Ecological Correlates of Ranging Behavior in Bearded Sakis (Chiropotes sagulatus) in a Continuous Forest in Guyana
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- Shaffer, C.A. Int J Primatol (2013) 34: 515. doi:10.1007/s10764-013-9682-z
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Group size and the distribution and quality of food resources are among the most important determinants of primate ranging behavior. In this study, I use the framework of the ecological constraints model to assess correlates of range size of a free-ranging group of bearded sakis (Chiropotes sagulatus). Bearded sakis are among the widest ranging neotropical primates, yet the lack of data from continuous forest populations has made understanding the factors influencing such large ranges difficult. I collected data on ranging behavior and diet during 44 full-day follows over 15 mo. The focal group used a home range of ca. 1000 ha and had daily path lengths of 2.8–6.5 km (mean = 4.0 km). Daily path length did not significantly correlate with group size, patch quality, food availability, or the spatial distribution of feeding trees. Monthly home range size significantly positively correlated with group size and patch quality. The focal group had significantly shorter paths when ripe fruit consumption was higher and had more diverse diets, visited more food patches, and used larger monthly home ranges when they consumed a higher percentage of seeds. The results of this study, combined with other recent studies of Chiropotes in continuous forest, suggest that large home ranges (approaching 1000 ha) are characteristic of the genus. Although range size may be related to group size and food patch size, I suggest nutrient mixing and the need to balance the effects of seed secondary compounds as additional explanations for the large ranges of bearded sakis.
KeywordsDaily path Home range Pitheciines
Much of the research in primate ecology focuses on how primates move about their environments during the course of the year. Although several factors are thought to determine the size of primate home and day ranges, group size and the distribution and quality of food resources are considered among the most important (Chapman 1988, 1990; Chapman and Chapman 2000; Clutton-Brock and Harvey 1977; Dias and Strier 2003; Isbell 1991; Janson 1992; Kirkpatrick et al. 1998; Koenig et al. 1998; Leighton and Leighton 1982; Milton and May 1976; Phillips 1995; Stevenson et al. 1998; Symington 1988; White and Wrangham 1988). One of the most commonly invoked models of primate ranging behavior is the ecological constraints model. The ecological constraints model explains ranging behavior in the context of intragroup feeding competition and makes several specific predictions about the relationship between group size, ecological variables, and home range size and daily path length (Chapman and Chapman 2000).
One of these predictions is that primate group size correlates positively with both daily path length and home range size (Chapman and Chapman 2000; Chapman et al. 1995). Using explanations derived from optimal foraging theory, researchers have hypothesized that the benefits of larger group size increase at a slower rate than the costs of intragroup feeding competition for a finite set of resources (Isbell 1991; Janson 1988; Janson and Goldsmith 1995; Wrangham et al. 1993). As individuals living in large groups should suffer from increased intragroup feeding competition, they must travel further each day and use larger supply areas to meet the increased nutritional requirements associated with more individuals in the group. Much of the data supporting the ecological constraints model has come from reports of positive correlations between group size and daily path length in primates with high fission–fusion dynamics (Chapman et al. 1995; Symington 1988; White and Wrangham 1988; Wrangham et al. 1993). Similar results have been reported for other primate species, including Alouatta (Stevenson et al.1998), Cebus (Phillips 1995; Stevenson et al.1998), and Brachyteles (Dias and Strier 2003), but some researchers have challenged the applicability of the ecological constraints model to all primates (Sussman and Garber 2011; Yeager and Kirkpatrick 1998).
The ecological constraints model also predicts that the ranging behavior of primates is related to the distribution and abundance of resources (Chapman and Chapman 2000). Specifically, primates exploiting resources that are patchily distributed in time and space should have larger ranges than those exploiting more uniformly distributed resources (Chapman and Chapman 2000; Snaith and Chapman 2007). When patches are further apart or contain fewer food items, primates must increase foraging effort by traveling further and visiting more patches to obtain the same amount of food as those feeding on more uniformly distributed food patches.
Recently, several researchers have emphasized nutritional ecology in models of primate foraging behavior (Felton et al. 2009; Lambert 2011; Rothman et al. 2012). These researchers point to the importance of understanding how primates balance macro- and micronutrients in assessing the factors influencing primate foraging decisions. Primates are faced with the challenge of maximizing nutrient balance while consuming different plant parts and different plant species. Primates must correspondingly adjust their ranging behavior to exploit foods that allow them to maximize energy uptake, maintain a proper nutrient balance, and/or avoid toxins and secondary compounds (Dearing et al. 2005; Robbins et al. 2007; Schoener 1971). Recent studies have shown nutrient mixing and the need to maintain a stable daily protein intake to be important determinants of primate patch use and ranging behavior (Felton et al. 2009; Righini and Garber 2012). Therefore, the type of resources that primates consume and the nutrient content of those foods may be just as, if not more, important in determining ranging behavior than group size or overall resource availability.
Although the predictions of the ecological constraints model have been supported in several studies of frugivorous primates, the applicability of the model to folivores is less clear (Snaith and Chapman 2007). Folivores are generally assumed to be less food-limited than frugivores as they exploit a more uniformly distributed and abundant resource (Isbell 1991; Kirkpatrick et al. 1998). In addition, the lower nutrient content of leaves means that nutrient mixing may play a more important role in determining the ranging behavior and group size of folivores than in frugivores (Gillespie and Chapman 2001; Snaith and Chapman 2007). Several researchers have found no correlation between group size and day range in primarily folivorous primates (Isbell 1991; Yeager and Kirkpatrick 1998). Others have reported ranging behavior consistent with the ecological constraints model in folivores and have emphasized the patchy distribution of the types of leaves exploited by most folivores (Gillespie and Chapman 2001; Snaith and Chapman 2007; Teichroeb and Sicotte 2009).
The applicability of the ecological constraints model to seed eating primates is poorly studied. Like leaves, seeds from unripe fruit have a higher temporal and spatial availability than ripe fruit and are, therefore, less patchy in space and time (Norconk and Veres 2011). Therefore, primate seed predators might be expected to have small home and day ranges. Yet the most granivorous primates, Chiropotes and Cacajao, have among the largest home ranges for their body size in the primate order (Norconk 2011). While seeds are generally considered a high-quality resource, many seeds contain high levels of indigestible fiber and secondary compounds such as tannins, phenolics, and alkaloids (Essau 1977; Janzen 1978; Kinzey 1992; Norconk et al. 2009). Thus, consumption of a highly seed-based diet may necessitate behavioral adaptations, including specialized foraging and ranging behavior, which enable primate seed predators to avoid toxins and secondary compounds (Norconk et al. 1998).
Bearded sakis (genus Chiropotes) are platyrrhines with a body mass of 2–3 kg that are characterized by their morphological adaptations for extracting and masticating mechanically protected seeds (Kinzey 1992; Smith and Jungers 1997). Consistent with this specialized morphology, bearded sakis are reported to spend >50 % of feeding time consuming seeds in almost all studies (Boyle et al. 2012; Gregory 2011; Kinzey and Norconk 1993; Norconk 1996; Norconk 2011; Peetz 2001; Shaffer 2013a). Until recently, bearded sakis were thought to have home ranges of 200–300 ha and daily path lengths of 1–3 km. Many of these early estimates were confounded by the fact that studies either were conducted on island habitats or in forest fragments or were of relatively short duration (Norconk 1996; Peetz 2001; van Roosmalen et al. 1988, cf. Ayres 1989). Recent studies in continuous habitats suggest that bearded sakis may have much larger ranges than previously reported, with daily path lengths in excess of 3 km and home ranges approaching 1000 ha (Boyle et al. 2009a, b; Gregory 2011; Pinto 2008). This makes them (along with the closely related genus Cacajao) the most widely ranging neotropical primates (Di Fiore et al. 2011; Norconk 2011). Unfortunately, the lack of data from continuous forest populations of bearded sakis has made understanding the factors influencing such large ranges difficult.
Here I describe the ranging behavior of a group of bearded sakis (Chiropotes sagulatus) in a continuous forest in Guyana. My primary research question is: What are the correlates of long daily paths and large home ranges in bearded sakis? I formulated several specific predictions using the framework of the ecological constraints model. The ecological constraints model predicts that larger groups should travel further than smaller groups because there is less food available per individual. Similarly, groups should travel further when food patches are smaller or food is less abundant. Therefore, I first predicted that bearded sakis should increase daily path length when daily subgroup size is larger and should have larger home ranges during the months when subgroup size is larger. Second, they should increase daily path length and home range size when patch size and quality are lower. Third, they should increase the size of their ranges during the months when overall food availability is lower.
I also formulated predictions based on the alternative (although not mutually exclusive) explanation that bearded saki ranging behavior is determined primarily by the type of foods that they consume. Specifically, that seed eating and the need to obtain the proper nutrient balance from a seed based diet are important factors dictating bearded saki ranging. According to this hypothesis, seed eating necessitates that bearded sakis exploit many different plant species to limit the amount of indigestible fiber in their diet and to avoid the accumulation of any particular secondary compound. This hypothesis predicts that bearded sakis should exploit more plant species on days when seed consumption is higher. In addition, they should increase distance traveled when seed consumption is higher to satisfy their need to sample from many different plants. Similarly, they should visit more food patches when consuming seeds, regardless of the abundance of food items those patches contain. Finally, they should decrease distance traveled when ripe fruit consumption is higher and they are less threatened by overconsumption of indigestible fiber and secondary compounds.
Study Site and Focal Subjects
This research was conducted as part of a 15-mo study (November 2007–January 2009) of the behavioral ecology of northern bearded sakis (Chiropotes sagulatus) in Conservation International’s Upper Essequibo Conservation Concession (UECC) in southern Guyana (Shaffer 2012, 2013a, b). The UECC is an 81,000-ha protected area located between 3°40′–3°20′S and 58°25′–58°5′W on the Essequibo River. The base camp for this study was a site on the west bank of the Essequibo River at 3°31′40′′N 58°14′10′′W (elevation 110 m). The study site encompasses a variety of forest types characteristic of lowland rainforests in Guyana (ter Steege 1993). The forest throughout the reserve is undisturbed and is contiguous with undisturbed forest outside of the reserve for hundreds of kilometers. There are marked seasonal differences in rainfall, with two wet seasons and two dry seasons. The primary rainy season runs from May to mid-August, when much of the annual rainfall occurs. The long dry season, characterized by monthly rainfall of <200 mm, lasts from January to May. See Shaffer (2012) for a complete description of the study site.
The focal group consisted of ≥65 individuals. Group composition was highly fluid and mean daily foraging party size was 39 ± 10 (SD) individuals (N = 44). The focal group regularly fissioned into smaller foraging parties, and group size correlated with fruit availability (Shaffer 2013b). Because of the highly fluid social structure of bearded sakis, it is difficult to identify what constitutes a group, subgroup, and foraging party. I defined a bearded saki group as all individuals that foraged together and were able to maintain vocal contact. I also defined groups with <45 observed individuals as subgroups or foraging parties (as they represented a subset of all individuals). If the group fissioned, I collected data only on one of the subgroups. Further information on this definition of Chiropotes groups can be found in Shaffer (2013b).
I collected data from January 2008 to January 2009. I used instantaneous scan sampling at 5-min intervals for behavioral data collection, with the first observed activity of each visible group member recorded as an individual activity record (Altmann 1974). At the beginning of each 5-min scan, I recorded the location of the approximate center of the study group using a handheld GPS unit (Garmin etrex VistaHCX). On all occasions that I observed the focal group feeding, I recorded the type of food item and species consumed and marked the location of the feeding tree with GPS. I then mapped the distribution of all of these trees (N = 2243) in ArcMap 10.0 (ESRI). Plant part categories included mature fruit pulp, immature fruit pulp, mature seeds, immature seeds, flowers, insects, and other.
I collected 561 h of observational data (6727 scans) on the focal study group. I recorded most of these data (6256 scans) during 44 full-day follows, which consisted of following the focal group from sleeping tree to sleeping tree (06:00–18:00 h). I conducted full-day follows 4–6 d/mo, with the exception of July and August. To ensure that bearded sakis were followed from sleeping tree to sleeping tree, I conducted all-day follows only after the location of the focal group had been determined the night before. I then followed the study group for 2–3 d in a row.
Subgroup size was generally consistent throughout the course of a single day or consecutive days but inconsistent on a monthly basis. If fissioning occurred during the course of a full-day follow (N = 3), I followed only one of the subgroups, producing a single day range estimate. I chose the subgroup with the largest number of individuals as the focal subgroup. Thus, the day range included the distance traveled by the same set of individuals, first traveling as part of a larger group, then as a subset of this group. Similarly, if a subgroup was joined by another, i.e., fusion (N = 2), the day range included the distance traveled by the same individuals first as a subgroup, then as part of a larger group. If both a fission and fusion occurred over the course of the same full-day follow, I excluded that day from analysis (N = 1) because I could not distinguish distinct individuals.
I conducted all research with the approval of the Environmental Protection Agency of Guyana, Conservation International–Guyana, and the Institutional Animal Care and Use Committee of Washington University. All research adhered to the principles for the ethical treatment of non-human primates of the International Primatological Society.
Assessment of Resource Availability
To assess the species composition and productivity of the forest throughout the bearded saki home range, I established 31 5 × 50 m botanical transects. For each transect, I measured the diameter at breast height (DBH), basal trunk area, and height for all trees ≥10 cm DBH marked them for identification, and monitored them once a month for the presence of ripe fruit, immature fruit, or flowers (Shaffer 2013a). I rated abundance of plant parts on a relative scale of 0–4 with scores indicating the percentage of total crown volume that contained fruit (or flowers). A score of (0) indicated no fruit, (1) indicated <25 %, (2) indicated 25–49 %, (3) indicated 50–74 %, and (4) indicated 75–100 %. I calculated monthly forest productivity by multiplying basal trunk area by phenology score for each tree that had either fruit or flowers in a given month, i.e., tree quality score. I then added these scores and divided them by the total monitored basal area to obtain an average Resource Availability Index (RAI) for each plant part for each month (Shaffer 2013a).
Definition of Food Patches
Home Range and Daily Path Lengths
I obtained estimates of daily path lengths by summing the distances between sequential five minute scan locations of the approximate center of the bearded saki group during 44 full-day follows. Although this method allows for highly accurate estimates of the horizontal distance traveled, it does not incorporate any measure of vertical travel throughout the day. Therefore, daily path estimates are underestimates of the actual distance traveled. However, the study site was relatively flat so these estimates are likely to be accurate.
Owing to the variability in methods used to estimate animal home range size, and the controversy regarding which is the most accurate, I used three different methods for this study (Boyle et al. 2009a, b; Hemson et al. 2005; Pimley et al. 2005; Seaman and Powell 1996; Worton 1987). These were the minimum convex polygon (MCP), fixed kernel, and adaptive kernel methods. To assess monthly variation in home range use, I calculated fixed kernel home range estimates for each month individually. To account for variation in sampling effort across months, I standardized monthly home range with a ratio of the number of observation hours collected for each month divided by the highest number of monthly hours. I then multiplied this ratio by home range size for each month. I used the least squares cross-validation smoothing parameter for all kernel analyses. I conducted kernel analyses using Geospatial Modeling Environment v 0.7.2.0 (Spatial Ecology LLC).
To quantify the distribution of bearded saki feeding trees, I conducted a nearest-neighbor cluster analysis in ArcMap 10.0. This method produces a ratio of observed nearest-neighbor (NN) distances to expected NN distances for each point in the analysis. This ratio is used to determine whether the points show a clustered distribution (NN ratio < 1), random distribution (NN ratio of ca. 1), or scattered or uniform distribution (NN > 1). The function uses a T-distribution to test whether the ratio is significantly different from 1.
I used Spearman's rank correlation to test the relationship between daily path length, home range size, and the following variables: group size, patch quality, total fruit availability (RAI), NN ratio of feeding trees, percent of seed feeding time, percent of ripe fruit feeding time, and number of species eaten per day. In addition, I developed two multiple regression models, one to predict day range length using group size and patch quality and the other with diet added as an additional independent variable. I log transformed all variables for multiple regression analysis to meet the assumption of normality. All probability levels for statistical tests are two tailed and the α level was set a priori at 0.05. All GIS analysis was performed in ArcGIS 10.0 (ESRI). All statistical analysis was conducted in SPSS 20.0 (IBM).
Food Availability, Diet, and Distribution of Feeding Trees
Monthly home range size (kernel density method), day range, total fruit availability, diet, number of species consumed per day, and NN ratio of feeding trees for Chiropotes sagulatus in Guyana from January 2008 to December 2008
Day range (m)
Home range (ha)
% Fruit pulp
No. of species
NN Z score
NN P value
Bearded sakis were highly granivorous but showed considerable monthly variation in the percent of time they spent feeding on different resources (Table I). For all months, seeds made up the highest percentage of feeding time, ranging from 97 % of the diet in May to 41 % in November. Bearded sakis had a very diverse diet, feeding from more than 175 different plant species. They fed from a large number of individual trees (mean = 67, max = 103, min = 25) and a large number of different species (mean = 17, max = 26, min = 5) each day. The percent of time spent eating seeds significantly positively correlated with number of species eaten per day (rs = 0.43, P = 0.003, N = 44). Daily seed consumption was also significantly correlated with mean daily patch quality (rs = 0.59, P = 0.012, N = 17). Thus, on days when bearded sakis spent more of their time feeding on seeds they exploited more tree species despite the fact that, on average, each food patch contained more food items. The percent of time spent eating ripe fruit (rs = −0.295, P = 0.050, N = 44) and insects (rs = −0.39, P = 0.011, N = 44) significantly negatively correlated with number of different species eaten per day.
Bearded saki feeding trees showed a significant clustered distribution when analyzed as a composite for all months (NN ratio = 0.79, Z = −18.85, P < 0.001, N = 2243). However, feeding trees showed considerable variation in distribution by month (Table I). Feeding trees were significantly clustered during four months, randomly distributed during 5 mo, and significantly uniform during 1 mo (Table I).
Daily Path Length
Correlations between home range size (kernel density method) and daily path length and several ecological variables (group size, fruit availability, diet, food patch quality for 50 m2 patches, and number of species eaten) for Chiropotes sagulatus in Guyana from January 2008 to December 2008
% Ripe fruit
No. of species eaten per day
Daily (N = 44)
Monthly (N = 10)
Monthly (N = 10)
The distribution of feeding trees (NN ratio) did not significantly correlate with daily path length (Table II). In fact, the month with the shortest average daily path length (June) was the month when feeding trees were most clustered. Therefore, bearded sakis did not travel significantly further when food was more patchily distributed, fruit was less abundant, patch quality was lower, or group size was larger.
Daily path length did not significantly correlate with the percentage of feeding time dedicated to seed eating or insect eating. In addition, path length did not significantly correlate with the number of different species eaten per day (Table II). However, path length significantly negatively correlated with ripe fruit consumption. Further, the number of 50 m2 food patches visited per day significantly positively correlated with seed eating and significantly negatively correlated with ripe fruit eating (Table II). A multiple regression model showed that group size, patch quality, and ripe fruit consumption explained 39 % of the variation in day range (R2 = 0.39, P = 0.050, df = 16), but only the partial correlation coefficient for ripe fruit consumption was significant (r = −0.49, P = 0.045).
Home Range and Core Areas
Bearded sakis showed considerable monthly variation in home range use (Table I). The focal group used the smallest monthly home range sizes during the short dry season (September–December), when resource abundance was lowest. Home range size significantly positively correlated with group size, monthly patch quality, and percentage of time spent eating seeds (Table II). However, home range size did not significantly correlate with percentage of time spent eating ripe fruit, total fruit availability or the spatial distribution of feeding trees.
Bearded sakis in this study ranged over a larger area, both in terms of home range size and daily path lengths, than virtually any other neotropical primate and as large an area as any primate of comparable body size (Di Fiore et al. 2011; Swedell 2011). All other studies of the genus Chiropotes have shown them to have large home and day ranges (Ayres 1981, 1989; Boyle et al. 2009b; Gregory 2011; Norconk 1996; Norconk and Kinzey 1994; Peetz 2001; Pinto 2008) but both the daily path lengths and home range of this study group exceed previous estimates for the genus. The most likely explanation for this difference is that most previous studies of the genus have been conducted in fragmented or island habitats. In many cases, ranging was limited to the size of the island or fragment. Several researchers studying bearded sakis in these types of habitat report shorter daily path lengths, increased reuse of feeding trees, and more circular movement patterns (Boyle and Smith 2010; Boyle et al. 2009b; Peetz 2001; Santos 2002). The little continuous forest data that is available for bearded sakis shows that the results of this study are likely representative of the normal ranging behavior for this genus in continuous forest (Boyle 2008; Boyle et al. 2009b; Gregory 2011; Pinto 2008). For example, a group of 33 Chiropotes sagulatus individuals in continuous forest in Brazil used >550 ha (Boyle et al. 2009b). Similarly, a group of up to 44 individuals in Suriname ranged over ≥700 ha (Gregory 2011) and a Chiropotes albinasus group of 56 individuals in continuous forest in Brazil used an area of ca. 1000 ha (Pinto 2008).
If large home ranges and daily path lengths are characteristic of bearded sakis, this raises the question of why they need to range over such large areas. The ability of bearded sakis to exploit such a wide variety of plant parts and species might suggest that they could subsist in a much smaller supply area. One possibility is that these large ranges are necessitated by the large sizes of bearded saki groups, as predicted by the ecological constraints model. Bearded saki daily path lengths did not correlate with group size but monthly home range size was correlated with group size. Similarly, daily path length did not correlate with patch quality but monthly home range size did. Neither daily path length nor monthly home range size correlated with the distribution of feeding trees or food availability.
Gregory (2011) found a significant correlation between group size and half daily path length for bearded sakis during the long-dry season in a continuous forest in Suriname, although this relationship was not significant during other seasons. In addition, the home range size per individual in this study (15.38 ha) is similar to that reported in many studies of both Ateles and Lagothrix (Di Fiore et al. 2011; Symington 1988). Several researchers have noted a positive relationship between group biomass and supply area (Dunbar 1988; Isbell 1991; Janson and Goldsmith 1995; Milton and May 1976). Therefore, it is possible that larger group sizes partially explain the large ranges characteristic of the genus Chiropotes. Nevertheless, the data reported here suggest that the relationship between group size and day range in bearded sakis is weaker than has been reported for other frugivorous primates with highly fluid social organizations, i.e., Ateles and Pan (Chapman and Chapman 2000; Janson and Goldsmith 1995; Wrangham et al. 1993). The increased temporal and spatial availability of seeds compared to ripe fruit may reduce the intragroup feeding competition experienced by bearded sakis, allowing them to form larger groups, as has been hypothesized for several folivorous primates (Fashing 2001; Snaith and Chapman 2007).
It is also possible that large ranges are related to the highly fluid social organization of bearded sakis. Many of the primate species with the largest ranges exhibit frequent subgrouping, e.g., Ateles, Pan, and Papio (Di Fiore et al. 2011; Swedell 2011; Symington 1988; Wrangham et al. 1993). Although large ranges in these taxa are often explained in the context of widely scattered and patchily distributed fruit, differential use of the home range by different subgroups also appears to play a role. Unfortunately, because I could not distinguish among individuals, I was unable to assess the extent to which home range use varied among different subgroups. It is possible that different subgroups range over a much smaller area than the 1000 ha, although these subgroups would still have long daily paths.
The results of this study suggest that bearded saki ranging behavior may be more strongly related to the type of food they consume than group size or the spatial distribution of feeding trees, with heavy reliance on seed eating necessitating larger ranges. There are several possible explanations for this relationship and data on the nutritional composition of bearded saki foods will be necessary to better assess the influence of seed eating on ranging behavior. However, I propose that bearded sakis may consume seeds from many different species to avoid high levels of indigestible fiber and to buffer themselves against the accumulation of any particular seed species’ secondary compounds and/or toxins. According to this hypothesis, the need to obtain the proper mix of nutrients from a heavily seed-based diet necessitates the utilization of many different tree species and, thus, correspondingly large ranges.
This hypothesis is supported by the fact that bearded saki daily path length significantly negatively correlated with the percentage of ripe fruit in the diet. As ripe fruit generally contains few secondary compounds, bearded sakis do not have to travel as far to obtain a balanced diet when they consume a higher percentage of fruit. Although neither percentage of seeds in the diet or number of species consumed per day significantly correlated with daily path length, bearded sakis fed from more species and traveled shorter distances during the months when the seed portion of their diet was lowest. In addition, they visited more patches when consuming a larger percentage of seeds, despite these patches containing more food items. These results support the predictions of the alternative hypothesis for bearded saki ranging behavior and suggest that seed eating, and the corresponding need to consume a variety of different seed species, necessitate large range sizes. Nutrient mixing may also explain why bearded sakis do not feed for very long from any single tree or any specific food patch even when there are very high concentrations of seeds (Shaffer 2012).
Bearded sakis are characterized by dental specializations for accessing mechanically protected seeds but the extent to which these dental adaptations are accompanied by a specialized gut morphology and/or physiology adapted to digesting seeds is unclear (Norconk et al. 2009). Seeds often contain high levels of toxins, difficult-to-digest secondary compounds, and indigestible fiber as protective mechanisms to avoid mastication (Janzen 1978). There have been very few studies on the gut morphology or digestive physiology of any of the Pitheciines. The limited data available suggest that bearded sakis have a relatively generalized gut morphology and have gut passage times similar to those of primates that primarily eat ripe fruit pulp, e.g. Ateles (Milton 1984; Norconk et al. 2009). They appear to lack highly specialized adaptations, such as the sacculated stomachs of Old World colobines, the complex small intestine of Propithecus, or the enlarged cecum of Alouatta (Davies 1991; Milton 1984; Norconk et al. 2009; Oates 1994).
Bearded sakis may partially buffer themselves against indigestible compounds by concentrating on immature seeds, the defenses of which are less well developed. In all studies of the genus Chiropotes, including this one, they show a strong preference for immature seeds (Norconk et al. 2011; Shaffer 2013a). In addition, the mechanically protected seeds for which bearded sakis demonstrate masticatory adaptations likely contain fewer secondary compounds than seeds lacking mechanical protection. Plants are limited in the energy they can devote to protecting their seeds and generally employ a strategy of either mechanical or chemical protection but rarely both (Bell 1984; Essau 1977; Janzen 1978; Kinzey 1992). Nevertheless, the limited data available on the nutritional composition of seeds eaten by Pitheciines suggests that they do contain higher percentages of indigestible fiber and/or secondary compounds than fleshy mature fruit (Ayres 1986; Norconk 1996; Norconk and Veres 2011; Norconk et al. 2009). Therefore, bearded sakis may have to visit many different feeding trees to avoid ingesting too much of any one type of secondary compound or toxin. By visiting the trees of many different species during the course of a single day (up to 26 in this study), they may be able to reduce their fiber and secondary compound load and obtain a sufficient nutrient mix.
Studies of other primates and other animals that consume a high percentage of seeds also support this hypothesis. Most seed predators have evolved morphological (e.g., sacculated forestomachs), physiological (e.g., reticulo-rumen fermentation), and/or behavioral (e.g., concentration on immature seeds, diversity of diet and regulation of intake of individual species, storage to promote decomposition, and geophagy) adaptations for avoiding/neutralizing seed secondary compounds (Bodmer 1991; Dearing et al. 2005; Janzen 1971). Although some colobine seed predators concentrate feeding on a few seeds, primates with less specialized gut morphologies appear to avoid consuming too many of any one seed species (Davies 1991; Lambert 2011; Norconk et al. 2009; Sussman et al. 2011; Swedell 2011). In addition, closely related and equally granivorous uakaris (genus Cacajao) have very diverse diets and exploit several different species over the course of a single day (Ayres 1986; Bowler and Bodmer 2009). Like bearded sakis, uakaris also exhibit very large home ranges (500–1200+ ha) and long daily path lengths (3–6+ km) (Ayres 1986; Boubli 1997; Bowler 2007). For example, Bowler and Bodmer (2009) reported that Cacajao calvus ucayalii fed from ≥164 different species, and possibly >200, while using a home rang exceeding 1200 ha.
The other member of the Pitheciinae, Pithecia, has much smaller home ranges (10–100 ha) than Cacajao and Chiropotes, despite consuming a similarly high amount of seeds (Norconk 2011). The most obvious difference between Pithecia and bearded sakis/uakaris is the much smaller group size of Pithecia (2–12 individuals) (Norconk 2011). This suggests that group size is a major determinant of range size variation among the Pitheciines. However, variability in digestive adaptations across the Pitheciinae may also explain differences in ranging behavior. Dietary and digestive studies suggest that Pithecia may be less limited than the other Pitheciines in their ability to exploit chemically protected seeds (Milton 1984; Norconk et al. 2002, 2009). The gut transit time of Pithecia is much longer than that of Chiropotes or Cacajao and may be related to digestive fermentation of fibrous seeds and/or leaves. Whereas bearded sakis and uakaris have transit times of ca. 5 h, among the shortest of any platyrrhine, Pithecia pithecia and P. monachus have transit times in excess of 15 h (Milton 1984; Norconk et al. 2002). In fact, the only platyrrhine genus with a longer transit time is the highly folivorous Alouatta. This dramatic difference suggests that Pithecia is well adapted to exploiting resources that are high in secondary compounds, like leaves, and, possibly, chemically protected seeds. Consistent with these adaptations, Norconk et al. (2009) found that Pithecia consume a diet high in lipids but also high in dietary fiber. The estimated energy value of their diet was much lower than that of Cacajao and Chiropotes. Similarly, Norconk et al. (2002) reported that the diet of Pithecia pithecia contained acid-detergent fiber levels twice as high and non detergent fiber levels 60 % higher than the diet of Chiropotes chiropotes, despite the similar percentage of seeds in both diets. An ability to exploit a wider range of chemically protected or fibrous seeds may increase the spatial availability of food items for Pithecia and allow them to utilize a smaller supply area.
The nutrient mixing hypothesis is not mutually exclusive with the ecological constraints model. Ranging behavior is likely determined by the complex interactions among a variety of ecological and social factors (Chapman and Chapman 2000; Clutton-Brock and Harvey 1977; Norconk and Kinzey 1994). Although group size and overall abundance of resources do not appear to be the primary determinates of bearded saki range size, they may strongly affect nutrient intake. As has also been hypothesized for folivores, a better predictor of range size and group size in bearded sakis may be the availability of digestible, high protein and low fiber resources, rather than simply abundance of food items (Chapman et al. 2003; Milton 1998). Anecdotal evidence suggests bearded sakis do not deplete patches extensively, as feeding trees often contained an abundance of food items when they left them, even when they fed in large groups (Shaffer 2012). However, larger groups may deplete the total nutrient value of patches more than smaller groups. Therefore, larger group sizes may necessitate longer daily paths and larger home ranges when high protein-to-fiber or lipid-to-fiber resources are less abundant. More research on patch depletion and the nutrient content of food resources is necessary to test the nutrient mixing hypothesis better and further assess the applicability of the ecological constraints model to bearded sakis and other seed predators.
I thank the Environmental Protection Agency of Guyana and Conservation International–Guyana for granting permission for me to conduct this research. I am grateful for the logistic support provided by CI–Guyana, in particular that of Eustace Alexander. I thank my local field assistants, especially Defraites Bowen, Henry James, and Hendricks Simon. I also thank Robert Sussman, Joanna Setchell, and two anonymous reviewers for their helpful comments on this manuscript. This research was approved by the Institutional Animal Care and Use Committee of Washington University in St. Louis. Financial support was provided by the National Science Foundation (No. 0648678), Lambda Alpha, and Conservation International–Guyana.