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).код для вставкиСкачать
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: email@example.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.