American Journal of Primatology 73:11891198 (2011)

REVIEW ARTICLE
Influence of Climatic Variables, Forest Type, and Condition on Activity Patterns
of Geoffroyis Spider Monkeys Throughout Mesoamerica
NIA SA
PEZ3,
LEZ-ZAMORA1, VICTOR ARROYO-RODRIGUEZ2, OSCAR M. CHAVES2, SO
NCHEZ-LO
ARTURO GONZA
FILIPPO AURELI4,5, AND KATHRYN E. STONER2
1
Division de Posgrado, Instituto de Ecologa, Xalapa, Veracruz, Mexico
2
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autonoma de Mexico (UNAM), Morelia, Michoacan, Mexico
3
Centre Especial de Recerca en Primats, Universitat de Barcelona, Barcelona, Spain
4
Research Center in Evolutionary Anthropology and Palaeoecology, School of Natural Sciences and Psychology, Liverpool John
Moores University, James Parsons Building, Byrom Street, Liverpool, United Kingdom
5
Instituto de Neuroetologa, Universidad Veracruzana, Xalapa, Mexico

Understanding how species cope with variations in climatic conditions, forest types and habitat amount
is a fundamental challenge for ecologists and conservation biologists. We used data from 18
communities of Mesoamerican spider monkeys (Ateles geoffroyi) throughout their range to determine
whether their activity patterns are affected by climatic variables (temperature and rainfall), forest
types (seasonal and nonseasonal forests), and forest condition (continuous and fragmented). Data were
derived from 15 published and unpublished studies carried out in four countries (Mexico, El Salvador,
Costa Rica, and Panama), cumulatively representing more than 18 years (221 months, 43,645 hr) of
behavioral observations. Overall, A. geoffroyi spent most of their time feeding (38.4714.0%, mean7SD)
and resting (36.6712.8%) and less time traveling (19.8711.3%). Resting and feeding were mainly
affected by rainfall: resting time increased with decreasing rainfall, whereas feeding time increased
with rainfall. Traveling time was negatively related to both rainfall and maximum temperature.
In addition, both resting and traveling time were higher in seasonal forests (tropical dry forest and
tropical moist forest) than in nonseasonal forests (tropical wet forest), but feeding time followed the
opposite pattern. Furthermore, spider monkeys spent more time feeding and less time resting (i.e.,
higher feeding effort) in forest fragments than in continuous forest. These findings suggest that global
climate changes and habitat deforestation and fragmentation in Mesoamerica will threaten the survival
of spider monkeys and reduce the distributional range of the species in the coming decades. Am. J.
Primatol. 73:11891198, 2011.
r 2011 Wiley Periodicals, Inc.
Key words: activity patterns; Ateles geoffroyi; climate change; fragmentation; rainfall; seasonality;
temperature
INTRODUCTION
Activity patterns (time spent feeding, traveling,
resting, and socializing) provide information on how
animals interact with the environment and invest time
and energy for survival and reproduction [Dunbar,
1988]. Studying activity patterns is crucial for better
understanding why a given taxon can survive in some
habitats but not in others [Dunbar et al., 2009], and for
indentifying the areas that are suitable for a species
within their geographical range [Korstjens et al., 2006].
As a consequence of accelerating global climate change
as well as unprecedented deforestation rates in tropical
regions during the last decades [Anderson et al., 2008;
FAO, 2011], it is fundamental to understand the ability
of species to develop behavioral modifications in their
activity patterns to cope with both climatic change and
habitat deforestation [Dunbar et al., 2009].
In many primate groups, activity patterns may
be affected by climatic variables [Dunbar, 1998;

r 2011 Wiley Periodicals, Inc.

Dunbar et al., 2009; Korstjens et al., 2006;

Wiederholt & Post, 2010], seasonality [Doran, 1997;
Korstjens et al., 2006], habitat characteristics [Isbell
et al., 1998], or some combination of these factors.
Ambient temperature and rainfall, and the seasonality of these characteristics, are the main climatic
variables driving activity patterns in many primates
[e.g., Ateles: Korstjens et al., 2006; Gorilla and
Contract grant sponsor: Consejo Nacional de Ciencia y Tecnologa (CONACYT), Mexico; Contract grant numbers: 200551043; 2006-56799.
Correspondence to: Arturo Gonza
lez-Zamora, Divisio
n de
Posgrado, Instituto de Ecologa A.C. km 2.5 Antigua Carretera
a Coatepec No. 351. 91070 Xalapa, Veracruz, Mexico.
E-mail: toztlan@yahoo.com.mx

Received 18 November 2010; revised 19 July 2011; revision

accepted 22 July 2011
DOI 10.1002/ajp.20989
Published online 6 September 2011 in Wiley Online Library (wiley
onlinelibrary.com).

 lez-Zamora et al.
1190 / Gonza

Colobus: Korstjens & Dunbar, 2007; Korstjens et al.,

2010; Pan: Lehmann et al., 2007; Theropithecus:
Dunbar, 1998]. For instance, to deal with climatic
stresses, such as high temperatures and/or
drought, primates frequently reduce traveling time
because this is an energetically costly activity,
allowing them to reduce energy expenditures
[Dunbar et al., 2009; Korstjens et al., 2006] and
to increase their resting time to avoid overheating
[e.g., Theropithecus gelada: Dunbar, 1988, 1992a;
Papio hamadryas: Stelzner, 1988; Pan troglodytes:
Kosheleff & Anderson, 2009].
Rainfall can also affect activity patterns of
primates because of the positive relationship
between rainfall and resource availability [Bronikowski
& Altmann, 1996; Deshmukh, 1984], particularly of
ripe fleshy fruits [i.e., the main food source of
frugivorous primates, such as spider monkeys;
lez-Zamora et al.,
Di Fiore et al., 2008; Gonza
2009; Stevenson & Link, 2010]. Primates need
to adjust their diet and activity patterns to cope
with resource scarcity in habitats and/or during
periods with lower rainfall regimes [e.g., Kaplin
et al., 1998; McConkey et al., 2002; Stevenson et al.,
2000].
Resource availability also can affect among
forests with different climatic seasonality because
vegetation structure and composition differ among
them [Gentry, 1982]. In contrast to tropical wet forests
(TWF) that show little seasonality, fleshy fruit availability may be limited in more seasonal forests [e.g.,
tropical moist forest (TMF), tropical dry forest (TDF)],
particularly during the dry season [Bunker & Carson,
2005; Murphy & Lugo, 1995]. Anthropogenic activities, such as deforestation, forest fragmentation and
logging, also can affect vegetation structure and
composition, modifying resource availability for primates [e.g., Arroyo-Rodrguez & Mandujano, 2006;
Chapman et al., 2000]. The density of larger trees
is typically lower in smaller forest fragments,
particularly of those species that are used as food
resources by frugivorous primates [Arroyo-Rodrguez
& Mandujano, 2006; Chaves et al., 2011a; Dunn et al.,
2009]. Therefore, because larger trees produce higher
amounts of fruits [Chapman et al., 1992], smaller
fragments contain a lower food supply for frugivorous
primates than larger fragments [Arroyo-Rodrguez &
Mandujano, 2006; Chapman et al., 1992; Dunn et al.,
2009]. These changes in food availability ultimately
can affect activity patterns. For example, time spent
feeding by gelada baboons (T. gelada) in Ethiopia is
inversely related to spatial and temporal food availability in three different habitats [i.e., two plateaus of
open grassland mosaics at different altitudes and with
distinct plant compositions and one African savannah;
Iwamoto & Dunbar, 1983]. In summary, activity
patterns seem to be a function of vegetation and
climatic characteristics [e.g., Caraco, 1979; Dunbar,
1992a,b; Dunbar et al., 2009].

Am. J. Primatol.

Activity patterns also depend on the social

system in which the species live [Dunbar et al.,
2009; Korstjens et al., 2006; Wrangham et al., 1993].
For instance, the ecological constraints model predicts that larger groups deplete food patches faster
than smaller groups, and hence individuals in larger
groups have to visit more patches each day, increase
day ranges, spend more time traveling, and in some
cases, expand their home ranges [Chapman, 1990;
Janson & Goldsmith, 1995; Milton, 1984; Wrangham
et al., 1993]. Primates that live in social systems with
a high degree of fissionfusion dynamics, such as
spider monkeys (Ateles spp.), adjust their subgroup
size to local food availability [Aureli et al., 2008;
Kummer, 1971] and annual rainfall (an indirect
measure of habitat quality) [Korstjens et al., 2006].
In these systems, individuals that belong to the same
community are rarely together, but they fission and
fuse in smaller subgroups of variable composition.
These fissionfusion dynamics are effective in flexibly managing activity patterns as larger subgroups
do not experience greater ranging costs than smaller
subgroups [Asensio et al., 2009]. Although Korstjens
et al. [2006] suggest that community size is a
stronger determinant of time budgets than subgroup
size, they actually find that the percentages of time
spent feeding and moving do not correlate with
community size or subgroup size using a large data
set on Ateles spp. Thus, unlike group size in
relatively cohesive groups, community size and
subgroup size are unlikely to play a major role in
the activity patterns in species characterized by a
high degree of fissionfusion dynamics.
Korstjens et al. [2006] investigated factors
affecting activity patterns of the entire genus Ateles;
however, research focusing on single species is
necessary to have a more detailed understanding of
their ecology in changing habitats. Although some
published studies document activity patterns of
Ateles geoffroyi in continuous forests of Mesoamerica
[e.g., Chapman, 1987a,b; Richard, 1970], no studies
to date have assessed the impact that climatic
variables, forest types, and forest condition may
have on activity patterns through the distributional
range. This information has critical evolutionary and
conservation implications. From an evolutionary
perspective, throughout its distributional range,
spider monkeys have adapted to certain areas or
comfort zones [sensu Anderson et al., 2008]
characterized by climatic niches to which the species
is tolerant [Korstjens et al., 2006]. These niches are
characterized by relatively little variation in regional
climatic conditions which allowed spider monkeys to
adapt to their activity patterns, diet, and social
behavior to the specific resource availability and
environmental characteristics found in different
forest types [Anderson et al., 2008; Dunbar et al.,
2009]. Unfortunately, predictive models about the
potential impact of climate change in Mesoamerica

Activity Patterns of Spider Monkeys / 1191

indicate that temperature will increase and precipitation will decrease in the next 2050 years
[Anderson et al., 2008]. These climatic alterations
could promote drastic changes in vegetation composition and structure as well as changes in phenological cycles, with important implications for animal
behavior, population sizes, and distribution [Hannah
et al., 2001; Parmesan, 2006]. Understanding how
species cope with variations in climatic conditions,
forest types, and conditions across their distributional range is, therefore, critical for assessing their
ability to cope with upcoming climatic alterations
and unprecedented anthropogenic disturbances.
In this study, we gathered data from a number
of studies and analyzed them to determine how the
activity patterns of A. geoffroyi are influenced by
ambient temperature, rainfall, forest type (i.e.,
seasonal and nonseasonal forests), and forest condition (i.e., continuous and fragmented). According to
socioecological models, we hypothesized that spider
monkeys can adjust their activity patterns in order to
deal with variation in climatic variables, forest types,
and forest conditions [e.g., Dunbar et al., 2009;
Korstjens et al., 2006; Wiederholt & Post, 2010].
Because resting is an energy-saving activity, we
predicted resting would be positively related to
ambient temperature and negatively related to
rainfall because of the inferred direct relationship
between rainfall and food availability [e.g.,
Bronikowski & Altmann, 1996; Deshmukh, 1984].
Similarly, owing to differential food availability, we
expected spider monkeys to spend more time resting
in seasonal forests than in nonseasonal forests and
in forest fragments than in continuous forests.
Traveling was expected to follow the opposite
pattern of resting to reduce travel-related energy
expenditures. Finally, as spider monkeys often
increase the time devoted to consumption of fibrous
and hard-to-digest plant items (e.g., leaves) when
availability and/or diversity of fleshy ripe fruits is
scarce [e.g., in forest fragments and during the dry
lez-Zamora
season: Chaves et al., 2011a,b; Gonza
et al., 2009], we predicted time spent feeding would
be negatively related to rainfall and higher in
seasonal and fragmented forests to compensate for
food scarcity under these situations.
METHODS
Literature Review
We reviewed available studies (published articles, book chapters, and unpublished theses) on
activity patterns of A. geoffroyi up to April 2011.
Initially, we used internet databases (SCOPUS, ISI
Web of Science, PrimateLit, Google scholar) to locate
relevant published work. We then identified additional studies cited within this primary literature
that had not been published. We attempted to obtain
as much of these unpublished data in the form of

theses or gray literature through university libraries

and by directly contacting the authors. Our data base
included 15 studies from 18 communities of
A. geoffroyi in four countriesMexico, El Salvador,
Costa Rica, and Panamarepresenting more than
18 years (221 months, 43,645 hr) of behavioral
observations (Table I). From all studies included in
the data base, we obtained the percent of time (or
scans) primates spent on feeding, resting, and
traveling (see the sampling method of each study in
Table I). We also calculated the percent of time
devoted to other activities (including social activities)
(Table I). However, we did not include data from this
category in our analyses because different authors
used different definitions for this category. When
available, we also obtained the size of the study
communities (Table I), but this factor was not
included in our analyses because, as expected, it
was not related to time resting (R2 5 0.02, P 5 0.66),
feeding (R2 5 0.00, P 5 0.95), or traveling (R2 5 0.00,
P 5 0.90). All data were obtained with noninvasive
methods, complying with the American Society of
Primatologists principles for the ethical study and
treatment of nonhuman primates.
Climatic Variables, Forest Type, and Forest
Conditions
Following Gentry [1982], we grouped forest
types into seasonal (TMF: 2,0002,800 mm rain/year
and TDF: o2,000 mm rain/year) and nonseasonal
forest (TWF: 42,800 mm rain/year). Based on the
size of the forest, we identified two forest conditions:
continuous and fragmented. All forest fragments
were very small (o31 ha), whereas continuous
lez-Zamora
forests were greater than 1,500 ha [Gonza
et al., 2009; Table I]. Additionally, we considered the
following three climatic variables that were available
for the time period of each study, using data from the
meteorological station located closest to each study
site: average monthly rainfall (PMEAN), maximum
temperature (TMAX), and minimum temperature
(TMIN). We selected these climatic variables because
both rainfall and temperature are important components of primate activity patterns models [e.g.,
Dunbar, 1992a; Dunbar et al., 2009; Korstjens &
Dunbar, 2007; Korstjens et al., 2006; Lehmann et al.,
2007]. We could not consider the effect of variation in
rainfall and temperature across the year because we
did not find relevant data to calculate an appropriate
measure for all the studies.
Data Analyses
Percent data were transformed to proportions
and proportion data were arcsine transformed. Then,
we tested if they were normally distributed (Shapiro
Wilk test: P40.11 for all data). To test the effect
of local climatic variables on activity patterns,
we performed three separate multiple regression

Am. J. Primatol.

Am. J. Primatol.

LT, Mexico
LT, Mexico
LT, Mexico
LT, Mexico
LT, Mexico
MA, Mexico
MA, Mexico
MA, Mexico
RA, Mexico
ZPO, Mexico
ZPO, Mexico
NOR, El Salvador
BCI, Panama
BCI, Panama
BCI, Panama
PL, Mexico
PL, Mexico
SR, Costa Rica
HLI, Costa Rica
ZBFE, Costa Rica
ZBFE, Costa Rica
CNP, Costa Rica

1
2
3
4
5
6A
6B
6C
6D
6F1
6F2
7
8
9
10
11E
11W
12
13
14A
14B
15

TWF (44,000)
TWF (44,000)
TWF (44,000)
TWF (44,000)
TWF (44,000)
TWF (2,880)
TWF (2,880)
TWF (2,880)
TWF (2,880)
TWF (2,880)
TWF (2,880)
TWF (43,000)
TMF (2,600)y
TMF (2,600)y
TMF (2,600)y
TDF (1,365)y
TDF (1,365)y
TDF (1,531)y
TMF (o2,500)
TWF (44,000)
TWF (44,000)
TWF (44,000)

D&W (12, )
D&W (11, 660)
D&W (11, )
Dry (6, 164)
Dry (6, 96)
D&W (15, 188)
D&W (15, 146)
D&W (15, 162)
D&W (15, 126)
D&W (15, 236)
D&W (15, 152)
Wet (4, 180)
D&W (12, )
D&W (12, )
D&W (13, 1,200)
D&W (47, )
D&W (47, )
D&W (33, 335)
D&W (11,)
D&W (16, )
D&W (16, )
D&W (12, )

Season
(study length)c
FAS
FAS
FAS
FAS
FAS
FAS
FAS
FAS
FAS
FAS
FAS
FAS & ISS
FAS
FAS & ISS
ISS
ISS
ISS
FAS
ISS
FAS
FAS
FAS

Recording
methodd
291.1
484.2
396.1
366.8
305.7
277.6
277.6
277.6
277.6
277.6
277.6
284.0

223.8
178.3
113.0
113.0
92.4

216.4
216.4
402.71

PMEAN
27.0
28.0
28.0
25.6
29.3
35.7
35.7
35.7
35.7
35.7
35.7
32.5

31.1
31.3
33.5
33.5
31.9

32.8
32.8

TMAX
22.1
22.5
21.3
20.2
22.4
12.9
12.9
12.9
12.9
12.9
12.9
22.6

23.2
24.2
14.1
14.1
22.1

18.5
18.5

TMIN

Climatic variables

FF (25)
FF (25)
FF (25)
FF (25)
FF (25)
CF (331,200)
CF (331,200)
CF (331,200)
CF (1,450)
FF (31)
FF (14)
CF (430)f
CF (41,500)
CF (41,500)
CF (41,500)
CF (ca. 3,700)
CF (ca. 3,700)
CF (410,800)
FF (170)
CF (700)
FF (300)
CF (41788)

Forest
condition
(size, ha)e
20.2
16.0
20.7
49.0
34.0
24.3
43.1
50.9
35.7
28.32
26.7
52.0
61.0
50.1
51.7
41.0
45.0
24.1
31
41
21
38.5

Rest
36.7
67.0
54
40.0
38.0
49.4
23.2
34.7
38.1
60.2
64.8
16.0
11.0
25.6
39.3
36.0
35.0
33.5
25
24
48
45

Feed
41.1
17.0
25.3
11.0
27.0
13.9
7.8
5.4
6.9
4.5
4.9
32.0
28.0
18.7
31.1
23.0
20.0
32.6
41
12
16
15.8

Travel
2
0
0
0
1
12.4
25.9
9.0
19.3
6.98
3.6
0
0
2
34.2
0
0
9.8
3
23
15
0.7

Other

Activity pattern (%)

19
25
30
21
19
23
26
28
27
28

21
16
41
42
24

Community
size

lez-Zamora [2003]; 5. Sa
nchez-Lopez [2008]; 6. Chaves et al. [2011b]; 7. Argueta-Rivas and RiveraReferences: 1. Bentez-Rodrguez [1989]; 2. Jimenez-Huerta [1992]; 3. Garca-Ordun
a [2002]; 4. Gonza
Hernandez [2004]; 8. Richard [1970]; 9. Milton [1993]; 10. Campbell [2000]; 11. Ramos-Fernandez & Ayala-Orozco [2003]; 12. Chapman et al. [1989]; 13. McDaniel [1994]; 14. Lindshield [2006];
15. Weghorst [2007]. References 15 studied the same community but in different time periods; Reference 6 studied three different groups in the Montes Azules Biosphere Reserve (A 5 Station site, B 5 Las
Ceibas site, C 5 7 site, and D 5 Reforma Agraria) and in two small fragments (F1 5 Batrizal private reserve and F2 5 Los Nidos private reserve); Reference 11 studied two different groups (E 5 East and
W 5 West). Reference 14 (A 5 undisturbed forest, B 5 disturbed forest).
a
Study sites: LT, Los Tuxtlas; MA, Montes Azules; RA, Reforma Agraria; ZPO, Zamora Pico de Oro; NOR, Normanda, BCI, Barro Colorado Island; PL, Punta Laguna; SR, Santa Rosa; HLI, Hacienda Los
Inocentes; ZBFE, La Zota Biological Fied Station.
b
Forest type: TWF, tropical wet forest; TMF, tropical moist forest; TDF, tropical dry forest. Samples with (y) represent seasonal forests, whereas those without (y) represent nonseasonal forests.
c
Season: D & W, dry and wet; Study length: months and hours. Samples with asterisk () were not included in the analyses.
d
Recording method: FAS, Continuous Focal Animal Sampling; ISS, Instantaneous Scan Sampling.
e
Forest condition: FF, forest fragment; CF, continuous forest.
f
This was considered continuous because the vegetation is similar to the original continuous forest, it is the largest fragment in the region, and has been protected for 10 years [see Argueta-Rivas & RiveraHernandez, 2004]. () data unavailable.

Study sitea

Ref.

Forest type
(rainfall, mm)b

TABLE I. Description of Study Sites and Activity Patterns of Ateles geoffroyi in Each Sample

lez-Zamora et al.
1192 / Gonza

Activity Patterns of Spider Monkeys / 1193

analyses. In each analysis the dependent variable was

the activity (resting, feeding, or traveling) and the
independent variables were PMEAN, TMAX, and TMIN.
Variance inflation factor (VIF) values above four
indicate possible multicollinearity between independent variables [Chatterjee et al., 2000]. In our models,
VIF never reached this value. In addition to the
complete models (i.e., including all three climatic
variables), we used backward stepwise regression
analyses and the Akaikes Information Criterion to
select the best model for each dependent variable
[Motulsky & Christopoulos, 2003].
We used students t-tests to assess possible
effects of forest type and forest condition on each
activity. Considering continuous forests, we tested
differences among seasonal (N 5 7 data points) and
nonseasonal forests (N 5 12). To test the effect of
forest condition, we compared continuous forest
(N 5 6) and fragments (N 5 6) of TWF, the only
forest type for which we had data for forest
fragments (Table I). We considered three samples
from the same group in the same fragment of Los
Tuxtlas (studies 1, 2, and 3 in Table I) as independent, because they were separated in time between
3 and 12 years, and both community sizes and
climatic conditions were notably different across the
three samples (see Table I). Although we used the
same independent variables for multiple tests, we did
not apply Bonferroni corrections to our results
because we only made three different tests (one per
activity), so we did not increase so much the
probability of the statistical error type I (rejects a
true Ho) by chance. Also, by applying Bonferroni
corrections, we could increase the probability of the
statistical error type II (do not reject Ho when is
false) [see Nakagawa, 2004].
Only data covering the entire year (i.e., annual
samples) were used in the statistical analyses. When
data were available only for the dry or wet season
(N 5 3; see Table I), the study was only used for
providing some general descriptive statistics. All
tests were performed with JMP (version 7.0, SAS
Institute Inc.) and STATISTICA (version 5.5, StatSoft) software.
RESULTS
Across sites and groups, spider monkeys spent
most of their time feeding (38.4714.0%, mean7SD)
and resting (36.6712.8%) and less time traveling
(19.8711.3%) and in other activities (7.6710.0%)
(N 5 22 data points from different groups or from the
same group but during different sampling periods;
Table I). However, there was large variation in time
spent in each activity among groups and sites
(Table I). Particularly, feeding time ranged from
11% in a continuous TMF (BCI, Panama) to 67% in a
TWF fragment (Los Tuxtlas, Mexico); resting ranged
from 16% (Los Tuxtlas, Mexico) to 61% (BCI,

Panama); and traveling ranged from 4.5 to 41.1%

in two TWF fragments in Mexico (Table I).
The best regression model indicated that resting
was mainly affected by PMEAN; when rainfall
decreased across studies monkeys spent more time
resting (Table II). Feeding time followed the opposite
pattern: the best model indicated that feeding was
positively associated with PMEAN (Table II). Finally,
traveling time was negatively related to both PMEAN
and TMAX (Table II). Importantly, the amount of
variance explained by these climatic factors (R2)
differed greatly among the models: it was only 20%
for resting and 26% for feeding, but 86% for traveling
(Table II).
The percentage of time spent resting differed
between forest types, being significantly higher in
seasonal forests than in nonseasonal forests
(t 5 2.30, df 5 17, P 5 0.03; Fig. 1A). Similarly,
traveling time was significantly higher in seasonal
forests than in nonseasonal forests (t 5 3.10,
df 5 17, P 5 0.006; Fig. 1A). Feeding time followed
the opposite pattern, being significantly higher in
nonseasonal forests than in seasonal forests (t 5 2.57,
df 5 17, P 5 0.02; Fig. 1A).
Activity patterns differed between continuous
forest and forest fragments (Fig. 1B). Although the
percent of traveling time did not differ significantly
between forest conditions (t 5 1.15, df 5 10,
P 5 0.28), monkeys spent more time feeding
(t 5 3.00, df 5 10, P 5 0.01) and less time resting
(t 5 4.19, df 5 10, P 5 0.002) in forest fragments
than in continuous forest (Fig. 1B).
DISCUSSION
Overall, our results demonstrate that there is a
large variation in time spent in each main activity
across communities of spider monkeys (A. geoffroyi)
throughout Mesoamerica, and that a large proportion of this variation can be explained by annual
rainfall, ambient temperature, forest types (seasonal
and nonseasonal), and conditions (continuous and
fragmented). These results are consistent with
recent socioecological studies on primates, and
support the idea that temperature, rainfall, and
degree of seasonality are important climatic variables driving the activity patterns of Neotropical
primates [Chaves et al., 2011b; Dunbar et al., 2009;
Korstjens et al., 2006; Wiederholt & Post, 2010]
and Paleotropical primates [Bronikowski &
Altmann, 1996; Dunbar, 1992b; Dunbar et al., 2009].
Furthermore, consistent with Chaves et al. [2011b],
our findings also indicate that spider monkeys can
change their activity patterns in forest fragments.
In agreement with our predictions, we found
that, in habitats with lower rainfall, spider monkeys
spend more time resting and that resting time was
higher in seasonal forests. Similarly, as predicted,
traveling time was strongly and negatively related to

Am. J. Primatol.

 lez-Zamora et al.
1194 / Gonza

TABLE II. Influence of Climatic Factors on Activity Patterns of Spider Monkeys (Ateles geoffroyi) Found in
Mesoamerica (We Indicate Both the Complete Models and the Most Parsimonious (i.e. Best Modelsa)).
Activity

R2adj

AIC

Factorsb

Parameterc

Fratio

Complete models
Resting

0.20

69.6

Feeding

0.15

67.6

Traveling

0.85

91.2

Intercept
PMEAN
TMAX
TMIN
Intercept
PMEAN
TMAX
TMIN
Intercept
PMEAN
TMAX
TMIN

0.328
0.0004
0.025
0.010
0.691
0.001
0.004
0.005
2.114
0.001
0.046
0.002

0.38
1.24
1.28
0.84
0.75
1.99
0.17
0.37
4.77
5.01
4.59
0.31

0.713
0.239
0.224
0.416
0.469
0.070
0.871
0.717
0.001
o0.001
o0.001
0.763

Best models
Resting

0.20

71.1

Feeding

0.26

71.3

Traveling

0.86

93.1

Intercept
PMEAN
Intercept
PMEAN
Intercept
PMEAN
TMAX

0.720
0.001
0.490
0.001
1.988
0.001
0.043

10.3
4.70
7.05
6.13
12.2
30.0
89.3

o0.001
0.048
0.010
0.027
o0.001
o0.001
o0.001

a
The best models were selected through backward stepwise regression analyses. We indicated the adjusted R2 and Akaikes Information Criterion for each
regression model.
b
Climatic factors: PMEAN, average monthly rainfall; TMAX, maximum temperature; TMIN, minimum temperature.
c
The sign of each parameter indicates the relationship (positive or negative) between each continuous factor and the response variable.

Am. J. Primatol.

Activity pattern (%)

60
50

Non-seasonal

Seasonal

40

**

30
20
10
0

Rest

70

50

Feed

Continuous forests

60

Activity pattern (%)

ambient temperature. Food availability for primates

(including spider monkeys) increases with rainfall
[Di Fiore et al., 2008; Kaplin et al., 1998; Stevenson,
2001; Stevenson et al., 2000], and those living in
seasonal forests are exposed to more stressful
conditions [e.g., temporal food scarcity, drought,
high ambient temperature; Murphy & Lugo, 1995;
Stoner & Timm, 2004]. Therefore, it is reasonable to
expect that, just like we found, monkeys devote more
time resting in seasonal forest and where rainfall is
lower. This could be an energy-saving strategy to
cope with resource limitations during the driest
periods and/or in the driest forests [Chaves et al.,
2011b]. In addition, as traveling and feeding represent energetically costly activities [Dunbar, 1988,
1992a; Dunn et al., 2009; Korstjens et al., 2006],
reducing travel time when ambient temperature is
higher could allow primates to minimize energy costs
and feeding effort owing to overheating [e.g., Dunbar
et al., 2009].
Interestingly, feeding time was positively related
to rainfall but not significantly to temperature,
suggesting that this activity could be more constrained by differences in food availability. Similarly,
feeding time was significantly higher in nonseasonal
forests (TWF). Spider monkeys have been reported
to spend more time feeding during the rainy season
[Chaves et al., 2011b; Felton et al., 2009], possibly
because feeding is an energetically costly activity
that needs to be minimized during the dry season

Travel
Forest fragments

*
**

40
30
20
10
0

Rest

Feed

Travel

Fig. 1. Activity patterns (average percentage of time7SE) of

Ateles geoffroyi according to forest type (seasonal and nonseasonal) (A) and forest condition (continuous and fragmented) (B).
Significant differences are indicated with asterisks (Po0.05;
Po0.01).

Activity Patterns of Spider Monkeys / 1195

[Dunbar et al., 2009; Korstjens et al., 2010]. Felton

et al. [2009] and Chaves et al. [2011b] also interpret
greater feeding time in the rainy season as a strategy
for spider monkeys to take advantage of peak
seasonal foods allowing them to ingest surplus
energy and store it as fat in preparation for the
impending period of food scarcity. Other primate
species accumulate fat during peaks of fruit abundance [Pongo pygmaeus: Knott, 1998; Lemur catta
and Eulemur sp.: Simmen et al., 2010; Lagothrix
lagotricha cana: Peres, 1994; Ateles paniscus: Milton,
1998; A. chamek: Wallace, 2005], which is a logical
strategy for animals experiencing fluctuating food
supply [Felton et al., 2009]. Further information on
nutritional ecology and energetic strategies of
A. geoffroyi is needed to test the fat accumulation
hypothesis.
In contrast with our prediction, traveling time
was negatively related to rainfall. We expected a
positive relationship between the two variables,
as low rainfall is usually associated with low
fruit availability [Bronikowski & Altmann, 1996;
Deshmukh, 1984]. Under these circumstances, a
reduction in traveling could be an energy-saving
strategy. The negative relation is likely owing to the
fact that, when more fruit sources are available,
the monkeys spend less time traveling because the
distance among food patches decreases. This idea is
supported by Chaves et al. [2011b], as they also find
that traveling time tended to be higher during the
dry season. However, Asensio et al. [2009] do not find
that traveling time changed with season, and argued
that monkeys adjust their subgroup sizes (i.e.,
smaller subgroups are found during the dry season)
to avoid travel costs associated with larger subgroups.
Nevertheless, because most of the studies analyzed in
our study did not provide data on average subgroup
sizes, we cannot determine the relative influence of
subgroup size on activity patterns.
In TWF (i.e., the only forest type for which we
had data for forest fragments), forest condition
affected the activity patterns of spider monkeys.
Specifically, monkeys spent more time feeding and
less time resting in forest fragments than in
continuous forest, and hence the feeding effort
[sensu Cavigelli, 1999] of monkeys was higher in
fragments. Similar differences in activity patterns
have been reported for Chiropotes satanas in Brazil
[Boyle & Smith, 2010; Boyle et al., 2009] and
Alouatta palliata in Mexico [Dunn et al., 2009].
Dunn et al. [2009] relate the variations in activity
patterns (and feeding effort) to the differences in diet
between groups: leaf consumption is higher in the
group inhabiting the smallest fragment, and this
group visits more food sources resulting in more
traveling, more feeding, and less resting. They argue
that this could be explained by the lower amount of
energy these primates probably gain per food patch,
as well as the need to diversify food sources when

consuming leaves (i.e., to obtain the best complement

of nutrients and avoid an overload of particular
toxins or digestibility-reducing compounds). Our
findings are consistent with this idea, as we found
in a previous study (using a data base similar to
that in this article) that spider monkeys have a
lez-Zamora
more folivorous diet in fragments [Gonza
et al., 2009], which could force them to diversify their
diet [see Chaves et al., 2011a; Felton et al., 2009;
Milton, 1981, 1998] and spend more time feeding and
less time resting. However, it is important to gather
data on activity patterns in fragmented seasonal
forests (TMF and TDF), to assess whether it is
possible to generalize this finding to other forest
types.
Conclusions and Recommendations for
Conservation
Our findings indicate that spider monkeys in
Mesoamerica can adjust their activity patterns in
order to cope with changes in temperature, rainfall,
forest type (seasonal and nonseasonal), and condition
(continuous and fragmented). However, it is still
unclear whether these behavioral adjustments will
insure their health and survival in the long term,
especially if we consider the current high rates of
deforestation and the impact that climate change will
have on Mesoamerican ecosystems in the next
few decades [Anderson et al., 2008; FAO, 2011;
Wiederholt & Post, 2010]. Studies evaluating the
relationships between changes in activity patterns
associated with climatic variables, forest type and
condition, and the demographic consequences (e.g.,
birth and death rates) in spider monkeys populations
are urgent for their conservation.
Based on our results, if ambient temperatures
increase and annual rainfall decrease approximating
the figures predicted by the climate change models
for Mesoamerica [Anderson et al., 2008], spider
monkeys will probably increase the enforced resting
time [i.e., resting needed for digestive and/or thermoregulatory purposes; Korstjens et al., 2010] limiting the time monkeys can devote to other critical
activities, such as feeding, traveling, and social
behavior. This could reduce their population sizes,
limit the distributional range of the species, and even
threaten their long-term survival in the coming
decades.
It is alarming that A. geoffroyi has been recently
listed as Endangered by the IUCN, because habitat
loss and fragmentation across its range has been
severe and the species has been estimated to have
declined by as much as 50% over the past 45 years
[Cuaron et al., 2008]. In addition, it has been
suggested that A. geoffroyi could be one of the first
Mesoamerican primate species to become locally
extinct in human-modified landscapes [Garber
et al., 2006]. The remaining populations are isolated

Am. J. Primatol.

 lez-Zamora et al.
1196 / Gonza

in few reserves and different-sized forest fragments

[Cuaron et al., 2008]. Our results demonstrate that
feeding effort is higher in forest fragments than in
continuous forests, and studies on other primates
indicate that an increase in feeding effort may
negatively affect fitness by increasing stress levels
[Papio anubis: Sapolsky, 1986; L. catta: Cavigelli,
1999; A. palliata: Jake Dunn, unpublished data].
Thus, our results support the idea that monkeys
could experience higher stress levels in fragments, as
it has been recently demonstrated by Rangel-Negrn
et al. [2009] by analyzing fecal cortisol levels of
spider monkeys living in conserved forests, fragmenn
ted forests, and captive conditions in the Yucata
Peninsula, Mexico.
Considering the potential negative effects that
climate change would have for spider monkeys,
particularly in fragmented landscapes in which
interfragment movements is highly limited [ArroyoRodrguez & Mandujano, 2009], conservation efforts
should be focused on the increase of landscape
connectivity. Landscape corridors are required to
facilitate species and population movements between
habitats in response to climate change [Ewers &
Didham, 2006]. In this sense, the Mesoamerican
Biological Corridora system of land planning
coordinated by the governments of the countries
located in the Mesoamerican regionwould connect
the largest reserves of Mesoamerica and could have a
crucial positive impact on the conservation
of primates and other plant and animal species
[Anderson & Jenkins, 2006; Miller et al., 2001].
Furthermore, increasing fragment size is critical to
reduce primates foraging effort and maintain larger
(and viable) primate populations.
It is important to recognize that our results are
limited by variation in data collection length,
methodology, and interobserver experience across
studies. To address this shortcoming, we recommend
that, although research designs need to be appropriate to the research questions and characteristics
of the study population and field site, we need to
standardize methodologies as much as possible. More
coordination among scientists working on the same
species and/or similar topics is needed in order to
build the data bases required to address important
issues. These data bases are fundamental in allowing
scientists carrying out more accurate comparisons
among studies in order to reach critical generalizations and build theories that can be put to use for
primate conservation.
ACKNOWLEDGMENTS
This study satisfied the legal requirements of
Mexican Secretary of Environment and Natural
Resources (SEMARNAT) and meets all the Mexican
animal care policies and the Principles of the
American Society of Primatologists for the Ethical

Am. J. Primatol.

Treatment of Nonhuman Primates. This work was

supported by grants from the Consejo Nacional de
Ciencia y Tecnologa (CONACYT), Mexico (200551043, 2006-56799). We thank ML Chavarra and R
Blanco from Santa Rosa National Park, the personnel of the Smithsonian Tropical Research Institute
Environmental Science Program, Biological Station
of Los Tuxtlas, Biology Institute of the Universidad
Climatologic
Nacional Autonoma de Mexico, Coba
Station of the Comision Nacional del Agua
Mexico (CNA, Mexico), and the Lacandona Climatic
Station of the Comision Federal de Electricidad
(CFE, Mexico) for providing climatic information.
We thank C.J. Campbell, P.S. McDaniel,
S.M. Lindshield, J.A. Weghorst, F. Garca,
J. Jimenez, N.A. Argueta, and G.M. Rivera for
allowing us to use some data of their unpublished
Thesis. We also thank A. Di Fiore and two anonymous referees for useful comments. SSL thanks the
technical support provided by the Instituto de
Neuroetologa (UV) and Universitat de Barcelona.
VAR thanks the financial support provided by the
Direccion General de Asuntos del Personal Academico (DGAPA-UNAM). VAR, KES, and OCB
acknowledge the technical assistance provided by
J.M. Lobato-Garca, H. Ferreira, and A. ValenciaGarca. The Instituto de Ecologa A.C and Centro
de Investigaciones en Ecosistemas (Universidad
Nacional Autonoma de Mexico) provided logistical
support.
FA is grateful to the financial support from the
North of England Zoological Society. The Instituto
de Ecologa A.C and Centro de Investigaciones en
noma de
Ecosistemas (Universidad Nacional Auto
Mexico) provided logistical support.
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