Research Article
Spider Monkeys in Human-Modified
Landscapes: The Importance of the Matrix
Tropical Conservation Science
Volume 10: 1–13
! The Author(s) 2017
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DOI: 10.1177/1940082917719788
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Vı́ctor Arroyo-Rodrı́guez1, Gloria Karina Pérez-Elissetche1,
José D. Ordóñez-Gómez2, Arturo González-Zamora3,
Óscar M. Chaves4, Sònia Sánchez-López5, Colin A. Chapman6,
Karenina Morales-Hernández7, Miriam Pablo-Rodrı́guez5,
and Gabriel Ramos-Fernández8
Abstract
With the extant of tropical forest degradation, primates increasingly inhabit forest patches embedded in anthropogenic
matrices. Such matrices are composed of different land cover types (e.g., agricultural lands and cattle pastures), but large
uncertainty remains about the ability of primates to use these land covers. Here, we assessed the use of the landscape matrix
by spider monkeys (Ateles geoffroyi) in 13 forest sites from three countries (Mexico, Costa Rica, and El Salvador). Based on ad
libitum records from >212 months of field observations, we found that spider monkeys used four types of land covers for
feeding or traveling: secondary vegetation, isolated trees, tree crops, and vegetation corridors. Secondary vegetation was
more frequently used than the other land covers. The number of land covers present in the matrix was positively related to
the number of land covers used for traveling and feeding. Monkeys consumed 53 plant species in the matrix, mostly native
and old-growth or late-successional forest species, although they also used three cultivated tree species. Most species were
trees, especially from preferred food species, although monkeys also used palms, lianas, and shrubs. Monkeys fed principally
from fruits, but they also used leaves, wood, and flowers. Most species were used from secondary vegetation and isolated
trees. These findings suggest that the landscape matrix can provide supplementary food sources for this endangered primate
and opportunities for traveling (i.e., spatial connectivity) in human-modified landscapes—information that can be used to
improve conservation strategies, especially under the context of land-sharing management strategies (e.g., agroforestry).
Keywords
Atelidae, behavioral flexibility, compositional heterogeneity, corridors, fragmentation, habitat loss, land sharing, landscape
supplementation
4
Introduction
With increasing land-use change across the tropics
(Achard et al., 2014), a large proportion of global biodiversity is found in human-modified tropical landscapes
(HMTLs; Melo, Arroyo-Rodrı́guez, Fahrig, Martı́nezRamos, & Tabarelli, 2013). Such landscapes are highly
heterogeneous, as they are usually composed of forest
1
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad
Nacional Autónoma de México, Morelia, Michoacán, Mexico
2
Cognitive Ethology Laboratory, German Primate Center, Göttingen,
Germany
3
Instituto de Investigaciones Biológicas, Universidad Veracruzana, Xalapa,
Veracruz, Mexico
Departamento de Biodiversidade e Ecologia, Pontificia Universidade
Católica do Rio Grande do Sul, Porta Alegre, Rio Grande do Sul, Brazil
5
Universidad Veracruzana, Xalapa, Veracruz, Mexico
6
Department of Anthropology and McGill School of Environment, McGill
University Montreal, Quebec, Canada
7
Primates – El Salvador y Grupo de Trabajo de Mastozoologı́a de El Salvador,
Santa Ana, El Salvador
8
Centro Interdisciplinario de Investigación para el Desarrollo Integral
Regional Unidad Oaxaca, Instituto Politécnico Nacional, Oaxaca, Mexico
Received 10 March 2017; Revised 14 June 2017; Accepted 16 June 2017
Corresponding Author:
Vı́ctor Arroyo-Rodrı́guez, Instituto de Investigaciones en Ecosistemas y
Sustentabilidad, Universidad Nacional Autónoma de México (UNAM),
Campus Morelia, Antigua Carretera a Pátzcuaro No. 8701, Ex-Hacienda de
San José de la Huerta, 58190 Morelia, Michoacán, Mexico.
Email: victorarroyo_rodriguez@hotmail.com
Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0
License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further
permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage).
2
patches surrounded by different types of human-created
land covers, including human settlements, agricultural
lands, cattle pastures, secondary forests, live fences, and
isolated trees (hereafter, anthropogenic matrix). Because
forest patches in these landscapes may support a limited
availability of food resources (e.g., Arroyo-Rodrı́guez &
Mandujano, 2006; Chaves, Stoner, & Arroyo-Rodrı́guez,
2012), forest animals, including most primates, can supplement their food intake by using resources from the
surrounding matrix, a process named ‘‘landscape supplementation’’ (Dunning, Danielson, & Pulliam, 1992). The
matrix can also be used by forest animals to move among
forest patches (Franklin & Lindenmayer, 2009), but different land covers show different resistance to interpatch
movements (da Silva, Ribeiro, Hasui, da Costa, & da
Cunha, 2015; Ricketts, 2001). Unfortunately, large uncertainty remains about the ability of most animal species to
use the matrix, the land cover types more frequently used
for feeding and traveling, and the food resources used in
each land cover. Such knowledge is urgently needed to
understand biodiversity patterns in HMTLs, and thus for
the construction of informed conservation planning
(Franklin & Lindenmayer, 2009; Prevedello & Vieira,
2010; Watling, Nowakowski, Donnelly, & Orrock,
2011), specially for threatened species such as most primates (Estrada et al., 2017).
Primates are often found in HMTLs (Marsh et al.,
2013), where a large number of patterns and processes
may threaten their survival (Arroyo-Rodrı́guez &
Mandujano, 2009; Estrada et al., 2017; Graham,
Matthews, & Turner, 2016). Yet, because most studies
in HMTLs assess the impact of forest patch characteristics (e.g., patch size, isolation) on the diet, behavior, and
demography of primates (Arroyo-Rodrı́guez et al., 2013;
Carretero-Pinzón, Defler, McAlpine, & Rhodes, 2016),
our understanding of the importance of the landscape
matrix for primates is incipient. This gap of information
may be related, at least partially, to the fact that forest
animals may perceive the matrix as a dangerous place
where they are more exposed to predation and hunting,
and thus, they avoid the use of this landscape element.
However, there is evidence that primates are able to use
different land covers in the matrix (Estrada et al., 2017),
including agroecosystems (Estrada, Raboy, & Oliveira,
2012), and other land covers, such as secondary forests,
live fences, subsistence orchards, and isolated trees; but
the available information is limited to only a few folivorous
(Colobus guereza: Harris & Chapman, 2007; Colobus angolensis: Anderson, Rowcliffe, & Cowlishaw, 2007; Alouatta
palliata: Asensio, Arroyo-Rodrı́guez, Dunn, & CristóbalAzkarate, 2009; Alouatta pigra: Pozo-Montuy, Serio-Silva,
Chapman, & Bonilla-Sánchez, 2013; Alouatta guariba:
Bicca-Marques & Calegaro-Marques, 1995; Chaves &
Bicca-Marques, 2017), omnivorous (Pan troglodytes
schweinfurthii: Reynolds, Wallis, & Kyamanywa, 2003),
Tropical Conservation Science 0((0) )
and frugivorous/insectivorous monkeys (Callicebus negrifrons: Trevelin, Port-Carvalho, Silveira, & Morell, 2007;
Cercopithecus ascanius: Baranga, Basuta, Teichroeb, &
Chapman, 2012). The available information for frugivorous primates, such as the spider monkey (genus Ateles),
is very scarce.
The Geoffroy’s spider monkey (Ateles geoffroyi) is distributed from southeastern Mexico to northwestern
Colombia (Di Fiore, Link, & Campbell, 2011). Given
its large body size (6–9.4 kg; Ford & Davis, 1992) and
mostly frugivorous diet (González-Zamora et al., 2009),
A. geoffroyi uses large home ranges (95–900 ha; Wallace,
2008). These ecological features make this species particularly sensitive to forest loss and fragmentation (Boyle &
Smith, 2010; Garber, Estrada, & Pavelka, 2006; Michalski
& Peres, 2005; Ramos-Fernández & Wallace, 2008).
Although there are some published reports of spider
monkeys using food resources from the matrix, mostly in
agricultural lands (Chaves et al., 2012; Estrada et al., 2006,
2012) and secondary forests (Ramos-Fernández &
Ayala-Orozco, 2003; Ramos-Fernández, Smith-Aguilar,
Schaffner, Vick, & Aureli, 2013), we lack information concerning the land cover types that are frequently used by
this species for feeding and traveling in the matrix. Such
information is needed to design biodiversity-friendly landscapes (sensu Melo et al., 2013); for example, increasing
resource availability and landscape connectivity for endangered species such as A. geoffroyi.
Here, we compiled ad libitum observations from 10
studies of spider monkeys carried out in 13 forest patches
surrounded by different land cover types in three countries (Mexico, Costa Rica, and El Salvador) to document,
for the first time: (a) the general patterns of land cover
types used for feeding and traveling in the matrix; and (b)
the life forms, plant species, and food items used as food
resources in each land cover. Because spider monkeys
are considered forest-specialist primates, we hypothesized
that monkeys can use the matrix for feeding and traveling, but mainly use those land cover types that are
structurally and compositionally more similar to the
forest patches in which they reside. Spider monkeys in
fragmented forests are known to increase their consumption of leaves (e.g., González-Zamora et al., 2009)—a
plant item with lower energetic content and higher
levels of secondary compounds and structural material
than other plant items, such as fruits (Felton, Felton,
Lindenmayer, & Foley, 2009a; Felton et al., 2009b;
Milton, 1981). Therefore, we hypothesized that monkeys
in the matrix will use primarily fruits (especially from
preferred tree species) to supplement their diet, and
thus increase the quality of their diet (Asensio et al.,
2009; Dunning et al., 1992). This hypothesis is particularly plausible considering that the matrix can be experienced by primates as a relatively hostile place, and thus,
they are not expected to leave forest patches to feed from
3
Arroyo-Rodrı́guez et al.
plant items such as leaves, which are readily available within their home patches (Asensio et al., 2009;
although note that leaf quality is highly variable: Snaith
& Chapman, 2005).
Methods
Data Base
We compiled ad libitum observations of spider monkeys
feeding or traveling (i.e., movements within and between
land cover types) in different land cover types in the
anthropogenic matrix surrounding their home forest
patches from 10 studies of their ecology and behavior
carried out in 13 forest sites from Mexico (n ¼ 9 patches),
El Salvador (n ¼ 3), and Costa Rica (n ¼ 1), totaling more
than 212 months ( > 17 years) of field observations
(Table 1). We did not take into account the parts of the
matrix used for resting, because we did not observed
sleeping sites in the matrix. As these studies were not
designed to assess matrix use by monkeys, we do not
have information on the time spent in each activity
and land cover type. Also, sampling efforts were highly
variable among studies (18 32 months per study,
mean SD). Therefore, we based this study on presence/absence data, considering a single event of feeding
Table 1. Characteristics of Forest Sites (n ¼ 13) Where Spider Monkeys (Ateles geoffroyi) Have Been Observed Using Different Land
Cover Types for Feeding and Traveling in the Anthropogenic Matrix Surrounding Their Home Forest Patches.
Forest
site
1
2
3
4
5
6
7
8
9
10
11
12
13
a
Location (coordinates)
Santa Rosa, Costa Rica
(10 53’ 1"N, 85 46’30"W)
Nancuchiname, El Salvador
(13 17’45"N, 88 34’30"W)
Normandı́a, El Salvador
(13 16’40"N, 88 32’00"W)
Chaguantique, El Salvador
(13 19’38"N, 88 38’12"W)
Punta Laguna, Mexico
(20 38’00"N, 87 37’00"W)
Lacandona, Mexico
(16 19’52"N, 90 51’06"W)
Lacandona, Mexico
(16 20’11"N, 90 48’20"W)
Lacandona, Mexico
(16 16’45"N, 90 50’16"W)
Lacandona, Mexico
(16 15’12"N, 90 49’60"W)
Los Tuxtlas, Mexico
(18 23’55"N, 94 44’25"W)
Los Tuxtlas, Mexico
(18 24’15"N, 94 44’46"W)
Los Tuxtlas, Mexico
(18 23’52"N, 94 44’33"W)
Los Tuxtlas, Mexico
(18 22’42"N, 94 46’95"W)
Mean
rainfall
(mm)
Vegetation
typea
Home
patch
size (ha)
Matrix
compositionb
Feedingc
Travelingc
1,600
TDF
10,800
IT, P, SV
IT, SV
IT, SV
1 (38)
1,550
TDF
60
P, SV, VC
VC
VC
2 (5)
1,550
TDF
33
C1, SV
C1, SV
2 (5)
1,550
TDF
430
C1, VC,
P, SV
VC, P, SV
SV
SV
3 (4)
1,500
TDF
200
C2, SV
C2, SV
2,800
TWF
67
2,800
TWF
28
2,800
TWF
141
IT, C3,
VC, SV
IT, C1,
C3, VC
SV
IT, C3,
VC, SV
IT, C3,
VC, SV
SV
4 (13),
5 (120)
6 (15)
2,800
TWF
1,125
>4,000
TWF
>4,000
C2, VC,
BG, SV
IT, C3,
VC, SV, P
IT, C1, C3,
VC, SV, P
IT, C3, SV, P
References
(study
length)d
IT
IT, SV
4.6
IT, C3,
VC, SV, P
IT, P, SV
7
8
7
8
6
(3),
(2)
(3),
(2)
(15)
IT, SV
IT, SV
9 (6)
TWF
9
IT, P, SV
SV
SV
9 (6)
>4,000
TWF
8
IT, P, SV
SV
SV
9 (6)
>4,000
TWF
24
IT, P, SV
IT, SV
IT, SV
10 (6)
Vegetation types following Gentry (1982): TDF ¼ tropical dry forest; TWF ¼ tropical wet forest.
Land cover types surrounding each forest site: BG ¼ backyard garden; C ¼ tree crops (C1: Mangifera indica; C2: Manilkara zapota; C3: Theobroma cacao);
IT ¼ isolated tree; P ¼ cattle pasture; SV ¼ secondary vegetation; VC ¼ vegetation corridor (i.e., live fences and riparian corridors).
c
Land cover types used for feeding and traveling in the landscape matrix (abbreviations correspond to those showed in the footnote b).
d
References and study length (i.e., number of months) ¼ 1. C. A. Chapman (unpublished data); 2. K. Morales-Hernández (unpublished data); 3. Argueta and
Rivera (2004); 4. M. Pablo-Rodrı́guez (unpublished data); 5. G. Ramos-Fernández (unpublished data); 6. Chaves, Stoner, and Arroyo-Rodrı́guez (2012); 7. J. D.
Ordóñez-Gómez (unpublished data); 8. G. K. Pérez-Elissetche (unpublished data); 9. A. González-Zamora (unpublished data); 10. S. Sánchez-López (unpublished data).
b
4
or traveling within a given land cover type as evidence of
occurrence (see below). The forest patches (i.e., discrete
forest masses separated by agricultural lands) we studied
ranged from 4.6 to 10,800 ha, and included both tropical
wet (n ¼ 8 patches) and tropical dry forests (n ¼ 5) following Gentry’s (1982) classification of tropical forests
(i.e., <2,000 mm rain/year in tropical dry forests, and
>2,800 mm rain/year in tropical wet forests). The composition of the landscape matrix was highly variable,
ranging from relatively homogeneous matrices composed
of three land covers (e.g., secondary vegetation, cattle
pastures, and isolated trees) to heterogeneous matrices
composed of six land covers: secondary vegetation,
tree crops (i.e., Mangifera indica, Psidium guajava, and
Theobroma cacao), vegetation corridors (i.e., live fences
and riparian corridors), cattle pastures, and isolated trees
(Table 1). Although old secondary forests can be difficult
to differentiate from old-growth forests, we focused on
secondary forests relatively easy to identify in the field,
mostly young regenerating forest stands (<30 years of
succession) dominated by light-demanding pioneer
genera, such as Cecropia, Ochroma, Piper, Miconia, and
Helioparpus, which usually form a discontinuous canopy
of less than 20 m tall, with a very high density of relatively
small stems. For each forest site we recorded: (a) the land
cover types present in the surrounding landscape matrix;
(b) the land cover types used for feeding and/or traveling;
and (c) the plant species, live forms, and plant items (e.g.,
fruit, flowers, leaves, and wood) used as food resources in
each land cover type. Due to the dominance of pioneer
(early colonizer) species that are typically indicative of
forest disturbance (Santos et al., 2008; Tabarelli, Peres,
& Melo, 2012), we followed the procedure described
by Arroyo-Rodrı́guez, Pineda, Escobar, and Benı́tezMalvido (2009) to classify the species based on their
successional status: early colonizers (or pioneer species),
late-successional (or non-secondary light demanding)
species, and old-growth forest (shade-tolerant) species.
This ecological group classification was based on information from several floras (e.g., Flora of Veracruz and
Neotropical Flora), as well as several species lists
(Arroyo-Rodrı́guez et al., 2009; Hernández-Ruedas
et al., 2014, and references therein). Plant nomenclature
was updated according to the Royal Botanical Garden
and the Missouri Botanical Garden databases (http://
www.theplantlist.org/, accessed on December 10, 2016).
Data Analyses
Each forest site was considered as an independent record.
We first calculated the proportion of forest sites that presented each land cover type (based on a total of 13 forest
sites). This proportion indicates the distribution of each
land cover type across forest sites, and can be considered
a proxy of availability (e.g., secondary vegetation
Tropical Conservation Science 0((0) )
occurred in all forest sites, but isolated trees were found
in 9 out of 13 sites; Table 1). We also calculated the proportion of forest sites where monkeys were observed feeding or traveling in each land cover type. As monkeys
cannot use land covers that are not present in a given
site, in this case, proportions are calculated considering
the distribution of each land cover across forest types,
and not based on the total number of forest sites (e.g.,
monkeys fed from isolated trees in 6 sites, but as this land
cover type was only present in 9 sites, they used isolated
trees for feeding in 67% of sites, and not 46% if we would
consider 13 sites; Table 1). We then assessed whether the
observed proportions differed from the proportions
expected based on the distribution of each land cover type
across forest sites with a 2 test. Using a simple linear regression, we also tested if the number of land cover types used in
each forest site were related to the number of land cover
types present in the surrounding matrix. Finally, as there
was a wide variation in the length of studies and forest
patch size (Table 1), and such variation can affect our results
and conclusions, we also used linear regressions to assess the
effect of study length and patch size on the number of plant
species used in the matrix and the number of land covers
used for feeding and traveling. All statistical analyses were
done with R software (R Core Team 2017) assuming a statistical threshold (alpha) of .05.
Results
Spider monkeys fed and traveled in four different matrix
types: secondary vegetation, isolated trees, tree crops (i.e.,
Mangifera indica, Manilkara zapota, and Theobroma
cacao) and vegetation corridors (i.e., live fences and riparian corridors; Table 1). In general, secondary vegetation
was more frequently used than the other land covers,
both for feeding and traveling (Figure 1). This pattern
may be related to the fact that all forest sites showed
secondary vegetation in their surrounding matrix,
whereas the rest of land covers were present in six to
nine forest sites (Table 1; Figure 1). In fact, the proportion of sites where monkeys were observed feeding
(2 ¼ 0.81, df ¼ 3, p ¼ .85) or traveling (2 ¼ 1.85, df ¼ 3,
p ¼ .60) within each land cover type did not differ from
what we can expect based on the distribution of such land
covers across forests sites (Figure 1). In this sense, we
found a positive association between the number of
land covers in the matrix and the number of land
covers used for traveling (r ¼ .66, p ¼ .02) and feeding
(r ¼ .54, p ¼ .059; Figure 2).
In total, spider monkeys consumed 53 plant species
belonging to 20 families (Table 2). Most species (83%)
were trees, but spider monkeys also used palms (7%),
lianas (6%), and shrubs (4%). All tree species, except
Mangifera indica, are native to the respective forest sites
and three species are cultivated (Mangifera indica,
5
Arroyo-Rodrı́guez et al.
13
Proportion of forest sites
1
Use for feeding
12
Use for traveling
0.9
0.8
10
6
0.7
6
Availability
9
4
0.6
4
7
0.5
3
6
3
0.4
0.3
0.2
0.1
0
Isolated trees
Secondary
vegetation
Vegetation
corridors
Tree crops
Figure1. Proportion (and total numbers above each column) of forest sites where spider monkeys (Ateles geoffroyi) fed or traveled in
different land cover types present in the anthropogenic matrix. The proportion of forest sites surrounded by each land cover is added as a
proxy of the availability of each land cover, and are calculated based on the total number of study sites (n ¼ 13). Yet, the proportion of
forest sites used for feeding and traveling are calculated considering the availability of each land cover across the sites.
Feeding
Traveling
Number of used land covers
5
4
Traveling
(R² = 0.43)
3
Feeding
(R² = 0.29)
2
1
0
2
3
4
5
6
Number of available land covers
Figure 2. Association between the number of land covers in the matrix (x-axis) and the number of land covers used by spider monkeys
(Ateles geoffroyi) for feeding and traveling in 13 forest sites from Mexico, El Salvador, and Costa Rica. Note that each point represents a
different forest site.
Theobroma cacao, and Psidium guajava). Most
species are old-growth forest species (42%) or latesuccessional species (34%), and only 19% are early colonizer species.
Regarding the frequency of use of each species, most
species (72%) were used in one single site (Table 1), and
nine species (17%) were used in two forest sites (i.e.,
Mangifera indica, Tapirira mexicana, Bursera simaruba,
Heliocarpus donnellsmithii, Theobroma cacao, Miconia
argentea, Brosimum sp., Ficus aurea, and Ficus yoponensis). The species most frequently used were Brosimum
alicastrum, Spondias mombin, and Ficus sp., which were
used in 3 out of 13 forest sites.
Regarding the plant items eaten, monkeys fed from
fruits of 29 species (55% of species) and leaves of 19
species (36%). Five species (Licania platypus, Swietenia
macrophylla, Ficus sp., Ficus aurea, and Ficus insipida)
were also used as a source of wood and two species
(Dussia mexicana and Luehea seemannii) as a source of
flowers (Table 2). In fact, Ficus spp. were used for their
fruits, leaves, and wood, and monkeys used two plant
items of seven species: Bursera simaruba, Enterolobium
6
Tropical Conservation Science 0((0) )
Table 2. Plant Species and Food Items Used by Spider Monkeys (Ateles geoffroyi) for Feeding in Different Land Cover Types Surrounding
13 Forest Sites Distributed in Three Countries (Costa Rica, El Salvador, and Mexico).
Family
Tree speciesa
Life
form
EGb
Plant
itemsc
Land
coverd
Proportion
of sitese
Ref.f
Anacardiaceae
Mangifera indica*
Metopium brownei
Spondias mombinz
Spondias radlkoferi
Tapirira mexicanaz
Philodendron tripartitum
Rhodospatha sp.
Astrocaryum mexicanumz
Attalea butyraceaz
Attalea cohune
Sabal mexicanaz
Cordia alba
Bursera sp.
Bursera simarubaz
Licania platypusz
Diospyros tetrasperma
Alchornea latifoliaz
Dussia mexicanaz
Enterolobium cyclocarpumz
Inga sp.z
Inga oerstediana
Leucaena sp.
Pithecellobium hymenaefoliumz
Guazuma ulmifoliaz
Heliocarpus donnellsmithii
Luehea seemannii
Robinsonella mirandae
Theobroma cacao
Miconia argenteaz
Swietenia macrophylla
Brosimum sp.z
Brosimum alicastrum
Castilla elasticaz
Ficus sp.z
Ficus americanaz
Ficus apollinarisz
Ficus aureaz
Ficus cotinifoliaz
Ficus crassinerviaz
Ficus insipidaz
Ficus maximaz
Ficus yoponensisz
Maclura tinctoria
Muntingiasp.z
Psidium guajava
Tree
Tree
Tree
Tree
Tree
Liana
Liana
Palm
Palm
Palm
Palm
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Shrub
Tree
C
OG
OG
OG
OG
OG
OG
OG
OG
OG
OG
OG
LS
LS
OG
OG
OG
OG
LS
LS
LS
LS
P
P
P
P
LS
C
P
OG
OG
OG
OG
LS
LS
LS
LS
LS
LS
LS
LS
LS
LS
P
C
F
F
F
L
L
L
L
L
F
F
F
F
F, L
W
F
F
Fl
F, L
L
F
F
L
Fl
L
F
F, L
W
F, L
L
F, L, W
F
F
L, W
F
F
W
L
F, L
F, L
F
IT, TC
SV
SV
SV
SV
IT
VC
IT
IT, TC
TC
IT
VC
IT, SV
SV
IT
SV
IT
SV
SV
VC
SV
IT
IT, TC
SV
SV
IT, SV
IT
TC
IT, SV
VC
IT, VC
SV
SV
TC, SV
IT
SV
IT, TC
SV
SV
IT
VC
SV
IT, VC
IT, SV
IT
0.15
0.08
0.23
0.08
0.15
0.08
0.08
0.08
0.08
0.08
0.08
0.08
0.08
0.15
0.08
0.08
0.08
0.08
0.08
0.08
0.08
0.08
0.08
0.08
0.15
0.08
0.08
0.15
0.15
0.08
0.15
0.23
0.08
0.23
0.08
0.08
0.15
0.08
0.08
0.08
0.08
0.15
0.08
0.08
0.08
2, 7, 8
5
3, 5, 6
9
9
9
7
9
7, 8
8
6
2
1
5, 9
6
5
10
9
5
7
3
7
8
5
9
9
10
6, 8
9, 10
8
6, 7
3, 9
3
6, 8, 9
10
9
6, 7
5
5
6
7
9
6
1
7
Araceae
Arecaceae
Boraginaceae
Burseraceae
Chrysobalanaceae
Ebenaceae
Euphorbiaceae
Fabaceae
Malvaceae
Melastomataceae
Meliaceae
Moraceae
Muntingiaceae
Myrtaceae
(continued)
7
Arroyo-Rodrı́guez et al.
Table 2. Continued
Family
Tree speciesa
Life
form
EGb
Plant
itemsc
Land
coverd
Proportion
of sitese
Rosaceae
Sapindaceae
Sapotaceae
Prunus serotina
Cupania glabraz
Manilkara zapotaz
Pouteria sapotaz
Smilax sp.
Cecropia sp.z
Cecropia obtusifoliaz
Cecropia peltataz
Tree
Tree
Tree
Tree
Liana
Tree
Tree
Tree
P
OG
OG
OG
OG
P
P
P
F
F
F
F
L
F
-
SV
TC
TC
TC, VC
TC
IT, SV
IT
SV
0.08
0.08
0.08
0.08
0.08
0.08
0.08
0.08
Smilacaceae
Urticaceae
Ref.f
7, 8
8
4
8
8
1
10
3
a
The plant species marked with asterisk (*) are exotic species (the rest are native species) and those with (z) represent top food species (i.e., species
corresponding to 80% of total feeding time) within a review of spider monkeys’ diet through their geographic range (González-Zamora et al., 2009).
b
Ecological groups: early colonizers or pioneer species (P), nonsecondary light demanding or late-successional species (LS), shade-tolerant or old-growth
forest species (OG), and cultivated species (C).
c
(Used plant items: fruits (F), flowers (Fl), leaves (L), and wood (W); -) unavailable information.
d
Land cover types where each plant species was used: tree crops (TC), isolated tree (IT), secondary vegetation (SV), and vegetation corridor (VC).
e
We indicate the proportion of sites where monkeys were observed feeding from each species (n ¼ 13 sites).
f
References correspond to those showed in Table 1.
30
Number of species
49.1%
25
41.5%
20
15
20.8%
10
15.1%
5
0
Secondary vegetation Isolated trees
Vegetation corridor
Tree crops
Figure 3. Number of plant species (and percentages from a total of 53 species) used by spider monkeys (Ateles geoffroyi) as a food source
in different land cover types within the anthropogenic matrix surrounding their home forest patches.
cyclocarpum, Miconia argentea, Brosimum sp., Ficus
aurea, Ficus yoponensis, and Maclura tinctoria.
Most plant species (26 species, 49%) were used in secondary vegetation, and a large number of species (22 species, 42%) were also used as isolated trees (Table 2;
Figure 3). Monkeys fed from a lower number of plant
species in tree crops (11 species) and vegetation corridors
(8 species). Because most species (40 species) were used in
one single land cover, the species turnover (b-diversity)
between land covers was very high (only 13 plant species
were used in two land covers, and no species was used in
three or more land covers; Table 2).
Differences in patch size and study length across studies were not related to the number of food species
(Figure 4(a) and (b)) and the number of land covers
used by spider monkeys for feeding and traveling
(Figure 4(c) and (d)). This suggests that matrix use by
spider monkeys was largely independent of patch size
and study length.
Discussion
This study shows that spider monkeys use different
land cover types from the anthropogenic matrix for feeding and traveling in HMTLs. We observed monkeys feeding from 53 plant species—a significant figure considering
that 16 groups of spider monkeys in five countries
(Mexico, Guatemala, El Salvador, Costa Rica, and
Panama) fed from 364 plant species (González-Zamora
et al., 2009). In fact, most of the plant species are
native and old-growth or late-successional forest species
considered top food species for spider monkeys
8
(a)
12
Number of food species
Tropical Conservation Science 0((0) )
10
10
8
8
6
6
4
4
2
2
R2 = 0.023
(b) 12
0
0
0
2
(c)
Number of used land covers
R2 = 0.074
4
Feeding
6
Traveling
4.5
4
3.5
3
2.5
2
1.5
1
0.5
0
8
10
R2feeding = 0.008
R2travelling = 0.000
0
2
4
6
8
10
Ln (home patch size)
0
1
(d)
2
Feeding
3
4
Traveling
4.5
4
3.5
3
2.5
2
1.5
1
0.5
0
5
6
R2feeding = 0.027
R2travelling = 0.044
0
1
2
3
4
5
6
Ln (study length)
Figure 4. Effect of home patch size and study length on the number of plant species used by spider monkeys (Ateles geoffroyi) as food
resources in the matrix (a to b), and the number of land covers used for feeding and traveling in 13 forest sites from Mexico, El Salvador,
and Costa Rica. All R2 values were not significant (p > .7, in all cases).
(González-Zamora et al., 2009). They consumed different
life forms (trees, lianas, palms, and shrubs) and plant items
(fruits, leaves, flowers, and wood), but as expected, fruits
were the most frequently plant item eaten. Although we
cannot quantify the importance of these feeding and traveling events for the fitness of these monkeys in HMTLs, our
findings demonstrate that some human-created land covers
in the matrix are not entirely hostile to this primate, but
rather contain usable resources, not only to supplement
their diet but also to move within and between land
cover types (Arroyo-Rodrı́guez & Mandujano, 2009;
Dunning et al., 1992; Franklin & Lindenmayer, 2009;
Tscharntke et al., 2012). Thus, our study adds to an
increasing line of evidence suggesting that forest edges do
not represent home range boundaries for different species
in fragmented forests (Dunning et al., 1992; Fahrig, 2013;
Mendenhall et al., 2014; Tscharntke et al., 2012; Watling
et al., 2011).
Although we have no information on the time spent
within each land cover outside their home forest patches,
we observed monkeys feeding and traveling in patches of
secondary vegetation, different types of tree crops, vegetation corridors, and isolated trees, including records
from both tropical wet forests and tropical dry forests
in Mexico, El Salvador, and Costa Rica. Such behaviors
can allow primates to supplement their diet in HMTLs
(Dunning et al., 1992). As increasingly demonstrated in
studies of primates (Anderson et al., 2007; Asensio et al.,
2009; Chaves & Bicca-Marques, 2017; Estrada et al.,
2012; Pozo-Montuy et al., 2013), supplementation
dynamics are likely of critical relevance for species
persistence in fragmented landscapes (Dunning et al.,
1992), especially because the availability of food
resources can be limited in forest patches, or because
patches can be too small to sustain viable populations
(e.g., Arroyo-Rodrı́guez & Mandujano, 2006, 2009).
Supporting the idea that monkeys are supplementing
their diet with resources obtained from the matrix, we
found that, as predicted, fruits were the most frequently
eaten plant item, followed by leaves, wood, and flowers.
Because fruits are expected to be scarce within forest
patches (e.g., Chaves et al., 2012; González-Zamora
et al., 2009, 2012), and have high concentrations of soluble carbohydrates (and energetic content), but low levels
of secondary compounds and structural material (Felton
et al., 2009a, 2009b; Milton, 1981), the consumption of
this food item in the matrix probably improved the quality of spider monkeys’ diet. The consumption of leaves,
wood, and flowers was also common in most forest sites,
probably as a strategy of protein, lipid, and mineral supplementation (Chaves, Stoner, Ángeles-Campos, &
Arroyo-Rodrı́guez, 2011a; Felton et al., 2009a, 2009b;
Rothman, Van Soest, & Pell, 2006). Yet, additional studies comparing the nutritional value of the diet within
their home forest patches versus the diet in the matrix
are needed to better understand the effect of these feeding
events in the matrix on primate’s diet and nutrition.
As expected, secondary vegetation was more frequently
used than other land covers. Yet, when comparing the
frequency of use of each land cover with their distribution
in the sites, our findings suggest that the use of each
land cover was directly proportional to their availability,
Arroyo-Rodrı́guez et al.
suggesting no selection of particular land covers. In fact,
the number of land covers in the matrix was positively
related to the number of land covers used for feeding
and traveling. Thus, although spider monkeys are strongly
threatened by forest loss and disturbance (Garber
et al., 2006; Ramos-Fernández & Wallace, 2008), this finding highlights the behavioral flexibility of spider monkeys
(Amici, Aureli, & Call, 2008; González-Zamora et al.,
2009; Schaffner, Rebecchini, Ramos-Fernandez, Vick, &
Aureli, 2012; Wallace, 2008), and the importance of matrix
heterogeneity for species conservation in HMTLs (Revilla,
Wiegand, Palomares, Ferreras, & Delibes, 2004; Ricketts,
2001; Tubelis, Cowling, & Donnelly, 2004). Each land
cover patch can support different resources, thus providing
higher resilience and stability in ecological processes, such
as feeding and dispersal (see the ‘‘landscape–moderated
insurance hypothesis’’; Tscharntke et al., 2012). The fact
that monkeys used different plant species in each land
cover suggests that vegetation composition differs widely
between land covers (high beta diversity). Thus, for
arboreal species such as spider monkeys, the presence of
different types of tree covers in the matrix can provide opportunities for traveling (landscape connectivity)
and feeding from different food resources (Revilla et al.,
2004; Ricketts, 2001; Tubelis et al., 2004). This is probably
important in severely deforested/degraded landscapes
where increasing interpatch isolation distances can limit
species persistence (Fahrig, 2013; Tubelis et al., 2004).
Implications for Conservation
Old-growth tropical forests are the main habitat of spider
monkeys, and thus, the preservation of this species-rich
ecosystem should be considered of highest priority for the
conservation of this endangered primate. The great value
of large forest remnants for primate conservation is
incontrovertible (Estrada et al., 2017), but what is questionable is the exclusion of the anthropogenic matrix
from conservation initiatives (Chapman, Chapman, &
Glander 1989; Hockings, Yamakoshi, & Matsuzawa,
2017; Nekaris et al., 2017; Perfecto & Vandermeer, 2010).
In this sense, the maintenance of native and some cultivated trees in the anthropogenic matrix is of critical
importance for spider monkeys, as all land cover
types used by this primate were composed of trees
(both native and cultivated). We refer to agroforests,
such as shade cacao plantations (Theobroma cacao),
mango (Mangifera indica), and guava (Psidium guajava;
e.g., Estrada et al., 2012; Hockings et al., 2017), and other
important landscape elements, such as vegetation corridors and isolated trees of native species (Asensio et al.,
2009). Overall, the maintenance of these trees in the
matrix has numerous benefits for both primates and
humans. The benefits for primates go beyond their
importance as supplementary food sources, as they are
9
also critical to increase landscape connectivity, favoring
interpatch dispersal movements (Pozo-Montuy et al.,
2013). The benefits for humans include key ecosystem
services, such as carbon sequestration, climate regulation,
and water quantity (Dı́az, Fargione, Chapin, & Tilman
2006). Furthermore, there are many cobenefits for
humans of having both higher tree cover and primates
in the landscape, including the soil nutrient enrichment
through primates’ defecations, seed dispersal and rapid
forest recovery (see below), education/inspiration, and
esthetic values (e.g., Dı́az et al., 2006; Feeley, 2005;
Hockings et al., 2017). Related to the education/
inspiration and esthetic values, local people can also
obtain important economic resources from ecotourism
associated with visits to primate groups, which is known
to be an economically significant activity in many locations worldwide (Serio-Silva, 2006; Wolfe, 1991).
The fact that secondary vegetation was more frequently
used by spider monkeys than other land covers supports
an increasing number of studies underlining the importance of secondary forests for biodiversity conservation
(Arroyo-Rodrı́guez et al., 2017; Martı́nez-Ramos et al.,
2016; Melo et al., 2013; Omeja et al., 2016; Wright &
Muller-Landau, 2006). Secondary forest does not only
serve as supplementary habitat for forest species
(Martı́nez-Ramos et al., 2016), but it also enhances landscape connectivity (Arroyo-Rodrı́guez et al., 2017), and
provides key ecosystem services (e.g., carbon sequestration; Martı́nez-Ramos et al., 2016). Here, we show that
secondary forests can be used by spider monkeys for feeding and traveling. Although additional studies are needed
to better understand the role of these behaviors on primates’ survival and well-being in HMTLs, some longterm studies demonstrate that spider monkeys can actually
live and even reproduce successfully in secondary forests,
at least when located next to old-growth forests (RamosFernandez & Ayala-Orozco, 2003; Ramos-Fernández
et al., 2013). Of course, this does not mean that secondary
forests alone are enough for the maintenance of primate
populations in the long term, but that they can be used to
improve the quality of the anthropogenic matrix, and
accelerate forest recovery through secondary succession
(see below). Tree crops, vegetation corridors, and isolated
trees can also contribute to improve the quality of the
matrix, as they can provide important food resources for
spider monkeys (note that most plant species consumed
from these land covers are classified as top food species
for this primate; González-Zamora et al., 2009).
A topic that merits particular attention is the fact that
spider monkeys are effective seed dispersers of a large
number of plant species (Chaves, Stoner, ArroyoRodrı́guez, & Estrada, 2011b; González-Zamora et al.,
2012). Thus, the use of all these land cover patches in
the matrix likely contributes to forest recovery in
HMTLs. Therefore, maintaining different types of tree
10
covers in the vicinity of occupied forest patches is not
only needed to conserve the remaining populations of
this endangered primate species in HMTLs but also to
preserve important ecological services, such as forest
regeneration.
Our results present a straightforward message for conservation biologists and managers, especially when conservation strategies involve the retention of habitat
patches in agricultural mosaics (land-sharing approach;
Perfecto & Vandermeer, 2010); namely, some land covers
in the landscape matrix contain food tree species for
primates and other taxa (Dunning et al., 1992), and thus
some matrix types can be beneficial to conserve and
expand spider monkey populations in fragmented forests.
Secondary forest cover is increasing across the Neotropics
due to migration of people to urban areas and the abandonment of productive lands (Aide et al., 2013). This represents good news for the conservation of spider monkeys,
and puts a priority on taking advantage of this changing
situation and managing regenerating landscapes and investigations into primate restoration ecology (Jacob, Vaccaro,
Sengupta, Hartter, & Chapman, 2008; Wright & MullerLandau, 2006; Melo et al., 2013).
Acknowledgments
GKPE thanks Prof. A. Estrada for his useful advice during the
development of her MSc thesis. Such advice contributed to improve
the present manuscript. We also gratefully acknowledge three anonymous reviewers for their valuable and constructive comments
and suggestions.
Author Contributions
Vı́ctor Arroyo-Rodrı́guez and Gloria K. Pérez-Elissetche planned
the research and designed methodology with the advice of G.
Ramos-Fernandez. Gloria K. Pérez-Elissetche organized the data
and Vı́ctor Arroyo-Rodrı́guez analyzed the data. Vı́ctor ArroyoRodrı́guez and Gloria K. Pérez-Elissetche wrote the first draft of
the manuscript. All authors provided data and contributed critically
to the drafts.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect
to the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following support for the
research, authorship, and/or publication of this article: This research
was supported by the American Society of Primatologist (2012 ASP
Conservation Grant). GKPE obtained a scholarship from CONACyT,
Mexico. The Instituto de Investigaciones en Ecosistemas y
Sustentabilidad (UNAM) provided logistical support.
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