Review Article Influence of Climatic Variables, Forest Type, and Condition On Activity Patterns of Geoffroyi's Spider Monkeys Throughout Mesoamerica
Review Article Influence of Climatic Variables, Forest Type, and Condition On Activity Patterns of Geoffroyi's Spider Monkeys Throughout Mesoamerica
Review Article Influence of Climatic Variables, Forest Type, and Condition On Activity Patterns of Geoffroyi's Spider Monkeys Throughout Mesoamerica
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derived from 15 published and unpublished studies carried out in four countries (Mexico, El Salvador,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;
lez-Zamora et al.
1190 / Gonza
Am. J. Primatol.
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
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
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
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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.
60
50
Non-seasonal
Seasonal
40
**
30
20
10
0
Rest
70
50
Feed
Continuous forests
60
Travel
Forest fragments
*
**
40
30
20
10
0
Rest
Feed
Travel
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