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Demography ranging patterns and activity budgets of black spider monkeys (Ateles paniscus chamek) in the Manu National Park Peru.

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American Journal of Primatology 15:45-67 (1988)
Demography, Ranging Patterns, and Activity Budgets of
Black Spider Monkeys (Ateles paniscus charnek) in the
Manu National Park, Peru
M. MCFARLAND SYMINGTON
Department of Biology, Princeton University, Princeton, New Jersey
Results of a long-term field study on the ecology and social organization of
two groups of black spider monkeys (Ateles paniscus chamek) in Peru are
reported. Demography, ranging patterns, and activity budgets provide
insight into some of the proximate determinants of fission-fusion social
organization in this species and illustrate the different strategies used by
males and females to gain access to critical resources. Longitudinal data
on known individuals provide evidence for male natal philopatry and
female emigration at sexual maturity in this population. Interbirth
intervals are long (mean = 34.5 months) in comparison with most other
primate species, and 5 of 15 infants seen within a few days of birth died or
disappeared before they were a year old. Home ranges are large (150-250
ha) and fairly discrete; overlap with neighboring groups is on the order of
10-15%. Males and females differed substantially in their ranging patterns; females, particularly those with infants, restricted much of their
ranging to a "core area" 20-33% the size of the total group range, whereas
males ranged more evenly over the entire area occupied by the group.
Daily path length varied over almost an order of magnitude from 465 m to
4,070 m, with a mean of 1977 m. Males spent more time traveling and less
time feeding than most females. These results are compared with those
obtained in previous studies of Ateles and with similar data from other
primate species to assess their implications for the evolution of fissionfusion sociality in spider monkeys. The ecological factors responsible for
the evolution of very similar social organizations in spider monkeys and
chimpanzees are discussed.
Key words: Ateles, spider monkey, social organization, chimpanzee
INTRODUCTION
Spider monkeys (family Cebidae, subfamily Atelinae, genus Ateles) are distributed throughout the Neotropical region from Mexico (23"N) to the southernmost reaches of the Amazon basin in Bolivia and Brazil (16"s) [Kellogg &
Goldman, 1944; Napier, 19761. They are one of the largest New World monkeys,
Received September 25, 1987;revision accepted January 13,1988.
M. McFarland Symington is now at Evolution and Human Behavior Program, Rackham Building,
University of Michigan, Ann Arbor, MI 48109-1070.Address reprint requests there.
0 1988 Alan R. Liss, Inc.
46 I Symington
with an adult weight of 7-9 kg [Coelho et al., 1976; Mittermeier, 19771. Some
controversy exists as to whether the four species ofAteles described by Kellogg and
Goldman 119441would be more properly classified as a single species [Hershkovitz,
19771. However, since Ateles geoffroyipanamensis and A . fusciceps robustus appear
to be sympatric in Panama [Rossan & Baerg, 19771 and preliminary findings
indicate some degree of cytogenetic heterogeneity among the South American
forms [Heltne & Kunkel, 19751, it seems appropriate to follow the more conservative taxonomy of Kellogg and Goldman a t this time [see also: Konstant et al.,
19851.
Spider monkeys have long been of special interest to primatologists, and more
recently, to behavioral ecologists, because of their anatomical and locomotory
similarities to apes [Erikson, 1963; Pilbeam, 19701 and their apparent social
convergence with chimpanzees [Klein, 1972; Cant, 1977; Wrangham & Smuts,
1980; Goodall, 1986; McFarland, 19861. Following Carpenter’s pioneering work on
Ateles geoffroyi in Panama [Carpenter, 19351, extensive field studies of spider
monkeys have been carried out at three sites in Central and South America [Ateles
belzebuth: Colombia, Klein, 1972; A . geoffroyi: Guatemala, Cant, 1977; A . paniscus: Surinam, van Roosmalen, 19801. In addition, a number of much shorter field
studies [Eisenberg & Kuehn, 1966; Richard, 1970; Durham, 1971; Coelho et al.,
1976; Izawa et al., 1979; Fedigan & Baxter, 1984; White, 19861and several studies
of captive animals [Eisenberg & Kuehn, 1966; Eisenberg, 1976; Rondinelli &
Klein, 19761 have been conducted.
These studies have provided biologists and anthropologists with remarkably
consistent descriptions of the gross features of the fission-fusion social organization
found in Ateles: individuals forage for fruit in subgroups or parties of variable size
and composition; the membership of these parties is drawn from a larger closed
social “network” [Klein, 19721 or “group” [van Roosmalen, 19801; and rarely, if
ever, are all members of a social group seen together. Knowledge of the details of
group structure and the proximate determinants of fission-fusion sociality in
spider monkeys remains incomplete, however, mostly because long-term data (i.e.,
>12 months) on known individuals have not been available. Since spatial
dispersion determines the frequency with which individuals interact and demography determines the number, age, and sex of potential interactants, both
represent important proximate determinants of social behavior and must be
considered in any complete analysis of social organization. In this paper some of
the results are reported from a long-term field study of Ateles paniscus chamek in
Peru, concentrating specifically on the demography of the study population and on
the ranging behavior of individuals. The longitudinal nature of this project,
combined with individual recognition, has allowed collection of data not previously
reported for Ateles.
MATERIALS AND METHODS
Study Site
All fieldwork was conducted in the immediate vicinity of the Cocha Cashu
Biological Station in the Manu National Park of southeastern Peru (11’ 51’S, 71”
19’ W). The park, established in 1973, is the largest rainforest park in the world,
comprising over 15,000 km2 on the western edge of the Amazon basin. Virtually
the entire area consists of several types of pristine tropical forest. Even prior to the
establishment of the park, most animal and plant populations were unaffected by
hunting or logging because of the low human population density in the region and
extremely limited outside access.
Spider Monkey Demography and Ranging I 47
The field station itself is located in lowland tropical moist forest [Holdridge,
19671 on the rich alluvial soils of the Manu River floodplain. The annual rainfall
of approximately 2,000 mm is markedly seasonal in its distribution. During the
continuous year I spent at Cocha Cashu, 1971 mm of rain fell, 80% of it during the
rainy season from October to April [Symington, 1987bl. This seasonality in rainfall
has profound effects on the phenology of fruit production at the site. An extensive
trail system comprising more than 28 km of trail covers a 5-7-km2 area
immediately surrounding the field station. A complete description of the climate
and vegetation a t the study site is given by Terborgh [1983].
Study Dates and Demographic Data
The study reported here was conducted during 21 months a t Cocha Cashu over
the 4-year period beginning in June 1982 and ending in June 1986. The first field
season (Jun+August 1982) was spent habituating the animals. Most observations
of spider monkeys during this period were made as unobtrusively as possible a t
large fruiting trees.
The second field season (June-September 1983) was spent learning to recognize all of the members of the study population. Because individuals did not travel
together as a cohesive unit, this process took somewhat longer than what is usually
necessary to learn all of the members of a troop of baboons or macaques. Individual
spider monkeys were easily recognizable, however, once the proper cues were
identified. These cues included the color, shape, and extent of bare skin around the
eyes and mouth; the presence, absence, or extent of golden hairs on the inner
thighs and buttocks [see Heltne & Kunkel, 19751; and scars, crooked fingers, sex,
and size. Within 2 months, individuals were rarely encountered that were not
recognizable. By the end of 4 months, it was clear that the trail system surrounding the field station completely contained the home ranges of two mutually
exclusive social groups of spider monkeys, as well as portions of the ranges of one
or two other groups.
In August 1984, the author returned to Cocha Cashu, and from September
1984 to August 1985 conducted a year-long study focusing on variability in
grouping behavior, in relation to the abundance and dispersion of fruit resources,
in the two groups of spider monkeys whose ranges were contained within the trail
system [Symington, in press]. During the course of that year only two individuals
(both peripheral females) were encountered that had not been recognized as
members of the study population during the previous field season. In June 1986 the
two study groups were censused a t Cocha Cashu.
The month of birth for all infants present in the study population in 1983 was
estimated from pelage and behavior reported previously for Ateles belzebuth
[Klein, 19721 and A . paniscus paniscus [van Roosmalen, 19801 and from direct
observations of growth and behavioral ontogeny in infants of known age (n =. 17)
(Table I). Thus, the demographic data presented below for group compositions and
births cover the 54-month interval from January 1982 to June 1986, while the data
for deaths and emigrations cover only the 36-month interval from July 1983 to
June 1986, when all of the members of the two study groups were recognized and
thus a particular individual’s absence could be detected.
Behavioral Data
Feeding, ranging, and activity data were gathered through full-day (N = 84)
and half-day (N = 59) follows of focal individuals. Each social group was the
subject of observations equivalent to five complete days (61.8 2 1.5 hours, N = 22)
each month except for December and January, when each group was followed only
48 i Symington
TABLE I. Characteristics Used In Estimating Infant Age*
Uu to age (mo)
DescriDtion
~
1
2
3
4-5
5-6
6-9
9-12
12-15
15-18
~
Pink palmar and plantar surfaces of hands and feet
Pelage sparse-infant appears gray
Tail rarely used to grasp mother’s body
Infant clings ventrally to mother’s body
Infant clings laterally to mother’s body
Infant rides dorsally-out of contact with mother <lo%
of time
Infant only rarely on mother’s back when feeding or
resting but usually <5 m away
Infant shows increasing independence but still rides on
mother’s back when traveling
Independent locomotion begins but infant still relies on
mother to carry it between trees or when tired
*Based on the author’s own observations of 17 infants of known age and previously published descriptions of
related species (see text).
once. All observations on a particular group were completed within a 10-day period
each month. Several females in each group served as “prime focals”; attempts were
made to follow these individuals every month or every other month. The rest of the
focal hours were distributed evenly over the remaining adult members of the
group. Males accounted for approximately 20% of the focal observations in each
month, slightly less than their abundance in the population. A total of 1,360 hours
of focal data were gathered during the 1984-1985 field season.
In order to simplify data collection and analysis, records were made of the
activity, location, and party size of the focal individual at 3-minute intervals
rather than continuously throughout the day. Although this is technically a form
of instantaneous sampling, the interval used was short enough that usually no
more than one transition occurred between consecutive samples; thus, the resulting data are essentially equivalent to that of focal-animal sampling for rate and
relative frequency estimates [Altmann, 19741. Activities were divided into four
mutually exclusive categories-feeding, resting, traveling, or other (mating,
fighting, etc.). Included in the category of feeding were all movements and
positional changes within a food tree. All food trees were tagged when visited and
then relocated for precise mapping and detailed measurements at a later time.
An individual’s location was determined with pace and compass measurements
relative to mapped food trees and trails. A 1-ha grid was superimposed on the
range maps produced from these locational data in order to simplify analysis. As
often as possible an individual was followed until it had settled into a sleep site for
the night; the sleep site was also recorded for any individual in the company of the
focal animal.
RESULTS
Group Composition
The home ranges and age-sex compositions of the two study groups during the
1984-1985 field season (excluding infants born during the year) are shown in
Figure 1.Members of one study group were never seen to associate with members
of the other study group or with individuals not recognized (with the exception of
the two peripheral females in the Lake group mentioned above). All of the
members of each group were seen together on one or two occasions; however, the
Spider Monkey Demography and Ranging I 49
Fig. 1. Map showing the home ranges and agehex compositions of the two study groups during the 1984-85
field season. Infants born during the year are not included. The location of the research station clearing is also
indicated.
amount of association between particular pairs of individuals within a social group
varied widely [Symington, 1987133.
Infants were defined as individuals not yet independently locomoting between
food sources. This period lasted for 17-21 months [Symington, 1987al. Individuals
were defined as juveniles from the time they began independent locomotion until
the time when they no longer always traveled with their mothers. The loosening of
the mother-daughter bond frequently coincided with the weaning of a younger
sibling; sons were observed to begin associating with the other males in their group
somewhat before this. Subadult males and females were visibly smaller than
adults. Females of unknown age were defined as subadult until their first
pregnancy. Males were defined as subadult until they were SO-90% the size of the
adult males in their group. Subadult males were probably sexually mature, and at
least one was reproductively active (see Dispersal and Philopatry, below).
50 I Symington
TABLE 11. Mortality and/or Dispersal By Sex and Age Class*
Sex
Age class
Male
Female
Adult
Subadult
Juvenile
Infant
Total
1
1
1
1
3
5
2
3
13
4
Undetermined
Total
4
6
3
5
18
*Based on the number of known individuals that disappeared from the study population, 1983-1986
Mortality
Table I1 shows the age-sex distribution of individuals that died or dispersed
from the study population between 1983 and 1986. Although it seems unlikely that
any of the eight infants and juveniles listed in Table I1 dispersed from the study
population, the body of only one of these immatures was observed: a 2-week-old
female infant being carried by its mother. Of the 15 infants born between August
1984 and August 1985, ten were still in their mothers’ company in June 1986. If
the four other infants that disappeared (but whose bodies were not seen) also died,
the mortality rate in the first year of life was 33%. Two infants that disappeared
during the author’s presence at the study site (in addition to the 2-week-old female
mentioned above) were last seen a t the ages of 4 weeks and 8 weeks respectively.
Mortality rates for subadult and adult animals may be substantially reduced
relative to those of younger animals. A single subadult male disappeared from the
study population over the 3-year period (his body was found), and there is evidence
that the large number of disappearances among subadult females may be due to
emigration rather than mortality (see Dispersal and Philopatry, below). Two of the
adult females, as well as the single adult male listed in Table 11, looked old at the
time of disappearance. They had lost much of the pigment in the skin around their
eyes, giving their faces a mottled appearance, and their necks appeared thin and
wrinkled. Both females had juvenile offspring that remained in the group after
their disappearance.
The third adult female had no offspring although she was fully adult. She
appeared pregnant in June 1985 (pregnancy is noticeable 1-2 months preterm).
One month later, she had an abortion or a stillbirth; a wet black object was
observed protruding from her vulva but when she was seen again the following day
there was no infant with her. She disappeared later that month.
Dispersal and Philopatry
There is strong circumstantial evidence that two of the five subadult females
listed in Table I1 emigrated to neighboring groups. One of these females was seen
interacting with six strange males at the northern boundary of the Lake group
range on the day before she disappeared. A second subadult female was seen being
chased by the males of her own group (East) and exhibiting all the behavioral signs
of estrus [Symington, 1987131during the week in which she disappeared. She, too,
was last seen at the northern boundary of her home range, well outside her usual
range, on the day before her disappearance. Both of these females had ceased to
travel with the adult females they had first been seen with as juveniles (assumed
to be their mothers) shortly before their disappearance. The other three subadult
females, all estimated to be between 4 and 5 years old, disappeared during periods
when the author was absent from the study site.
Spider Monkey Demography and Ranging I 51
In contrast, four males that were first seen as juveniles were observed to lessen
association with their (assumed) mothers around the age of four years and to begin
associating more with the adult males of their own group. All four of these males
were still present in the same group where they were first recognized in 1983 as of
June 1986, even though three of them were estimated to be approximately 6 years
old a t that time. In addition, at least one of these males was reproductively active,
having been observed mating with an adult female member of his group in October
1984, and again with a different female in June 1986.
Natality
Births occurred throughout most but not all of the year [Symington, 1987bl.
Interbirth intervals ranged from 25 to 42 months (34.5 & 5.8, mean & S.D., N =
17). Because the interval between the time when a female was first observed to be
receptive and the subsequent birth of her infant exceeded the author’s longest
period of absence from the study site [latency to conception 2 4 months, Symington,
1987b; gestation = 7.5 months, Eisenberg, 19731, the possibility that a female
could have conceived, gestated, given birth, and lost the infant without being
detected was unlikely. Much of the range of variation in interbirth intervals can be
explained by a mother’s rank and the sex of her previous offspring [Symington,
1987al.
Group Ranges
The home ranges outlined in Figure 1 include many peripheral areas not
frequently visited by most members of a social group. Figure 2a,b illustrates the
intensity of range use in each group according t o how many months a particular
quadrat was entered. These figures show that areas of overlap with neighboring
groups were used relatively infrequently and that the majority of a group’s ranging
was restricted to areas used by them exclusively.
The home ranges illustrated in these figures probably provide a good estimate
of the total area used by each group. Figure 3 shows the cumulative number of
quadrats entered by each group over the course of the year. The fact that the curves
reach an asymptote indicates that 153 and 231 ha accurately represent the total
range size of the East and Lake groups, respectively. Twenty-four hectares were
entered by members of both groups; this represents an overlap of 16% for the East
group and 10% for the larger Lake group.
Although the exact extent to which these ranges represent defended territories
is not yet known [Symington, 1987b1, four agonistic interactions were observed
between members of neighboring groups. These interactions consisted of the males
of one group vocalizing at and chasing the members of the other group. In only one
case was the interaction between members of the two habituated study groups. In
that particular instance, a party of three males from the Lake group was detected
by a larger mixed party from the East group in a quadrat where individuals from
both groups had previously been observed. Three adult males from the East group,
joined by two subadult males, succeeded in chasing away the three Lake group
males, who did not stop until they were 200-250 m within their own range. Figure
4 shows the location of all four intergroup disputes, as well as locations within the
home ranges of the Lake and East groups where spider monkeys were encountered
that did not belong to either study group.
Female Ranging Behavior
Patterns of range use by the adult female members of a group differed between
individuals. These differences are clearly illustrated by the ranging behavior of the
52 I Symington
Fig. 2. a: East group home range use, 1984-85. Grid squares are shaded according to the number of months
(out of a possible 11) that a focal individual was observed to enter that quadrat. b Lake group home range use,
1984-85, as above.
Spider Monkey Demography and Ranging / 53
-
Total-
153
Sep Oct N o v D I J F e b M a r A p r M a y J u n J u l Aug
Month
Fig. 3. Cumulative ranges of the two study groups showing the number of new quadrats entered during each
month.
prime focal females for which focal observations equaled or exceeded 50 hours.
Figure 5a shows the different patterns of range use for two females in the East
group, and Figure 5b shows the same for two females in the Lake group. The
shading indicates the number of months in which a female was observed to enter
a particular quadrat. These females were clearly concentrating the majority of
ranging within a fairly small proportion of the group's total home range.
The 80%core areas for these females were calculated by summing the smallest
number of different grid squares that accounted for 80% of the quadrats occupied
across months. The results for all eight prime focal females are summarized in
Table 111. Although the amount of time each female was observed varied, no
correlation was found between the 80% or 100% range for a female and the total
number of hours or the number of full days on which she was a focal individual.
The mean 80% core areas were 50 ha in the East group and 48 ha in the Lake
group. In the East group the core area was approximately one-third the size of the
total group range. In the larger Lake group it was approximately 20%.
Male Ranging Behavior
Although none of the study group males were observed for as many hours as
the prime focal females discussed above, the ranging behavior of males and
females can be compared for those males and females with approximately the same
number of focal hours. Owing t o less extensive observations on these individuals,
a proportionately greater amount of their 100%range was composed of quadrats
that were entered in only 1month. This sparseness of quadrat occupancy resulted
in a core area which was 100% correlated with total range when core area was
calculated as in the previous section. To allow for sparseness of quadrat occupancy,
an individual's core area was estimated as the minimum convex polygon containing all sleep sites and all grid squares entered in more than 1 month. Core areas
calculated in this manner tended to be slightly (but not significantly) larger than
those calculated by the 80% occupancy method for the 8 females in the previous
section (Wilcoxon matched-pairs, T = 6, P > .05, N = 8).
Figure 6a shows the minimum convex polygon (MCP)core areas for a male and
female of the East group, and Figure 6b shows the same for a male and female of
the Lake group. Males distributed their movements over a greater proportion of
the total group range than did females observed for a similar number of hours. The
data for all males and females observed 23-31 hours in a t least 4 months are
summarized in Table IV. The mean MCP core area for three Lake group males was
almost twice as large as that for four Lake group females (mean male MCP core
area = 64 ha; mean female MCP core area = 34 ha; Mann-Whitney U3,4 = 0;
54 I Symington
15 16 17 18 19 2 0 2 1 2 2 23 24 25 2S 27 2 8 2 0 30
U
N
0
S
T
U
V
W
Fig. 4. Map showing the location of intergroup interactions (XX)and sightings of individuals not belonging to
either group (*) relative to the home ranges of the two study groups (East group = dotted line, Lake group =
solid line).
P '= .028). The same relationship between male and female ranging patterns was
found in the East group (male = 57 ha; female = 28 ha; U3,3 = 0; P = .05).
Daily Path Length
Figure 7 shows the distribution of daily path lengths for all full day follows (N
84). There was no significant difference between groups in path length (Fl,82=
.18; P = 0.681, so the data from both groups were combined for Figure 7. Path
length varied over almost an order of magnitude, from 465 m to 4,070 m with a
mean of 1977 (S.E. = 99 m). A great deal of the variation in daily path length can
be explained by the size of party an individual was in, which in turn depends on the
abundance and distribution of available food [Symington, in press]. All path
lengths shown are for females, except one of 3,415 m recorded for a male in
November. This was 20% longer than the next longest path length recorded in that
month.
=
Spider Monkey Demography and Ranging I 55
TABLE 111. Ranging Behavior of Eight Adult Females*
Female
Group
100%
range
(ha)
EMM
JOD
DAR
BET
KAT
LAU
TIN
CIN
East
East
East
Lake
Lake
Lake
Lake
Lake
107
117
118
64
80
79
117
52
80%
core
(ha)
Proportion
of group
range
No.
focal
hours
52
45
54
46
41
53
66
34
.34
.29
.35
.18
.16
.21
.26
.14
55
80
54
50
99
75
62
52
No.
full
days
*Only those females who were the subject of 50 or more hours of focal observation from September 1984-August
1985 are included.
Activity Budgets
Figure 8 shows the activity budgets for the East and Lake groups over the
course of the 1984-85 field season. There were no consistent differences between
groups in the percentage of time spent feeding, resting, or traveling (Wilcoxon T =
19,25,24; P > .lo; N = 11). The “Other” category was omitted from Figure 8
because it accounted for less than 1%of the total activity budget in all months.
Consolidation of data across groups and across months allows calculation of an
average activity budget, as follows: feeding = 29% 2 2%; resting = 45% +- 1%;
traveling = 26% & 1%.
Significant differences existed between the activity budgets of males and
females. Males spent less time feeding (22.5%vs. 30.7%;Wilcoxon T = 7; P = .02;
N = 11) and more time traveling (30.0% vs. 20.9%; T = 7; P = .02) than did
anestrous females (i.e., females with infants). Males also spent less time feeding
(22.5% vs. 31.7%; T = 2; P < .005) than did females with older juvenile offspring
(18-36 months), but no differences were found in the amount of time spent
traveling by males and females with older juvenile offspring.
DISCUSSION
Group Composition
The highly dispersed social organization of Ateles [Klein & Klein, 1975;
McFarland, 19861 makes it difficult for a fieldworker to be sure that he or she is
familiar with all of the members of a social unit. The fact that females associate
preferentially with some females and little or not at all with others [Symington,
1987bl aggravates this problem. Unless one makes an effort to observe the
wider-ranging and more-difficult-to-follow males, it is possible to watch spider
monkeys for many months without encountering every member of a social group.
With this caveat, two previous studies have reported group compositions that
appear to be fairly complete. Klein’s [1972] study of Ateles belzebuth a t La
Macarena in Colombia involved two groups. One group included 5 adult males, 12
adult females, and 10 immatures, while the other group included 3 adult males, 11
adult females, and 6 immatures. The single group studied by van Roosmalen
[1980] included 3 adult males, 8 adult females, 1 subadult female, and 6
immatures. The two groups studied a t Cocha Cashu were very similar in composition, although somewhat larger, with 5 adult males, 15-16 adult females, 4
subadults, and 13-15 immatures. Groups at all three sites had 0.70-0.90 imma-
i/
56 I Symington
a
5
6
7
8
s
1 0 1 1 1 2 1 3 1 4 I S 1 6 1 7 111 1 s 2 0 2 1 2 2 2s 2 4 2 5 2 6 2 7 2 8 IB S O
I
J
K
L
Y
N
0
P
0
R
S
T
u
V
W
X
V
z
EMM
N
0
P
80% C m An.
=
52 ha
Q
R
S
T
U
V
W
X
V
Fig. 5 . a: Maps showing the home range use (shaded area) of two adult female members of the East group,
1984-85, relative to t h e total group range (solid line). Grid squares are shaded according to the number of
months the female was observed to enter a particular quadrat during focal observations. The letter S indicates
quadrats where the female was observed to sleep. Each female was the subject of approximately 50 hours of
observation distributed over the course of the year (see Table 111).b Maps showing the same as above for two
adult female members of the Lake group.
Spider Monkey Demography and Ranging / 57
b
/
58 I Symington
a
RUS
Q
I
J
K
L
Y
w
0
P
a
R
5
1
U
V
W
X
V
2
CLE
YCP Con A m a m
R
S
T
U
V
W
X
V
Fig 6. a: Maps showing the core areas, as calculated by the minimum convex polygon method (see text for
explanation), of an adult male (top) and an adult female (bottom) member of the East group. Shading and
legend as in Figures 5a,b b Maps showing the same as above for an adult male (top) and an adult female
(bottom) member of the Lake group
Spider Monkey Demography and Ranging I 59
b
VIC
I
J
K
L
Y
N
0
P
a
R
5
T
U
V
W
X
I
z
I
J
K
L
Y
Y
0
P
a
R
5
T
U
V
60 I Symington
TABLE IV. Comparison of Minimum Convex Polygon Core Areas of Males and
Females*,+
Lake
males
MCP core
area
(ha)
ROG
VIC
ROK
56
a5
51
Lake
females
NEL
SHO
LIND
POL
MCP core
area
(ha)
East males
MCP core
area
(ha)
RUS
ERN
RED
63
49
58
34
ia
41
43
East
females
CLE
ANN
TV
MCP core
area
(ha)
28
31
26
*See text and Figures 6a and 6b.
tBased on all individuals with between 23 and 31 hours of focal observation.
500
1200
1900
2600
3300
4
10
DAILY PATH LENGTH (in)
Fig. 7. Histogram showing the distribution of daily path lengths in 84 full-day follows of focal individuals
distributed evenly over the 12-month period from September 1984 to August 1985. Path length changes
seasonally depending on the average size of foraging parties.
turedadult female and 2.6-3.1 adult females/adult male. Thus, in overall demographic structure (i.e., group size and socionomic sex ratio), spider monkeys appear
to lie somewhere near the middle of the range reported for multimale groups of
cercopithecine primates [Melnick & Pearl, 19871. In the spider monkey population
a t Cocha Cashu, however, the female-biased sex ratio among adults appears t o be
present from birth [Symington, 1987al.
Causes of Mortality
If the four infants that disappeared from the study population, but whose
bodies were not seen, are assumed to have died, this would represent a 33%
mortality rate in the first 12 months. The only comparable data are from the
reintroduced population of AteZes geoffroyi on Barro Colorado Island, which had
only one documented case of infant mortality in 18 births [Milton, 19811. It is
extremely unlikely that predation is responsible for any deaths or disappearances
observed within the first 6 months in Ateles, since infants remain firmly attached
to their mother's ventrum for almost the entire period (see Table I). Early infant
mortality in humans is frequently due to nutritional insufficiency on the part of
the mother [Jain et al., 19701. If this is also the case in spider monkeys, the
extremely low population density of Ateles on BCI (2 indkm'), as compared with
that of Cocha Cashu [25-30 ind/km'; Terborgh, 1983; White, 19861, would
presumably result in reduced intraspecific feeding competition [see Symington, in
press] and thus decreased nutritional stress on females, which could account for
the much lower rate of infant mortality observed on BCI. It is noteworthy that the
Spider Monkey Demography and Ranging I 61
East Community
S
0
N O N F
M
A
Y
J
J
A
J
J
A
Month
Lake Community
S
0
N D N F
M
A
M
Month
0= Rest
= Feed
= Travel
Fig. 8. Monthly activity budgets, based on the activity of focal individuals recorded instantaneously a t
3-minute intervals throughout the day for a period equivalent to 5 days, for the two study groups, September
1984 to August 1985. Feeding time included the inspection of food, bringing it to the mouth, biting, chewing, and
swallowing, a s well as positional changes within a food tree.
one reported case of infant mortality occurred in February, which is a period of low
fruit abundance on BCI [Foster, 19823.
Higher rates of infant mortality have been reported for other nonhuman
primate species. Altmann et al. 119771 reported approximately 50% mortality in
the first 12 months for yellow baboons in Amboseli, and Cheney et al. [1981]
reported 60% mortality for vervet monkeys a t the same site. Glander [1980]
reported 100% infant mortality for offspring of primiparous females and approximately 30%infant mortality for the offspring of multiparous females in a 10-year
study of mantled howlers (Alouatta palliatu) in Costa Rica. Crockett and Rudran
[1987] reported a slightly lower mortality rate in the first 12 months (20%) in a
population of red howlers (Alouatta seniculus) in Venezuela.
Ecological factors such as predation and food stress were implicated as the
primary sources of infant mortality in the Amboseli primate populations, while
social factors such as infanticide ( A . seniculus) and agonistic interactions between
females (A. palliata) appear to have been responsible for much of the infant
mortality in the two howler monkey populations. Infant mortality in the Cocha
Cashu population of Ateles may be due to a combination of ecological and social
factors. Four of the five infants that died or disappeared within 12 months of their
birth were born to low-ranking mothers, who were defined as such on the basis of
their low priority of access to fruit and other food resources [Symington 1987al.
Mortality in the adult age class may be substantially reduced. If all four of the
62 I Symington
adults listed in Table I1 are assumed to have died rather than to have emigrated,
then the annual rate of mortality in this age class is approximately 3.3%. This
accords well with Glander’s [19801 estimate of 3.0% annual mortality among
prime-aged adult howler monkeys. Adult spider monkeys may be relatively
immune to predation, a t least by raptors, because of their large body size, and the
importance of parasites and disease as sources of adult mortality are unknown.
However, falls have been implicated in the deaths of three spider monkeys found
in the vicinity of Cocha Cashu (only one, the subadult male listed in Table 11,was
a member of the study population). The two other individuals were both females;
one was judged t o be quite old from the degree of wear on her teeth, and the other
had a leg bone which had been broken and then healed, presumably the result of
a previous nonfatal fall. Falls were found to be a significant source of mortality in
the more slowly and carefully locomoting howler monkeys on BCI [Milton, 19821,
and these observations indicate that falls may also be a problem for spider
monkeys a t Cocha Cashu.
Female Emigration and Male Natal Philopatry
Although only two of the subadult females listed in Table I1 were observed a t
the time of their disappearance, it seems likely that most, if not all, of these five
females left their natal groups to join neighboring groups. The two females who
were observed a t the time of disappearance emigrated to unhabituated groups,
which made it impossible to maintain subsequent contact with them. No immigrations into the study groups were observed between 1983 and 1986, but based on
observations of two subadult females who were present in the East group in June
1983 and who had their first infants in August 1984and April 1985,it seems likely
that there is a period of adolescent sterility between a female’s emigration from her
natal group and her first pregnancy.
The pattern of male natal philopatry and female dispersal that appears to
occur in Ateles is an unusual one in primates and in mammals in general
[Greenwood, 1980; Waser & Jones, 19831. The only other primate species in which
both male retention and female transfer have been reported are common and
pygmy chimpanzees; gorillas; red colobus; and, to some extent, hamadryas baboons, who, although they do not breed within the same one-male unit where they
were born, most often remain within the same clan [Pusey & Packer, 19871. It is
difficult to judge whether female dispersal is a cause or effect of male philopatry in
these species, but in common chimpanzees, red colobus, and hamadryas baboons,
male reproductive strategies appear to rely heavily on cooperation, as may also be
the case for spider monkeys.
Some of the most complete data on the subject of dispersal and philopatry come
from the long-term studies of common chimpanzees (Pan troglodytes schweinfurthii) at Gombe and Mahale. It is the norm a t both sites for males to breed in their
natal groups (or communities, as they are referred to in the chimpanzee literature)
[Pusey, 19793, and for females to emigrate upon sexual maturity [Nishida, 1979;
Goodall, 19861. At Gombe, however, although males have never been seen to
transfer, fanales have been observed breed in their natal communities, frequently
after a short period of residence in, or a series of visits to, a neighboring
communit: It is too early to say a t this point whether male spider monkeys at
Cocha Cashu ever leave their natal groups to reside elsewhere, or whether females
ever remain in or return to their natal groups to breed. Evidence from the social
relationships observed among adult females at Cocha Cashu does not support this
second possibility [Symington, 1987bl.
Spider Monkey Demography and Ranging I 63
Interbirth Intervals
The average interbirth interval of 34.5 +- 5.8 months found in this population
of spider monkeys is one of the longest that has been reported for a non-ape
primate species, but it is consistent with previous estimates of interbirth interval
in free-ranging Ateles. The average length of seven interbirth intervals on BCI was
31.9 +- 3.0 [Milton, 19811, and an average of 4 years (range 46-50 months) was
given for A. paniscus paniscus in Surinam, although the number of intervals this
figure was based on was not reported [van Roosmalen, 19801. In baboons and both
species of howler monkeys, interbirth intervals are considerably shorter [21,22.5,
and 17 months, respectively; Altmann et al., 1977; Glander, 1980; Crockett &
Rudran, 19871.
The conservation implications of the long interbirth interval reported here for
Ateles deserve special attention. Because they reproduce so slowly, populations are
even more vulnerable than other primates to hunting and other habitat disturbances. Even now in much of Peru and Bolivia, spider monkeys simply are not
found outside of protected parks and reserves [Freese et al., 19821. Increasing
human encroachment on much of Amazonia can only lead to further population
declines and extinctions within the next 10 years.
Differential Ranging Behavior of Males and Females
The ranging patterns of male and female spider monkeys at Cocha Cashu
appear to differ considerably. Females restrict a great deal of their ranging to a
“core area” of approximately 50 ha, which is 20-33% the size of the total group
range. Core areas calculated for males are almost twice this size. The term “core
area” is not meant to imply any exclusivity of use in this context. Indeed, in order
for the group ranges to accommodate the number of females that they do, overlap
between these core areas must be substantial. The existence of these core areas
does imply, however, that females are, a t least to some extent, spacing themselves
out.
Very similar differences in male and female ranging have been previously
described for the common chimpanzees at Gombe [Wrangham & Smuts, 19801. In
these analyses, female chimpanzees were found to have core areas ranging from
24% to 40% of the total community range, and these core areas were, just as in
spider monkeys, almost exactly one half the size of those calculated for males (2.1
vs. 4.1 km?. Male chimpanzees a t Gombe and Mahale participate in territorial
border patrols and have been observed to cooperatively attack and injure members
of neighboring communities [Goodall et al., 1979; Nishida et al., 19851. Although
only four intergroup interactions have been observed thus far in this project,
cooperative territorial defense appears to occur in spider monkeys and may be
responsible for the increased travel time and larger ranges of males in this species.
Implications for the Evolution of Fission-Fusion Social Organization
The results of the study reported here indicate that female spider monkeys do
not travel together in cohesive groups; instead, they concentrate their ranging in
individual core areas dispersed throughout the group range. Receptive females are
dispersed in time as well as in space because of their long interbirth intervals and
lack of birth seasonality. Thus, although the size and sex ratio of spider monkey
social groups are no different from those of most multimale primate groups, the
strategies used by male spider monkeys to gain access to receptive females need to
be considerably different from the strategies used by males in these other species.
Since female groups cannot be joined, defended, or monopolized, males must either
64 I Symington
defend individual females or, alternatively, defend a territory containing resources
likely to attract females.
Male spider monkeys seem to have adopted the latter strategy, but because
females range over relatively large areas (see Table 1111, the size of territory that
could be defended by a single male would be unlikely to contain even a single
receptive female. However, since cooperation between individuals has been shown
to disproportionately increase the economically defendable area by lowering the
per-capita cost of territorial defense [Brown, 19821, male spider monkeys are in a
position to benefit from cooperating with other males to jointly defend a territory
large enough to contain the ranges of several females. And although kinship is not
a necessary precondition for the evolution of cooperative behavior [Wrangham,
19821, male spider monkeys may gain inclusive fitness benefits by remaining in
their natal groups and cooperating primarily with relatives.
The above scenario applies equally well to the evolution of fission-fusion social
organization in common chimpanzees [McFarland, 19863. The underlying reason
for the similarity in chimpanzee and spider monkey social organization appears to
have much to do with the way food resources are distributed. Both species spend a
large proportion of time feeding on ripe fruit, a high-quality resource that is
distributed in discrete, variably-sized patches that are scattered throughout a
group’s home range [Klein & Klein, 1977; Wrangham, 1977; Symington, in press].
The amount of intragroup feeding competition involved in exploiting a resource
distributed in this manner places a great deal of pressure on females to forage
solitarily, thus, the existence of female core areas in each species [Wrangham,
1979; Wrangham & Smuts, 1980; this study].
The same energetic considerations that result in the semisolitary nature of
female chimpanzees and spider monkeys appear to be of less importance to the
males of a social group than are the reproductive advantages of cooperation. Some
of these reproductive advantages are beginning t o be understood for common
chimpanzees [Goodall, 1986; Nishida & Hiraiwa-Hasegawa, 19871. The next step
toward a more complete understanding of the unusual social organization shared
by chimpanzees and spider monkeys will be to determine whether the reproductive
advantages gained by males are similar in Ateles and Pan.
CONCLUSIONS
1. In Ateles, individuals travel in parties of highly variable size and composition. The membership of these parties is drawn from a larger, discrete social unit
whose size and composition depends upon the normal demographic processes of
birth, immigration, death, and emigration, and is thus analogous to a typical
multimale primate group. Two groups whose compositions were known completely
consisted of 5 adult males, 15-16 adult females, 4 subadults, and 13-15 immatures. Individuals were observed to associate non-agonistically only with other
members of their own group and never with members of another group.
2. The two study groups had annual home ranges of 153 and 231 ha. Overlap
with neighboring groups was on the order of 10-15%, and there were some
indications of territorial defense, a t least on the part of males.
3. Ten of fifteen infants born over a 13-month period were still with their
mothers one year later. If all five missing infants died, then mortality in the first
year of life was approximately 33%.Mortality and/or emigration among adults was
approximately 3% per year.
4. Longitudinal data on known individuals provide evidence for male natal
philopatry and female emigration at sexual maturity in this population.
5. Interbirth intervals were 34.5 & 5.8 months.
Spider Monkey Demography and Ranging I 65
6. Ranging behavior and activity budgets of males and females were very
different. Females traveled less and restricted much of their ranging to an
individual “core area” 20-33% the size of the total group range, whereas males
spent more time traveling and appeared to range more evenly over the entire area
occupied by the group.
7. The very similar social organizations of chimpanzees and spider monkeys
may result from similar selection pressures, i.e., high levels of intragroup feeding
competition that prevent females from foraging in stable groups and reproductive
advantages gained by males through cooperation.
ACKNOWLEDGMENTS
I would like to thank J. Symington for his invaluable assistance in the field
and the Direccih General de Forestal y de Fauna, Lima, for permission to work in
Manu; the Evolution and Human Behavior Program at the University of Michigan, which kindly provided me with office facilities during the preparation of this
manuscript; and J. Terborgh, D. Rubenstein, P. Grant, and F. White, who supplied
helpful comments on previous drafts. Financial support from the Organization of
American States, Princeton University,
- . and World Wildlife Fund-US is gratefully
acknowledged.
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