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Atelinae adaptations Behavioral strategies and ecological constraints.

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AMERICAN JOURNAL OF PHYSICAL. ANTHROPOLOGY 88515-524 (1992)
Atelinae Adaptations: Behavioral Strategies and
Ecological Constraints
KAREN B. STRIER
Department of Anthropology, University of Wisconsin-Madison,
Madison, Wisconsin 53706
KEY WORDS
ality
Atelin, Alouatta, Diet, Ranging behavior, Season-
ABSTRACT
Comparisons between the four genera that make up the
Atelinae reveal two distinct behavioral patterns, one in which energy expenditure is minimized (Alouatta) and one in which energy intake is maximized
(Lagothrix,Ateles, and Brachyteles). Among the atelins, Lagothrix and Ateles
devote over 75% of their annual feeding time to fruit, while Brachyteles devotes between 50% and 67% of their feeding time to leaves. Pronounced
seasonality in the Atlantic coastal forest inhabited by Brachyteles may be
responsible for its more folivorous diet. Alouatta falls in the body size range of
Lagothrix and is much smaller than Ateles and Brachyteles. Nonetheless,
Alouatta is more folivorous than sympatric atelins. The atelins also share a
rapid, suspensory mode of locomotion that appears to enable them to minimize travel time between widely dispersed fruit sources. Alouatta, by contrast, employs a slower, but more energetically efficient, quadrupedal locomotion. Ranging patterns among the Atelinae are consistent with both diet and
locomotor abilities: Atelins travel daily distances up to 5,000 m; Alouatta
ranges are much shorter. Further distinctions are evident in Atelinae grouping patterns. Alouatta remains in small cohesive groups that occupy home
ranges less than 60 ha in size. Both Lagothrix and Ateles have large groups
that fission to reduce the costs of intragroup feeding competition when preferred fruits occur in small patches within much larger community ranges.
While greater reliance on low-energy foods such as leaves may release
Brachyteles from similar competitive constraints, their tendency toward fluid
grouping associations is consistent with the pursuit of a frugivorous
diet. o 1992 WiIey-Liss, Inc.
The Atelinae are the largest and most ern Amazon, Alouatta occurs with Ateles. In
widely distributed New World primates. the western Amazon, Alouatta overlaps with
Four genera make up the subfamily: Lago- both Ateles and Lagothrix. In the Atlantic
thrix, or woolly monkeys, with two species; coastal forest of southeastern Brazil, AlAteles, or spider monkeys, with four species; ouatta is sympatric with Brachyteles, the
Brachyteles, or muriquis, a monotypic ge- only other Atelinae whose range extends so
nus; and Alouatta, or howler monkeys, the far from the equator (Wolfheim, 1983).
Morphological and behavioral analyses of
most diverse with seven species (Table 1).
Alouatta has the most extensive geo- ateline phylogenetic relationships reveal
graphic distribution, ranging from southern two distinct patterns that distinguish AlMexico through northern Argentina and ouatta from the other three genera, collecthroughout the Amazon basin. It is sympat- tively referred to as the atelins (Fig. 1).Alric with a t least one other Atelinae except in
the most extreme parts of its ranges.
Received July l l, 1990; accepted September 12,1991
Throughout Central America and the east0 1992 WILEY-LISS, INC
516
K.B. STRIER
species tend to be more folivorous than
smaller ones. Their absolutely greater nutriGenus
Species
tional requirements necessitate the incluLagothriz
Zagotricha
sion of abundantly available foods, such a s
flavicauda
leaves, in their diet, while their relatively
Ateles
geof f r oyi
lower basal metabolic rates permit them to
fusciceps
belzebuth
rely on these lower quality foods, which repaniscus
quire longer passage times to extract energy
Brachyteles
arachnoides
and nutrients (Gaulin, 1979).
Alouatta
belzebul
Nonetheless, the relationship between
fusca
seniculus
body size and diet among the Atelinae is not
palliata
clearcut. Body weights among female
coibensis
Atelinae average from 4.5 kg for Alouatta
pigra
caravo.
fusca to 9.5 kg for Brachyteles (Fig. 2). There
is substantial variation within each genus
From Mittermeier et al.. 1988.
as well as overlap between Alouatta and
Lagothrix and between Ateles and Brachyouatta appears to follow a strategy that teles. Although recent weight data from freeminimizes energy expenditure, while the ranging Brachyteles indicate that it is only
atelins appear to maximize energy intake slightly larger than Ateles (Lemos de Sa and
(Rosenberger and Strier, 1989). These strat- Glander, in preparation), it is much more
egies have been associated with folivory in folivorous (Fig. 3). Alouatta and Lagothrix
Alouatta (Milton, 1980) and frugivory in Ate- are the smallest genera, but Alouatta is
les (Klein and Klein, 1977; van Roosmalen, more folivorous than Lagothrix and Ateles
1980; Symington, 1988a) and more recently and in some cases Brachyteles. Brachyteles
Lagothrix (Defler, 1987; Soini, 1987). In falls within the range of folivory observed in
Brachyteles, however, this dichotomy is con- Alouatta; although it is much larger, it is not
founded; although Brachyteles resembles proportionately more folivorous.
One explanation for these unexpected
Alouatta in its folivorous diet, it resembles
the other atelins in its ranging and grouping findings is that dietary representations
patterns. While these latter resemblances based on annual averages obscure the imsupport the generally accepted phylogenetic portance of seasonal variability. When seaseparation between Alouatta on the one sonal variation in diet is examined in the
hand and Ateles, Brachyteles, and Lagothrix three genera (Ateles, Brachyteles, and Alon the other, the strong craniodental and ouatta) for which published data exist (Tadietary similarities between Brachyteles ble 21, it is clear that categorizations such as
and Alouatta (Zingeser, 1973) suggest at “frugivorous” and “folivorous” are misleadleast a functional convergence between ing. For example, the Ateles groups devoted
an average of 75-78% of their feeding time
them.
This paper reviews field data on ateline to fruit, but in one study where rainfall was
diets, ranging parameters, and grouping highly seasonal (Chapman, 19871, fruit conpatterns from a comparative perspective. sumption dropped and leaf consumption
The effects of body size, locomotor abilities, rose dramatically during certain months
and seasonality are considered because of (see also van Roosmalen, 1980). Both
their significance in understanding the be- Brachyteles study populations fall within
the range of Alouatta in the proportion of
havioral strategies of the Atelinae.
feeding time devoted to fruit and leaves. In
BODY SIZE AND DIET
fact, the variation between these genera is
Body size is a n important predictor of diet less profound than that between different
among closely related species (Kay, 1984). Alouatta populations.
The importance of seasonality to diet is
Although all primates greater than 1 kg in
body weight consume both fruit and leaves evident from comparisons between the six
(Hladik, 1978, 1981; Richard, 19851, larger Alouatta studies in which annual diet and
T A B L E 1. Recognized Atelinae species
517
ATELINAE ADAFTATIONS
Lagothrix
Alouatta
Brachyteles
Ateles
I;
Fig. 1. Phylogenetic relationships of Atelinae (From Rosenberger, 1981).
12.0
11.5
h
9
g.-Eul
v
~
8
m
2
,f!
Q
3
11.0
10.5
9.0
9.5
-
-I
8.58.0
7.5
7.0
-
/achnoides
belzebufh
--
geoffroyi
6.5-
5.0 454.0 6.0
5.5
3.5
Alouatta
Lagothrix
Ateles
Brachyteles
Genus
Fig. 2. Variation in adult female body weights. Points represent mean values for each species; bars
indicate range of variation for each genus. Mean values and ranges taken from Ford and Davis (this
issue); four adult female weights for Brachyteles uruchnoides from Lemos de Sa and Glander (in preparation) are included.
rainfall have been reported (Fig. 4).The average proportion of leaves included in the
diet was inversely related to rainfall (Spearman rank correlation, rs = 0.89, n = 6 ,
P < 0.051, supporting the suggestion that
interspecific differences in Alouatta diets
are smaller than habitat differences within
species (Crockett and Eisenberg, 1987). A
similar trend appears to occur within the
atelins (Fig. 41, although the relationship
between rainfall and folivory in Ateles and
Brachyteles is not significant (rs = -0.80,
n = 4,P > 0.05).
One way to distinguish further between
the effects of seasonality on dietary strategies is to examine data obtained on sympat-
K.B. STRIER
518
folivory in Brachyteles and the fact that Alouatta fusca is more folivorous, on average,
than more equatorial Alouatta species indiBrachyteles
cate the importance of seasonal food availability in the Atlantic forest where these
species live. Alouatta caraya, studied in
northern Argentina, where annual rainfall
averaged 1,200 mm, exceeded all other
Atelinae by devoting an average of 76% of
their annual feeding time to leaves (Table 2;
Zunino and Rumiz, 1986).
Suggesting that Brachyteles employs a
strategy of maximizing energy intake by exploiting fruit when it is available does not
minimize the importance of leaves in its
Ateles
diet. As was indicated above, all Brachyteles
populations studied to date consume substantial quantities of leaves, as expected
from body size energetics and reflected in
their craniodental morphology (Zingeser,
1973).Nonetheless, Brachyteles differs from
k I I 8I I 9I I 1I 0 1 1I 1 ’ iI 2 Alouatta in its digestive strategy. Alouatta
is characterized by slow passage rates,
Mean Female Body Weight(kg)
which allow for the efficient absorption of
plant nutrients, while Brachyteles, by conFig. 3. Proportion of feeding time devoted to leaves
by mean female body weight. Bars represent range of trast, exhibits a surprisingly rapid passage
rate that resembles that of both Ateles and
annual averages reported for each genus, as indicated in
Table 2. Lugothrix diet was estimated from Soini (1987). Lagothrix (Milton, 1984b). Although fast
passage time in Brachyteles has been attributed to a strategy emphasizing rapid turnric taxa studied under similar ecological con- over of low-quality foods (Milton, 1984b), a
ditions. Figure 5 shows the diets of three more parsimonious explanation may be that
sets of sympatric Atelinae: Ateles and Al- it is a shared characteristic retained from a
ouatta at two sites and Brachyteles and Al- frugivorous atelin ancestor.
ouatta at one site. As indicated previously,
Ateles is the most frugivorous, and Brachy- LOCOMOTION AND RANGING BEHAVIOR
Intergeneric comparisons of locomotor
teles falls within the range of both Alouatta
palliata populations. However, Brachyteles patterns support the distinction between Alis nearly 50% more frugivorous than sym- ouatta and the other atelins, including
patric Alouatta fusca studied during the Brachyteles. Brachyteles resembles the
same time period a t Fazenda Montes Claros. other atelins in its mode of suspensory locoAlthough the absolute proportion of feeding motion, which permits more rapid long distime these species devote to fruit is lower, tance travel than does the quadrupedal locothe difference between these species’diets is motion employed by Alouatta. Cant (1986)
proportionate to that between Ateles and Al- discussed the importance of rapid travel beouatta palliata a t the two sites represented. tween widely dispersed fruit sources for AteThese comparisons reveal a fundamental les and suggested that the high energy exdifference between the feeding strategies of pended per unit time in suspensory travel
Brachyteles and Alouatta. Even under con- (Parsons and Taylor, 1977) is compensated
ditions of similar food availability, Alouatta for both by the energy-rich fruits that can be
is more folivorous than Brachyteles, whose exploited and by the actual time saved in
annual diet includes a greater proportion of travel. Suspensory locomotion may confer a
leaves than the diets of other atelins. Both similar advantage in Brachyteles, permit-
I
>
519
ATELINAE ADAPTATIONS
TABLE 2. Seasonality in Atelinae diets (ranges are compiled or estimated from variation reported by authors)'
Rainfall
(mm)
Species
Ateles belzebuth
(Klein and Klein, 1977)
Ateles geoffroyi
(Chapman, 1987, 1988a,b)
Ateles paniscus
(van Roosmalen, 1980)
(Symington 1987, 1988a)
Brachyteles arachnoides
(Milton, 1984a)
(Strier, 1986, 1991a)
Alouatta caraya
(Zuni0 and Rumiz, 1986)
Alouatta fusca
(Mendes, 1989)
Alouatta palliata
(Glander, 1978)
(Milton, 1980)
(Estrada, 1984)
(Chapman,l987)
Alouatta seniculus
(Gaulin and Gaulin, 1982)
Percent fruit
Mean
Range
Percent leaves
Mean
Range
?
83
78-100
7
3-22
900-2,400
78
0-100
12
0--80
2,000-2,400
1,971
83
75
58-96
55-99
8
16
1-23
<I-38
1,263
1,186
21
32
4-59
13-66
67
51
41-93
28-78
1,200
24
?
76
?
1,186
16
-I--30
71
-64--78
1,431
2,730
4,500
900-2,400
13
42
51
29
-9--15
10--65
0-80
0-55
64
48
49
49
-59--67
-25-44
20-100
0-95
1,942
42
?
53
?
'For duration of studies, see Rosenberger and Strier (1989).
6 -1
5-
0
Y
E
0
LT
Alouatta
0 Atelins
0
4-
3-
0
0
0
0
0
0
21 -
0
0
0
4
5
0
0
1
2
3
Rank
Rainfall
6
Fig. 4. Rank rainfall and degree of folivory in Alouatta and two atelins, Brachyteles and Ateles.
Rainfall and annual averages for each species are taken from sources in Table 2 when reported annual
rainfall variation was 1500 mm.
ting it to include a larger proportion of fruit Roosmalen, 1980), although average daily
in its diet than sympatric, quadrupedal Al- ranges are generally lower. Alouatta travels
substantially less each day and utilizes
ouatta.
Table 3 shows data on ranging parame- smaller home ranges. Brachyteles is interters compiled from a subset of longterm mediate, exhibiting a high degree of instudies on Atelinae. The two most frugivo- traspecific variation. Both day range and
rous genera, Ateles and Lagothrix, have the home range were greater at the site where
longest average day ranges and the largest Brachyteles was more frugivorous. Furtherhome ranges; Ateles have been reported to more, Brachyteles at Fazenda Montes Claros
travel daily distances of up to 5,000 m (van exploited a home range over twice as large,
K.B. STRIER
520
80
60
2
.-9
0
2
40
LL
3?
20
0
BCI, Panama
Milton (1981)
Santa Rosa, CR
Chapman (1987)
FMC, Brazil
Strier (1986)
2,730 mm
900-2,400 rnrn
1156 rnm
Fig. 5. Dietary comparisons between sympatric atelins (Ateles and Brachyteles) and Alouatta. Site,
source, and annual rainfall are given below each comparison.
TABLE 3. Rangingparameters and group size
Species
Lagothriz lagothricha
(Defler, 1987)
(Nishimura, 1990)
Ateles paniscus
(Symington, 1988a,b)
Brachyteles arachnoides
(Miton, 1984a)
(Strier, 198713, 1991a)
Alouatta fusca
(Mendes, 1989)
Alouatta palliata
(Milton, 1980)
(Estrada, 1984)
Alouatta seniculus
(Gaulin and Gaulin, 1982)
Day
range (m)
Home
range (ha)
Group
size
Percent
fruit
3,000
?
740
450/350
20-23
45/13
?
?
1,977
1531231
40/37
75
630
1,283
70
168+
7
26
21
32
523
8
7
16
443
123
31
60
17
9
42
51
706
22
9
42
and traveled on average over twice as far
daily as sympatricAlouatta. Thus it appears
that both the locomotor and the ranging patterns among the Atelinae support a division
between Alouatta and the atelins that is
consistent with their dietary strategies.
Differences in group size may confound
both intra- and interspecific comparisons.
Across primates with similar diets, larger,
heavier groups generally require larger food
supply areas (Milton and May, 1976; Clutton-Brock and Harvey, 19771, but how large
the area is is also determined by food density. For example, in Symington’s (1988b)
study of two Ateles groups of roughly similar
size, home ranges differed by nearly 50%
depending on habitat quality.
GROUPING PATTERNS
Grouping patterns among the Atelinae
show considerable variability. Alouatta
groups are typically smaller than atelin
groups (Table 3), although group fissioning
in atelins may result in feeding parties that
are quite similar in size to those ofAlouatta.
On a continuum with fluid groups at one
extreme and cohesive groups at the other,
Ateles and Lagothrix fall at one end, while
Alouatta falls at the other. Fluid atelin
groups are believed to reflect the patchy na-
ATELINAE ADAPTATIONS
Minimizers
ENERGY
521
Maximizers
Bracbytetes, Ateles, Lagotbrix
Alouatta
3
folivory
'-4
Diet
-b
frugivory
short
-4
Day Range
-b
long
small
-4
Home Range
-b
large
-4
Grouping
-b
fluid
cohesive
Fig. 6. Schematic representation of behavioral divergence in Atelinae.
ture of their fruit resources. Atelin groups typical of this genus than previous observafission to avoid feeding competiton at small tions a t Montes Claros have suggested.
It is possible that Brachyteles can remain
fruit patches and reunite a t larger patches
where a greater number of individuals can in more cohesive groups than other atelins
feed together. A number of studies have because their ability to include greater proshown a strong positive relationship be- portions of leaves in their diet mediates the
tween food patch size and subgroup, or constraints of feeding competition at patchy
party, size in Ateles (Klein and Klein, 1977; resources. This proposition, however, is unSymington, 1988a; Chapman, 1988a). Be- likely for two reasons. First, other atelins
cause Alouatta includes a greater proportion retain their fluid grouping patterns while
of more evenly distributed leaves in its diet, relying heavily on leaves when fruits are
it does not face comparable levels of intra- seasonally scarce (see above). Second, longigroup feeding competition, and groups can tudinal data indicate that Brachyteles may
remain cohesive. The physical constraints of maintain more fluid associations when
patch size may still, however, be important large fruit patches are unavailable or when
in determining feeding associations in oth- groups become too large to feed together in
erwise cohesive groups (see, e.g., Leighton fruit patches (Strier, 1989; Strier et al.,
1992).
and Leighton, 1982; Strier, 1989).
Despite their intraspecific variability,
Brachyteles appear to resemble the atelins
DISCUSSION
in their fluid grouping patterns. At Fazenda
Despite a high degree of intrageneric variBarreiro Rico, one Brachyteles group comprising seven individuals had fluid associa- ation, Lagothrix and Ateles are clearly distions (Milton, 1984a). Groups of 14 tinct from Alouatta in their feeding, rangBrachyteles at Fazenda Esmeralda (Lemos ing, and grouping patterns (Fig. 6). The
de Sa, 1988) and 26 a t Fazenda Montes atelins are more frugivorous, have longer
Claros (Strier, 1987a,b)traveled as cohesive day ranges and larger home ranges, and
units. However, a s the size and biomass of have more fluid grouping associations than
the Montes Claros group have increased Alouatta. These differences persist in comover the last 8 years, the group has begun to parisons between sympatric species, sugshow increased tendencies toward fission- gesting that these genera pursue divergent
ing (Strier, 1989, 1991b; Strier et al., 1992). strategies that are consistent with their food
It may be that the fluid groups observed by passage rates, divergent modes of locomoMilton (1984a) at Barreiro Rico are more tion, and evolutionary history.
522
K.B. STRIER
Brachyteles is more folivorous than the
other atelins, but, in sympatric comparisons
with Alouatta, it is more frugivorous than
would be expected from its large body size,
just as Ateles is more frugivorous than sympatric Alouatta in less seasonal habitats.
The ranging behavior of Brachyteles reflects
the rapid bursts of long-distance travel associated with suspensory locomotion between
high-quality dispersed fruit resources; its
fluid grouping patterns resemble those of
other atelin groups, which fission to avoid
feeding competition a t fruit patches.
Folivory in Brachyteles may be regarded
as a secondary adaptation imposed on an
otherwise atelin strategy involving maximizing energy intake (see Rosenberger and
Strier, 1989). This reasoning follows Rosenberger and Kinzey’s (1976) “critical function” hypothesis, which posits that what an
animal must be able to do during periods of
food shortage is more important to understanding its functional morphology than its
overall annual diet. From this perspective,
the morphological and behavioral adaptations for folivory in Brachyteles are critical
during seasonal fruit shortages. They are
not, however, necessarily representative of a
folivorous strategy in which energetic expenditure is restricted by an energy-poor
diet (but see Milton, 1984a).
Seasonality in food availability may also
account for the high variation in folivory
across Alouatta. It does not, however, obscure the divergence between Alouatta and
atelin behavior. All Atelinae are more folivorous in more seasonal habitats, but Alouatta
is even more so. The fact that Alouatta is
sympatric with a t least one other atelin
throughout most of its range suggests that
niche divergence between these genera is an
important feature of their evolutionary relationships.
Comparative approaches are essential to
elucidate behavioral ecological relationships
(Clutton-Brock and Harvey, 1984). They
also provide a basis for evaluating phylogenetic relationships reconstructed from morphological traits (Rosenberger and Strier,
1989). It is difficult, for example, to interpret the significance of folivory in Brachyteles without comparative data on other
Atelinae in diverse habitats. Sympatric
comparisons between closely related species
are particularly important in providing a basis to distinguish between diet and overall
behavioral strategies.
ACKNOWLEDGMENTS
I am grateful to the Brazilian government
and CNPq for permission to conduct research in Brazil and to Dr. Celio Valle for his
sponsorship and support. E. Veado, F.D.
Mendes, and J. Rimoli contributed to the
longitudinal data collection in the field; L.
Johnson and M. Steele assisted in the preparation of the illustrations. The field research was supported by NSF grants BNS
8305322, BNS 8619442, and BNS 8958298;
the Fulbright Foundation; grant 213 from
the Joseph Henry Fund of NAS, Sigma Xi,
the World Wildlife Fund, and the L.S.B.
Leakey Foundation. A version of this paper
was presented at the 58th Annual Meeting
of the American Association of Physical Anthropologists. I thank P. Garber and W.
Kinzey for inviting me to participate in their
symposium and P. Garber, S. Ford, and the
anonymous reviewers for their comments on
the manuscript. R.M. Lemos de Sa and K.E.
Glander generously permitted me to cite
their recent (and as yet unpublished) weight
data for Brachyteles.
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