Received: 7 October 2020 | Revised: 6 January 2021 | Accepted: 24 January 2021

DOI: 10.1002/ajp.23237

RESEARCH ARTICLE

Food availability, plant diversity, and vegetation structure

drive behavioral and ecological variation in Endangered
Coimbra‐Filho's titi monkeys

João P. Souza‐Alves1,2,5 | Renata R. D. Chagas2 | Marina M. Santana3 |

4 1,5
Sarah A. Boyle | Bruna M. Bezerra

1
Postgraduate Program in Animal Biology, Department of Zoology, Federal University of Pernambuco, Recife, Brazil
2
Postgraduate Program in Biological Science, Department of Systematics and Ecology, Federal University of Paraíba, João Pessoa, Brazil
3
Postgraduate Program in Ecology and Conservation, Federal University of Sergipe, São Cristóvão, Brazil
4
Department of Biology, Rhodes College, Memphis, Tennessee, USA
5
Department of Zoology, Laboratory of Ecology, Behavior and Conservation (LECC), Federal University of Pernambuco, Recife, Brazil

Correspondence
João P. Souza‐Alves, Department of Zoology,
Laboratory of Ecology, Behavior and
Conservation (LECC), Federal University of
Pernambuco, Av. Prof. Moraes Rego, 1235,
University City, Recife, 50670‐901
Pernambuco, Brazil.
Email: souzaalves1982@gmail.com
Funding information
International Primatological Society
Conservation Grants; Fundação de Amparo à
Ciência e Tecnologia do Estado de
Pernambuco, Grant/Award Number: BFP‐
0149‐2.05/19; Conselho Nacional de
Desenvolvimento Científico e Tecnológico,
Grant/Award Number: CNPq productivity
grant (309256/2019‐4)
Abstract
There is wide variability in primate behavior and ecology. Understanding how fru-
givorous primates behave under different habitat fragmentation levels is key for
effective conservation and management of species and their habitats. We evaluated
the seasonality in activity budget, diet, and ranging behavior of two groups of
Endangered Coimbra‐Filho's titi monkeys (Callicebus coimbrai). One group inhabited
a 14‐ha forest fragment, whereas the other lived in a 522‐ha fragment. We mea-
sured the monthly density of trees and lianas available as food sources over
8 months. We also collected behavioral and group location data every 5 min, from
dawn to dusk, using the scan sampling method. The two forest fragments differed
seasonally in the number of fruiting food‐resource available. In the 14‐ha fragment,
we found that the time spent by titi monkeys feeding, foraging, resting, and tra-
veling differed seasonally. In the 522‐ha fragment, titi monkeys exhibited seasonal
differences in time spent sleeping, socializing, foraging, and revisiting food sources.
In both titi monkey groups, diets varied seasonally. Our findings indicate that
Coimbra‐Filho's titi monkeys can exhibit behavioral flexibility in their activity
budgets, diets, and movement patterns. Such flexibility is important for this species
to survive in fragmented habitats and may be linked to three key factors: species‐
specific resource availability, plant species diversity, and the vegetation structure of
each forest fragment.

KEYWORDS
Atlantic Forest, behavioral pattern, daily path length, dietary diversity, home range

Am J Primatol. 2021;83:e23237. wileyonlinelibrary.com/journal/ajp © 2021 Wiley Periodicals LLC | 1 of 11

https://doi.org/10.1002/ajp.23237
2 of 11 | SOUZA‐ALVES
1 | INTRODUCTION
Biodiversity is expected to continue reducing worldwide, with habi-
tat losses being most significant in the tropics (Barlow et al., 2016;
Segan et al., 2016). Recent habitat declines have been associated
with human‐mediated land‐uses (Pardini et al., 2017), including hu-
man settlements, livestock farming, and agricultural growth (DeFries
et al., 2010; Giam, 2017). Such activities and the expected negative
impacts of climate change will likely harm global biodiversity, espe-
cially in highly fragmented ecosystems (Aukema et al., 2017).
The destruction of the Atlantic Forest in northeast Brazil dates
from the colonial period with the appearance of sugar cane planta-
tions and livestock (Galindo‐Leal & Câmara, 2003). Much of the
continuous Atlantic Forest of the region was split into a landscape
consisting of small (<10 ha) and isolated forest fragments (Melo et al.,
2013; Silva & Tabarelli, 2000). These fragmented landscapes are
highly susceptible to taxonomic homogenization (Lôbo et al., 2011)
and structural modification (Augusto et al., 2000). In contrast with
large forest fragments, small ones tend to have reduced plant rich-
ness and basal area, increased treefall gaps, lower canopy height, and
less canopy cover (Arroyo‐Rodríguez et al., 2007; Hill & Curran,
2003; Souza‐Alves et al., 2014, 2018). Small fragments may also
differ larger fragments in their phenological processes (Fuchs et al.,
2003), marked edge effects, and high levels of anthropogenic dis-
turbances (Cochrane & Laurance, 2002; Laurance & Yensen, 1991).
Habitat loss and fragmentation negatively impact primates
(Estrada et al., 2017, 2018) by reducing resource availability due to
changes in floristic diversity and vegetation structure (Souza et al.,
2012). Also, the amount of available habitat reduces (Baranga et al.,
2013), and the potential for disease transmission increases
(Goldberg et al., 2008). Furthermore, climate change may result in
population size decreases for some primates (Gouveia et al., 2016;
Moraes et al., 2020). Such changes to the primates' habitat may lead
to modifications in behavioral and ecological patterns (e.g., activity
budget, diet, and ranging behavior; Strier, 2007). Understanding the
responses to such habitat modifications is fundamental to designing
and implementing effective population management and conserva-
tion plans (Marsh, 2013).
Multiple studies have addressed how primates modify their be-
havior when faced with forest fragments of various sizes (Colobus
guereza and Procolobus pennantii: Chapman et al., 2007; Propithecus
diadema: Irwin, 2008; Alouatta palliata: Cristóbal‐Azkarate & Arroyo‐
Rodríguez, 2007; Ateles geoffroyi: Chaves et al., 2011, 2012;
Chiropotes sagulatus: Boyle et al., 2009; Boyle & Smith, 2010). While
some primates modify their diets (Boyle et al., 2012; Chaves et al.,
2012; Mekonnen et al., 2018), others spend more time feeding
(Carretero‐Pinzón et al., 2016) or limit the time spent moving (Boyle
& Smith, 2010). Primates may also adjust their activity budget based
on resource seasonality. Some primates spend more time resting
during periods of fruit scarcity (e.g., energy‐minimizing strategy)
while others change the onset and cessation of daily activities (e.g.,
time‐maximizing strategy) (Oates, 1987). For example, Callicebus ni-
grifrons fed more frequently during the lean season, consuming more
ET AL.
fruits when resources were abundant (Caselli & Setz, 2011). Hoolock
hoolock consumed more fleshy fruit when it was highly available in
the rainy season (Neha et al., 2020). Macaca assamensis devoted more
time to rest when resources were scarce and moved more when
resources were abundant (Li et al., 2020). Furthermore, primates
may adopt strategies to efficiently use their home range when food is
randomly distributed (e.g., resource maximization) or when there is a
focus on accumulating a minimum threshold of resources (e.g., area
minimization) (Mitchell & Powell, 2004).
Pitheciids (sakis, uacaris, and titi monkeys) range across much of
South America, and they inhabit a variety of habitats (e.g., Amazon,
Atlantic Forest, Caatinga, Cerrado) where resource abundance and
distribution can vary seasonally (Boyle, 2016). Thus, these primates
are good subjects for studies of habitat variations and behavioral
changes. Several studies addressed the behavioral patterns, diet, and
home ranges of the titi monkeys (see review in Bicca‐Marques &
Heymann, 2013). However, solely one study examined behavioral
differences between titi monkeys (Plecturocebus cupreus) living in
different habitats (i.e., primary forest and edge forest; Kulp &
Heymann, 2015)—Titi monkeys is a complex Pitheciidae group, the
Callicebinae, comprising 35 species so far distributed into three
genera: Callicebus, Cheracebus, and Plecturocebus (Boubli et al., 2018;
Byrne et al., 2016). Therefore, we still lack knowledge of how most
titi monkeys respond to different habitat fragmentation levels to
better understand their behavioral and ecological flexibility.
To contribute to the understanding of the behavioral and eco-
logical flexibility in titi monkeys, particularly in human‐modified ha-
bitats, we examined the seasonality of activity budget, diet, and
ranging behavior of two groups of the Endangered Coimbra‐Filho's
titi monkeys (Callicebus coimbrai) inhabiting forest fragments of dif-
ferent sizes (14 and 522 ha). Specifically, we determined whether
there were seasonal differences within each of the two titi monkey
groups for (a) behavioral activities (time awake, time spent in the
behavioral activities), (b) feeding activities (relative contribution of
plant items to the diet, dietary diversity, daily number of trees and
lianas used as a food source, and residence time on the food sources),
and (c) ranging behavior (home range size, daily path length, hourly
movement rates, and number of revisited trees). We tested the hy-
pothesis that a potential reduction in habitat quality (i.e., the density
of food sources, plant diversity, and structural vegetation) in the
small fragment influences Coimbra‐Filho's titi monkeys' seasonal
behavioral and ecological strategies.
We had four main predictions: (1) titi monkeys inhabiting the
small fragment would minimize the amount of time spent on activ-
ities that are energetically costly (energy‐minimization strategy),
thereby reducing their exploitation of dietary fleshy fruits and in-
creasing the ingestion of alternative items; (2) titi monkeys inhabiting
the large fragment would adopt an energy‐maximization strategy by
having high levels of fleshy fruit in their diet, and spending time
engaged in activities that have high energetic costs; (3) during the
period with lower resource availability (less fleshy fruits) Coimbra‐
Filho's titi monkeys in the small fragment would exploit a greater
diversity of food sources; (4) during the period of greater resource
SOUZA‐ALVES ET AL.
availability (greater density of fleshy fruits) the titi monkeys in the
large fragment would increase the consumption of fleshy fruits, thus
to reduce the diversity of exploited plants.
2 | METHODS
All contributors declared that the studies adhered to the legal
requirements of Brazil, where we conducted the fieldwork. The
study complied with the ethical requirements of the institutions
and government concerned. The study adhered to the Code of
Best Practices for Field Primatology of the American Society of
Primatologists (https://www.asp.org/society/resolutions/Ethical-
TreatmentOfNonHumanPrimates.cfm) and of the International
Primatological Society (www.asp.org/resources/docs/Code%
20of_Best_Practices%20Oct%202014.pdf).
2.1 | Study area
We monitored two groups of titi monkeys in two Atlantic forest
fragments in the Brazilian state of Sergipe (Figure 1). The smaller,
FIGURE 1 Locations of two study areas—Fazenda Trapsa (14 ha) and Mata do Junco Wildlife Refuge (522 ha) in northeastern Brazil
| 3 of 11
14‐ha fragment (11°12'S, 37°14'W) was located at Fazenda Trapsa in
the municipality of Itaporanga d'Ajuda, southern Sergipe, Brazil. This
forest fragment was situated within approximately 600 ha, inserted
in a matrix of pasture and areas with selective and indiscriminate
logging and fire. It was occasionally flooded, and it contained only
one titi monkey group (Chagas & Ferrari, 2011).
The 522‐ha forest fragment was located in the Mata do Junco
Wildlife Refuge (10°32'S, 37°03'W), located in the eastern region of
Sergipe, municipality of Capela, Brazil. This protected area was
established to protect populations of the titi monkeys and the
Lagartixo stream. This forest fragment's matrix was composed of
sugar cane, and there were approximately 250 settlement families in
the surrounding area. The group density of titi monkeys in this study
fragment was previously estimated at 7.8 groups/km2 (Rocha, 2011).
These two study sites vary in floristic composition and forest
structure (Souza‐Alves et al., 2014, 2018). Annual rainfall ranged
from 345 to 2988 mm (2000–2010) at Fazenda Trapsa, and from 205
to 2473 mm (2003–2011) at Mata do Junco (Semarh, 2012). Both
areas exhibited similar climatic conditions during the study period
(November 2011–July 2012) with monthly rainfall levels ranging
from 0 to 204 mm (mean 66.3 ± SD 74.7 mm) at Fazenda Trapsa, and
9.7–130.7 mm (mean 57.4 ± SD 39 mm) at Mata do Junco.
4 of 11 | SOUZA‐ALVES
2.2 | Study groups
We monitored two well‐habituated groups of titi monkeys
(Santana et al., 2014; Souza‐Alves & Ferrari, 2010) between
November 2011 and February 2012, and between April and July
2012 (8 months). The group inhabiting the 14‐ha fragment con-
sisted of two adult males, one adult female, one subadult female,
and one juvenile female at the beginning of the study period. The
adult female disappeared in May 2012, and the subadult female
was considered to have reached maturity by the end of the study
period as she was noted copulating in July 2012 (J.P. Souza‐Alves,
personal observation). At the end of the study period, the group
consisted of four individuals. The group in the 544‐ha fragment
consisted of a breeding pair and three immature individuals
(juveniles or subadults) and twins born in November 2011
(Santana et al., 2014). The twins were carried exclusively by the
father until March 2012, when one of the infants (approximately
4 months old) disappeared, leaving the group with six members at
the end of the study period.
2.3 | Food availability estimates
Every month we monitored the availability of plant resources at both
sites. Using randomly chosen transects, we quantified the number of
trees and lianas bearing fruits (Sutherland, 2006 and Owens et al.,
2015). In the 14‐ha fragment, we used four 250 m × 10 m transects
(monthly area sampled: 1 ha), while in the 522‐ha fragment, we used
two pre‐existing 750 m × 10 m transects (monthly area sampled =
1.5 ha). We then calculated the density of food sources available by
tallying the number of food sources (trees and lianas summed) with
fruit each month divided by the total area sampled every month
(14‐ha fragment: 1 ha; 522‐ha fragment: 1.5 ha).
2.4 | Behavioral and ecological monitoring
We monitored the two groups from dawn (04:00 h) until dusk
(18:00 h) on 5 consecutive days each month, for a total of 397 h in
the small fragment and 455 h in the large fragment. We collected
quantitative behavioral data using scan sampling methods (Altman,
1974), with a 1‐min scan conducted at 5‐min intervals throughout
the daily activity period (see Souza‐Alves et al., 2011). The behaviors
collected during each scan were rest (immobile position: standing,
sleeping, or sitting), move (mobile activity: walking, climbing, running,
or leaping), feed (mastication and consumption of plant and/or ani-
mal material), forage (localized searches for plant or animal material),
and social interaction (interaction involving two or more monkeys,
e.g., embracing, touching, grooming, duet and territorial vocaliza-
tions, or playing), based on previously defined behaviors (Talebi &
Lee, 2010). When the monkeys fed during a scan, we recorded the
feeding item (i.e., fruit, new or mature leaf, seed, flower, insect) and
then marked and numbered each plant that the monkeys used.
ET AL.
We tallied the number of food sources (trees and lianas) used
every month by each of the two titi monkey groups. We also cal-
culated the time spent with each of the feeding trees and lianas,
defined as the time at the arrival of the first individual until the last
individual's exit.
2.5 | Ranging behavior
At the start of every behavioral scan sample, we recorded the titi
monkey groups' location using a handheld 60 CSx Garmin© GPS and
then downloaded these location data to ArcGIS 9.3. We estimated
seasonal home ranges using minimum convex polygon (MCP)
through the Home Range Extension for ArcGIS 9.3 (Rodgers & Carr,
2002). We did not use kernel density estimators for calculating home
range because these methods can overestimate home range size
when sample size is small and when animal groups are maximizing
their use of a small forest fragment (Boyle et al., 2009). We based the
MCP analyses on 100% of the recorded points because an initial
analysis indicated that the best fit for the MCP analyses was based
on 100% of the points because the points were not located far from
each other. Using MapSource Garmin© software, we calculated daily
path length (dpl) using the same data points as used for the home
range analyses. We then quantified the number of feeding trees that
were visited twice or more during a day of data collection. We es-
timated hourly movement rates (HMR) using data from days when
we had at least 7 h of data from the group follows (i.e., 7 h of group
contact). We calculated HMR (m/h) by dividing path length (m) by
total time traveled (h) each day.
2.6 | Data analysis
Our analyses' main goals were to determine if there were seasonal
differences in food availability, behavior, diet, and ranging behavior
for each of the two titi monkey groups and to define the foraging
strategy used by each group of titi monkeys. We analyzed the data
for the two groups of monkeys separately because the sample size
(1 group for each of the two fragment size classes of large and small)
was small.
For the seasonal analyses, we compared the wet and dry sea-
sons. Based on historical records of rainfall over 10 years, we con-
sidered monthly precipitation of <100 mm as a cutoff point for the
definition of the dry season. Using this cutoff to define the seasons,
the rainy season lasted 2 months longer (February–August) in the
14‐ha fragment than in the 522‐ha fragment (April–August). There-
fore, we used data from November to February (dry season) and
April to July (rainy season).
We summarized the results for each variable monthly. We cal-
culated the mean ± SD for all variables.
We tested if there was a seasonal difference in the number of
fruiting food‐resource trees and lianas within each of the two forest
fragments using Fisher's exact test. We estimated the amount of
SOUZA‐ALVES ET AL. | 5 of 11

time the titi monkeys spent awake daily by calculating the number of all of these analyses using R version 3.5.0 (R Core Team, 2018).
hours from the time the monkeys first left a sleeping site in the Statistical significance was set at p < .05. When necessary, we log‐
morning until they entered a sleeping site at the end of the same day. transformed the data to meet the assumption of normality.
We tested if there were seasonal differences in the amount of time
the titis were awake each day using Fisher's exact test. Because our
contingency tables were larger than 2 × 2, we used a Monte Carlo 3 | RES ULTS
simulation (2000 replicates). This procedure was performed for all
Fisher's exact tests we ran during the data analyses of this study. 3.1 | Food availability estimates
We calculated the activity budget by considering the percent
contribution of each behavior's scan sample records (pi) and then We registered 109 and 37 food sources in the small and large
estimating the mean duration of each behavior using ti = pi × T, where fragments, respectively. The availability of food resource trees and
T is the mean duration (in minutes) of the daily activity period lianas bearing fruits within the home range of each titi monkey group
(Ferrari & Hilário, 2014). We converted the ti values to adjusted varied between the dry and rainy seasons in both the 14‐ha (Fisher's
percentages (api) by api = ti/1440 × 100, where 1440 is the number of test: p < .001) and 522‐ha forest fragment (Fisher's test: p = .003).
minutes in a 24‐h period. We used this approach because the dura- The mean density of food resources in the 14‐ha fragment along the
tion of the daily period may be an important component of primate transects was 17.3 individuals/ha (±SD 12.8) during the dry season
behavioral strategies in relation to feeding resources (see more de- and 10 individuals/ha (±SD 7.4) during the rainy season. In the 522‐
tails in Ferrari & Hilário, 2014). We used the same calculations for ha fragment, the mean density of food resources was 6.3 individuals/
activity budget as for diet to determine the percent contribution of ha (±SD 4.3) during the dry season and 3.0 individuals/ha (±SD 3.2)
the various plant species used as a food resource by the monkeys. during the rainy season.
We tested predictions #1 and #2 by comparing the dry and rainy
seasons in regard to the titi monkeys' behaviors and diet within each
of the two forest fragments using binomial z scores, z = xi – m/√(Nqp), 3.2 | Activity budget
where xi is the number of records of each behavioral/diet category i
to the determined study group, N is the total number of records of In the 14‐ha fragment, there was no seasonal difference in the
behavioral/diet category i for both groups, p and q are the proportion amount of time that Coimbra‐Filho's titi monkey group was awake
of records for each group separately, and m is Nxp. The α‐value of (Fisher's test: p = .455; Table 1). However, in the 522‐ha forest
these analyses was 0.01 (Bonferoni's correction) to avoid false‐ fragment, titi monkeys spent more time awake during the dry season
positive results (Martin & Bateson, 1993). Also, for predictions #1 than in the rainy season (Fisher's test: p < .001; Table 1).
and #2, we used a Fisher's exact tests to determine if there were In the 14‐ha fragment, the monkeys spent more time feeding/
seasonal differences in the feeding activities (i.e., number of com- foraging and less time resting during the dry season compared to the
monly used food‐resource trees producing fruit, time resident on rainy season; however, there were no seasonal differences in the
fruit feeding trees and lianas [i.e., the total number of records spent amount of time spent moving or engaged in social behavior (Table 2).
in each fruiting source multiplied by 5‐scan min]). In the 522‐ha fragment, the titi monkeys spent more time engaged in
Moreover, to investigate the foraging strategies (predictions #1 social activities and less time foraging during the dry season
and #2) of both Coimbra‐Filho's titi monkey groups during periods of
higher and lower food resources (density of fruiting trees and lianas),
we compared the potential energy loss and gain between the two T A B L E 1 Seasonal variation in the amount of time spent awake
each day for two groups of Coimbra‐Filho's titi monkeys in 14‐ha
periods. Specifically, we used activities that have high energy de-
and 522‐ha Atlantic forest fragments of northeastern Brazil
mands (home range, dpl, HMR, and the number of revisits to the food
resource in the small and large fragments: Krebs & Davies, 1993) as Mean duration (h) of daily time awake
(earliest waking hour and latest sleep hour)
proxies for energetic expenditure, and then summed the time the Season Month 14‐ha fragment 522‐ha fragment
monkeys spent exploiting fleshy fruits, seeds and flowers (Lambert,
Dry November 11:12 (4:40–16:20) 12:00 (4:45–17:40)
2011) as a proxy for energetic gain (Heiduck, 2013; Nagy‐Reis &
December 10:48 (5:20–17:02) 12:00 (5:25–17:55)
Setz, 2017). We then tested if there were seasonal differences in
January 08:48 (5:25–16:00) 11:32 (5:36–17:39)
activities with high energetic demand using Fisher's exact test with a
February 09:51 (5:35–16:01) 11:16 (5:37–17:21)
Monte Carlo simulation (2000 replicates).
Mean ± SD 10:09 ± 1:04 11:42 ± 00:21
We assessed monthly diet diversity using the Shannon–Wiener
Rainy April 10:49 (5:20–17:30) 11:28 (5:10–17:35)
index (Hˈ) to analyze the records of plant species exploited by the titi
May 09:16 (6:04–17:22) 11:00 (5:45–17:05)
monkeys. We tested for differences between seasons in each forest
June 09:44 (5:55–16:30) 11:27 (5:32–17:20)
fragment using a Student's t‐test (prediction #3 and #4). We used a
July 08:48 (6:20–16:43) 10:18 (5:47–17:12)
Jaccard's similarity index to test for similarities across seasons in the
Mean ± SD 9:39 ± 00:51 11:03 ± 00:32
plant species exploited within each forest fragment. We performed
6 of 11 | SOUZA‐ALVES ET AL.

T A B L E 2 Seasonal activity budgets

Mean ± SD of time spent (minutes) in dry and rainy season for titi monkeys in the 14‐ha and 522‐ha
14‐ha fragment 522‐ha fragment Atlantic Forest fragments of northeastern
Category Dry Rainy z (p value)a Dry Rainy z (p value)a Brazil
Rest 1019 ± 52 1122 ± 32 −2.20 (0.013) 1042 ± 79 1048 ± 26 0.09 (0.537)

Feed 160 ± 20 93 ± 11 4.21 (<0.001) 168 ± 37 136 ± 50 1.92 (0.027)

Move 134 ± 10 139 ± 27 −0.29 (0.383) 154 ± 22 155 ± 31 0.02 (0.511)

Forage 95 ± 8 64 ± 7 2.46 (0.006) 19 ± 7 74 ± 42 −5.65 (<0.001)

Social 30 ± 29 20 ± 18 1.41 (0.078) 40 ± 46 22 ± 4 2.32 (0.010)

a
Significant differences are marked in bold, as indicated when p ≤ .01.

compared to the rainy season; however, there were no seasonal
differences in the amount of time spent resting, feeding, or moving
(Table 2).
3.3 | Diet composition
In the 14‐ha fragment, titi monkeys devoted more time exploiting
fruit and new leaves during the dry season. During the rainy season,
they devoted more time to eat leaves and flowers (Figure 2). During
the dry season, these titi monkeys in the 14‐ha fragment con-
centrated their feeding behavior on three tree species that re-
presented 80% of the diet records: Eugenia ligustrina fruits—
Myrtaceae (41%), Xylopia frutescens seeds—Annonaceae (22%), and
Pouteria sp. fruits—Sapotaceae (17%). However, during the rainy
season, these three species represented only 20% of this titi monkey
group's diet records. These monkeys in the 14‐ha fragment con-
tinued to eat the fruits of E. ligustrina during the rainy season. Still,
the monkeys also exploited many other species, including Guapira
opposite new leaves (Nyctaginaceae) and two liana species: Jacque-
montia glaucescens flowers (Convolvulaceae) and Adenocalymma
comosum new leaves (Bignoniaceae). In the 14‐ha fragment, the
monkeys' diet was more diverse during the rainy season (Hˈ = 3.0)
than the dry season (Hˈ = 2.9: t = −2.114, df = 1224.7, p = .034). The
plant species composition exploited by titi monkeys in the 14‐ha
fragment presented low similarity between dry and rainy sea-
sons (J = 0.3).
In the 522‐ha fragment, titi monkeys ate fruit more during the
rainy season, and new leaves, and seeds more during the dry season
(Figure 2). Pouteria gardneri fruits (22%) and Tabebuia stenocalix
leaves—Bignoniaceae (16%) were used most by the titi monkeys as
diet items during the dry season (Electronic Supporting Information
Material S1). Diet diversity was higher during the dry season
(Hˈ = 2.5) than the rainy season (Hˈ = 2.2) in the large fragment
(t = 3.512, df = 972.6, p < .001). The similarity of plant species
exploited by titi monkeys in the dry and rainy seasons was relatively
higher (J = 0.7) in the 522‐ha fragment compared to the 14‐ha
fragment.
In the 14‐ha fragment, the daily number of trees and lianas
used as food sources was similar between dry and rainy seasons
(14.6 ± SD 4.5 vs. 12.6 ± SD 4.2, respectively; Fisher's test: p = .102).
However, the titi monkeys spent more time on these food sources
during the dry season than the rainy season (409 ± SD 279 min vs.
189 ± SD 54 min, respectively; Fisher's test: p < .001). In the 522‐ha
fragment, during the rainy season the titi monkeys used a greater
number of trees and lianas daily as food sources (dry season: 10.9
trees ± SD 7.6; rainy season: 17.5 trees ± SD 6.2; Fisher's test:
p < .001), and the monkeys spent more time on these food sources
(dry season: 258 ± SD 67 min; rainy season: 354 ± SD 171 min;
Fisher's test: p < .001).
3.4 | Ranging behavior
In the 14‐ha fragment, titi monkeys had a longer dpl and higher HMR
during the dry season, but there were no seasonal differences in
home range size and number of revisited food sources (Table 3). In
the 522‐ha fragment, the titi monkeys had a longer dpl during the
rainy season, but HMR was higher in the dry season. The number of
revisited food sources and home range size did not vary between
seasons (Table 3).
4 | DISCUSS ION
Our findings demonstrated that Coimbra‐Filho's titi monkeys can
modify their behaviors seasonally, which is likely a response by the
monkeys to maximize their use of resources and space as fruit
availability fluctuates. These strategies may help the titi monkeys
cope with living in forest fragments that vary in size, that likely have
been exposed to different levels and types of anthropogenic dis-
turbances, and that contain variable amounts of food resources for
the monkeys.
In the small 14‐ha fragment in the resource‐rich dry season, titi
monkeys spent more time feeding, foraging, and residing on food
sources (energetic gain variables). They also spent less time resting
and walked longer distances with a higher HMR (energetic ex-
penditure variable) during such periods. Such behavioral changes
have been documented in multiple primate species, including ones
living in fragments. For example, black‐fronted titi monkeys
SOUZA‐ALVES ET AL. | 7 of 11

F I G U R E 2 Total time (min) during the 8‐months study period that Coimbra‐Filho's titi monkeys devoted to exploiting different food items
in the large fragment and small forest fragment in the dry and rainy season. Significant differences for large fragment (522 ha) are indicated by
an asterisk (fruit: z = −7.116, p < .001; leaf: z = 4.844, p < .001; new leaf: z = 8.382, p < .001; flower: z = 1.269, p = .102; seed: z = 5.479, p = .003),
and for small fragment (14 ha) are indicated by an asterisk (fruit: z = 3.538, p = .002; leaf: z = −3.037, p < .001; new leaf: z = −3.176, p < .001;
flower: z = −6.582, p < .001; seed: z = 1.877, p = .030). It was not possible to test for seasonal differences in invertebrate consumption due to
small sample size

(Callicebus nigrifrons) spent less time on energy‐demanding activities
(traveled less and for shorter distances) when fruit availability was
low (Nagy‐Reis & Setz, 2017). In a comparison of Bale monkey
(Chlorocebus djamdjamensis) groups living in forest fragments or in
continuous forest, Bale monkeys in the forest fragments modified
their diets when there was low food availability (Mekonnen et al.,
2018). It was noted that ursine colobus (Colobus vellerosus) in forest
fragments spent less time moving and more time resting (Wong &
Sicotte, 2007). Overall, our findings indicated that the titi monkeys
living in the smaller forest fragment also adopted a strategy similar
to other Neotropical primates in that they saved energy during
periods of fruit shortage (energy‐minimizing strategies: sensu
Schoener, 1971).
Conversely, in the larger forest fragment titi monkeys appeared
to have a different behavioral strategy than that of the monkeys in
the smaller forest fragment. There, they spent less time awake but
increased the amount of time they spent foraging in the rainy season
(low food availability). Also, they walked longer distances (energetic
expenditure variable) and had a higher residence time on
food sources (energetic gain variable). During this period, they also
spent less time engaged in social behaviors such as grooming; how-
ever, such behavior is not considered as energetically demanding
8 of 11 | SOUZA‐ALVES
Mean ± SD of ranging behaviors
14‐ha fragment 522‐ha fragment
Ranging
behavior Dry Rainy Fisher's test Dry
dpl (m) 748 ± 131 610 ± 234 p > .001 978 ± 364
Home 8.3 ± 2.6 8.3 ± 4.1 p = .574 6.5 ± 1.5
range (ha)
# revisited food 1.0 ± 1.3 0.5 ± 0.7 p = .882 0.55 ± 0.7
sources
HMR 77 ± 17.9 67 ± 25.5 p < .001 115 ± 70.1
Note: Bold values are significant difference, as indicated when p ≤ 0.05.
(Russell & Phelps, 2013). Thus, for the titi monkeys living in the
larger fragment, during periods of lower fruit availability, the mon-
keys increased the amount of time of their nightly roost (more rest)
but allocated more time during their awake hours to forage
(e.g., energy‐maximizing strategy: Stephens & Krebs, 1986).
The effects of habitat loss and fragmentation tend to be less
severe in larger forest fragments than in small fragments
(Mekonnen et al., 2018). Primates in larger forest fragments are
sometimes able to use a greater diversity of plants as food re-
sources, and consequently, have more versatility in choosing what
to eat (Arroyo‐Rodríguez & Mandujano, 2006). During periods of
lower fruit availability (rainy season), titi monkeys in the smaller
forest fragment spent less time eating fleshy fruits but increased
the amount of time they spent consuming leaves and flowers. This
seasonal variation in diet is also reflected in the relatively low level
of similarity between plants consumed during the two seasons in
the small fragment. Furthermore, the titi monkeys in the smaller
fragment ate plants from a greater diversity of species during the
rainy season (lower fruit availability).
In larger forest fragment, titi monkeys had a higher diversity of
plant species in their diet, and spent less time eating fleshy fruits
when fruits were more available (dry season). When fruit availability
was lower (rainy season), the monkeys increased their fruit con-
sumption, but they had a lower diversity of plant species in their
diet. Four plant species (Tapirira guianensis—Anacardiaceae: 27%
of feeding records; Miconia prasina—Melastomataceae: 17%;
Protium heptaphylum—Burseraceae: 14%; and P. gardneri: 13%) re-
presented more than 70% of the fruit consumed by the monkeys
during the rainy season. Our findings suggest that titi monkeys living
in large and small forest fragments exhibit seasonal variability in
their foraging behavior and diet composition, implying that such
flexibility may help the monkeys to optimize their energy intake
through their diet. These diet differences may be linked to species‐
specific resource availability, plant species diversity, and each forest
fragment's vegetation structure.
Primates often modify their home range size when experiencing
adverse situations such as food scarcity (Irwin, 2008; Mekonnen
et al., 2018). However, in our study, for both groups of titi monkeys,
home range size was similar during low and high fruit availability
ET AL.
T A B L E 3 Ranging behaviors
performed by titi monkey groups during
the dry and rainy season in the small and
large forest fragment at Northeastern
Rainy Fisher's test Brazil
1116 ± 395 p > .001
6.7 ± 2.2 p = .962
1.55 ± 1.1 p = .400
103 ± 36.6 p < .001
periods. Furthermore, Coimbra Filho's titi monkeys' home range si-
zes were similar to size in the large and small fragments over the
8 months of this study (Table 3). The sizes of the study groups' home
ranges were within the typical range found in Callicebus spp. (Bicca‐
Marques & Heymann, 2013), suggesting that the titi monkeys in the
14‐ha fragment had sufficient space and resources. Nevertheless, we
cannot rule out that existing neighboring titi groups may have in-
fluenced the home range size of the study group in the larger frag-
ment. Titi monkeys are territorial (Kinzey & Becker, 1983), with
encounters between individuals of different groups often leading to
agonistic contact (i.e., fights).
Our findings bring some evidence of the adverse effects of habitat
loss and fragmentation on titi monkeys' behavior and ecology. Never-
theless, despite the extent of the effects observed for our study species
and sites, we must be cautious when extrapolating these findings to all
Callicebinae. The impact of habitat loss and fragmentation is highly
variable and depends on the type of matrix, fragment size, isolation
level, and shape (Arroyo‐Rodríguez & Fahrig, 2014). Unfortunately, it is
impossible to evaluate these variables' influence on the behavior and
ecology of the Coimbra‐Filho's titi monkeys we studied due to the small
sample size (i.e., two forest fragments only). One would need to monitor
more than one primate group per size class of forest fragment to test
the effect of fragment size on titi monkey behavior and ecology (see
Boyle & Smith, 2010; Boyle et al., 2012; Chaves et al., 2011, 2012;
Mekonnen et al., 2018). Nevertheless, our study yielded a significant
contribution to an Endangered primate species inhabiting a highly
fragmented landscape in Brazil.
Here we demonstrate that Endangered Coimbra‐Filho's titi
monkeys seem to adjust their behavioral, diet, and ranging patterns
to cope with fragments that have undergone different levels of de-
struction and fragmentation. Home range size appears to be con-
served in this species, remaining roughly the same in both the 14 and
522 ha fragments. Coimbra‐Filho's titi monkeys may use changes in
foraging‐time and resource‐choice as strategies to maximize re-
source consumption, which so far may have been essential for their
survival in highly fragmented and anthropogenically disturbed areas.
Continued long‐term monitoring of titi monkeys in fragments of
different sizes and vegetation structures will elucidate if the stra-
tegies employed by titi monkeys are enough for their long‐term
SOUZA‐ALVES ET AL.
survival (Chapman et al., 2013). Short‐ and long‐term efforts to
maintain and conserve forest fragments of different sizes within the
known occurrence range of Callicebinae species and within the areas
predicted as suitable for these animals' occurrence are vital to
ensure their continued survival.
A C K N O W L E D GM E N T S
We thank Stephen Ferrari, Víctor Arroyo‐Rodríguez, Karen
Strier, Paul Garber, and Anthony Rylands for the valuable com-
ments on the original version of this manuscript. We are also
grateful to SEMARH/SE, CPB/ICMBio, and everyone that logis-
tically supported this study. During this study, JPS‐A was sup-
ported by CAPES Ph.D. scholarship and the International
Primatological Society Conservation Grants. RRDC and MMS
were supported by a CAPES. JPS‐A is supported by FACEPE
(Grant no. BFP‐0149‐2.05/19). BB is supported by a CNPq pro-
ductivity grant (309256/2019‐4). We are grateful to Dr. Karen
Bales and two anonymous reviewers for valuable comments on
this manuscript's early versions.
C O NF L IC T O F IN T E R ES T S
The authors declare that there are no conflict of interests.
AUTHOR CONTRIBUTIONS
Conceptualization (lead); formal analysis (equal); investigation (equal);
methodology (lead); project administration (equal); writing original draft
(lead): João Pedro Souza‐Alves. Formal analysis (equal); investigation
(equal); methodology (supporting); writing review and editing (equal):
Renata Chagas. Formal analysis (equal); writing review and editing
(equal): Sarah A Boyle. Formal analysis (equal); writing review and
editing (equal): Bruna Bezerra.
P E E R R E V I EW
The peer review history for this article is available at https://publons.
com/publon/10.1002/ajp.23237
DATA AV AILA BILITY STATEMENT
The data that support the findings of this study are available from
the correspondence author upon reasonable request.
ORCID
João P. Souza‐Alves http://orcid.org/0000-0002-8517-1276
Sarah A. Boyle http://orcid.org/0000-0001-9498-6787
Bruna M. Bezerra http://orcid.org/0000-0003-3039-121X
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SU PP O RT I N G I N FO RM ATI ON
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How to cite this article: Souza‐Alves JP, Chagas RRD,
Santana MM, Boyle SA, Bezerra BM. Food availability, plant
diversity, and vegetation structure drive behavioral and
ecological variation in Endangered Coimbra‐Filho's titi
monkeys. Am J Primatol. 2021;83:e23237.
https://doi.org/10.1002/ajp.23237