Content uploaded by Elizabeth M.C. Coggeshall
Author content
All content in this area was uploaded by Elizabeth M.C. Coggeshall on Sep 08, 2022
Content may be subject to copyright.
Original Research Article
Folia Primatol 2021;92:49–57
Mantled Howler Monkeys (Alouatta palliata) in
a Costa Rican Forest Fragment Do Not Modify
Activity Budgets or Spatial Cohesion in Response
to Anthropogenic Edges
Amy L. Schreier
a, c Laura M. Bolt
b, c Dorian G. Russell
c, d
Taylor S. Readyhough
a Zachary S. Jacobson
c, e Carrie Merrigan-Johnson
c, f
Elizabeth M.C. Coggeshall
c, g
a Department of Biology, Regis University, Denver, CO, USA; b Department of Anthropology, University of Waterloo,
Waterloo, ON, Canada; c The Maderas Rainforest Conservancy, Miami, FL, USA; d Department of Environmental
Science, American University, Washington, WA, USA; e Department of Anthropology and Archaeology,
University of Calgary, Calgary, AB, Canada; f Department of Anthropology, University of Toronto at Mississauga,
Mississauga, ON, Canada; g Department of Anthropology, Central Washington University, Ellensburg, WA, USA
Received: February 24, 2020
Accepted: September 23, 2020
Published online: December 8, 2020
Amy Schreier
Department of Biology, Regis University
3333 Regis Blvd. D-8
Denver, CO 80221 (USA)
aschreier @ regis.edu
© 2020 S. Karger AG, Basel
karger@karger.com
www.karger.com/fpr
DOI: 10.1159/000511974
Keywords
Anthropogenic edge effects · Habitat destruction ·
Behavioural edge effects · Tropical rain forest
Abstract
Forest fragmentation increases forest edge relative to forest
interior, with lower vegetation quality common for primates
in edge zones. Because most primates live in human-modi-
fied tropical forests within 1 km of their edges, it is critical to
understand how primates cope with edge effects. Few stud-
ies have investigated how primates inhabiting a fragment
alter their behaviour across forest edge and interior zones.
Here we investigate how anthropogenic edges affect the ac-
tivity and spatial cohesion of mantled howler monkeys (Al-
ouatta palliata) at the La Suerte Biological Research Station
(LSBRS), a Costa Rican forest fragment. We predicted the
monkeys would spend greater proportions of their activity
budget feeding and resting and a lower proportion travel-
ling in edge compared to forest interior to compensate for
lower resource availability in the edge. We also predicted
that spatial cohesion would be lower in the edge to mitigate
feeding competition. We collected data on activity and spa-
tial cohesion (nearest neighbour distance; number of indi-
viduals within 5 m) in forest edge and interior zones via in-
stantaneous sampling of focal animals. Contrary to predic-
tions, the monkeys spent equal proportions of time feeding,
resting and travelling in forest edge and interior. Similarly,
there were no biologically meaningful differences in the
number of individuals or the distance between nearest
neighbours in the edge (1.0 individuals; 1.56 m) versus the
interior (0.8 individuals; 1.73 m). Our results indicate that A.
palliata at LSBRS do not adjust their activity or spatial cohe-
sion patterns in response to anthropogenic edge effects,
suggesting that the monkeys here exhibit less behavioural
flexibility than A. palliata at some other sites. To develop ef-
fective primate conservation plans, it is therefore crucial to
study primate species’ responses to fragmentation across
their geographic range. © 2020 S. Karger AG, Basel
Downloaded by:
University Toronto Libr.
142.150.190.39 - 1/29/2021 9:14:26 PM
Schreier et al.
Folia Primatol 2021;92:49–57
50
DOI: 10.1159/000511974
Introduction
The destruction of tropical forests is a major threat to
global biodiversity [Haddad et al., 2015]; clearing land for
agriculture and cattle pastures are the leading sources of
this degradation [Estrada, 2015]. In Costa Rica, for ex-
ample, forests have been cut down, and their land has
been appropriated for agriculture since the 1970s [Garber
et al., 2010]. Consequently, remaining forest patches are
separated from one another by a matrix of pasture and
farmland, which negatively impacts some forest animals
that live there, including primates. Habitat fragmentation
is one of the main threats to primate species globally, with
more than half of all primate species experiencing consid-
erable population decline as a result [Boyle et al., 2013;
Chapman et al., 2013; Nijman, 2013; Estrada et al., 2017].
Although in some cases forest fragments may be com-
parable to continuous forests in size and productivity
[e.g., Zárate and Stevenson, 2014], many primate popula-
tions that inhabit forest fragments contend with de-
creased habitat size [Haddad et al., 2015; McKinney et al.,
2015] and, consequently, reduced food availability [e.g.,
Arroyo-Rodríguez and Mandujano, 2006; Arroyo-Rodrí-
guez et al., 2007; Chaves et al., 2012]. Primates generally
rely on large, abundant trees [e.g., van Roosmalen, 1985;
Chapman, 1988; Estrada et al., 1999b; Dunn et al., 2010;
Bolt et al., accepted], but fragments have fewer tree spe-
cies, and trees are less abundant and smaller than those in
continuous forests [e.g., Didham and Lawton, 1999; Ar-
royo-Rodríguez and Mandujano, 2006; Dunn et al., 2009;
Chaves et al., 2012]. Furthermore, forest fragmentation
causes a greater amount of forest edge relative to forest
interior [Laurance, 1991; Broadbent et al., 2008]. Abiotic
conditions including temperature, moisture, sunlight,
and wind differ at anthropogenic edges compared to for-
est interior [Laurance et al., 1998a; Chen et al., 1999],
which can lead to plant and animal species loss nearer to
the edge [Broadbent et al., 2008]. While in some cases for-
est vegetation is not impacted by edge effects [e.g., Phil-
lips et al., 2006] and edge zones may experience increased
recruitment of pioneer species and thus provide high-
quality resources for herbivores [Laurance et al., 1998b;
Meyer et al., 2009], vegetation quality for primates is gen-
erally lower at forest edges than interior with lower plant
biomass and fewer tall trees closer to the edge [e.g., Es-
trada et al., 1999a; Arroyo-Rodríguez and Mandujano,
2006; Lehman et al., 2006]. Because most primate species
live in human-modified forests within 1 km of the edge
[Estrada et al., 2017], almost a third of which are within
100 m of forest edges [Haddad et al., 2015], it is critical to
understand how primates contend with edge effects in
anthropogenically modified tropical forests.
To persist in forest edges, primates likely need to re-
duce feeding competition to secure sufficient food re-
sources in these poorer-quality habitats [Bicca-Marques,
2003; Arroyo-Rodríguez and Mandujano, 2006]. One
way to accomplish this is to alter their activity budgets to
spend more time feeding to ensure sufficient food intake
and to reduce energy expenditure by spending less time
travelling and more time resting [Silva and Ferrari, 2009;
Boyle and Smith, 2010]. While evidence is preliminary as
to how primates alter their activity patterns in edge zones
compared to forest interior [e.g. McGoogan, 2011; de
Vries, 2017], research has been more focused on activity
budgets in primates living in fragments compared with
those in continuous forests. Among platyrrhines, Brazil-
ian bearded saki monkeys (Chiropotes satanas chiropotes)
spent more time resting and less time travelling in small
fragments compared to large and continuous forests
[Boyle et al., 2009], and Central American spider mon-
keys (Ateles geoffroyi) living in fragments in Mexico spent
more time feeding and less time travelling compared to
those living in continuous forest [Chaves et al., 2011].
Across three groups of mantled howler monkeys (Alouat-
ta palliata) living in fragments of varying sizes in Los
Tuxtlas, Mexico, time spent travelling increased with
fragment size, although there were no clear differences in
resting or feeding time [Juan et al., 2000]. A. palliata liv-
ing in areas heavily modified by humans in the Curú
Wildlife Refuge in Costa Rica spent more time feeding
than those in areas less impacted by humans, although
there was no difference in time spent resting [McKinney,
2019]. A. palliata activity patterns in edge versus interior
zones of a forest fragment have not yet been examined.
In response to limited food availability in fragments,
primates can also adjust their group size and spatial cohe-
sion to reduce feeding competition [e.g., Chapman et al.,
1995]. For example, group cohesion was lower in dia-
demed sifakas (Propithecus diadema) living in fragments
compared to those in continuous forest [Irwin, 2007].
Specifically, distances between nearest neighbours were
greater in fragments than in continuous forest, with near-
est neighbour differences across forest type most extreme
in feeding contexts. In forest fragments, the sifakas relied
more heavily on smaller, more dispersed resources like
mistletoe, requiring them to spread out further across
multiple food patches [Irwin, 2007]. In the Curú Wildlife
Refuge in Costa Rica, A. palliata group cohesion was low-
er in areas more heavily modified by humans [McKinney,
2019]. Additional focused study on the effects of anthro-
Downloaded by:
University Toronto Libr.
142.150.190.39 - 1/29/2021 9:14:26 PM
Howler Monkeys Do Not Modify Activity
or Spatial Cohesion in Forest Edges
51
Folia Primatol 2021;92:49–57
DOI: 10.1159/000511974
pogenic edges on A. palliata spatial cohesion is critical to
understanding if and how this species can persist in an
increasingly fragmented landscape consisting of greater
proportions of forest edge compared to interior.
In this study we examine anthropogenic edge effects
on the activity patterns and spatial cohesion of Alouatta
palliata at La Suerte Biological Research Station (LSBRS),
a fragmented tropical rain forest in north-eastern Costa
Rica. A. palliata are folivore-frugivores [di Fiore et al.,
2011; Garber et al., 2015; Aristizibal et al., 2017; Righini
et al., 2017] that live in large multimale, multifemale so-
cial groups of about 10–15 individuals, although group
size can top 40 [Bezanson et al., 2008; Ryan et al., 2008; di
Fiore et al., 2011]. Groups are typically spatially cohesive
[Milton, 1980; Crockett and Eisenberg, 1987] but have
been observed separating into subgroups in some in-
stances [Leighton and Leighton, 1982; Chapman, 1990;
Bezanson et al., 2008], probably to increase foraging ef-
ficiency [Dias and Rodríguez-Luna, 2006]. Howler mon-
keys spend most of their time resting [e.g., Estrada et al.,
1999b], likely because leaves contain toxins and complex
compounds that are difficult to digest [Milton, 1979,
1980].
Previous research at LSBRS showed lower tree species
richness, diameter at breast height (DBH) and canopy
cover in anthropogenic edges (< 100 m from forest bound-
ary) compared to forest interior [Bolt et al., 2018, 2019].
Given that greater canopy cover and the presence of large
trees provide high-quality primate habitat [Arroyo-Ro-
dríguez and Mandujano, 2006; Dunn et al., 2009; Chaves
et al., 2012], and tree DBH is a reliable proxy for fruit
abundance [e.g., Leighton and Leighton, 1982; Peters et
al., 1988; Chapman et al., 1992], vegetation quality for
monkeys in forest edge zones at LSBRS is lower than that
of forest interior. Furthermore, A. palliata population
density at LSBRS is 73.8 individuals/km2 [Schreier and
Bolt, 2020], strikingly higher than at other mantled howl-
er sites where density typically ranges from 5 to 30 indi-
viduals/km2 [e.g., Estrada, 1982; Stoner, 1996; Clarke et
al., 2002b]. This combination of high population density
and reduced vegetation quality in edge zones suggests
more substantial feeding competition at LSBRS than oth-
er A. palliata sites.
Previous studies at LSBRS reported that A. palliata
group encounter rates did not differ significantly between
anthropogenic forest edge and interior zones [Bolt et al.,
2018, 2020b], although howling behaviour did vary across
habitat zones. Howling bouts were longer and consisted
of more howls in the forest interior, presumably to an-
nounce their presence to other howler monkey groups in
forest locations with high-quality vegetation [Bolt et al.,
2019, 2020a]. These results suggest that while the mon-
keys inhabit anthropogenic edge and interior forest at LS-
BRS evenly despite vegetation differences across forest
zones, anthropogenic edges affect howling behaviour and
may therefore also influence other aspects of behaviour.
We hypothesize that A. palliata at LSBRS will alter
their activity budget and spatial cohesion in response to
forest edges. Given differences in vegetation quality
across forest zones at LSBRS [Bolt et al., 2018, 2019, 2020a,
b], coupled with the high population density that likely
increases feeding competition, we predict that A. palliata
will spend greater proportions of their activity budget
feeding and resting, and a lower proportion of their activ-
ity budget travelling in the edge than the forest interior to
ensure sufficient food intake and reduce energy expendi-
ture. Furthermore, we predict that monkeys will be less
spatially cohesive in the edge compared to the forest in-
terior in order to reduce feeding competition.
Methods
Study Site
We conducted this study at LSBRS in north-eastern Costa Rica
(10°26’ N, 83°46’ W). LSBRS is a tropical lowland fragmented rain
forest totalling approximately 3 km2 of primary forest, secondary
forest and regenerating pastures [Pruetz and Leasor, 2002; Garber
et al., 2010]. The main forested area where we conducted research
comprises two connected forest patches (“Large Forest” = 0.935
km2 and “Small Forest” = 0.35 km2) as well as a partially cleared
area for “camp” (0.071 km2) [Molina, 2015; Bolt et al., 2018]. The
area around the reserve consists mainly of pasture and coconut
plantations [Molina, 2015; Brandt and Singleton, 2018]. LSBRS is
a model site at which to examine the effects of anthropogenic edg-
es on A. palliata activity and spatial cohesion patterns because of
the distinct edges surrounding the forest fragment. Barbed wire
fences indicate the property perimeter, flagging the sharp bound-
ary between preserved forest in LSBRS and surrounding developed
land [Molina, 2015].
Along with mantled howler monkeys, white-faced capuchin
(Cebus capucinus) and Central American spider monkeys (A. geof-
froyi) inhabit the forests at LSBRS. For the current study, we ob-
served 11 groups of howler monkeys, 3 in the Small Forest and 8
in the Large Forest, which is consistent with previous population
surveys [Pruetz and Leasor, 2002; Garber et al., 2010]. The mean
group size was 9.1 individuals (SD 3.2).
Data Collection
We collected data on A. palliata activity and spatial cohesion
patterns from May to August 2017, May to August 2018 and De-
cember 2018 to January 2019. Most of the groups we sampled in-
habited either the edge or interior zone, although a few groups
ranged across both forest zones. The monkeys were all habituated
to the presence of researchers; they did not howl or move away
from researchers when we approached and observed them. Re-
Downloaded by:
University Toronto Libr.
142.150.190.39 - 1/29/2021 9:14:26 PM
Schreier et al.
Folia Primatol 2021;92:49–57
52
DOI: 10.1159/000511974
searchers sampled monkeys daily between 5.00 and 18.00 h. We
aimed to collect approximately equal amounts of data across an-
thropogenic edge and interior forest zones. We defined edge as 100
m from any anthropogenic forest boundary, following previous
edge effect studies [e.g., Laurance et al., 2002; Pohlman et al., 2009]
and consistent with prior studies at LSBRS [Bolt et al., 2018, 2019,
2020b]. Indeed, results from vegetation surveys at LSBRS show
that canopy cover and DBH are both lower within 100 m of the
forest edge compared to forest greater than 100 m from the forest
boundary [Bolt et al., 2018, 2019, 2020b].
We conducted 30-min samples on single howler monkeys (in-
fants were not sampled), during which we conducted instanta-
neous scan samples at 2-min intervals [Altmann, 1974]. At each
scan we recorded the focal animal’s activity (i.e., rest – remain in
one location on substrate; feed – manipulate food or water with
hands, feet, mouth; travel – move along a substrate (not while feed-
ing); social – includes grooming, playing, aggression, submission;
or other – any behaviour not mentioned above) [Paterson, 2001].
To quantify spatial cohesion, we recorded the number of individu-
als within a 5-m radius of the focal subject during each scan [cf.
Chapman, 1990] and estimated the distance (in metres) to the
nearest monkey in any of the distance classes: 0, 0.5, 1, 2, 3, 4, 5, 6,
7, 8, 9, 10 m or > 10 m, and age/sex class of neighbour monkeys was
recorded whenever possible [Irwin, 2007]. During each 30-min
sample, we recorded the location of the focal animal within LSBRS
using a Garmin GPSMAP 62s hand-held navigator. Because indi-
vidual monkey identities were unknown in this population, we
cannot be certain how many times each individual was sampled
over the course of the study period. We aimed to sample groups
equally across forest zones with no more than 2 researchers col-
lecting data on a single monkey group at any given time. At least
2 h had to elapse before resampling a monkey, and a single monkey
could not be resampled more than twice in a day; in practice, it was
rare that any monkey was sampled more than once in a 3-hour
period. We used body size and tail length differences across group
members, and more distinct characteristics when present, to pre-
vent resampling individuals. If the monkey being sampled was out
of view for 10 min or more of the 30 min sample, the sample was
discarded. In preparation for this study, researchers conducted in-
stantaneous sampling of focal animals simultaneously. We calcu-
lated interobserver agreement by calculating the number of scans
in agreement across observers by the total number of scans, and
data collection began once researchers reached 94% agreement.
Data Analysis
We base our analyses on 792 h of 30-min focal samples (1,629
30-min samples; 26,064 2-min scans), 427 h (878 30-min samples;
14,048 2-min scans) in anthropogenic edges and 365 h (751 30-
min samples; 12,016 2-min scans) in forest interior. To test our
hypothesis that A. palliata will alter their activity budget in re-
sponse to forest edges, we fit 3 binomial generalized linear mixed
models (GLMMER), one for each activity (i.e., resting, feeding,
travelling) with fixed effect for forest zone. To quantify the effect
of forest zone on spatial cohesion, we fit generalized linear mixed
models (GLMM), with distributions chosen based on data type.
For number of individuals within 5 m of the focal subject, we used
a Poisson distribution with log-link function. For distance to
nearest neighbour, we first log-transformed the data (log(x + 1))
to meet assumptions of normality and used a Gaussian distribu-
tion with identity link function. For each model, we included a
random effect for each 30-min focal sample to control for the au-
tocorrelation across 2-min scans in each 30-min focal sample. To
test whether our response variables differed by forest zone, we also
fit a null (i.e., intercept-only) model for each response (i.e., each
activity, number of individuals within 5 m, distance to nearest
neighbour) and compared Akaike information criteria (AICs)
within each model pair (i.e., null and forest zone) [Burnham et al.,
2011].
Exploratory data analyses showed consistent results across age-
sex classes and we thus include adult males, adult females and ju-
veniles in all analyses reported here. Similarly, spatial cohesion re-
sults did not differ significantly based on activity, and we thus in-
clude the complete data set (comprising all activity types) in our
present analyses. All statistical analyses were conducted in open
source statistical software R (version 3.4.1 [R Core Team, 2017])
with the following packages: “tidyr” and “dplyr” for data manipu-
lation [Wickham et al., 2017; Wickham and Henry, 2017] and
“lme4” for GLMM [Bates et al., 2015]. α-Values < 0.05 were con-
sidered significant.
Results
Overall, A. palliata spent 67.5% of their activity budget
resting, 12.5% feeding and 11.3% travelling. The monkeys
spent equal proportions of their activity budget resting
(67.8% in edge vs. 67.2% in interior), feeding (12.4% in
edge vs. 12.5% in interior) and travelling (11.1% in the
edge vs. 11.5% in interior) in anthropogenic edge and for-
est interior zones. There were no significant differences
in the odds of resting (p = 0.570), feeding (p = 0.572) or
travelling (p = 0.735; binomial GLMMER) across forest
interior and anthropogenic edge. The forest zone models
did not improve the model fits compared to the null mod-
els (as evidenced by higher AIC in the forest zone models
than the null models for resting [AIC = 24,573.8 vs.
24,572.1], feeding [AIC = 14,647.3 vs. 14,645.7] and trav-
elling [AIC = 16,537.9 vs. 16,536.0]; Table 1), further
showing that forest zone is not a strong predictor of activ-
ity budget.
Across forest zones, the mean number of individuals
within 5 m was 0.86 (range = 0–12; confidence interval,
CI: 0.81–0.92). GLMM results indicated that the mean
number of individuals within 5 m was 0.96 in the edge
(CI: 0.84–1.09) and 0.77 in the interior (CI: 0.70–0.84;
p = 0.001). AIC was lower in the forest zone model
(AIC = 54,179.0) than the null model (AIC = 54,188.1;
Table 2). The median distance to the nearest neighbour
across forest zones was 1.64 m (range = 0–13 m; CI: 1.52–
1.76). Results of GLMM showed that median distance did
not differ between the forest interior (1.56 m; CI: 1.35–
1.80) and anthropogenic edge (1.73 m; CI: 1.53–1.92; p =
0.156). Including forest zone did not improve the model
Downloaded by:
University Toronto Libr.
142.150.190.39 - 1/29/2021 9:14:26 PM
Howler Monkeys Do Not Modify Activity
or Spatial Cohesion in Forest Edges
53
Folia Primatol 2021;92:49–57
DOI: 10.1159/000511974
fit compared to the null model (AIC = 26,023.7 vs.
26,023.6; Table 2), further demonstrating that forest zone
does not predict distance to nearest neighbour.
Discussion
Our hypothesis that A. palliata inhabiting LSBRS, a
Costa Rican forest fragment, would modify their activity
budget and spatial cohesion patterns in response to an-
thropogenic edges due to the lower vegetation quality
compared to forest interior was not supported. Despite
vegetation at the LSBRS being richer in forest interior
compared to the edge [Bolt et al., 2018, 2019, 2020a, b],
and the high A. palliata population density at this site
[Schreier and Bolt, 2020], the monkeys spent equal pro-
portions of their activity budget resting, feeding and trav-
elling in edge and interior forest zones. There were also
no biologically meaningful differences in the number of
individuals or distance between nearest neighbours in the
edge versus the interior. These results suggest that the
monkeys at LSBRS exhibit less behavioural flexibility
than their conspecifics at some other sites [e.g., Clarke et
al., 2002a; McKinney, 2019] and highlight the need to
study primate species’ responses to fragmentation across
their geographic ranges in order to develop effective pri-
mate conservation plans.
Our results that activity patterns did not vary in re-
sponse to forest fragmentation are not consistent with
work from Los Tuxtlas, Mexico, where A. palliata spent
more time travelling as fragment size increased [Juan et
al., 2000], and the Curú Wildlife Refuge in Costa Rica
where the monkeys spent more time feeding in areas
more heavily modified by humans [McKinney, 2019].
However, in line with our results, Cristóbal-Azkarate and
Arroyo-Rodríguez [2007] found no relationship between
howler activity patterns and fragment size in Los Tuxtlas,
nor did Bicca-Marques [2003] in his survey of 6 different
howler monkey species across 27 study sites throughout
Central and South America.
Therefore, both our results at LSBRS as well as those
from elsewhere in the geographic range of A. palliata sug-
gest that some howler populations can subsist in areas
with reduced resource availability without modifying
their activity budgets. This may be due to the fact that
leaves are readily available even in poorer-quality habi-
tats. At LSBRS, leaves made up about 60% of the mon-
keys’ diet in both forest edge and interior [Russell, 2018],
indicating availability of foliage across forest zones. Thus,
there may be no need to increase feeding time in the edge.
Activity Model AIC log likelihood Deviance Residual df
Resting Forest zone model 24,573.8 –12,283.9 24,567.8 25,367
Null model 24,572.1 –12,284.0 24,568.1 25,368
Feeding Forest zone model 14,647.3 –7,320.7 14,641.3 25,367
Null model 14,645.7 –7,320.8 14,641.7 25,368
Travelling Forest zone model 16,537.9 –8,266.0 16,531.9 25,367
Null model 16,536.0 –8,266.0 16,532.0 25,368
AIC, Akaike information criterion; df, degree of freedom.
Table 1. Binomial generalized mixed
model comparisons for activity budget of
Alouatta palliata at La Suerte Biological
Research Station
Spatial cohesion
variable
Model AIC log likelihood Deviance Residual
df
Individuals within
5 m, n
Forest zone model 54,179.0 –27,086.5 54,173.0 21,461
Null model 54,188.1 –27,092.0 54,184.1 21,462
Distance to nearest
neighbour
Forest zone model 26,023.7 –13,007.8 26,015.7 19,897
Null model 26,023.6 –13,008.8 26,017.6 19,898
AIC, Akaike information criterion; df, degree of freedom.
Table 2. Generalized mixed model
comparisons for spatial cohesion of
Alouatta palliata at La Suerte Biological
Research Station
Downloaded by:
University Toronto Libr.
142.150.190.39 - 1/29/2021 9:14:26 PM
Schreier et al.
Folia Primatol 2021;92:49–57
54
DOI: 10.1159/000511974
It is also possible that howler monkeys are constrained in
their ability to alter their activity budgets compared to
other primates [Arroyo-Rodríguez and Dias, 2010].
While howler gut morphology is not particularly special-
ized for a leaf-heavy diet, their gut retention time is long,
enabling efficient digestion of leaves [Milton, 1980, 1998].
Howler monkeys, therefore, need to devote the majority
of their time to resting to ensure effective digestion re-
gardless of habitat quality, limiting how much they can
vary time spent engaged in other activities. Another way
howler monkeys might deal with reduced food availabil-
ity in fragments is by diversifying their diet and increas-
ing the number of tree species they consume [Silver and
Marsh, 2003]. We hope to address this hypothesis at
LSBRS in the near future when we have a robust howler
diet data set.
Spatial cohesion did not vary across anthropogenic
edges and forest interior either. There was no difference
in the median distance between nearest neighbours across
forest zones; while the mean number of individuals with-
in 5 m was statistically significantly different between an-
thropogenic edges and forest interior, we argue that this
variation is not biologically meaningful (0.8 vs. 1.0 of a
monkey are both, after all, essentially one monkey, and
the significant value is likely an artefact of large sample
size). These results are consistent with those of Stevenson
et al. [2015] who found that adult woolly monkeys (Lago-
thrix spp.) were found within 5 m of other adults at the
same frequency across two forest sites that differed in size
and continuity, suggesting there were sufficient resources
in the smaller fragment to maintain the same level of so-
cial cohesion. The fact that A. palliata at LSBRS did not
vary their cohesion patterns across forest zones despite
lower vegetation quality in the edge may be explained by
the fact that, overall, they fed and rested from trees that
were much larger than the average tree size at LSBRS.
Mean DBH of both feeding and resting trees was almost
5 times that of average tree DBH in the interior and 4
times as large in the edge [Schreier and Bolt, unpubl.
data], and feeding trees were taller than the average tree
height at LSBRS in both forest zones [Russell, 2018; Bolt
et al., accepted]. The howler monkeys therefore selected
the largest trees in both the edge and interior. A. palliata
at other fragmented sites also prefer larger trees than the
average size in their forests [Munoz et al., 2006]. While
the higher DBH and canopy cover in the forest interior at
the LSBRS [Bolt et al., 2018; Bolt et al., 2019] shows that
there are fewer large trees spread further apart in the edge,
selecting the very largest trees likely allows the monkeys
to remain in and near the limited number of preferred
trees in this forest zone. By feeding on the largest trees –
that accommodate many monkeys at once – in both forest
zones, the monkeys may not need to vary spatial cohesion
to reduce feeding competition. The presence of large
feeding trees throughout LSBRS may therefore enable
howler monkeys to spend equal proportions of their ac-
tivity budget feeding and to maintain consistent spatial
cohesion patterns across forest zones.
The monkeys’ spatial cohesion patterns may also be a
consequence of the high density of A. palliata at LSBRS.
While the population density of 73.8 individuals/km2
[Schreier and Bolt, 2020] is comparable to that of other
howler monkey species in a few sites [e.g. González et al.,
2002; Palma et al., 2011], it is substantially higher than at
other sites. Population density of A. palliata at Los Tuxt-
las, for example, is only 23.3 individuals/km2 [Estrada,
1982]. In Costa Rica, population density is 30 individuals/
km2 at La Pacifica [Clarke et al., 2002b], grew from 4.9 to
7.9 individuals/km2 at Santa Rosa National Park [Fedigan
et al., 1998) and is 7–15 individuals/km2 at La Selva Bio-
logical Station despite the similar group sizes and sex ra-
tios as at LSBRS [Stoner, 1996; Bolt et al., 2019]. These
results are consistent with other work that shows A. pal-
liata density is inversely related to forest size [Cristóbal-
Azkarate et al., 2005; Mandujano and Escobedo-Morales,
2008]. The especially high density of monkeys at the LS-
BRS may necessitate members of both edge and interior
groups to remain in close proximity simply due to the
high number of individuals and limited space.
Our results that A. palliata at LSBRS do not modify
their activity budgets or spatial cohesion patterns in re-
sponse to edge effects are consistent with the species’ rep-
utation for being tolerant to habitat disturbance [Arroyo-
Rodríguez and Dias, 2010]. However, unlike A. palliata at
other sites that alter their behaviour in response to an-
thropogenic habitat modification [e.g., Clarke et al.,
2002a; McKinney, 2019], those at LSBRS exhibit limited
behavioural flexibility in response to lower vegetation
quality. It is possible that recent habitat destruction to
make way for banana and pineapple plantations in the
area surrounding LSBRS has necessitated an influx of
monkeys into this remaining forest fragment, leading to
the very high A. palliata population density here. That the
monkeys inhabit edge zones and forest interior equally
[Bolt et al., 2018] may only be a current phenomenon due
to overcrowding.
Future behavioural observations at LSBRS will shed
light onto whether the monkeys begin to modify their ac-
tivity and spatial cohesion patterns in edges over time in
response to the lower habitat quality. It is important to
Downloaded by:
University Toronto Libr.
142.150.190.39 - 1/29/2021 9:14:26 PM
Howler Monkeys Do Not Modify Activity
or Spatial Cohesion in Forest Edges
55
Folia Primatol 2021;92:49–57
DOI: 10.1159/000511974
note that previous work showed that howling behaviour
differs across edge and interior zones at LSBRS [Bolt et
al., 2019, Bolt et al., 2020a], suggesting that A. palliata are
flexible in at least some aspects of their behavioural rep-
ertoire. Differences in howling behaviour across various
forest regions may be sufficient for reducing feeding com-
petition at LSBRS; if so, it might obviate the need to alter
activity and/or spatial cohesion patterns. Future work
should examine the relationship between howling and
feeding to determine whether changes in howling be-
haviour effectively mitigate feeding competition at the
LSBRS. With most primates worldwide living in close
proximity to a forest edge [Estrada et al., 2017], it is cru-
cial to understand how primates deal with edge effects.
This study explicitly examines how primates behavioural-
ly cope with edge effects and underlines the importance
of studying primate responses to forest fragmentation
across species’ geographic ranges to effectively inform
conservation plans.
Acknowledgements
We are grateful to Renee Molina and the Maderas Rainforest
Conservancy for permission to conduct research at the LSBRS and
for support in the field. We thank Madison Azzara, Christina
Doelling, Lili Hagg, Stacy Hill, Kenyah Lawler, Alyssa MacAus-
land, Jenna Owens, Jesse Rosso, Renate Schlaht and Elizabeth
Sheehan for behavioural data collection. Finally, we thank Kristo-
for Voss for statistical guidance, and Michael Ennis and Ryan Jan-
zen for project support. Funding for this research was provided by
the University Research and Scholarship Council at Regis Univer-
sity, the Cosmos Club Foundation and the Explorer’s Club.
Statement of Ethics
Permission to conduct research at the LSBRS was granted by
the Maderas Rainforest Conservancy, and the research adhered to
the legal requirements of Costa Rica. Protocols were approved by
the Regis University Institutional Animal Care and Use Commit-
tee.
Conflict of Interest Statement
The authors have no conflicts of interest to declare.
Funding Sources
Funding for field work was awarded by the Regis University
Research and Scholarship Council, Cosmos Club Foundation and
Explorer’s Club.
Author Contributions
A.L.S. was responsible for project design, data collection, data
analysis and interpretation, and writing and revising the manu-
script. L.M.B. was responsible for project design, data collection,
data analysis and interpretation, and writing and revising the man-
uscript. D.G.R. collected and analysed data, and contributed to the
writing and revision of the manuscript. T.S.R. analysed data and
contributed to the writing and revision of the manuscript. Z.S.J.
collected data and contributed to the writing and revision of the
manuscript. C.M.-J. collected data and contributed to the writing
and revision of the manuscript. E.M.C. collected data and contrib-
uted to the writing and revision of the manuscript. All authors ap-
proved the final version of the submitted paper.
References
Altmann J (1974). Observational study of behav-
ior: sampling methods. Behaviour 49: 227–
265.
Aristizibal JF, Rothman JM, Garcia-Feria LM, Se-
rio-Silva JC (2017). Contrasting time-based
and weight-based estimates of protein and en-
ergy intake of black howler monkeys (Alouat-
ta pigra). American Journal of Primatology 79:
1–8.
Arroyo-Rodríguez V, Dias PA (2010). Effects of
habitat fragmentation and disturbance on
howler monkeys: a review. American Journal
of Primatology 72: 1–16.
Arroyo-Rodríguez V, Mandujano S (2006). For-
est fragmentation modifies habitat quality for
Alouatta palliata. International Journal of Pri-
matology 27: 1079–1096.
Arroyo-Rodríguez V, Mandujano S, Benitez-
Malvído J, Cuende-Fanton C (2007). The in-
fluence of large tree density on howler mon-
key (Alouatta palliata mexicana) presence in
very small rain forest fragments. Biotropica
39(6): 760–766.
Bates D, Maechler M, Bolker B, Walker S (2015).
Fitting linear mixed-effects models using
lme4. Journal of Statistical Software 67(1):
1–48.
Bezanson M, Garber PA, Murphy JT, Premo LS
(2008). Patterns of subgrouping and spatial
affiliation in a community of mantled howl-
ing monkeys (Alouatta palliata). American
Journal of Primatology 70(3): 282–293.
Bicca-Marques JC (2003). How do howler mon-
keys cope with habitat fragmentation? In Pri-
mates in Fragments (Marsh LK, ed.), pp 283–
303. New York, Kluwer Academic/Plenum
Press.
Bolt LM, Cavanaugh MN, Schreier AL (accepted).
Lone males: solitary and group-living male
howler monkey (Alouatta palliata) behavior-
al ecology in a Costa Rican rainforest. Ameri-
can Journal of Physical Anthropology.
Bolt LM, Russell DG, Coggeshall EMC, Jacobson
ZS, Merrigan-Johnson C, Schreier AL
(2020a). Howling by the river: howler mon-
key (Alouatta palliata) communication in an
anthropogenically altered riparian forest in
Costa Rica. Behaviour 157: 77–100. DOI:
10.1163/1568539X-00003582.
Bolt LM, Schreier AL, Russell DG, Jacobson ZS,
Merrigan-Johnson C, Barton MC, Coggeshall
EMC (2019). Howling on the edge: mantled
howler monkey (Alouatta palliata) howling
behaviour and anthropogenic edge effects in
a fragmented tropical rainforest in Costa Rica.
Ethology 125: 593–602.
Downloaded by:
University Toronto Libr.
142.150.190.39 - 1/29/2021 9:14:26 PM
Schreier et al.
Folia Primatol 2021;92:49–57
56
DOI: 10.1159/000511974
Bolt LM, Schreier AL, Voss KA, Sheehan EA, Bar-
rickman NL (2020b). Down by the riverside:
riparian edge effects on three monkey species
in a fragmented Costa Rican forest. Biotropica
52: 541–553. DOI: 10.1111/btp.12769.
Bolt LM, Schreier AL, Voss KA, Sheehan EA, Bar-
rickman NL, Pryor NP, Barton MC (2018).
The influence of anthropogenic edge effects
on primate populations and their habitat in a
fragmented rainforest in Costa Rica. Primates
59(3): 301–311.
Boyle SA, Smith AT (2010). Behavioral modifica-
tions in northern bearded saki monkeys (Chi-
ropotes satanas chiropotes) in forest fragments
of central Amazonia. Primates 51: 43–51.
Boyle SA, Lenz BB, Gilbert KA, Sprionello WR,
Santamaría-Gómez M, et al (2013). Primates
of the Biological Dynamics of Forest Frag-
ments Project: a history. In Primates in Frag-
ments (Marsh LK, ed.), pp 57–74. New York,
Kluwer Academic/Plenum Press.
Boyle SA, Lourenco WA, da Silva LR, Smith AT
(2009). Travel and spatial patterns change
when northern bearded saki monkeys (Chi-
ropotes satanas chiropotes) inhabit forest frag-
ments. International Journal of Primatology
30: 515–531.
Brandt LSE, Singleton M (2018). Record of Baird’s
tapir Tapirus bardii at the La Suerte Biological
Field Station in the Caribbean Lowlands of
Costa Rica. Peer Journal 6: e27128v1. DOI:
10.7287/peerj.preprints.27128v1.
Broadbent EN, Asner GP, Keller M, Knapp DE,
Oliveira PJC, Silva JN (2008). Forest fragmen-
tation and edge effects from deforestation and
selective logging in the Brazilian Amazon. Bi-
ological Conservation 141(7): 1745–1757.
Burnham KP, Anderson DR, Huyvaert KP (2011).
AIC model selection and multimodel infer-
ence in behavioral ecology: some background,
observations, and comparisons. Behavioral
Ecology and Sociobiology 65(1): 23–35.
Chapman C (1988). Patterns of foraging and
range use by three species of neotropical pri-
mates. Primates 29: 177–194.
Chapman CA (1990). Ecological constraints on
group size in three species of Neotropical pri-
mates. Folia Primatologica 55: 1–9.
Chapman C, Chapman L, Wrangham R, Hunt K,
Gebo D, Gardner L (1992). Estimators of fruit
abundance of tropical trees. Biotropica 24:
527–531.
Chapman CA, Ghai R, Jacob A, Mugume Koojo
S, Mugume Koojo S, Reyna-Hurtado R, et al
(2013). Going, going, gone: a 15-year history
of the decline of primates in forest fragments
near Kibale National Park, Uganda. In Pri-
mates in Fragments (Marsh LK, ed.), pp 89–
104. New York, Kluwer Academic/Plenum
Press.
Chapman CA, Wrangham RW, Chapman LJ
(1995). Ecological constraints on group size:
an analysis of spider monkey and chimpanzee
subgroupings. Behavioral Ecology and Socio-
biology 36: 59–70.
Chaves OM, Stoner KE, Arroyo-Rodríguez V
(2011). Seasonal differences in activity pat-
terns of Geoffroyi’s spider monkeys (Ateles
geoffroyi) living in continuous and fragment-
ed forests in Southern Mexico. International
Journal of Primatology 32: 960–973.
Chaves OM, Stoner KE, Arroyo-Rodríguez V
(2012). Differences in diet between spider
monkey groups living in forest fragments and
continuous forests in Mexico. Biotropica 44:
105–113.
Chen J, Saunders SC, Crow TR, Naiman RJ, Bro-
sofske KD, Mroz GD, et al (1999). Microcli-
mate in forest ecosystem and landscape ecol-
ogy: variations in local climate can be used to
monitor and compare the effects of different
management regimes. Bio Science 49(4): 288–
297.
Clarke MR, Collins DA, Zucker EL (2002a). Re-
sponses to deforestation in a group of mantled
howlers (Alouatta palliata) in Costa Rica. In-
ternational Journal of Primatology 23: 365–
381.
Clarke MR, Crockett CM, Zucker EL, Zaldivar M
(2002b). Mantled howler population of Haci-
enda La Pacifica, Costa Rica, between 1991
and 1998: effects of deforestation. American
Journal of Primatology 56: 155–163.
Cristóbal-Azkarate J, Arroyo-Rodríguez V
(2007). Diet and activity pattern of howler
monkeys (Alouatta palliata) in Los Tuxtlas,
Mexio: effects of habitat fragmentation and
implications for conservation. American
Journal of Primatology 69: 1012–1029.
Cristóbal-Azkarate J, Vea J, Asensio N, Rodri-
guez-Luna E (2005). Biogeographical and flo-
ristic predictors of the presence and abun-
dance of mantled howlers (Alouatta palliata
mexicana) in rainforest fragments at Los Tux-
tlas, Mexico. American Journal of Primatology
67: 209–222.
Crockett CM, Eisenberg JF (1987). Howlers: vari-
ations in group size and demography. In Pri-
mate Societies (Smuts BB, et al, eds.), pp 54–
68. Chicago, University of Chicago Press.
De Vries M (2017). How “Edgy” Are Tamarins? A
Preliminary Investigation of Spatial Variation
in the Behaviour of Two Sympatric Callitrich-
ids. MS thesis, University of Toronto.
Dias PAD, Rodriguez-Luna E (2006). Seasonal
changes in male associative behavior and sub-
grouping of Alouatta palliata on an island. In-
ternational Journal of Primatology 27: 1635–
1651.
Didham RK, Lawton JH (1999). Edge structure
determines the magnitude of changes in mi-
croclimate and vegetation structure in tropi-
cal forest fragments. Biotropica 31: 17–30.
Di Fiore A, Link A, Campbell CJ (2011). The
atelines: behavioral and sociological diversity
in a New World monkey radiation. In Pri-
mates in Perspective (Campbell CJ, et al, eds.),
pp 155–158. New York, Oxford University
Press.
Dunn JC, Cristóbal-Azkarate J, Vea JJ (2009). Dif-
ferences in diet and activity patterns between
groups of Alouatta palliata associated with
the availability of big trees and fruit of top
food taxa. American Journal of Primatology
71: 654–662.
Dunn JC, Cristóbal-Azkarate J, Vea JJ (2010). Sea-
sonal variations in the diet and feeding effort
of two groups of howlers in different sized
fragments. International Journal of Primatol-
ogy 31: 887–903.
Estrada A (1982). Survey and census of howler
monkeys (Alouatta palliata) in the rain forest
of “Los Tuxtlas,” Veracruz, Mexico. American
Journal of Primatology 2: 363–372.
Estrada A (2015). Conservation of Alouatta: so-
cial and economic drivers of habitat loss, in-
formation vacuum, and mitigating popula-
tion declines. In Howler Monkeys. Develop-
ments in Primatology: Progress and Prospects
(Kowalewski M, et al, eds.), pp 383–409. New
York, Springer.
Estrada A, Anzures A, Coates-Estrada R (1999a).
Tropical rain forest fragmentation, howler
monkeys (Alouatta palliata), and dung bee-
tles at Los Tuxtlas, Mexico. American Journal
of Primatology 48: 253–262.
Estrada A, Garber PA, Rylands AB, Roos C, Fer-
nandez-Duque E, Di Fiore A, et al (2017). Im-
pending extinction crisis of the world’s pri-
mates: why primates matter. Science Advances
3: e1600946.
Estrada A, Juan-Solano S, Martínez TO, Coates-
Estrada R (1999b). Feeding and general activ-
ity patterns of a howler monkey (Alouatta
palliata) troop living in a forest fragment at
Los Tuxtlas, Mexico. American Journal of Pri-
matology 48: 167–183.
Fedigan LM, Rose LM, Avila RM (1998). Growth
of mantled howler groups in a regenerating
Costa Rican dry forest. International Journal
of Primatology 19: 405–432.
Garber P, Molina A, Molina R (2010). Putting the
community back in community ecology and
education: the role of field schools and private
reserves in the ethical training of primatolo-
gists. American Journal of Primatology 72:
785–793.
Garber PA, Righini N, Kowalewski MM (2015).
Evidence of alternative dietary syndromes
and nutritional goals in the genus Alouatta. In
Howler Monkeys. Developments in Primatol-
ogy: Progress and Prospects (Kowalewski M, et
al, eds.), pp 85–109. New York, Springer.
González V, Zunino G, Kowalewski M, Bravo S
(2002). Densidad de monos aulladores (Al-
ouatta caraya) y composición y estructura de
la selva de inundación en una isla del Río
Paraná medio. Revista del Museo Argentino de
Ciencias Naturales nueva serie 4: 7–11.
Haddad NM, Brudwig LA, Clobert J, Davies KF,
Gonzalez A, Holt RD, et al (2015). Habitat
fragmentation and its lasting impact on
Earth’s ecosystems. Science Advances 1:
e1500052.
Downloaded by:
University Toronto Libr.
142.150.190.39 - 1/29/2021 9:14:26 PM
Howler Monkeys Do Not Modify Activity
or Spatial Cohesion in Forest Edges
57
Folia Primatol 2021;92:49–57
DOI: 10.1159/000511974
Irwin MT (2007). Living in forest fragments re-
duces group cohesion in diademed sifakas
(Propithecus diadema) in Eastern Madagascar
by reducing food patch size. American Jour-
nal of Primatology 69: 434–447.
Juan S, Estrada A, Estrada-Coates R (2000). Con-
trastes y similitudes en el uso de recursos y
patron general de actividades en tropas de
monos aulladores (Alouatta palliata) en frag-
mentos de selva en Los Tuxtlas, Mexico. Neo-
tropical Primates 8: 131–135.
Laurance WF (1991). Edge effects in tropical for-
est fragments: application of a model for the
design of nature reserves. Biological Conser-
vation 57: 205–219.
Laurance WF, Ferreira LV, Rankin-de Merona
JM, Laurance SG (1998a). Rainforest frag-
mentation and the dynamics of Amazonian
tree communities. Ecology 79: 2032–2040.
Laurance WF, Ferreira LF, Rankin-De Merona
JM, Laurance SG, Hutchings RW, Lovejoy TE
(1998b). Effects of forest fragmentation on re-
cruitment patterns in Amazonian tree com-
munities. Conservation Biology 12: 460–464.
Laurance WF, Lovejoy TE, Vasconcelos HL, Bru-
na EM, Didham RK, Sampaio E, et al (2002).
Ecosystem decay of Amazonian forest frag-
ments: a 22-year investigation. Conservation
Biology 16: 606–618.
Lehman S, Rajaonson A, Day S (2006). Edge ef-
fects on the density of Cheirogaleus major. In-
ternational Journal of Primatology 27: 1569–
1588.
Leighton M, Leighton DR (1982). The relation-
ship of size of feeding aggregate to size of food
patch: howler monkeys (Alouatta palliata)
feeding in Trichilia cipo fruit trees on Barro
Colorado Island. Biotropica 14: 81–90.
Mandujano S, Escobedo-Morales LA (2008).
Population viability analysis of howler mon-
keys (Alouatta palliata mexicana) in a highly
fragmented landscape in Los Tuxtlas, Mexico.
Tropical Conservation Science 1: 43–62.
McGoogan K (2011). Edge Effects on the Behav-
iour and Ecology of Propithecus coquereli in
Northwest Madagascar. PhD dissertation,
University of Toronto.
McKinney T (2019). Ecological and behavioural
flexibility of mantled howlers (Alouatta pal-
liata) in response to anthropogenic habitat
disturbance. Folia Primatologica 90: 456–469.
McKinney T, Westin JL, Serio-Silva JC (2015).
Anthropogenic habitat modification, tourist
interactions and crop-raiding in howler mon-
keys. In Howler Monkeys. Developments in
Primatology: Progress and Prospects (Kow-
alewski M, et al, eds.), pp 281–311. New York,
Springer.
Meyer ST, Leal IR, Wirth R (2009). Persisting hy-
per-abundance of leaf-cutting ants (Atta spp.)
at the edge of an old Atlantic forest fragment.
Biotropica 41: 711–716.
Milton K (1979). Factors influencing leaf choice
by howler monkeys: a test of some hypotheses
of food selection by generalist herbivores.
American Naturalist 114: 362–378.
Milton K (1980). The Foraging Strategies of Howl-
er Monkeys. New York, Columbia University
Press.
Milton K (1998). Physiological ecology of howlers
(Alouatta): energetic and digestive consider-
ations and comparison with Colobinae. Inter-
national Journal of Primatology 19: 513–548.
Molina R (2015). A brief history of the Molina
family, and the birth of the Maderas Rainfor-
est Conservancy at the La Suerte and Omete-
pe Field Stations – a narrative. In Central
American Biodiversity: Conservation, Ecology
and a Sustainable Future (Huettman F, ed.),
pp 199–214. New York, Springer Science +
Business Media.
Munoz D, Estrada A, Naranjo E, Ochoa S (2006).
Foraging ecology of howler monkeys in a ca-
cao (Theobroma cacao) plantation in Comal-
calco, Mexico. American Journal of Primatol-
ogy 68: 127–142.
Nijman V (2013). One hundred years of solitude:
effects of long-term forest fragmentation on the
primate community of Java, Indonesia. In Pri-
mates in Fragments (Marsh LK, ed.), pp 33–46.
New York, Kluwer Academic/Plenum Press.
Palma AC, Vélez A, Gómez-Posada C, López H,
Zárate DA, Stevenson PR (2011). Use of
space, activity patterns, and foraging behavior
of red howler monkeys (Alouatta seniculus) in
an Andean forest fragment in Colombia.
American Journal of Primatology 73: 1062–
1071.
Paterson JD (2001). Primate Behavior: An Exer-
cise Workbook. Prospect Heights, Waveland
Press.
Peters R, Cloutier S, Dube D, Evans A, Hastings
P, Kaiser H, et al (1988). The allometry of the
weight of fruit on trees and shrubs in Barba-
dos. Oecologia 74: 612–616.
Phillips OL, Rose S, Mendoza AM, Vargas PN
(2006). Resilience of southwestern Amazon
forests to anthropogenic edge effects. Conser-
vation Biology 20: 1698–1710.
Pohlman C, Turton S, Goosem M (2009). Tempo-
ral variation in microclimatic edge effects
near powerlines, highways and streams in
Australian tropical rainforest. Agriculture for
Meteorology 149: 84–95.
Pruetz J, Leasor H (2002). Densities of primate
species in forest fragments at La Suerte Bio-
logical Field Station, Costa Rica. Neotropical
Primates 10: 4–9.
R Core Team (2017). R: a language and environ-
ment for statistical computing. R Foundation
for Statistical Computing, Vienna, Austria.
https://www.R-project.org/.
Righini N, Garber PA, Rothman JM (2017). The
effects of plant nutritional chemistry on food
selection of mantled howler monkeys (Al-
ouatta pigra): the role of lipids. American
Journal of Primatology 79: 1–15.
Russell D (2018). The Influence of Edge Effects on
Mantled Howler Monkey (Alouatta palliata)
Food Resource Use and Availability in a Frag-
mented Forest. MS thesis, American Univer-
sity, Washington.
Ryan S, Starks P, Milton K, Getz W (2008). Inter-
sexual conflict and group size in Alouatta pal-
liata: a 23-year evaluation. International Jour-
nal of Primatology 29: 405–420.
Schreier AL, Bolt LM (2020). Howling for food
and females: a cross-site comparison of man-
tled howler monkey (Alouatta palliata) howl-
ing behavior in Costa Rica. American Journal
of Physical Anthropology 171: 254.
Silva SSB, Ferrari SF (2009). Behavior patterns in
southern bearded sakis (Chiropotes satanas)
in the fragmented landscape of eastern Brazil-
ian Amazonia. American Journal of Primatol-
ogy 71: 1–7.
Silver SC, Marsh LK (2003). Dietary flexibility,
behavioral plasticity, and survival in frag-
ments: lessons from translocated howlers. In
Primates in Fragments: Ecology and Conserva-
tion (Marsh LK, ed.), pp 251–265. New York,
Kluwer Academic/Plenum Press.
Stevenson PR, Zárate DA, Ramírez MA, Henao-
Díaz F (2015). Social interactions and proxi-
mal spacing in woolly monkeys: lonely fe-
males looking for male friends. In Dispersing
Primate Females (Furuichi T, et al, eds.), pp
45–71. Tokyo, Springer.
Stoner K (1996). Population density of the man-
tled howler monkey (Alouatta palliata) at La
Selva Biological Reserve, Costa Rica: a new
technique to analyze census data. Biotropica
26: 332–340.
Van Roosmalen M (1985). Habitat preferences,
diet, feeding strategy and social organization
of the black spider monkey (Ateles paniscus
paniscus Linnaeus 1758) in Surinam. Acta
Amazonica 15: 1–238.
Wickham H, Henry L (2017). tidyr: easily tidy
data with “spread()” and “gather()” functions.
R package version 0.7.1. https://CRAN.R-
project.org/package = tidyr.
Wickham H, Francois R, Henry L, Müller K
(2017). dplyr: a grammar of data manipula-
tion. R package version 0.7.4. https://
CRAN.R-project.org/package = dplyr.
Zárate DA, Stevenson PR (2014). Behavioral ecol-
ogy and interindividual distance of woolly
monkeys (Lagothrix lagothricha) in a rainfor-
est fragment in Colombia. In The Woolly
Monkey (Defler TR, Stevenson PR, eds.), pp
227–245. New York, Springer.
Downloaded by:
University Toronto Libr.
142.150.190.39 - 1/29/2021 9:14:26 PM
