Primates
DOI 10.1007/s10329-016-0556-9
ORIGINAL ARTICLE
Foraging strategies of black-fronted titi monkeys (Callicebus
nigrifrons) in relation to food availability in a seasonal tropical
forest
Mariana B. Nagy-Reis1 • Eleonore Z. F. Setz1
Received: 31 May 2016 / Accepted: 13 July 2016
Ó Japan Monkey Centre and Springer Japan 2016
Abstract Many primates have to cope with a temporal
scarcity in food availability that shapes their foraging
strategies. Here we investigated the changes in diet,
activity, and ranging behavior of a group of black-fronted
titi monkeys (Callicebus nigrifrons) according to the
availability of the main high-nutritional-density item in
their diet and the foraging strategy adopted when this food
is scarce. We monitored one habituated group using
instantaneous scan sampling over 1 year (533 h of observation, 61 days) in a seasonal tropical forest fragment
(245 ha). We simultaneously collected data on food
availability with fruit traps. The titi monkeys consumed
fleshy fruits, the main high-nutritional-density item of their
diet, in accordance with its availability, and the availability
of this item modulated the ingestion of vegetative plant
parts, a relatively low-nutritional-density food. During high
fleshy fruit availability, the titi monkeys consumed more
fleshy fruits, flowers, and invertebrates. They also traveled
more, but concentrated their activity in a central area of
their home range. Conversely, during fleshy fruit scarcity,
they increased the breadth of their diet, switching to one
richer in seeds and vegetative plant parts, and with greater
Electronic supplementary material The online version of this
article (doi:10.1007/s10329-016-0556-9) contains supplementary
material, which is available to authorized users.
& Mariana B. Nagy-Reis
mariana.nbreis@gmail.com
Eleonore Z. F. Setz
setz@unicamp.br
1
Department of Animal Biology, Biology Institute,
Universidade Estadual de Campinas, UNICAMP, Bertrand
Russel, 1505, Mailbox: 6109, Campinas, SP 13083-970,
Brazil
plant diversity. At the same time, they reduced most
energy-demanding activities, traveling less and over
shorter distances, but using their home range more broadly.
Corroborating the optimal foraging theory, titi monkeys
altered foraging strategies according to temporal food
fluctuations and responded to low fleshy fruit availability
by changing their diet, activity, and ranging behavior. The
adoption of a low-cost/low-yield strategy allowed us to
classify them as energy minimizers.
Keywords Feeding ecology Seasonality Diet Space
use Activity pattern Optimal foraging theory
Introduction
Optimal foraging theory suggests that animals optimize
their energy yield while foraging (MacArthur and Pianka
1966; Pyke et al. 1977). The relationship between energy
gained while feeding (‘‘benefits’’) and energy expended to
acquire and process the food (‘‘costs’’) usually defines the
foraging strategies of animals (Norberg 1977; Krebs and
Davies 1993). Whether a food item should be consumed is
independent of its abundance, and depends only on the
abundance of the higher-rank food (Pyke et al. 1977; e.g.
Harrison 1984). As the abundance of a preferred food type
increases, the number of food types included in the optimal
diet will shrink (Pyke et al. 1977). Therefore, because the
availability of most resources varies in time, seasonality
tends to influence the food choice of animals (Garber 1987;
Hemingway and Bynum 2005).
Seasonality in resource production has lead to the evolution of morphological, behavioral, and physiological
adaptations in consumers (van Schaik et al. 1993).
Resource availability can affect diet, ranging, and behavior
123
Primates
of primates (Hemingway and Bynum 2005). During low
resource availability, for instance, primates can respond
with dietary changes, increasing or decreasing their dietary
breadth (e.g. Pithecia chrysocephala, Setz 1993; Cercopithecus doggetti, Kaplin et al. 1998; Callicebus nigrifrons,
Caselli and Setz 2011; Macaca silenus, Santhosh et al.
2015) and/or switching food types or plant species ingested
(e.g. Alouatta seniculus, Lagothrix lagotricha cana,
Pithecia albicans, Saguinus sp., Sapajus apella, Peres
1994; Callicebus melanochir, Müller 1996). Some species
rely on fallback foods, which are resources that become
particularly important when preferred foods are scarce
(Marshall et al. 2009; Lambert 2011). Fallback foods can
be either resources of lower-nutritional-density (lower
inherent energy yield) that are abundant in the habitat but
require more processing time (e.g. vegetative plant parts),
or resources of higher-nutritional-density (greater inherent
energy yield) that are more difficult to find and are typically mechanically protected (longer handling time; e.g.
seeds; Lambert 2011).
Primates can also respond to food availability with
behavioral and ranging changes. The amount of time
traveling and travel distances, two potential measures of
energy expenditure (Krebs and Davies 1993), can vary
according to the foraging strategy of the species. Energy
minimizers (Schoener 1971) feed on alternative abundant
items and reduce the energy expended foraging, conserving energy during lean seasons (low-cost/low-yield
strategy; e.g. Colobus polykomos, Dasilva 1992; Ateles
chamek, Wallace 2005; Callicebus melanochir, Heiduck
2013). Contrarily, energy maximizers (Schoener 1971)
spend more time and energy searching for food, maintaining a similar energy intake across seasons (high-cost/
high-yield strategy; e.g. Gorilla beringei, Vedder 1984;
Rothman et al. 2008). Analogously, since home ranges
can be a function of the availability and distribution of
resources, limited by the costs of resource acquisition,
home range usage can also be related to these two
strategies regarding optimal use of energy (Mitchell and
Powell 2004). Similar to energy maximizers, resource
maximizers use the highest resource/area ratio possible,
whereas area minimizers, similar to energy minimizers,
use the minimum area needed to obtain the lowest
resource value required for survival and reproduction
(Mitchell and Powell 2004). Aside from altering home
range size and usage (e.g. Sapajus apella, Zhang 1995),
primates may also rely on a specific microhabitat within
their home range (e.g. Gorilla beringei, Vedder 1984;
Ateles paniscus chamek, Cebus albifrons unicolor, Saimiri
sp., Peres 1994), or may even switch habitat types (e.g.
Lagothrix lagotricha, Defler 1996; Alouatta seniculus,
Palacios and Rodriguez 2001; Ateles chamek, Wallace
2006).
123
Small-bodied frugivores (\1.5 kg) are more likely to be
susceptible to environmental variations such as food fluctuations, since small-bodied animals are highly vulnerable
to seasonality (Lindstedt and Boyce 1985), and in addition,
frugivores depend on a seasonally fluctuating resource (van
Schaik et al. 1993). Titi monkeys (33 species recently
divided into three genera: Callicebus, Cheracebus, and
Plecturocebus; Byrne et al. 2016) are highly frugivorous
small-bodied primates (Easley 1982; Müller 1996; Caselli
and Setz 2011; Souza-Alves et al. 2011; Kulp and Heymann
2015) from a poorly studied but diverse and widespread New
World clade, many of which live in seasonal environments
(especially members of the genus Callicebus). Therefore,
they represent a good model to study the relationship
between food availability and the foraging and behavioral
strategies of frugivorous primates. To investigate these
relationships, we studied a group of black-fronted titi monkeys (Callicebus nigrifrons) in a seasonal environment.
It is already known that Callicebus nigrifrons is
behaviorally flexible and can alter its diet and activity
pattern between seasons (Caselli and Setz 2011), but the
effects of food availability on other aspects of the species’
foraging behavior is still unknown. Here, we investigate
how temporal variations in food may affect the diet and
activity patterns of black-fronted titi monkeys (Callicebus
nigrifrons). We also evaluate for the first time the ranging
behavior of a group and assess their foraging strategies
under differing availability of fleshy fruits (the main highnutritional-density item of their diet). First, we tested how
monthly availability of different foods influenced the
consumption of each food item. Based on a previous study
(Caselli and Setz 2011), and on the provisions of optimal
foraging theory (Pyke et al. 1977; Harrison 1984), we
predicted that only the consumption of the main high-nutritional-density item of their diet (i.e. fleshy fruits) would
be positively linked to availability, and its availability
would negatively affect the consumption of a relatively
lower-nutritional-density food item (i.e. vegetative plant
parts). In addition, we expected that in periods when fleshy
fruits were in short supply, the titi monkeys would use a
broader set of foods, increasing food diversity (Pyke et al.
1977) and diet niche width. We also predicted that during
these periods, growth forms displaying alternative periodicity in their phenology (i.e. that produce fruits when most
plants do not; e.g. lianas at our study site; Garcia et al.
2014) would be of high importance in their diet. Second,
we investigated which type of foraging strategy (high-cost/
high-yield or low-cost/low-yield) titi monkeys adopt when
fleshy fruits (their preferred high-nutritional-density item)
is scarce. We predicted that if titi monkeys were energy
maximizers and adopted a high-cost/high-yield strategy,
they would increase energy-consuming activities and possibly increase home range size and usage (resource
Primates
Fig. 1 Study hypotheses for the influence of fleshy fruit availability on the foraging strategies of a group of frugivorous primates (titi monkeys,
Callicebus nigrifrons)
maximization) in order to maintain a high consumption of
fleshy fruit. In contrast, we expected that if they were
energy minimizers and adopted a low-cost/low-yield
strategy, the titis would consume fewer fleshy fruits but
more alternative items, and would reduce energy-consuming activities and home range size and usage (areaminimization; see Fig. 1 for hypotheses schema).
Methods
Study site
The study was carried out at Ribeirão Cachoeira, a 245 ha
Atlantic Forest remnant (22°500 S, 46°550 W) located in an
environmental protection area in Campinas, State of São
Paulo, southeastern Brazil. The forest vegetation is classified as seasonal semi-deciduous (Santos 1998), and is
characterized by seasonal variations in fruit availability
(Garcia et al. 2014). The climate is mild rainy, with a wet
and warm season from October through March and a dry
and colder season from April through September (Santos
1998; Fig. 2). The mean temperature is around 22 °C, and
annual precipitation about 1424 mm, including the year
during which we conducted the study (Cepagri 2012;
Ciiagro 2016).
Study group and monitoring
We habituated (from March through May 2010) and
monitored (from June 2010 through May 2011) one group
of free-ranging black-fronted titi monkeys (Callicebus
nigrifrons). During the study, the composition of the group
varied from three to five individuals. We collected data
from dawn to dusk (‘‘complete days’’) or from the time the
group was found until it was lost. Since there are differences in day length between months, we standardized the
sampling effort to 45 observation hours per month (±SD
5 h). We sampled a mean of five observation days per
month (±SD 1.08 day), in which approximately three
observation days (±SD 0.74 day) were ‘‘complete days’’.
We considered only ‘‘complete days’’ (N = 36) and days
with observation hours C90 % of the mean observation
hours in ‘‘complete days’’ of the same month (N = 4) to
estimate daily path length and traveling speed (N = 40 days
in total). For all other analyses, we used data from ‘‘complete
days’’ (N = 36) and days with observation hours C50 % of
the mean observation hours in ‘‘complete days’’ of the same
month (N = 25), totaling 533 observation hours and 61
observation days. The sampling effort, observation period,
and the distribution of scan samples throughout the day were
similar between resource-lean months (N = 2683 behavior
records; N = 550 diet records; approx. 144 obs. hours;
123
Primates
Fig. 2 Mean monthly
temperature and precipitation at
Campinas (source: Cepagri
Unicamp, based on
meteorological data collected
between 1988 and 2008)
18 days) and resource-rich months (N = 2556 behavior
records; N = 563 diet records; approx. 125 obs. hours;
14 days), enabling comparisons between them.
Food resource availability
Temporal variation in fleshy fruit, dry fruit/seed, and
flower availability was obtained from 100 rectangular fruit
traps (Smythe 1970; each with dimensions of
18.4 9 27.8 cm) distributed along five line transects
evenly spaced within the study group’s home range. The
fruit traps were positioned 20 m apart and 1 m perpendicular to each transect (Terborgh 1983). The total area
sampled by the traps (5.12 m2) is equivalent to 0.003 % of
the group’s home range area, which is in agreement with
other studies, which typically use 0.00003–0.017 %
(Chapman et al. 1994). We chose to use fruit traps because
they allowed us to easily estimate monthly food availability
from several growth forms (trees, shrubs, and lianas)
simultaneously with the behavioral and diet data collection.
This was important, because lianas, for instance, supply a
considerable amount of food for titi monkeys (Caselli and
Setz 2011; Souza-Alves et al. 2011), and at our study site,
can display different periodicity in their phenology compared to other growth forms (Garcia et al. 2014).
Every 15 days we collected all fleshy fruits (fruits with
pulp or aril), dry fruits or seeds (fruits without pulp or aril,
winged seeds, and capsules), and flowers from the fruit
traps and weighed them separately. We did not include
seeds from fleshy fruits in our estimate of seed availability
because we had evidence of a lack of effective predation of
these in titis (1154 of 1195 ingested fleshy fruit seeds were
intact in their feces; N = 51 fecal samples collected
simultaneously with our data).
123
Fleshy fruits are the main item in the diet of titi monkeys
(Easley 1982; Müller 1996; Caselli and Setz 2011; SouzaAlves et al. 2011). These fruits typically have a high
amount of soluble carbohydrates, and so have high-nutritional-density (Garber 1987; Strier 2007; Lambert 2011).
Consequently, we used the monthly biomass of fleshy fruits
collected in the fruit traps to measure the availability of the
main high-nutritional-density item of their diet. In order to
investigate titi monkeys’ response during lean periods, we
determined two periods of contrasting fleshy fruit availability based on the amount of fleshy fruits collected by the
traps (Fig. 3). We considered the leanest months to be
those in which we collected a biomass of fleshy fruit lower
than the lower limit of the 95 % confidence interval (CI),
and the richest months as those with a biomass higher than
Fig. 3 Fleshy fruit biomass collected by the fruit traps during the
lean and rich months at the study group’s home range (located in
Ribeirão Cachoeira remnant, southeastern Brazil)
Primates
its upper limit. The lean period coincided with the driest
months in our study area (mid-dry season: June, July, and
August). The richest months were October, December, and
April.
Diet and activity pattern
We recorded the behavior and diet of each visible member
of the group with instantaneous scan sampling every 5 min
(Altmann 1974). Behaviors were divided into the following: feeding (manipulating, processing, chewing, and
swallowing food), resting (standing, sitting, or laying, not
performing any activity), traveling/moving, and other
activities (vocalizing, playing, and grooming). To determine the diet of the group, we divided the items consumed
into fleshy fruits, dry fruits/seeds, vegetative plant parts
(leaves and buds/shoots), flowers, and invertebrates.
Whenever possible, we also recorded whether the item
ingested was from lianas or trees/shrubs. The activity
pattern and the composition of the group’s diet were estimated by producing estimates per day of the amount of
time spent eating each food item or performing each
activity, and then calculating the relative frequency of each
behavior in the total budget and each item in the total diet.
The plants were identified in the field by botanists (see
acknowledgments), with the help of a field guide (Ramos
2007), and data from an extensive botanical survey conducted at our study site (Santos 1998). The list of plant
species used as food sources by the titi monkeys (Online
Resource 1) was obtained using the all-occurrence method
(Altmann 1974).
Space use
We recorded the geographical position of the study group
every 10 min with a GPS unit. We also recorded the
location of all important feeding sites (those trees/shrubs or
lianas/vines in which at least half of the group foraged
together during at least 20 min). We calculated the daily
path length by adding the distances between consecutive
geographical position points using GPS TrackMaker 13.7
software (Ferreira 2010). Traveling speed was obtained by
dividing each daily path length by total travel time on that
same day.
We calculated the group’s home range area with the
minimum convex polygon (MCP; Hayne 1949) and adaptive kernel (Worton 1989) methods, using 95 % of the
geographical position points. To estimate the utilization
distributions (UDs), we used kernelUD with the default
method for the estimation of the smoothing parameter (the
ad hoc method). A UD describes the collective intensity of
use of different areas by group members, giving the
probability of relocating the group at any place within its
range during a specified time period (Powell 2000; Calenge
2006). We ran these analyses in R software version 3.1.1
(R Development Core Team 2014) using the ‘‘adehabitatHR’’ package (Calenge 2011). To estimate the percentage of monthly home range overlap (from MCP estimates)
within each productivity period, we used the package
‘‘rgeos’’ (Bivand et al. 2015).
Data analysis
We tested the strength of the relationship between monthly
food availability (monthly biomass of each item collected;
independent variable) and monthly consumption of each
food item (dependent variable) using linear regressions for
fleshy fruits and dry fruits/seeds, and Spearman rank correlation tests for flowers (since this data did not follow the
assumptions of parametric tests). We also investigated the
relation between the consumption of a generally lowernutritional-density food (i.e. vegetative plant parts) and the
availability of the main high-nutritional-density item of
their diet (i.e. fleshy fruit) using a linear regression.
Whenever necessary, we used log or arcsin (for proportions) transformations.
To investigate the foraging strategy of titi monkeys
when the main high-nutritional-density item of their diet
(i.e. fleshy fruits) was scarce, we compared the potential
‘‘costs’’ and ‘‘benefits’’ between lean and rich periods. We
used energy-demanding activities (i.e. travel time, travel
speed, and travel distance; Krebs and Davies 1993) as
measures of the energetic cost of foraging, and the amount
of time feeding on overall high-nutritional-density items
(i.e. fleshy fruits, flowers, and seeds; Garber 1987; Strier
2007; Lambert 2011) as a measure of energy gained while
feeding (‘‘benefits’’; similar to Harrison 1985; Agetsuma
1995; Agetsuma and Noma 1995; Heiduck 2013). We
considered fleshy fruits as the main high-nutritional-density
item in the titi monkey diet, since these fruits are the major
component of their diet with readily available energy
(Caselli and Setz 2011), and they also may need less
manipulation and processing time than other high-nutritional-density food item, such as seeds (Lambert 2011).
First, we produced estimates per day of diet, activity
budget, distances traveled, and traveling speed, and
monthly estimates of home range size. We then calculated
the absolute difference between the mean of each variable
(food item, activity category, daily path length, traveling
speed, and home range size) in lean and rich periods, and
compared this difference to the distribution of differences
expected under the null hypothesis (variables are similar
between the two periods) to calculate the associated twotailed P value. The distribution of the differences expected
under the null hypothesis was generated by 1000 randomizations of the values between lean and rich periods
123
Primates
Table 1 Percentage of feeding samples (±SD) in which each food
item was consumed by Callicebus nigrifrons during an annual cycle
(N = 61 obs. days), lean months (N = 19 obs. days), and rich months
(N = 14 obs. days), and observed differences between the two
productivity periods, the simulated differences expected under the
null hypothesis, and associated P values
Item consumption (%)
Annual
Obs. diff.
Lean
Rich
Sim. diff.
P
Fleshy fruits
47 ± 30
27 ± 21
55 ± 27
28
8
\0.01*
Seeds and dry fruits
22 ± 22
35 ± 23
6±8
29
7
\0.01*
Vegetative plant parts
19 ± 16
30 ± 20
14 ± 10
16
5
0.02*
5 ± 12
5
2
0.05*
Flowers
2±6
\1 ± 2
Invertebrates
10 ± 12
7 ± 12
19 ± 15
12
4
0.01*
Liana items
51 ± 32
72 ± 27
54 ± 30
18
8
0.09
* P B 0.05
followed by their comparison (Monte Carlo simulation;
Manly 1997). We performed the analysis of each variable
separately with R 3.1.1 software (R Development Core
Team 2014). We also tested whether dietary plant species
diversity, which was calculated with the Shannon diversity
index (He0 , based on the number of feeding records for each
plant species), was different between the two productivity
periods, using a diversity t test in PAST 8.9 software
(Hammer et al. 2001).
Results
Relation between diet and food availability
Titi monkeys consumed fleshy fruits in proportion to their
availability (linear regression: F = 5.32, df = 1,
R2 = 0.35, P = 0.04). By contrast, the ingestion of vegetative plant parts, a lower-nutritional-density item, was
negatively related to the availability of fleshy fruits (linear
regression: F = 7.37, df = 1, R2 = -0.42, P = 0.02).
Seeds/dry fruits and flowers were eaten regardless of their
availability (linear regression: F = 0.58, df = 1,
R2 = 0.06, P = 0.46; and Spearman correlation:
rs = -0.42, N = 12, P = 0.18, respectively).
Variation in diet, activity pattern, and ranging
behavior between months of contrasting fleshy fruit
availability
During the months with the lowest fleshy fruit availability
(lean months), the titi monkeys consumed more seeds and
vegetative plant parts, and a greater diversity of plant
species (plant diversity in lean season: He0 = 2.6; plant
diversity in rich season: He0 = 2.3; diversity t test:
t = 3.06, df = 1019, P \ 0.01), while they ingested lower
percentages of fleshy fruits, insects, and flowers (Table 1).
Liana consumption was similarly high between lean and
rich months (accounting for more than 50 % of feeding
123
records; Table 1), and supplied all types of food items
(Online Resource 1).
During fleshy fruit scarcity, the group spent less time
traveling/moving and distances traveled were shorter, but
other activities, traveling speed, and monthly home range
size were similar between the two productivity periods
(Tables 2, 3). Home range exploitation, however, was more
diffuse during the lean months, when the feeding resources
(of which 90 % were lianas) were more diffusely spaced
throughout the habitat. During this period, there was no
overlap between the three monthly home ranges, and titis
shifted their core area (i.e. areas more frequently used;
Fig. 4). In contrast, during the three rich months, the titi
monkeys concentrated their activities near the center of
their home range, where one-third of the resources were
located, with a monthly overlap of 30 % (Fig. 4).
Discussion
We have demonstrated the relation between temporal food
fluctuations and food consumption by a group of titi
monkeys (Callicebus nigrifrons), and how they alter their
foraging behavior according to the availability of the main
high-nutritional-density items of their diet. Corroborating
both our first prediction and optimal foraging theory (Pyke
et al. 1977; Harrison 1984), the group of titi monkeys
consumed only the main high-nutritional-density items of
their diet (i.e. fleshy fruits) in accordance with their
availability over the course of 1 year, and the availability
of this item modulated the consumption of a relatively
lower-nutritional-density item, the vegetative plant parts.
The results did not support our prediction that the titi
monkeys would rely more on lianas during lean periods.
Despite the large number of feeding sites comprising lianas
in the lean months, the titi monkeys fed on lianas in high
proportions throughout the year. In contrast, the data corroborated the prediction that, in an optimal diet, the
inclusion of food types would increase as the abundance of
Primates
Table 2 Percentage of total behavior records spent in each activity
(±SD) by Callicebus nigrifrons during an annual cycle (N = 61 obs.
days), lean months (N = 19 obs. days), and rich months (N = 14 obs.
days), and observed differences between the two productivity periods,
the simulated differences expected under the null hypothesis, and
associated P values
Activity budget (%)
Annual
Obs. diff.
Lean
Sim. diff.
P
Rich
Traveling
21 ± 6
19 ± 5
24 ± 7
5
2
0.05*
Feeding
31 ± 9
28 ± 10
29 ± 8
1
2
0.81
Resting
45 ± 9
49 ± 11
43 ± 9
6
3
0.08
3±3
3±2
4±3
1
1
0.34
Other activities
* P B 0.05
Table 3 Travel distances (daily path length), traveling speed, and
home range size (±SD) of Callicebus nigrifrons during an annual
cycle (N = 40 obs. days), lean months (N = 11 obs. days), and rich
months (N = 10 obs. days), and observed differences between the
two productivity periods, the simulated differences expected under
the null hypothesis, and associated P values
Space use
Travel distances (m)
Travel speed (m/min)
Home range size (ha; MCP)
Annual
Lean
Rich
1222 ± 530
631 ± 376
1412 ± 495
Obs. diff.
Sim. diff.
P
781
218
\0.01*
7±3
5±4
7±2
2
1
0.09
17
7±4
8±3
1
3
0.89
Home range size for the annual cycle was calculated as the total area used during the entire study period, while home range size presented for
lean and rich periods are monthly estimates
* P B 0.05
preferred food types decreased (Pyke et al. 1977). When
the availability of fleshy fruits was lowest, the titi monkeys
consumed a greater diversity of plant species and increased
the ingestion of dry fruits/seeds and vegetative plant parts.
The ability of the group of titi monkeys to increase
dietary breadth and switch food items at times of fleshy
fruit shortage suggests that they have diet flexibility, which
is the most common response to food scarcity in primates
(Hemingway and Bynum 2005). Other species of titi
monkeys also switch food items, with the exception of
Cheracebus torquatus, which lives near the equator and
exhibits less seasonal variation in food choice (Easley
1982). During fruit availability bottlenecks, Callicebus
melanochir will feed more on seeds (Heiduck 1997),
C. coimbrai (Souza-Alves et al. 2011) and Plecturocebus
brunneus (Wright 1985) on leaves, and Cheracebus lugens
on seeds and flowers (Palacios et al. 1997). Here, seeds
were a prominent fallback food, supporting other findings
that titi monkeys may play an important role as seed
predators during food scarcity, despite lacking the full
range of dental adaptations to seed-eating present in other
pitheciines (Heiduck 1997; Palacios et al. 1997; dos Santos
et al. 2012; Palacios and Rodriguez 2013). It is important to
note, however, that these were generally unripe seeds in
hard-husked fruits or ripe seeds from softer fruits (see
Online Resource 1). The increased reliance upon seed
predation characterizes the evolutionary history of
pitheciids (Kay et al. 2013). Titi monkeys (a basal group in
the phylogeny of the pitheciines), uakaris, and sakis represent a morphocline of increasingly specialized dental
features for sclerocarpic foraging (Kay et al. 2013). In this
sense, sclerocarpy may have begun by progressively
pushing back the ripeness point at which seeds could be
exploited, minimizing the impact of resource bottleneck.
Since unripe seeds usually have elevated concentrations
of secondary compounds (Kinzey 1992), by increasing
dietary breadth along with seed ingestion, our study group
might have lowered the risk of over-ingestion of any given
toxin through dietary diversification (Glander 1982; Palminteri et al. 2016). In a proximate scale (i.e. ecological),
behavioral flexibility such as the capability to switch the
diet and increase seed consumption may be an important
adaptive response to seasonal environments, reducing the
impact of seasonal fruit shortages (Norconk 2011), since
the nutritional composition of seeds consumed by titi
monkeys is similar to that of the fleshy fruit parts eaten
(Heiduck 1997).
When testing which type of foraging strategy titi monkeys adopt when their main high-nutritional-density item is
scarce, we found evidence that they are energy minimizers
and adopt a low-cost/low-yield strategy. By switching from
a diet of large amounts of fleshy fruits and a moderate
amount of invertebrates, to a diet richer in seeds and leaves,
the study group might have maintained similar gross
123
Primates
Fig. 4 Home range of the Callicebus nigrifrons study group with
monthly used home ranges (95 % MPCs), the utilization distribution
(UD) estimates (using the adaptive kernel method), and the location
of the most important feeding sources used during lean (left) and rich
(right) months. The UD grayscale indicates the probability of finding
the group in a particular location, with more frequently used areas in
darker colors. Polygon with thicker line indicates total annual home
range; polygons with dotted lines indicate monthly home ranges;
triangles indicate trees, and circles indicate lianas
energy intake and nutritional balance between the two
periods of contrasting productivity. This is because, in
general, seeds are rich in lipids (Kinzey and Norconk
1993), and are therefore an alternative high-nutritionaldensity food (Lambert 2011), while leaves (especially
young leaves) may have a high protein content, similar to
invertebrates (Garber 1987; Lambert 2011). But because of
the higher expenses associated with extended handling and
processing time that results from hard pericarps and higher
levels of secondary compounds in seeds and the higher
fiber content in leaves (Kinzey and Norconk 1993; Lambert
2011), the energy yield during lean months may have been
lower. As a result, the titi monkeys reduced some energydemanding activities, such as traveling, which was also
expected under the optimal foraging theory (MacArthur
and Pianka 1966; Pyke et al. 1977).
Typically, when primates increase the consumption of
items that require more processing time, they also travel
less (e.g. Sapajus apella, Zhang 1995; Pan troglodytes
verus, Doran 1997; Propithecus verreauxi, Norscia et al.
2006; Ateles chamek, Wallace 2006; C. melanochir, Heiduck 2013; P. brunneus, Wright 2013). Although in our
study the traveling speed was similar between the two
productivity periods, travel distances (daily path length)
and travel time—two other potential measures of energy
expenditure (Krebs and Davies 1993)—were reduced during the lean months. Moreover, despite keeping similar
home range sizes, the low degree of monthly home range
overlap and the broader utilization distribution during the
lean months indicate that the study group used the home
range area more diffusely as fleshy fruits became scarce, in
addition to using the habitat more efficiently (considering
that they were traveling shorter distances per day, and
consequently expending less energy). This less
concentrated use of their home range during lean months
may be related to the distribution of feeding resources,
which seems to be more widely spaced in the habitat, or to
the increase in diet breadth, since finding a greater diversity
of plants may require a more extensive use of the habitat
(Palminteri et al. 2016). Although our results suggest a
relationship between home range usage and resource distribution, further studies focusing on resource distribution
are needed to confirm this spatial use pattern.
Lastly, it is important to note that fruit traps capture only
food items fallen from the canopy; therefore, they measure
a residual quantity of the available resources (total resource
production minus the amount eaten by frugivores), which
potentially underestimates resource production (Terborgh
1983). Although this method does not provide an estimate
of overall resource abundance, it provides reliable data on
seasonal fluctuations in resource availability (Terborgh
1983; Chapman et al. 1994), and so was appropriate for our
study.
We conclude that the study group of titi monkeys
responds to the availability of the main high-nutritionaldensity item of its diet (i.e. fleshy fruits) in a manner
similar to that predicted by optimal foraging theory
(MacArthur and Pianka 1966; Pyke et al. 1977). The titi
monkeys displayed foraging behaviors similar to the lowcost/low-yield strategy in response to fleshy fruit scarcity,
feeding on alternative items and reducing energy expenditure; this allows us to classify them as energy minimizers
(Schoener 1971). Our study also highlights the importance
of seeds as fallback foods for titi monkeys, and of lianas
and plant species from the families Myrtaceae, Rubiaceae,
and Moraceae as important feeding sources for primates in
fragmented areas, which should therefore be considered in
habitat restoration projects in this part of Brazil.
123
Primates
Acknowledgments This research was funded by São Paulo Research
Foundation (FAPESP, Grant No. 2009/12124-0). We also received
field equipment and support from Fund to Education, Research and
Extension (FAEPEX/Unicamp), Program of Academic Excellence
(PROEX/Capes/Unicamp), and Idea Wild. We are grateful to the
Colinas do Atibaia gated community for permission to conduct this
research at Ribeirão Cachoeira. We thank J.Y. Tamashiro (Botanical
Department, UNICAMP), L.C. Garcia, and J.A. Gomes for plant
species identification; C. B. Caselli, C.C. Gestich, E. FernandezDuque, M. Clement, and anonymous reviewers for valuable suggestions and comments on earlier versions of this paper.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval All applicable international, national, and/or
institutional guidelines for the care and use of animals were followed.
All research reported in this article was non-invasive, and no experiments were conducted on animals.
References
Agetsuma N (1995) Foraging strategies of Yakushima macaques
(Macaca fuscata yakui). Int J Primatol 16:595–609
Agetsuma N, Noma N (1995) Rapid shifting of foraging pattern by
Yakushima macaques (Macaca fuscata yakui) in response to
heavy fruiting of Myrica rubra. Int J Primatol 16:247–260
Altmann J (1974) Observational study of behavior: sampling
methods. Behaviour 40:227–267
Bivand R, Rundel C, Pebesma E, Hufthammer KO (2015) Package
‘‘rgeos’’: Interface to geometry engine. http://cran.r-project.org/
web/packages/rgeos/rgeos.pdf. Accessed 5 Aug 2015
Byrne H, Rylands AB, Carneiro JC et al (2016) Phylogenetic relationships of the New World titi monkeys (Callicebus): first appraisal of
taxonomy based on molecular evidence. Front Zool 13:10
Calenge C (2006) The package adehabitat for the R software: a tool
for the analysis of space and habitat use by animals. Ecol Modell
197:516–519
Calenge C (2011) Home range estimation in R: the adehabitat HR
package. http://cran.r-project.org/web/packages/adehabitatHR/
vignettes/adehabitatHR.pdf. Accessed 1 Aug 2011
Caselli CB, Setz EZF (2011) Feeding ecology and activity pattern of
black-fronted titi monkeys (Callicebus nigrifrons) in a semideciduous tropical forest of southern Brazil. Primates 52:351–359
Cepagri (2012) Centro de Pesquisas Meteorológicas e Climáticas
Aplicadas à Agricultura—UNICAMP. http://www.cpa.unicamp.
br/. Accessed 10 March 2012
Chapman CA, Wrangham R, Chapman LJ (1994) Indices of habitatwide fruit abundance in tropical forests. Biotropica 26:160–171
Ciiagro (2016) Centro Integrado de Informações Agrometeorológicas—Instituto Agronômico de Campinas. http://www.ciiagro.sp.
gov.br/. Accessed 2 Feb 2016
Dasilva GL (1992) The western black-and-white colobus as a low
energy strategist: activity budgets, energy expenditure and
energy intake. J Anim Ecol 61:79–91
Defler TR (1996) Aspects of the ranging pattern in a group of wild
woolly monkeys (Lagothrix lagothricha). Am J Primatol
38:289–302
Doran D (1997) Influence of seasonality on activity patterns, feeding
behavior, ranging, and grouping patterns in Taı̈ chimpanzees. Int
J Primatol 18:183–206
dos Santos GP, Galvao C, Young RJ (2012) The diet of wild blackfronted titi monkeys Callicebus nigrifrons during a bamboo
masting year. Primates 53:265–272
Easley SP (1982) Ecology and behavior of Callicebus torquatus,
Cebidae Primates. Ph.D. Dissertation. Washington University,
St. Louis
Ferreira JO (2010) GPS TrackMaker. GeoStudio Technology Ltd.
Belo Horizonte, Brasil. http://www.gpstm.com/. Accessed 8 Dec
2010
Garber P (1987) Foraging strategies among living primates. Annu
Rev Anthropol 16:339–364
Garcia LC, Hobbs RJ, Santos FAM, Rodrigues RR (2014) Flower and
fruit availability along a forest restoration gradient. Biotropica
46:114–123
Glander KE (1982) The impact of plant secondary compounds on
primate feeding behavior. Yearb Phys Anthropol 25:1–18
Hammer O, Harper D, Ryan PD (2001) PAST: paleontological
statistic software package for education and data analysis.
Paleontologia Eletrônica 4:9
Harrison MJS (1984) Optimal foraging strategies in the diet of the
green monkey, Cercopithecus sabaeus, at Mt. Assirik, Senegal.
Int J Primatol 5:435–471
Harrison MJS (1985) Time budget of the green monkey, Cercopithecus sabaeus: some optimal strategies. Int J Primatol 6:351–376
Hayne DW (1949) Calculation of size of home range. J Mammal
30:1–18
Heiduck S (1997) Food choice in masked titi monkeys (Callicebus
personatus melanochir): selectivity or opportunism? Int J
Primatol 18:487–502
Heiduck S (2013) Costs of foraging in the Southern Bahian masked
titi monkey (Callicebus melanochir). In: Veiga LM, Barnett AA,
Ferrari SF, Norconk MA (eds) Evolutionary biology and
conservation of titis, sakis and uacaris. Cambridge University
Press, Cambridge, pp 208–214
Hemingway CA, Bynum N (2005) The influence of seasonality on
primate diet and ranging. In: Brockman DK, Schaik CP (eds)
Seasonality in primates: studies of living and extinct human and
non-human primates. Cambridge University Press, Cambridge,
pp 57–104
Kaplin BA, Munyaligoga V, Moermond TC (1998) The influence of
temporal changes in fruit availability on diet composition and
seed handling in blue monkeys (Cercopithecus mitis doggetti).
Biotropica 30:56–71
Kay RF, Meldrum DJ, Takai M (2013) Pitheciidae and other
platyrrhine seed predators. In: Veiga LM, Barnett AA, Ferrari
SF, Norconk MA (eds) Evolutionary biology and conservation of
titis, sakis and uacaris. Cambridge University Press, Cambridge,
pp 3–12
Kinzey WG (1992) Dietary and dental adaptations in the Pitheciinae.
Am J Phys Anthropol 88:499–514
Kinzey WG, Norconk MA (1993) Physical and chemical properties of
fruit and seeds eaten by Pithecia and Chiropotes in Surinam and
Venezuela. Int J Primatol 14:207–227
Krebs JR, Davies NB (1993) An introduction to behavioral ecology.
Blackwell Science, Oxford
Kulp J, Heymann EW (2015) Ranging, activity budget, and diet
composition of red titi monkeys (Callicebus cupreus) in primary
forest and forest edge. Primates 56:273–278
Lambert JE (2011) Primate nutritional ecology: feeding biology and diet
at ecological and evolutionary scales. In: Campbell CJ, Fuentes A,
MacKinnon KC, Bearder SK, Stumpf RM (eds) Primates in
perspective. Oxford University Press, New York, pp 482–495
Lindstedt SL, Boyce MS (1985) Seasonality, fasting endurance, and
body size in mammals. Am Nat 125:873–878
MacArthur RH, Pianka ER (1966) On optimal use of a patchy
environment. Am Nat 100:603–609
123
Primates
Manly BFJ (1997) Randomization and Monte Carlo methods in
biology. Chapman and Hall, New York
Marshall AJ, Boyko CM, Feilen KL, Boyko RH, Leighton M (2009)
Defining fallback foods and assessing their importance in
primate ecology and evolution. Am J Phys Anthropol
140:603–614
Mitchell MS, Powell RA (2004) A mechanistic home range model for
optimal use of spatially distributed resources. Ecol Modell
177:209–232
Müller K-H (1996) Diet and feeding ecology of masked titis
(Callicebus personatus). In: Norconk MA, Rosenberger AL,
Garber PA (eds) Adaptative radiations of Neotropical primates.
Plenum, New York, pp 383–401
Norberg RA (1977) An ecological theory on foraging time and
energetics and choice of optimal food-searching method. J Anim
Ecol 46:511–529
Norconk MA (2011) Sakis, uakaris, and titi monkeys: behavioral
diversity in radiation of primate seed predation. In: Campbell CJ,
Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM (eds)
Primates in perspective. Oxford University Press, New York,
pp 122–139
Norscia I, Carrai V, Borgognini-Tarli SM (2006) Influence of dry
season and food quality and quantity on behavior and feeding
strategy of Propithecus verreauxi in Kirindy, Madagascar. Int J
Primatol 27:1001–1022
Palacios E, Rodriguez A (2001) Ranging patterns and use of space in
a group of red howler monkeys (Alouatta seniculus) in a
southeastern Colombian rain-forest. Am J Primatol 55:233–251
Palacios E, Rodriguez A (2013) Seed eating by Callicebus lugens at
Caparu Biological Station, on lower Apaporis River, Colombian
Amazonia. In: Veiga LM, Barnett AA, Ferrari SF, Norconk MA
(eds) Evolutionary biology and conservation of titis, sakis and
uacaris. Cambridge University Press, Cambridge, pp 225–231
Palacios E, Rodrı́gues A, Defler TR (1997) Diet of a group of
Callicebus torquatus lugens (Humboldt, 1812) during the annual
resource bottleneck in Amazonian Colombia. Int J Primatol
18:503–522
Palminteri S, Powell GV, Peres CA (2016) Determinants of spatial
behavior of a tropical forest seed predator: the roles of optimal
foraging, dietary diversification, and home range defense. Am J
Primatol 78:523–533
Peres CA (1994) Primate responses to phenological changes in an
Amazonian Terra Firme forest. Biotropica 26:98–112
Powell RA (2000) Animal home ranges and territories and home
range estimators. In: Boitani L, Fuller TK (eds) Research
techniques in animal ecology: controversies and consequences.
Columbia University Press, New York, pp 66–110
Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a
selective review of theory and tests. Q Rev Biol 52:137–154
R Development Core Team (2014) R: A language and environment
for statistical computing. Vienna, Austria. R Foundation for
Statistical Computing. http://www.R-project.org/. Accessed 2
Oct 2014
123
Ramos VS (2007) Árvores da floresta estacional semidecidual: guia
de identificação de espécies. Edusp, São Paulo
Rothman JM, Dierenfeld ES, Hintz HF, Pell AN (2008) Nutritional
quality of gorilla diets: consequences of age, sex, and season.
Oecologia 155:111–122
Santhosh K, Kumara HN, Velankar AD, Sinha A (2015) Ranging
behavior and resource use by lion-tailed macaques (Macaca
silenus) in selectively logged forests. Int J Primatol 36:288–310
Santos K (1998) Flora arbustivo-arbórea do fragmento de floresta
estacional semidecidual do Ribeirão Cachoeira, Campinas, SP.
Masteŕs dissertation. Universidade Estadual de Campinas,
Campinas
Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol
Syst 2:369–404
Setz EZF (1993) Ecologia alimentar de um grupo de parauacus
(Pithecia pithecia chrysocephala) em um fragmento florestal na
Amazônia central. Ph.D. Dissertation. Universidade Estadual de
Campinas, Campinas
Smythe N (1970) Relationships between fruiting seasons and seed
dispersal methods in a Neotropical forest. Am Nat 104:25–35
Souza-Alves JP, Fontes IP, Chagas RD, Ferrari SF (2011) Seasonal
versatility in the feeding ecology of a group of titis (Callicebus
coimbrai) in the Northern Brazilian Forest. Am J Primatol
73:1–11
Strier KB (2007) Primate behavioral ecology. Pearson, Boston
Terborgh JT (1983) Five New World primates: a study in comparative
ecology. Princeton University Press, Princeton
van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of
tropical forests: adaptive significance and consequences for
primary consumers. Annu Rev Ecol Syst 24:353–377
Vedder AL (1984) Movement patterns of a group of free-ranging
mountain gorillas (Gorilla gorilla beringei) and their relation to
food availability. Am J Primatol 7:73–88
Wallace RB (2005) Seasonal variations in diet and foraging behavior
of Ateles chamek in southern Amazonian tropical forest. Int J
Primatol 26:1053–1075
Wallace RB (2006) Seasonal variations in black-faced spider monkey
(Ateles chamek) habitat use and ranging behavior in a southern
Amazonian tropical forest. Am J Primatol 68:313–332
Worton BJ (1989) Kernel methods for estimating the utilization
distribution in home-range studies. Ecology 70:164–168
Wright PC (1985) The costs and benefits of nocturnality for Aotus
trivirgatus (the night monkey). Ph.D. Dissertation. City University of New York, New York
Wright PC (2013) Callicebus in Manu National Park: territory,
resources, scent marking and vocalizations. In: Veiga LM,
Barnett AA, Ferrari SF, Norconk MA (eds) Evolutionary biology
and conservation of titis, sakis and uacaris. Cambridge University Press, Cambridge, pp 232–239
Zhang S (1995) Activity and ranging patterns in relation to fruit
utilization by brown capuchins (Cebus apella) in French Guiana.
Int J Primatol 16:489–507