Feeding Rates and Daily Path Range of the Colombian Woolly Monkeys as Evidence for Between- and...

Reviewed Article

Folia Primatol 2000;71:399–408

Feeding Rates and Daily Path Range of theColombian Woolly Monkeys as Evidencefor Between- and Within-GroupCompetition

Pablo R. Stevensona Maria Clara Castellanosb

Departments of aAnthropology and bEcology and Evolution,State University of New York at Stony Brook, N.Y., USA

Received: June 7, 1999Accepted after revision: June 14, 2000

Maria Clara CastellanosDepartment of Ecology and EvolutionState University of New York at Stony BrookStony Brook, NY 11794-5245 (USA), Tel. +1 631 632 8603Fax +1 631 689 7626, E-Mail [email protected]

ABCFax + 41 61 306 12 34E-Mail [email protected]

© 2001 S. Karger AG, Basel0015–5713/00/0716–0399$17.50/0

Accessible online at:www.karger.com/journals/fpr

Key WordsDay range W Group size W Feeding rates W Intergroup competition W Intragroupcompetition W Lagothrix lagothricha W Woolly monkeys

AbstractData on fruit feeding rates and daily path length were compared for four

groups of woolly monkeys in Tinigua National Park, Colombia. Indirect evidencewas found for feeding competition both within and between groups. Feeding rateswere similar across groups of different sizes, but daily path lengths were longer insmall and large groups when compared to medium-sized groups. The results sug-gest that the optimal group size in this study site is close to 20 individuals. Althoughthe sample size was small and it was difficult to assess the influence of home rangequality in some of the comparisons, this is one of the few studies providing empiri-cal evidence supporting the importance of intergroup competition affecting groupsize in primates.

Copyright © 2001 S. Karger AG, Basel

Introduction

A number of factors related to individual food acquisition and predation risk havebeen suggested as affecting group size in primates [1]. Some models of the evolution ofprimate social systems, for example, have emphasized the role of within-group (or intra-group) competition for resources as the main factor setting an upper limit to group size

400 Folia Primatol 2000;71:399–408 Stevenson/Castellanos

[2–5]. Some individuals in large groups have limited access to food and suffer reducedresource acquisition, especially if the group feeds on small and discrete patches, and alimited number of individuals are able to use a particular patch at the same time,depending on the degree of group cohesion [6]. These models predict that individuals inlarger groups will, on average, have a lower food intake, or that they will need to travellonger distances to compensate for the reduced foraging efficiency due to competition.Although there are very few empirical studies comparing individual energy intake inprimate groups of different sizes, some authors have found no significant differencesbetween members of large and small social units [7–9]. The most common explanationfor this is that large groups travel farther to obtain an adequate food intake. A positivecorrelation has been found between group size and both home and daily path ranges [10,11], and a comparative analysis of 16 frugivorous primate species showed that relativeranging cost (an index based on path length) is a good predictor of group size [12]. Thispattern of increased travel distance for large groups has also been documented in otherrecent studies [13–15], but see Henzi et al. [16].

Sociological models, on the other hand, have proposed enhanced food intake forindividuals in large groups, which may be related to higher and more constant discove-ry rates [2, 4], and to the defense of preferred resources [17] or the capacity to holdbetter-quality territories [6]. Wedge-capped capuchin females (Cebus olivaceus) inlarge groups showed higher fecundity (which is usually correlated with feeding success)than females of the subordinate, small groups [18]. In terms of discovery rates, how-ever, studies on brown capuchins, Cebus apella, and tamarins, Saguinus spp., showedthat larger groups did not visit more fruit trees per distance traveled [19, 20]. Finally,in terms of resource defensibility there are many anecdotal examples of aggressiveinteractions between groups at fruit trees, but very few studies have quantified theeffects of the displacement of small groups. In one study on brown capuchins it wasfound that within-group competition was more than 10 times as intense as competitionbetween groups (intergroup competition) [21], and for this species the costs of within-group competition, in terms of food intake, outweigh the potential feeding benefits ofbeing in a large group [22].

Given the lack of data supporting feeding advantages for large groups (but seeRobinson [18] and Miller [23]), it has been commonly argued that protection againstpredators may have been the most important selective force promoting group-living inprimates [1, 24–27]. Infanticide avoidance has also been suggested as another majorfactor influencing primate social systems [28].

The woolly monkey (Lagothrix lagothricha) is one of the largest Neotropical pri-mates [29], and its relative large size appears to be associated with a low predation rate.In our study site at Tinigua National Park, Colombia, we have not witnessed any preda-tion or infanticide attempts during more than 2,000 h of focal observations and ad libi-tum observations over more than 10 years [P. Stevenson and A. Nishimura, unpubl.data]. Although it is well known that it is very difficult to quantify predation rates andevaluate predation risk [30, 31], these observations suggest that foraging strategies, rath-er than predation risk, may play a major role in the grouping patterns of this species.The aim of this study is to compare individual feeding rates and daily path distances forwoolly monkey groups of different sizes, in order to assess the importance of within- andbetween-group competition over a range of group sizes.

Widely distributed in central and western Amazonia, woolly monkeys prefer tofeed on ripe fruits, but they also consume young leaves, seeds and animal prey [32–37].

CR-1

Group Size in Woolly Monkeys Folia Primatol 2000;71:399–408 401

Table 1. Composition of four woolly monkey groups observed for this study at Tinigua National Park,Colombia

Group Year Adultmales

Adultfemales

Subadultmales

Subadultfemales

Juveniles Infants Total

1988 4 5 0 2 2 1 14CR-2 1988 8 10 0 4 5 2 B33CR-12 1990 4 5–7 1–2 1–0 2–6 4–2 17–21CR-12 1996 6–7 10–11 0–1 1–2 5–8 5–3 27–32

Group sizes for woolly monkeys are very variable, ranging between 10 and 49 individu-als [38]. There is a correlation between feeding party size and patch size (as diameter atbreast height of feeding trees) for this species [38, 39]. However, the explanatory powerof this relationship is very low, probably due to the fact that group members sometimesspread over large areas to forage [38] and visit different fruit trees simultaneously. Theingestion of insects may also reduce the cost of feeding in discrete patches [35]. There isalso evidence suggesting within-group competition, with the occurrence of aggression infeeding trees being associated with an index of the density of individuals feeding togeth-er [39].

If within-group competition is the major factor affecting individual food acquisi-tion for woolly monkeys, we would predict: (1) a decrease in individual feeding rates asgroup size increases or (2) similar individual feeding rates but with an increase in dailypath length with increasing group size. If between-group competition is important atleast in some range of group sizes, we predict: (1) that the smaller groups would showlower individual feeding rates or (2) smaller groups would travel longer distances com-pared to medium-size groups, to compensate for a decrease in foraging efficiency.

Methods

Study Site and Study GroupsThis study was carried out in a tropical rain forest on the eastern border of Tinigua National

Park, west of Sierra de La Macarena (2º40) N, 74º10) W, 350 m elevation) on the right bank of the RÈoDuda, Departamento del Meta, Colombia. The region has a highly seasonal rainfall pattern, with a dryperiod from December to March and more than 100 mm of precipitation per month during the rest ofthe year. The average annual rainfall is 2,622 mm, and the mean temperature is 25 °C [40]. The topog-raphy of the area is hilly, with rolling hills dissected by streams and flat flooded areas along theriver. There are three main vegetation types in the area [35]: (1) mature forest, located on hill ridges;(2) open-degraded forest, in areas suffering erosion, and (3) flooded forest, along the river plains.

Seven sympatric primate species (Lagothrix lagothricha, Ateles belzebuth, Alouatta seniculus,Cebus apella, Callicebus cupreus, Saimiri sciureus and Aotus brumbackii ) are common in the area.Primates are the most abundant mammals in terms of density and biomass [41], and the woolly mon-keys are the most abundant of the primates (30 individuals/km2).

Four woolly monkey groups of different sizes were observed (table 1). A small group (CR1-88)composed of 14 individuals was studied between February and July 1988 [34]. A larger second group(CR2-88) was also observed during this period, but the number of individuals was not determined. Asingle count of this group the year before the study indicated a group size of about 33 animals [42].


Fig. 1. Fruit feeding rates (as the percentage of instantaneous samples feeding on fruits) of Colombianwoolly monkeys at different hours of the day for the period between February and July 1997. Feedingwas quantified using instantaneous sampling every 10 min on focal animals.

Two years later (1990), a smaller group (called CR12-90) was found, which included at least onemember (an adult male) of CR2-88. The group was composed of 17 individuals [43]. This suggestedthat either the large group (CR2-88) had split into smaller groups or the original count had includedmembers of two different social units. CR2-88 was included in this analysis, in spite of the lack of anaccurate estimate of group size, in order to control for potential differences in ecological factorsbetween years, and because it was larger than the smallest group (CR1-88). The group CR12-90 wasfollowed from March 1990 to April 1991, when its size varied from 17 to 21 [35]. The same group wasstudied 6 years later, from August 1996 to July 1997 (hereafter CR12-96), when it had increased to27–32 individuals.

Field ProceduresFeeding time was measured as the number of minutes that focal individuals were feeding on

fruits, the preferred food of woolly monkeys [35]. A total of 376 h of observations were completedduring the first period (1988), 672 h during the second period (1990–1991) and 720 h during the thirdperiod (1996–1997). Only continuous focal animal samples of at least 4 h were included in the analysis(mean = 392 min, range 240–660). We considered only samples obtained during the period of highestfruit production (February–July) to allow for comparison with the first study period, which lasted onlyfor 6 months. This period of the year appears to be the most important in terms of energy intake forwoolly monkeys. They store fat at this time, which is then used during the time of fruit scarcity [29].

Feeding rates were calculated as a percentage of the total number of minutes feeding on fruits persampling time. Feeding rates vary during the day, being lowest around midday [35], and for this reasonthey were corrected according to sampling hour to avoid bias (fig. 1). Estimates of feeding rates includ-ing only midday hours were, therefore, increased; those from only early morning and late afternoonwere slightly reduced, and those including midday hours, early morning or late afternoon remainedrelatively unchanged. Data from individuals of different age/sex classes were pooled for analysesbetween groups, because no differences were found in feeding rates between different age/sex classes(Kruskal-Wallis H = 2.35, p = 0.50).

For the second and third study periods, daily path distances were estimated from 12-hour con-tinuous follows (including consecutive days), that were drawn on a map of the study site after each dayof observation. During the first study period it was not possible to follow the monkeys from dawn todusk, and samples of at least 8 h were used to estimate day ranges, assuming a constant travel rate


Fig. 2. Average feeding rate (as the percentage of time spent feeding on fruits) of each of the fourgroups of woolly monkeys studied that vary in number of individuals. The bars represent the standarddeviation.

during the day. This procedure may underestimate total day ranges because movement during theperiod of fruit abundance tends to be higher in the early morning and late afternoon [35], exactly whenobservations were deficient during the first year.

We used Kruskal-Wallis single-classification ANOVA [44] to test for differences in feeding ratesand daily path distances between the groups. Mann-Whitney tests were used for comparisons betweenpairs of groups. The Bonferroni method was used when comparing two groups for a posteriori statisti-cal analysis [44].

Results

The smallest group tended to show lower feeding rates, although there was no sta-tistically significant difference in feeding rates between groups of different sizes (H =1.04, p = 0.79; fig. 2). Daily path distances were significantly different between thegroups (H = 17.24, p ! 0.001), the smallest (CR1-88) and the largest (CR12-96) travelingfurther each day than the other groups. This difference indicates that medium-sizedgroups experienced the lowest foraging cost in terms of travel (fig. 3). A posteriori com-parisons, excluding the group of uncertain size, indicated differences between the smalland the medium-size groups (U = 397.5, p ! 0.01), and also between the medium andthe large group (U = 202.0, p ! 0.01). In contrast, no differences were detected betweenthe small and the large group in terms of travel distance (U = 125.0, p = 0.28).

Discussion

This study suggests an important role of both between- and within-group competi-tion associated with group size in the Tinigua woolly monkeys. The fact that smallgroups travel further than medium-sized groups is in agreement with the predictions of


Fig. 3. Average daily path length traveled by each of the four groups of woolly monkeys studied, whichvary in number of individuals. The bars represent the standard deviation.

intergroup competition, indicating that small groups have to move further each day toachieve individual feeding rates similar to those of larger groups. Similarly, individualsin large groups travel further each day than animals in the medium-sized group, aspredicted by within-group competition. Although our data set includes only four groupswithin the possible size range, the optimal group size in this community seems to beclose to that of the medium-sized group (n = 17–21). Interestingly, the average groupsize for this site is around 20 (n = 7) [35]. For woolly monkeys, female migration is animportant factor contributing to changes in group size (see fig. 2 in Nishimura [45]).Dispersal is possibly influenced by ecological and social factors [43, 46]. It is possiblethat group size may be regulated by permanent fission of large groups to reduce within-group competition, as documented for other primate species [47]. Our preliminaryunpublished observations have indicated that group members spread more in largergroups, as has been reported for muriquis, Brachyteles arachnoides [48].

Differences in daily path length may not depend exclusively on group size.Although the method used to estimate path length in the first study period was not veryrigorous (see Methods), the travel distance is believed to be underestimated. If cor-rected, the new estimates would accentuate the differences between small and mediumgroups, emphasizing the benefits of foraging in medium and large groups, in spite ofwithin-group competition. An alternative explanation for the results could be that fruitavailability differed between study periods. The difference, however, remains betweenthe small and the large groups studied at the same time (CR1-88 and CR2-88), whenfruit availability was similar for each. Fruit production was measured during the lasttwo study periods and it was found to be very similar [49]. The monthly fruiting pattern,according to the number of trees producing ripe fruit in phenological transects, washighly correlated between the two years (r2 = 0.60). Therefore, seasonality in fruit pro-duction seems to be very regular between years at this site and is reflected in the general-ized diet of the woolly monkeys. For example, 84% of the fruit species consumed during


the first study period in 1988 [34], were also consumed in 1996–1997. Likewise, all butone of the top 20 fruit species consumed during the second study period (1990–1991)[35] were also those consumed in 1996–1997. The similarity in diets in the differentyears indicates that feeding times may reflect energy intake for all the study groups,because basically the same kind of food was available for all study periods.

In summary, the evidence suggests that both within- and between-group competi-tions are playing a role in the social system of the woolly monkeys, where large and smallgroups have to travel more than medium-sized groups to acquire similar amounts offood for each individual. In particular, between-group competition is a factor that doesnot have much empirical support in the primate literature [1], but in this study thesmallest group had the lowest feeding rates and long daily paths, results that areexpected if between-group competition is taking place. Two questions arise from thispossibility: (1) how could group size affect individual foraging success in woolly mon-keys? and (2) is there anything in particular in the social system of woolly monkeys thatresults in between-group competition playing an important role? With respect to thefirst question, in theory, intergroup competition may be important when groups are ableto defend access to particular trees [50] or have preferential access to a good-qualityterritory [1]. There is circumstantial evidence for woolly monkeys supporting both argu-ments. For instance, aggressive interactions within groups have been reported for thewoolly monkeys at Tinigua and a dominance hierarchy between groups was proposedbased on intergroup agonistic interactions [35], suggesting that large groups or sub-groups have preferential access to favorite food resources. This factor gains importanceif we consider also the substantial home range overlap among groups [35]. On the otherhand, the central portion of the home range for the small group was composed mainly ofopen degraded forest, according to the vegetation map of the area. This forest typeproduces less fruit than the mature forest (0.4 vs. 1.1 ton Wha–1

Wyear–1, respectively) [51],and the difference in home range quality may be a factor explaining the low feedingrates and long travel distances for the small group (CR1-88). This difference in homerange quality also agrees with the unexpected result that over the same time period alarge group (CR2-88) did not use a larger home range than the small one [52].

The fact that predation on woolly monkeys seems to be infrequent in our study siteallows the possibility that intergroup competition may be a major factor favoringincreases in group size for small groups. If between-group competition is important forother primate species as well, then the approach of calculating individual foraging effi-ciency, as the intercept of the regression relating daily path length to group size [53],should be used with caution. For instance, a solitary woolly monkey would have totravel longer distances in a scenario where larger groups are able to monopolize impor-tant fruit trees. This trend is not properly reflected if a linear relationship between groupsize and travel distance is assumed for all group sizes. In order to use relative rangingcost from daily path lengths it is necessary to check for nonlinear relationships (as inJanson and Goldsmith [12]), to discard the potential effect of between-group competi-tion. A second factor that may affect the use of the relative ranging cost approach is thefact that foraging strategies can change among primate species when food abundancevaries seasonally. Both woolly and spider monkeys in Tinigua, for instance, reduce theirenergy investment in foraging by reducing travel distance when fruits are scarce [51].This is probably associated with large body size that increases the capacity to use leavesas a secondary food source during fruit scarcity [35] and the ability to store fat whenfruits are abundant [29].


It is important to point out that some aspects of the social system of woolly mon-keys are very unusual in terms of ecological and social models that explain primatesocial systems [5, 28]. It is not clear why a male-bonded society that relies heavily onfruits does not present a fluid fusion-fission social system as in Ateles and Pan [54],which are also large and highly frugivorous. Similarities between spider and woollymonkeys societies are also to be expected because they are phylogenetically closely relat-ed [55]. A possible ecological explanation is that the high proportion of arthropods con-sumed by Lagothrix at Tinigua (as opposed to Ateles ) reduces within-group competitionfor fruits and allows for more cohesive social groups [35]. However, for large primatessuch as woolly monkeys, arthropod consumption probably represents an insignificantenergy source when compared to fruits [56]. This remains to be investigated. As men-tioned above, another important factor that may reduce within-group competition is anincrease in group dispersion as group size increases, reducing increases in day range inlarger groups. The reason why Lagothrix groups are more cohesive than those of Ateles,which has a true fission-fusion social system, is still unclear. Further research is neededon social aspects such as the effectiveness of long-distance calls in both genera [57, 58]and the potential effects of intergroup competition as a factor promoting group cohe-siveness.

Acknowledgments

We want to thank Los Andes University and La Unidad de Parques del Ministerio del MedioAmbiente, for letting us work at the Tinigua field station. We are especially grateful to Dr. CharlesJanson and an anonymous reviewer for their comments. This study was possible thanks to supportfrom the Japan-Colombia Cooperative Study of Primates, La Fundacion para la Promocion de laInvestigacion y la Tecnologıa (Banco de la Republica), the Fondo para la Proteccion del MedioAmbiente ‘José Celestino Mutis’ (FEN Colombia) and the Instituto Colombiano para el Desarrollo dela Ciencia y la Tecnologıa (COLCIENCIAS), through their fellowship program for doctoral studies.

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