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Brief communication A preliminary study on the influence of physical fruit traits on fruit handling and seed fate by white-handed titi monkeys (Callicebus lugens).

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 147:482–488 (2012)
Brief Communication: A Preliminary Study on the
Influence of Physical Fruit Traits on Fruit
Handling and Seed Fate by White-Handed Titi
Monkeys (Callicebus lugens)
Silvia J. Alvarez1,2* and Eckhard W. Heymann1
1
2
Abteilung Verhaltensökologie & Soziobiologie, Deutsches Primatenzentrum, D-37077 Göttingen, Germany
Göttingen Centre for Biodiversity and Ecology, Georg-August-University of Göttingen, D-37073 Göttingen, Germany
KEY WORDS
frugivory; sclerocarpic foraging; Pitheciidae; puncture resistance; crushing resistance
ABSTRACT
Callicebus and the pitheciins are closely
related; however, differences in their diets and dental
morphology suggest that they differ in the use of
mechanically protected food. We describe physical traits
of fruits consumed by white-handed titi monkeys (Callicebus lugens) and determine their influence on fruit part
selection and immediate seed fate after fruit handling.
We tested two hypotheses about the effects of mechanical
fruit traits on fruit part selection and seed fate: (1) fruits
selected for seed consumption are harder than fruits
selected for their fleshy parts and (2) consumed seeds
are softer than seeds with other fates. In addition, we
analyzed the influence of other physical fruit traits on
fruit part selection and seed fate. C. lugens included 69
species in its diet, from which it mainly consumed their
fleshy parts. It also consumed seeds, alone or with fleshy
fruit parts, but most of them ended up close to parent
trees after being dropped or spat out. The first hypothesis was supported while the second was rejected, indicating that C. lugens tends to rely on hard fruits for obtaining seeds, while seed hardness had no influence on
fruit part selection and seed fate, contrasting with the
pattern reported for Pithecia and Chiropotes in
other studies. Ripeness was the most influential factor
for fruit part and seed fate discrimination. Results suggest a tendency to sclerocarpic foraging in C. lugens
when feeding on seeds. Am J Phys Anthropol 147:482–
488, 2012. V 2012 Wiley Periodicals, Inc.
The majority of primates include fruit in their diet
(Lambert, 2007). Fruit selection by vertebrate frugivores
relies on a variety of fruit characteristics, including
physical, chemical, and nutritional traits, which determine accessibility and influence diet composition as well
as fruit processing behaviors (Jordano, 1992). Physical
traits act as sensory cues that affect fruit finding,
manipulation, mastication, and digestion (Lucas et al.,
2001), influencing morphological, physiological, and behavioral adaptations of frugivores (Herrera, 1987, 1992;
Levey, 1987).
Frugivorous primates feed on a diverse array of fruit
parts and handle fruits in three main ways: (1) by swallowing whole fruits or fleshy fruit parts together with
seeds (i.e., discarding fruit skin or pericarp) and defecating intact seeds; (2) by eating the pulp and spitting out
or dropping seeds; or (3) by chewing and digesting seeds
(Lambert and Garber, 1998; Chapman and Russo, 2007).
These ways of handling fruits impose different biomechanical constraints on primates, resulting in a diversity
of morphological and behavioral adaptations that
respond to the challenges of ingestion and mastication
(Rosenberger, 1992; Norconk et al., 2009). For instance,
when preying on seeds, primates potentially face three
main types of plant defense mechanisms: hard fruit pericarps, hard seed coats, and/or secondary compounds or
toxins (Hulme and Benkman, 2002).
Seed predation is frequent in only a few platyrrhines
including the pithecids and capuchin monkeys (Kinzey,
1992; Kinzey and Norconk, 1993; Galetti and Pedroni,
1994; Boubli, 1999; Norconk and Conklin-Brittain, 2004;
Bowler and Bodmer, 2011). Pitheciins are highly special-
ized seed predators, classified as sclerocarpic foragers
based on their diet of soft seeds obtained from hardhusked fruits (Kinzey and Norconk, 1990, 1993). Therefore, dental adaptations including large, robust, widely
flaring canines, molars with low relief, and other morphological features have evolved (Kinzey, 1992; Anapol
and Lee, 1994; Martin et al., 2003; Wright, 2005; Lucas
et al., 2008). Much attention has been given to fruit and
seed hardness as factors that shape dental morphology
in the pitheciins (Kinzey and Norconk, 1990; Kinzey,
1992; Norconk et al., 2009).
Titi monkeys (Callicebus spp.) represent the sister
group of the pitheciins and the most diverse genus of the
family Pitheciidae (van Roosmalen et al., 2002; Defler et
al., 2010). Their diet generally consists of fleshy fruit
parts, although seeds are also frequently ingested
(Kinzey et al., 1977; Heiduck, 1997; Palacios et al., 1997;
Palacios and Rodriguez, in press). In contrast to pitheciins, Callicebus lacks highly specialized adaptations for
C 2012
V
WILEY PERIODICALS, INC.
C
Grant sponsors: Margot Marsh Biodiversity Foundation, Idea
Wild.
*Correspondence to: Silvia J. Alvarez, 3205 Biology Psychology
Building, University of Maryland, College Park, MD 20742, USA.
E-mail: silvitaja@gmail.com
Received 2 February 2011; accepted 21 December 2011
DOI 10.1002/ajpa.22021
Published online 27 January 2012 in Wiley Online Library
(wileyonlinelibrary.com).
PHYSICAL FRUIT TRAITS FOR Callicebus lugens
feeding on sclerocarpic fruits (i.e., hard-husked fruits)
but its gut proportions and dental morphology suggest
an ability to feed on seeds (Kinzey, 1992; Ferrari and
Lopes, 1995). Obtaining information on the characteristics of fruits exploited by titi monkeys adds to the understanding of sclerocarpic foraging evolution as well as its
ecological and behavioral implications. Therefore, in this
preliminary study, we aimed to determine physical traits
of fruits consumed by Callicebus lugens and their variation according to fruit part selected and seed handling.
Considering the phylogenetic affinity of Callicebus and
the pitheciins, and given that most plants with nonzoochorous dispersal syndromes tend to protect seeds
with hard coats against animals (Hulme and Benkman,
2002), we tested two hypotheses on mechanical traits of
fruits consumed by C. lugens during the 4 months covered by this study. First, fruits from which C. lugens
preys on seeds were expected to be harder than fruits
selected for fleshy parts, based on the difference in fruit
hardness between Ateles paniscus (i.e., pulp eater) and
Chiropotes satanas (Kinzey and Norconk, 1990). As a
second hypothesis, seeds preyed on by C. lugens were
expected to be softer than ‘‘dispersed’’ or discarded seeds,
given a negative correlation between hard husks and
seed hardness found in the diet of Pithecia pithecia and
C. satanas (Kinzey and Norconk, 1993).
METHODS
Study site
We conducted the study in southeastern Colombia, at
the Parque Nacional Natural Yaigojé Apaporis (Estación
Biológica Mosiro Itajura-Caparú) in the Apaporis river
basin (18040 S, 698300 W). Annual temperature averages
25.18C, while annual precipitation averages 3,950 6
486.3 mm and follows a bimodal regime without a dry
season (Defler and Defler, 1996). ‘‘Igapó’’ forests and different types of lowland non-floodable mature forests are
present in the area (Palacios and Rodriguez, 1995; Palacios et al., 2009). Ripe fruit production presents two
peaks, one in February, determined by three abundant
species of Lecythidaceae, and a second one between April
and July. A period of fruit scarcity occurs from November to January (Vargas and Stevenson, 2009).
Data collection
The study focused on a habituated family of whitehanded titi monkeys (C. lugens) consisting of an adult
male, an adult female, a juvenile, and an infant. We followed the family 5–10 days/month between February
and May 2007 for a total of 240 h.
We used scan sampling at 15 min intervals to determine general diet composition and relied on all-events
sampling for registering plant species and for gathering
behavioral data on frugivory, including duration of feeding event, consumed part (pulp, aril, seeds, or both pulp/
aril and seeds), ripeness (ripe or unripe), and seed handling (swallowed, dropped/spat, or chewed) for every
fruit-feeding event. A feeding event started when the
first individual took a fruit and finished when the last
individual abandoned the tree or stayed in it but stopped
eating for at least 5 min. Whenever possible, we collected feces and examined them for seed content.
To identify plant species and to determine fruit and
seed physical traits, we sampled 5–10 fruits and seeds
showing similar ripeness levels to those taken by
483
C. lugens. For each fruit, we determined: type (e.g., capsule, drupe, pod, etc.), color, size (length, width 1, and
width 2), mass, volume, pulp/aril dry mass, number of
seeds, water percentage of fleshy parts, and puncture resistance. We also determined these traits (except type,
color, and puncture resistance) and crushing resistance
for seeds, as well as flesh/seed ratio based on their dry
mass. To estimate fruit or seed volume, we measured the
displaced water volume in a graduated cylinder, except
for very large or very small units, which we calculated
based on the three linear size measures and by assuming an elliptic form. We measured dry masses in the
field, after drying fruits on metal sheets under the sun
until changes in mass reached zero. On the basis of wet
and dry mass differences, we calculated water percentage in fleshy fruit parts and seeds.
We used a force gauge (FDL60, Wagner Instruments) to
measure puncture resistance as the indentation force produced per unit area (penetrometer area 5 9.6 mm2). For
plant tissues, puncture resistance resembles the stress
that starts plastic deformation of a portion the size of the
penetration area, which is also defined as yield stress and
is related to hardness (Lucas et al., 2000, 2001).
For seed crushing resistance, we mailed fresh fruits
stored in sealed plastic bags to the Laboratory of Materials Research at the Universidad Nacional de Colombia
in Bogota. Crushing resistance of seeds resulted from
calculating the force (kilograms) needed for permanent
deformation of seeds based on compression stress (Lucas
et al., 2001). The crushing test relied on the load input
measured with load cells (ENERPAC).
To estimate availability of hard and soft fruits, we
monitored fruiting trees every 2 weeks along five transects of 300 m length each, located within the territory of
the study family. We registered all trees and lianas carrying fruits and standing at a maximal perpendicular
distance of 5 m to transect. Five to 10 fruits from each
fruiting species were sampled for puncture resistance
tests in each survey.
Data analysis and statistics
We excluded infant records, feeding events lasting less
than 1 min and single feeding events of the juvenile whenever it was not feeding on the same plant as its parents, in
order to avoid biases derived from potential differences in
fruit use between juveniles and adults. Variation of categorical traits (i.e., color, fruit type, and ripeness) in relation to selected fruit part was evaluated using v2 tests
with Monte-Carlo significance estimations (Manly, 2007).
For continuous variables, we estimated species averages
based on measures of 10 individual fruits and further
grouped them according to fruit part consumed and seed
fate. We analyzed normally distributed variables through
one-way ANOVAs with post hoc Scheffé tests, while applying Kruskal–Wallis tests with post hoc tests for asymptotical data for nonparametric variables.
We tested the hypotheses regarding differences in
puncture and crushing resistance, respectively, using a
Mann–Whitney U-test to compare fruits from which
C. lugens exclusively consumed fleshy fruit parts and
those from which seeds (alone or with pulp) were
ingested. Hard and soft fruit preferences were determined based on monthly availability of plants (i.e., the
relative abundance of trees with hard or soft fruits),
showing mean puncture resistances above and below 0.6
kg/mm2, respectively (following Kinzey and Norconk,
American Journal of Physical Anthropology
484
S.J. ALVAREZ AND E.W. HEYMANN
Fig. 1. Percentage of species and feeding time for (a) fruit
part (flesh1seeds refers to fruits where C. lugens fed both on
pulp or aril and on seeds) and (b) seed fate of fruits consumed
by C. lugens.
1990). We also classified fruit species used by C. lugens
in these two categories and applied Manly’s selection
ratios (wi) for preference analyses (Manly et al., 2002).
We identified fruit and seed traits that best explained
variation in fruit part selection and seed fate based on
multinomial logistic regressions, only including variables
weakly intercorrelated (i.e., Spearman rank correlation
\0.7) and showing significant differences in univariate
analyses (i.e., ANOVA and Kruskal–Wallis tests). We
tested regression models stepwise and used AIC to identify the most optimal model. Comparisons of nested
model deviances using v2 statistics were applied to identify the most influential variable (Zuur et al., 2007). We
used the software SPSS 12.0 (SPSS) for univariate statistics and R 2.13.0 (The R Foundation for Statistical
Computing) for preference analyses (package adehabitat)
and multinomial logistic regressions. The significance
level was set at a 5 0.05 for all statistical tests, except
for preference analysis, in which the Bonferroni level 5
0.025 was used.
RESULTS
Callicebus lugens fed on fruits (74.5%), arthropods
(19.5%), vegetative parts (5.5%), and flowers (0.5%),
American Journal of Physical Anthropology
based on 503 feeding records from scan sampling. Fruits
represented at least 69 species and 30 families, from
which Theobroma obovatum (Sterculiaceae), Dacryodes
peruviana (Burseraceae), and Inga cf. thibaudiana
(Fabaceae) were the most frequently consumed species.
It selected the majority of species (62.3%) for fleshy parts
(pulp or arils), followed by those selected both for fleshy
parts and seeds (21.7%), with a similar trend in terms of
feeding time (Fig. 1a). In fruits selected both for fleshy
parts and for seeds, these were taken at the same time
or separately, depending on ripeness, that is, seeds when
unripe and fleshy parts when ripe.
Callicebus lugens handled fruits in different ways,
thereby influencing seed fate. Seeds of 71% of species
ended up dropped or spat close to parental trees after it
consumed their fleshy parts, while only 11.6% of species
were dispersed through feces. Dropped seeds also occupied most of its feeding time (Fig. 1b).
Puncture resistance of fruits averaged 0.46 kg/mm2
(n 5 56; SD 5 0.26). Soft-coated fruits (puncture resistance \ 0.6 kg/mm2) accounted for 78% of the species and
68% of the feeding time. Nevertheless, C. lugens was
able to open sclerocarpic fruits ([0.6 kg/mm2) with puncture resistance values higher than 1.2 kg/mm2 such as
Gustavia poeppigiana (1.65 kg/mm2).
Puncture resistance differed significantly among fruits
varying in fruit part selected (H 5 3.804, df 5 2, P \
0.05). Fruits consumed for fleshy parts had softer pericarps than fruits selected for seeds or for both fleshy
parts and seeds (U 5 198, W 5 901, Z 5 22.753, P \
0.01; Fig. 2a), which supported our first hypothesis.
Puncture resistance also differed among seed fates (H 5
10.220, df 5 3, P \ 0.05; Fig. 2b).
Crushing resistance of seeds averaged 15.6 kgf (n 5
48, SD 5 24.8), ranging between 3.1 kgf and 123.0 kgf
but without showing significant variation among fruits
according to fruit part selected (H 5 1.393, df 5 2, P 5
0.498; Fig. 3a) or seed fate (H 5 1.882, df 5 3, P 5
0.597; Fig. 3b). Thus, the second hypothesis (i.e., seeds
preyed on are softer than discarded or dispersed seeds)
was not supported. However, there was a trend in mean
crushing resistance decreasing from seeds of fruits
selected for their fleshy parts alone (18.4 kgf) to those
selected for seeds together with fleshy parts (11.0 kgf) or
alone (8.4 kgf).
Overall fruit availability decreased in April and May,
with a higher proportion of hard fruits over soft fruits
available in February (v2 5 38.841, df 5 3, P \ 0.001;
Table 1). When considering fruit use in relation to puncture resistance, the pattern of soft and hard fruits consumption varied among months during the 4-month
sample period (v2 5 63.552, df 5 3, P \ 0.001). Soft
fruits represented between 62 and 81% of the diet,
whereas hard fruits varied between 19 and 38% (Table
1). Preference for soft and hard fruits varied between
months. C. lugens preferred soft fruits in February and
March and avoided them in April, whereas it avoided
hard fruits in February and March (Table 1).
Ripeness varied significantly among species according
to fruit part consumed by C. lugens (v2 5 512.993, df 5
4, P = 0.001), which relied mostly on ripe fruits for fleshy
parts in contrast to unripe fruits for seeds. Most used
fruits were in the form of capsules, drupes, and pods,
with consumption of different fruit parts and seed fate
varying significantly with fruit type (fruit parts: v2 5
30.921, df 5 10, P 5 0.001; seed fate: v2 5 62.921, df 5
15, P = 0.001), for example, C. lugens mainly obtained
485
PHYSICAL FRUIT TRAITS FOR Callicebus lugens
Fig. 2. Puncture resistance of fruit species consumed by C. lugens, considering (a) fruit part consumed (flesh1seeds refers to
fruits where C. lugens fed both on pulp or aril and on seeds) and (b) seed fate (f: dispersed with feces, d: dropped; d/p: dropped and
preyed upon; p: preyed upon). Box plots show median values with 25th and 75th percentiles; whiskers were set at minimum and
maximum values; circles mark outliers. Horizontal lines indicate pair wise significant differences (P 0.05); numbers in brackets
correspond to sample sizes.
Fig. 3. Crushing resistance of fruit species consumed by C. lugens (a) for different fruit parts (flesh1seeds refers to fruits where
C. lugens fed both on pulp or aril and on seeds) and (b) with different seed fates (f: dispersed with feces, d: dropped; d/p: dropped
and preyed upon; p: preyed upon). Box plots show median values with 25th and 75th percentiles; whiskers represent maximum and
minimum values; circles mark outliers; numbers in brackets correspond to sample sizes.
TABLE 1. Soft and hard fruit preferences by C. lugens
Month
February
Soft
Hard
March
Soft
Hard
April
Soft
Hard
May
Soft
Hard
Proportion in diet
Availability
Selection index (wi)
SE (wi)
Lower value (CI 95%)
Upper value (CI 95%)
P
0.701
0.299
0.395
0.605
1.775
0.495
0.258
0.058
1.197
0.365
2.353
0.625
**
***
0.810
0.190
0.610
0.390
1.320
0.493
0.123
0.081
1.044
0.312
1.596
0.674
**
***
0.616
0.384
0.793
0.207
0.777
1.853
0.063
0.503
0.636
0.726
0.918
2.980
***
n.s.
0.774
0.226
0.866
0.134
0.894
1.686
0.048
0.550
0.786
0.454
1.002
2.918
n.s.
n.s.
v2 tests were applied for statistical testing (*: P 0.025; **: P 0.01; ***: P 0.001).
seeds from capsules. There was no relationship between
color and fruit part consumed (v2 5 3.727, df 5 10, P 5
0.969) or seed fate (v2 5 13.082, df 5 15, P 5 0.645).
Fruit volume ranged from 0.03 to 130.70 cm3, but
most fruit had volumes \5 cm3. The number of seeds
per fruit varied between one and about 1,000, with the
American Journal of Physical Anthropology
486
S.J. ALVAREZ AND E.W. HEYMANN
TABLE 2. Physical characteristics (mean 6 SD) of consumed fruits according to fruit parts selected by C. lugens and differences
among them
Fruit part
Fruit characteristic
Total sample
Fruit length (cm)
Fruit width 1 (cm)
Fruit width 2 (cm)
Fruit volume (cm3)
Fruit mass (g)
Puncture resistance (kg/mm2)
Seeds/fruit
Pulp dry mass (g)
Flesh/seed ratio
Pulp water (%)
Seed length (cm)
Seed width 1 (cm)
Seed width 2 (cm)
Seed volume (cm3)
Seed mass (g)
Seed dry mass (g)
Seed water (%)
Crushing resistance (kgf)
6.1
2.1
1.8
17.4
16.4
0.46
30.2
1.0
0.60
74.8
1.5
1.0
0.8
1.2
1.4
0.8
41.2
15.63
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
7.2
1.1
1.1
27.6
6.9
0.26
134.5
2.3
1.39
21.7
0.8
0.6
0.5
1.7
1.8
1.1
19.6
24.86
Fleshy part 1 seed
Fleshy part
7.5
2.13
1.6
20.5
19.9
0.41
43.0
0.8
0.65
82.1
1.6
1.0
0.8
0.9
1.2
0.7
38.8
18.43
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
8.5
0.90
0.9
27.6
27.6
0.18
164.5
1.6
1.64
10.7
0.6
0.4
0.4
1.1
1.2
0.8
15.7
29.24
3.1
2.5
2.5
19.5
17.9
0.59
3.6
1.5
0.43
75.0
1.7
1.4
1.1
1.7
1.8
0.9
52.2
11.02
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
1.6
1.4
1.3
34.6
31.5
0.36
4.8
3.9
0.45
14.1
0.7
0.6
0.4
1.8
1.9
0.9
15.4
13.53
Seed
P
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
n.s.
n.s.
*
n.s.
n.s.
*
n.s.
n.s.
*
**
n.s.
**
n.s.
n.s.
n.s.
n.s.
**
n.s.
4.1
2.6
2.0
15.9
14.5
0.63
9.4
1.2
0.20
32.8
1.8
1.1
0.9
2.0
2.2
1.3
55.3
8.36
2.2
1.2
1.5
23.6
23.4
0.34
19.7
2.6
0.39
38.3
0.9
0.7
0.8
3.7
3.9
2.6
12.2
4.73
*: P 0.05; **: P 0.01; ***: P 0.001.
TABLE 3. Physical characteristics (mean6SD) of consumed fruits and differences among seed fate of fruits selected by C. lugens
Fruit characteristic
Fruit length (cm)
Fruit width 1 (cm)
Fruit width 2 (cm)
Fruit volume (cm3)
Fruit mass (g)
Puncture resistance (kg/mm2)
Seeds/fruit
Pulp dry mass (g)
Flesh/seed ratio
Pulp water (%)
Seed length (cm)
Seed width 1 (cm)
Seed width 2 (cm)
Seed volume (cm3)
Seed mass (g)
Seed dry mass (g)
Seed water (%)
Crushing resistance (kgf)
Dispersed
1.1 6 0.6
1.1 6 0.7
1.1 6 0.7
1.6 6 2.9
1.6 6 2.7
0.33 6 0.09
161.0 6 317.8
0.4 6 0.6
Excluded
79.1 6 7.8
0.4 6 0.4
0.3 6 0.3
0.2 6 0.2
0.1 6 0.1
0.1 6 0.2
0.1 6 0.1
17.5 6 26.5
7.86 6 3.40
Dropped
Seed fate
Dropped/Preyed
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
3.2
2.8
2.7
24.1
22.3
0.63
4.4
1.9
0.52
73.5
1.8
1.4
1.0
1.9
1.9
0.9
53.2
12.24
9.6
2.2
1.6
21.8
21.2
0.40
5.0
0.9
0.35
82.4
1.8
1.1
0.9
1.1
1.4
0.8
40.7
29.39
8.8
0.9
0.9
28.1
28.2
0.18
5.3
1.6
0.28
11.0
0.5
0.3
0.4
1.2
1.2
0.8
12.3
31.49
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
1.7
1.5
1.4
39.4
35.1
0.40
5.3
4.4
0.48
15.3
0.7
0.7
0.4
2.0
2.1
1.0
16.1
15.06
Preyed on
P
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
***
**
*
***
***
*
***
*
*
*
***
***
***
***
***
***
***
n.s.
3.6
2.3
1.9
12.0
10.7
0.58
6.6
0.8
0.18
48.5
1.7
1.2
1.0
1.8
1.9
1.1
53.2
7.80
2.0
1.0
1.2
19.6
19.4
0.29
16.1
2.1
0.31
38.6
0.8
0.6
0.7
3.0
3.1
2.0
12.8
4.14
*: P 0.05; **: P 0.01; ***: P 0.001.
majority of fruits (62%) having less than five seeds. A
high percentage of fruit species (80%) also showed a relatively low flesh/seed ratio (below 0.5) while only 10% of
the species had a flesh/seed ratio larger than 1.0. Most
fruit species (65%) carried seeds that were 1–2 cm long
and weighed less than 1 g.
Fruits grouped according to fruit part consumed by C.
lugens differed in some physical traits other than puncture
resistance (Table 2). Fruits selected for fleshy parts were
slightly smaller than those selected for both fleshy parts
and seeds due to width differences. Water content and
flesh/seed ratio of fruits selected for seeds were significantly lower than in those selected for fleshy parts alone or
with seeds. Seeds of fruits used for fleshy parts and seeds
were larger than those selected for fleshy fruit parts or
seeds alone, while consumed seeds presented higher water
contents than seeds of fruits selected for fleshy parts.
Almost all physical fruit traits varied when analyzed
in relationship to seed fate (Table 3). Differences in some
American Journal of Physical Anthropology
traits highlighted distinct features of fruits selected for
seeds by C. lugens, including lower flesh/seed ratio and
pulp dry mass than fruits from which they dropped or
both dropped and preyed on seeds. Seeds preyed on by
C. lugens were heavier than dropped or dispersed seeds.
Multinomial logistic regressions for fruit part were
tested for combinations of the variables: fruit type, ripeness, fruit width, seed width, puncture force, flesh/seed
ratio, water percentage of fleshy fruit part, and seed
water percentage. The model that best explained fruit
part consumed included all the traits considered except
fruit type, fruit width, and flesh/seed ratio (AIC 5
30.50). Ripeness had a larger influence on fruit part
selection than any other trait (LRT 5 246.65, P \
0.001) followed by water percentage of fleshy fruit part
(LRT 5 213.35, P \ 0.001) and seed width (LRT 5
212.82, P \ 0.001). Puncture force was important for
discriminating between fruits selected for fleshy parts
and those selected for both fleshy parts and seeds.
487
PHYSICAL FRUIT TRAITS FOR Callicebus lugens
TABLE 4. Seed eating and mechanical fruit traits in pitheciins and C. lugens
Fruit trait
C. satanasa,b
P. pitheciab
C. lugens
Percentage of species used for seeds
Percentage of seed-eating time
Maximum puncture resistance of exocarp (kg/mm2)
Puncture resistance of exocarp (mean 6 s.d.)
Maximum crushing resistance of endocarp (kgf)
Crushing resistance of endocarp (mean 6 s.d.)
89.7
52–91
37.8
2.15 6 0.37
9.1
4.63 6 0.55
6.63 6 1.35
95.1
38–88
6.8
1.20 6 0.29
37.0
8.76 6 2.13
26.1 (21.0c)
15 (26.9–48.3c)
1.65
0.46 6 0.26
13.0
8.36 6 4.73
a
b
c
Values reported for Chiropotes satanas in Surinam (Kinzey and Norconk, 1990) and Venezuela (Kinzey and Norconk, 1993).
Values reported for Pithecia pithecia in Venezuela (Kinzey and Norconk, 1993).
In brackets, seed proportions in C. lugens diet reported previously (Palacios et al., 1997).
Physical traits used to model variation in seed fate
were fruit type, ripeness, fruit width 1, fruit width 2,
seed width, puncture force, flesh/seed ratio, dry pulp
mass, number of seeds, water percentage of fleshy fruit
part, and seed water percentage. The best model
included ripeness, puncture force, flesh/seed ratio, dry
pulp mass, number of seeds, and seed water percentage
(AIC 5 48.06). As seen in the model for fruit part, ripeness showed the highest influence on seed fate discrimination (LRT 5 261.14, P \ 0.001), followed by number
of seeds (LRT 5 235.46, P \ 0.001) and flesh/seed ratio
(LRT 5 229.13, P \ 0.001). Estimated regression parameters suggest that flesh/seed ratio, puncture force,
seed water, and pulp dry mass were important variables
for separating dropped seeds from other seed fates. The
number of seeds was important for discriminating
between preyed upon and dropped seeds.
DISCUSSION
When Callicebus lugens consumed fruit, it fed on the
pulp or aril of most species (62%), although seeds alone
or together with fleshy parts represented a frequent
resource both in terms of species (38%) and feeding time
(28%). Previous research classified C. lugens as a frugivore-granivore based on the high proportion of seeds in
its diet (Palacios et al., 1997; Palacios and Rodriguez, in
press).
Overall, puncture resistance values obtained during
the 4-month sample period indicate the use of mostly
soft fruits by C. lugens, although fruits selected for their
fleshy parts had softer skins than fruits selected for
seeds. Average puncture resistance was lower than for
fruits consumed by Pithecia pithecia and Chiropotes
satanas (Kinzey and Norconk, 1990, 1993; Table 4).
When considering the maximum puncture resistance, it
is still much below those registered for the pitheciins but
slightly higher than for a primate with a soft fruit diet
such as Ateles paniscus (1.4 kg/mm2; Kinzey and
Norconk, 1990). The results in this preliminary study
suggest that C. lugens might represent an intermediate
frugivorous strategy between pulp consumers and specialized seed predators among Neotropical primates. The
whole range of variation in puncture resistance, based
on a longer sampling period, is still needed for a more
accurate picture of its frugivorous strategy.
In comparison to pitheciins, during the 4-month sample period, crushing resistance of seeds averaged slightly
lower than P. pithecia but higher than C. satanas
(Kinzey and Norconk, 1993; Table 4). Contrastingly,
mean crushing resistance of seeds swallowed whole by
A. paniscus was much higher (21.16 kgf; Kinzey and
Norconk, 1990). A negative correlation between chemical
defense in seeds and seed coat hardness (Kinzey, 1992;
Norconk and Conklin-Brittain, 2004) suggests that seeds
consumed by C. lugens may contain high antifeedant
concentrations, because it feeds on relatively soft unripe
seeds. Results from C. personatus show a tendency toward high concentration of tannins in consumed seeds
(Heiduck, 1997) and P. pithecia seems to accept high concentrations of tannins and dietary fiber by selecting
lipid-rich seeds (Norconk and Conklin-Brittain, 2004).
Other physical traits (e.g., low flesh/seed ratio and low
water contents in pulp) that influenced fruit part selection and seed fate, varied in accordance to the trends
found for fruit and seed hardness in this preliminary
study and points to some similarities between C. lugens
and the rest of the Pitheciidae in the use of dry husked
fruits for seed consumption (Kinzey and Norconk, 1993;
Boubli, 1999; Norconk, 2007).
Physical traits of fruits influenced fruit handling in C.
lugens during the 4-month sample period. The whitehanded titi monkey’s ability to exploit seeds from relatively softer fruits than those used by pitheciins might
represent a model for the frugivorous strategy in the
early stage of the evolution of sclerocarpic foraging.
ACKNOWLEDGMENTS
The authors thank Conservación Internacional Colombia for assistance during field work, Roberto Yucuna for
his invaluable help in the field, the Laboratory of Materials Research at Universidad Nacional de Colombia for
providing equipment and services to measure crushing
resistance. The authors are especially thankful to Stefanie Heiduck and the anonymous reviewers for their comments to improve this manuscript.
LITERATURE CITED
Anapol F, Lee S. 1994. Morphological adaptation to diet in platyrrhine primates. Am J Phys Anthropol 94:239–261.
Boubli JP. 1999. Feeding ecology of black-headed uacaris
(Cacajao melanocephalus melanocephalus) in Pico da Neblina
National Park, Brazil. Int J Primatol 20:719–749.
Bowler M, Bodmer R. 2011. Diet and food choice in Peruvian
red uakaris (Cacajao calvus ucayalii): selective or opportunistic seed predation? Int J Primatol 32:1109–1122.
Chapman CA, Russo SE. 2007. Primate seed dispersal. In:
Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder
SK, editors. Primates in perspective. New York: Oxford University Press. p 510–525.
Defler TR, Bueno ML, Garcı́a J. 2010. Callicebus caquetensis: a
new and critically endangered titi monkey from southern
Caquetá, Colombia. Primate Conserv 25:1–9.
Defler TR, Defler S. 1996. Diet of a group of Lagothrix lagothricha in southeastern Colombia. Int J Primatol 17:161–189.
American Journal of Physical Anthropology
488
S.J. ALVAREZ AND E.W. HEYMANN
Ferrari SF, Lopes MA. 1995. Comparison of gut proportions in
four small-bodied Amazonian cebids. Am J Primatol 35:139–
142.
Galetti M, Pedroni F. 1994. Seasonal diet of capuchin monkeys
(Cebus apella) in a semideciduous forest in South-East Brazil.
J Trop Ecol 10:27–39.
Heiduck S. 1997. Food choice in masked titi monkeys (Callicebus personatus melanochir): selectivity or opportunism? Int
J Primatol 18:487–502.
Herrera CM. 1987. Vertebrate dispersed plants of the Iberian
Peninsula: a study of fruit characteristics. Ecol Monogr
57:305–331.
Herrera CM. 1992. Interspecific variation in fruit shape: allometry, phylogeny and adaptation to dispersal agents. Ecology
72:1832–1841.
Hulme PE, Benkman CW. 2002. Granivory. In: Herrera CM,
Pellmyr O, editors. Plant-animal interactions, an evolutionary approach. UK: Blackwell Publishing. p 132–154.
Jordano P. 1992. Fruits and frugivory. In: Fenner M, editor.
Seeds: the ecology of regeneration in plant communities. Wallingford, UK: CAB International. p 105–155.
Kinzey WG. 1992. Dietary and dental adaptations in the Pitheciinae. Am J Phys Anthropol 88:499–514.
Kinzey WG, Norconk MA. 1990. Hardness as a basis of fruit
choice in two sympatric primates. Am J Phys Anthropol 8:5–
15.
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 12:207–227.
Kinzey WG, Rosenberger AL, Heisler PS, Prowse DL, Trilling
JS. 1977. A preliminary field investigation of the yellow
handed titi monkey, Callicebus torquatus torquatus, in northern Peru. Primates 18:159–181.
Lambert JE. 2007. Primate nutritional ecology, feeding biology
and diet at ecological and evolutionary scales. In: Campbell
CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK, editors. Primates in perspective. New York: Oxford University
Press. p 482–495.
Lambert JE, Garber PA. 1998. Evolutionary and ecological
implications of primate seed dispersal. Am J Phys Anthropol
45:9–28.
Levey DJ. 1987. Seed size and fruit-handling techniques of
avian frugivores. Am Nat 129:471–485.
Lucas PW, Beta T, Darvell BW, Dominy NJ, Essackjee HC, Lee
PKD, Osorio D, Ramsden L, Yamashita N, Yuen TDB. 2001.
Field kit to characterize physical, chemical and spatial
aspects of potential primate foods. Folia Primatol 72:11–25.
Lucas PW, Constantino P, Wood B, Lawn B. 2008. Dental
enamel as a dietary indicator in mammals. Bioessays 30:374–
385.
Lucas PW, Turner IM, Dominy NJ, Yamashita, N. 2000. Mechanical defenses to herbivory. Ann Bot 86:913–920.
Manly BFJ. 2007. Randomization, bootstrap and Monte Carlo
methods in biology. Boca Raton, FL: Taylor & Francis Group,
LLC.
Manly BFJ, McDonald LL, Thomas DL, McDonald TL, Erickson
WP. 2002. Resource selection by animals: statistical design
American Journal of Physical Anthropology
and analysis for field studies. Boston: Kluwer Academic Publishers.
Martin LB, Olejniczak AJ, Maas MC. 2003. Enamel thickness
and microstructure in pitheciin primates, with comments on
dietary adaptations of the middle Miocene hominoid Kenyapithecus. J Hum Evol 45:351–367.
Norconk M, Conklin-Brittain N. 2004. Variation on frugivory:
the diet of Venezuelan white-faced sakis. Int J Primatol 25:1–
26.
Norconk MA. 2007. Sakis, uakaris, and titi monkeys. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK,
editors. Primates in perspective. New York: Oxford University Press. p 123–138.
Norconk MA, Wright BW, Conklin-Brittain NL, Vinyard CJ.
2009. Mechanical and nutritional properties of food as factors
in platyrrhine dietary adaptations. In: Garber PA, Estrada A,
Bicca-Marques JC, Heymann EW, Strier KB, editors. South
American primates: comparative perspectives in the study of
behavior, ecology, and conservation. New York: Springer. p
279–319.
Palacios E, Rodriguez A. 1995. Caracterización de la dieta y
comportamiento alimentario de Callicebus torquatus lugens.
Unpublished thesis, Universidad Nacional de Colombia.
Palacios E, Rodriguez A. in press. Seed eating by Callicebus
lugens at Caparú Biological Station, on the lower Apaporis
River, Colombian Amazonia. In: Barnett A, Veiga L, Ferrari
S, Norconk M, editors. Evolutionary biology and conservation
of titis, sakis and uakaries. Cambridge: Cambridge University
Press.
Palacios E, Rodriguez A, Alarcón-Nieto G. 2009. Aspectos fı́sicos
y biológicos del bajo Rı́o Apaporis y la Estación Biológica
Mosiro Itajura-Caparú. In: Alarcón-Nieto G, Palacios E, editors. Estación Biológica Mosiro Itajura-Caparú: biodiversidad
en el territorio del Yaigojé-Apaporis. Bogota: Conservación
Internacional Colombia. p 29–40.
Palacios E, Rodriguez 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.
Rosenberger AL. 1992. Evolution of feeding niches in New
World monkeys. Am J Phys Anthropol 88:525–562.
Van Roosmalen MGM, Van Roosmalen T, Mittermeier RA. 2002.
A taxonomic review of the titi monkeys, genus Callicebus
Thomas, 1903, with the description of two new species, Callicebus bernhardi and Callicebus stephennashi, from Brazilian
Amazonia. Neotropical Primates (Suppl) 10:1–52.
Vargas IN, Stevenson PR. 2009. Patrones fenológicos en la Estación Biológica Mosiro Itajura-Caparú: producción de frutos
estimada a partir de transectos fenológicos y trampas de frutos. In: Alarcón-Nieto G, Palacios E, editors. Estación Biológica Mosiro Itajura-Caparú: biodiversidad en el territorio del
Yaigojé-Apaporis. Bogota: Conservación Internacional Colombia. p 99–114.
Wright BW. 2005. Craniodental biomechanics and dietary toughness in the genus Cebus. J Hum Evol 48:473–492.
Zuur AF, Ieno EN, Smith GM. 2007. Analyzing ecological data.
New York: Springer.
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