in which females spend more time feeding, have higher feeding rates,
and/or consume more food than males do (Rodman, 1977; Waser, 1977;
Wright, 1984; Kinzey, 1987; Boinski, 1988). These feeding behaviors do not
have to be mediated through aggressive-submissive interactions. Similarly,
female coordination of group movements between food patches could result
in greater control over food type and quality (Boinski, 1991). There are many
anthropoid species in which females primarily coordinate group movements
(Cebus capucinus: Freese and Oppenheimer, 1981; Boinski, 1993; Cercopithecus aethiops: Struhsaker, 1967; Colobus guereza: Oates, 1977; Macacafascicularis: van Noordwijk and van Schaik, 1987; Macaca mulatta: Neville, 1968;
Papio cynocephalus anubis: Rowell, 1969; Saimiri oerstedi: Boinski, 1988;
Mitchell et al., 1991; Theropithecus gelada: Dunbar and Dunbar, 1975),
though males are often responsible for coordinating group travel in some
species (Table I). The distinguishing factor between male-led groups and
female-led groups is that in the former, females are not bonded and tend to
migrate from their natal group, while the majority of the species in the latter
are typically female-bonded and do not emigrate to new groups. Wrangham
(1980) argued that when females are bonded, they can exercise more influence over group movements, implying that this ability is important in regards
to resource acquisition. The majority of group-living prosimians, however,
are not female-bonded (Kappeler, 1997; Table I).
The purpose of our study is to describe group movements between
food patches in two contrasting prosimian species in southeastern Madagascar: the large-bodied, diurnal Propithecus diadema edwardsi (4-6 kg)
(Wright, 1995; Overdorff and Strait, unpublished data), and the smaller,
cathemeral Eulemur fulvus rufus (2.7 kg) (Overdorff and Strait, unpublished data). Wright (1995) reported Propithecus diadema edwardsi to be
female-dominant, though rates of aggression are very low (Hemingway,
1995). In contrast, Eulemur fulvus rufus is not female dominant (Pereira
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Erhart and Overdorff
Table I. Socioecological characteristics of primate species with female- or male-controlled
group movementsa
Species
Females control
Paplo cynocephalus
anubisb
Theropithecus geladac
Macaca fascicularisd
Macaca mulattae
Cercopithecus aethiopsf
Colobus guerezag
Saimiri oerstedih
Cebus capucinusi
Lemur cattaj
Eulemur coronatusk
E. fulvus sanford k
E. f. rufus l
E. rubiventerm
Propithecus diadema
edwardsin
Males control
Pan troglodyteso
Gorilla gorillap
Papio hamadryasq
P. cynocephalus ursinusr
Colobus badiuss
Alouatta paliattat
aFB,
F/M
ratio
I/D
Females
F>M
53
FB
FB
FB
FB
FB
NFB
FB
FB
NFB
NFB
NFB
NFB
NFB
Females
Females
Females
Females
Females
Neither
Females
Females
Neither
Neither
Neither
Neither
Neither
F>M
F>M
F> M
F>M
F>M
F> M
F>M
Equal
Equal
Equal
Equal
Equal
Equal
NFB
NFB
NFB
NFB
NFB
NFB
Males
Males
Males
Neither?
Males
Neither
F>M
F>M
F> M
F> M
F>M
F>M
Bond
Philopatry
FB
Diet
Food
distribution
O
NP
62
67
80
70
68
76
69
100
96
99
103
98
105
FO
O
O
O
FO
FR/I
FR/I
FR/FO
FR
FR
FR
FR
FR/SD
NP
NP
NP
NP
NP
PA
PA
PA
PA
PA
PA
PA
PA
77
60
59
50
98
75
O
FO
0
O
FO
FO/FR
PA
NP
PA
NP
NP
NP
Female-bonded; NFB, nonfemale-bonded. F/M ratio, number of females (F) to males
(M) in groups. I/D, (Female body mass/male body mass)100 (Smith and Jungers, 1997).
Overall diet category: O, omivory; FO, folivory; FR, frugivory; SD, seed-eating; I, insectory.
Food distribution: PA, patchy; NP, nonpatchy.
bRowell (1969).
c Dunbar and Dunbar (1975).
d Van Noordwijk and van Schaik (1987).
e Neville (1968).
f Struhsaker (1967).
gOates (1977).
hBoinski (1988); Mitchell et al. (1991).
iFreese and Oppenheimer (1981); Boinski (1993).
jSussman (1974); Sauther and Sussman (1993).
kArbelot-Tracqui (1983); Wilson et al. (1989).
This study; Overdorff (1993a).
mOverdorff (1993a).
"This study; Hemingway (1996, 1998).
oGoodall (1968).
"Watts (1994).
q Rummer (1968); Sigg and Stolba (1981).
r Barton et al. (1996); Byrne et al. (1990); Henzi and Lycett (1995).
s Wrangham (1980); Struhsaker (1980).
tCrockett and Eisenberg (1987); Milton (1980).
Group Movements
931
et al., 1990), but aggression among them can be high seasonally (Overdorff,
1998). Females are not bonded in either species. Given the presumed
energetic costs experienced by prosimian females when reproductive (Richard et al., 1991; Young et al., 1990; but see Kappeler, 1996; Tilden and
Oftedal, 1997) and the possible ecological stress experienced during reproductive periods (Overdorff et al., 1999), coordination of group travel to
food sources would have clear advantages. We therefore predict that female
prosimians will be influential in initiating and coordinating group movements between food sources despite weak or absent female dominance and
feeding priority and the lack of female bonds.
DATA COLLECTION
We sampled all occurrences of group movements, following Altmann
(1974). We modified methods developed by Boinski (1991) and used them
to determine if males or females coordinated group movements between
food patches and rest sites. We noted the identity of the initiator—the
individual that made a start attempt—within a food source, after pauses
during travel <5 min or after a resting bout. If >50% of the group followed
the initiator within 10 min, we compared the azimuth of the group trajectory
in relation to the center of the remaining group to the initiator's position
using a compass; this was a successful group movement. A false-start occurred when an individual attempted to initiate a group movement but
<50% of the group members followed within 10 min.
The individual that was at the leading edge of the group once the
group began moving was the leader. At 10-min intervals, we noted the
order of individuals to determine if the leader was the same individual or
if there had been a change in leadership, in which case we recorded a new
compass bearing. We distinguished between an initiator and leader because
the individual may not necessarily be the same (Kummer, 1968; Rowell,
1969). Rowell (1969) found that when several male Papio cynocephalus
anubis males left a feeding or resting spot and moved in different directions,
group members did not follow until an older female set off in the direction
of one of the males, at which time other females followed her and the
group then moved to the next site. By Boinski's (1991) definition, the
initiations made by these males would be coded as false starts, while the
older females would be recorded as leaders because they successfully initiated group movements. Data presented in Table III refer to (1) successful
initiations made by leaders and (2) unsuccessful initiations or false starts
for adults in both study species. We analyzed group movement data via
the G test with William's correction.
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Erhart and Overdorff
Table II. Group composition of study groups of Propithecus diadema edwardsi
(PDE) and Eulemur fulvus rufus (EFR)
Species
Adult males
Adult females
Juveniles
Infants
1
3
4
3
1
2
2
1
1
1a
PG
0
PDE I
PDE II
ERF
a Infant
survived 24 hr.
RESULTS
Group Movements
We observed a total of 146 and 192 successful group movements in
groups I and II, respectively, of Propithecus diadema edwardsi and we
recorded 165 successful group movements for the group of Eulemur fulvus
rufus (Tables II and III). Females initiated and led group movements
significantly more often than males did in each study group (PDE I: G =
47.73, df = 1, p < .0001; PDE II: G = 183.66, df = 1, p <.0001; EFR:
G = 51.12, df = 1, p <.0001). This sex difference is significant whether females led their groups to rest sites or food patches (Figs. 1 and 2). There
is no significant difference between the number of false starts and the sex
of the initiator in either group of Propithecus (Table III; PDE I: G = .058,
df = 1, p = n.s.; PDE II: G = 76, df = 1, p = n.s.) and there is a slight,
but not significant trend for male Eulemur (Fig. 3; EFR: G = 4.06, df =
1, p = n.s.).
In groups with multiple females, one was primarily responsible for
initiating and leading group movements (Fig. 4). Females in groups I and
II of Propithecus initiated about the same number of movements to resting
sites and food patches (Table HI; PDE I: G = 1.59, df = 1, p = n.s.; PDE
Table HI. Context of male and female successful initiations of group movements and
false starts for study groups of Propithecus diadema edwardsi (PDE) and Eulemur fulvus
rufus (EFR)
PDE I
Leadership
Rest
Feed
Travel
False starts
ERF
PDE II
Male
Female
Male
Female
Male
Female
1
1
145
73
19
12
173
64
46
20
119
27
0
0
7
53
19
18
6
1
5
83
26
4
18
8
20
72
20
2
933
Group Movements
Fig. 1. Male and female leadership of groups to rest sites in Propithecus diadema edwardsi
and Eulemur fulvus rufus. ***p < .0001.
II: G = 1.23, df = 1, p = n.s.), while female Eulemur initiated more
movements to food patches (G = 10.91, df = 1, p < .001; Table III).
In all cases, once a female initiated a group movement, she remained
the leader until the group stopped to feed or rest in both groups of Propithecus. The only time adult male initiated a group movement in group I,
he led them to a sleeping site at the end of the day. In group II, one adult
male initiated 16 of the 19 observed bouts for males; however, group II's
female had assumed the leadership position by the next 10-min time interval.
In the group of Eulemur the initiator remained the leader in each
group movement. Male Eulemur initiated and led their group significantly
more often than male Propithecus did (Table III; G = 32.53, df = 2,
p < .0001).
DISCUSSION
Based on the results of this study, female Propithecus diadema edwardsi
and Eulemur fulvus rufus reliably coordinate group travel. This result is in
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Erhart and Overdorff
Fig. 2. Male and female leadership of groups to food patches in Propithecus diadema edwardsi
and Eulemur fulvus rufus. ***p < .0001.
agreement with reports of female leadership in other prosimians such as
Eulemur coronatus, E. fulvus sanfordi (Arbelot-Tracqui, 1983; Wilson et
al., 1989; but see Freed, 1996), and Lemur catta (Sauther and Sussman,
1993). Among anthropoids, female leadership can be explained by femalebondedness as the degree of sexual dimorphism, diet, and distribution of
food varies (Table I; exception Salmiri oerstedi: Boinski, 1988; Mitchell et
al., 1991). This explanation, however, is not helpful to understand female
leadership patterns among prosimians since the majority of prosimians are
not female-bonded (Kappeler, 1997).
Why do female prosimians lead groups? Our results do not indicate
that this bias can be attributed to female dominance or feeding priority as
currently defined. We saw no aggression in feeding contexts for either
group of Propithecus (Erhart and Overdorff, 1998; Erhart and Overdorff,
unpublished data), thus we are unable to confirm the existence of female
dominance or feeding priority in this species. As in other studies of Eulemur
fulvus rufus (Pereira et al., 1990), we documented aggression during feeding,
but males and females did not differ in the amount of aggression directed
to other group members (Erhart and Overdorff, unpublished data). One
Group Movements
935
Fig. 3. Male and female false starts in Propithecus diadema edwardsi and Eulemur
fulvus rufus.
nonaggressive way in which females may be able to influence their daily
foraging efficiency and nutritional intake, and possibly impact their longterm reproductive success, is by initiating and coordinating group movements to food patches (Boinski, 1991). Through these activities, females
may influence several aspects of their diet: (1) which food or plant species
are used, (2) which individual food sources are used, (3) how far the group
travels to reach food sources, and (4) how long the group spends in any
one food source. Each of these behaviors could allow females to increase
their daily nutritional intake when reproductively stressed and to minimize
energy costs. This appears to be the case based on the fact that the female
responsible for the majority of group movements in groups with multiple
females was of reproductive age, produced an infant, and also had the
highest cumulative reproductive success of any female in the social group
(Overdorff et al., 1999; Erhart and Overdorff, unpublished data; Overdorff
and Strait, unpublished data).
Why do some males in some species lead group movements? This
pattern may be related to the fact that while females increase their reproductive success through food acquisition, males increase their reproductive
success through mate acquisition (Wrangham, 1980). Male-led species share
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Erhart and Overdorff
Fig. 4. Female leadership of groups with multiple females in both species.
several important characteristics: (1) there are more females than males in
the group, (2) males are philopatric and thus much more familiar with their
group's range than immigrant females are, and (3) food is either nonpatchy
and abundant or patchy but not easily defensible (Table I). Males may also
be devoting time to vigilance for predators or nonresident males.
Although female Eulemur led groups more often than males, male
Eulemur led groups more often than male Propithecus did. This difference
may be related to the degree of territoriality and frequency of intergroup
encounters. Eulemur fulvus rufus have large overlapping home ranges and
encounter other groups frequently (Overdorff, 1993b), while Propithecus
diadema edwardsi have smaller ranges and encounter other groups rarely
(Hemingway, 1995; Overdorff and Erhart, n.d.).
In future studies we plan to quantify differences between females in
different reproductive stages and nonreproductive individuals regarding
access to food, types of food eaten and the particular parts of plants consumed, and the nutritional components of selected plants. Another question
that needs further clarification is whether by leading groups leaders actually
acquire more and better foods than other group members. An understand-
937
Group Movements
ing of these key variables is necessary to estimate reliably the absolute
effects of leadership on diet and ultimately on individual reproductive
success.
ACKNOWLEDGMENTS
We thank Benjamin Andriamihaja, Patricia Wright, ANGAP, and the
Department of Water and Forests of Madagascar. We are grateful to Sue
Boinski and an anonymous reviewer; their comments greatly improved this
manuscript. We acknowledge Albert Telo, Aimee Razafiarimalala, and the
staff of the Ranomafana National Park Office for their assistance. Partial
funding was provided by a University of Texas Summer Research Grant
to D. J. Overdorff for the 1996 summer field season.
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