Ranging Patterns in Relation to Seasonality and ... - Springer Link

C 2006) International Journal of Primatology, Vol. 27, No. 2, April 2006 ( DOI: 10.1007/s10764-006-9028-1

Ranging Patterns in Relation to Seasonality and Frugivory Among Cercopithecus campbelli, C. petaurista, and C. diana in the Ta¨ı Forest Paul J. Buzzard1,2 Received July 14, 2004; revision April 14, 2005; accepted April 26, 2005; Published Online May 23, 2006

My objective is to better understand the influences of seasonality and frugivory on ranging patterns for 3 guenon species of the Ta¨ı Forest: Cercopithecus campbelli, C. petaurista, and C. diana). Over a 17-mo period, I gathered data on the daily path length, home range size, and home range use for 2 habituated groups of each species. The ranging patterns of the 3 species were very similar to each other and across seasons. Further, the ranging patterns were not closely related to fruit abundance or consumption. Each species had a long-ranging strategy with long daily ranges relative to home range size and little repeated use of areas on successive days, which may relate to territory and boundary patrols, especially for Cercopithecus diana. I compare them with other guenon communities and demonstrate that the ranging patterns of the 3 species are more similar than the ranging patterns of sympatric guenons in other communities. I discuss the results in relation to the association of Cercopithecus campbelli and C. petaurista with C. diana for antipredator benefits. KEY WORDS: Cercopithecus; frugivory; guenons; ranging behavior; seasonality.

INTRODUCTION Studies of ranging behavior are useful for understanding the interface between aspects of animal behavior and ecology (Reynolds and Laundre, 1 Department

of Anthropology, New York Consortium in Evolutionary Primatology, Columbia University, New York, New York. 2 To whom correspondence should be addressed; Current address: Fauna Flora InternationalChina Programme, Beijing, People’s Republic of China; e-mail: [email protected]. 559 C 2006 Springer Science+Business Media, Inc. 0164-0291/06/0400-0559/0

560

Buzzard

1990). In primates, ranging behavior is closely related to the search for food, and my objective here is to demonstrate the effects of seasonal variation in food availability and frugivory on the daily path length and home range size of 3 forest guenons: Cercopithecus diana, C. campbelli, and C. petaurista. Seasonal variation in food availability and the degree of frugivory can have large influences on the ranging of primates and other animals (Oates, 1987). Primates and other animals respond to reduced food availability by either reducing daily travel ranges and feeding on lower quality food items (e.g., Trachypithecus pileatus, Stanford, 1991) or increasing daily travel ranges in search of high-quality food items (e.g., Cebus apella, Terborgh, 1983). Fruit consumption and the degree of frugivory have a large impact on primate ranging because of the shorter digestion time required for fruit than for leaves (Demment and Laca, 1991) and the higher spatial and seasonal variance in the availability of fruit compared to leaves (Janson and Chapman, 1999). Day range length and home range size increase with proportions of fruit in the diet in most cases across and within species (Janson and Goldsmith, 1995). Studies of Cercopithecus species show that they are primarily frugivorous (Chapman et al., 2002). In the Ta¨ı Forest, however, foliage made up the majority of feeding records for Cercopithecus petaurista in 12 out of 13 mo though fruit was also important (Buzzard, unpublished). At Ta¨ı, guenon diets diverged during fruit scarcity (minor dry season, Buzzard, unpublished). Cercopithecus campbelli ate more prey at this time while C. petaurista ate more fruit and flowers and C. diana ate more foliage. The variation in diet across both species and time intraspecifically allows me to evaluate the influence of seasonality and frugivory by 1) documenting interspecific differences in ranging patterns (daily path length and home range size) and relating the differences to the degree of frugivory, and 2) relating changes in ranging patterns to changes in the availability of fruit. I analyzed only variation in ranging patterns in relation to fruit availability because fruit abundance varied much more during the year than leaf or invertebrate abundance did (Buzzard, unpublished) and because day range length and home range size increase with proportions of fruit in the diet in most cases (Janson and Goldsmith, 1995). Because all species showed dietary divergence during fruit scarcity, I predicted that all species would also show variation in ranging patterns then. Further, because Cercopithecus petaurista consumed less fruit than the other species did, I predicted that both daily path length and home ranges would be smaller in Cercopithecus petaurista than in the other species.

Ranging Patterns, Seasonality, and Frugivory Among Cercopithecus spp.

561

METHODS Study Site ˆ d’Ivoire (between I carried out the study in the Ta¨ı National Park, Cote 5◦ 10 N to 6◦ 20 N and 4◦ 20 W to 6◦ 50 W). Ta¨ı National Park is one of the last remaining substantial blocks of West African forest and consists of ca. 3300 km2 of forest. The forest is classified as a tropical evergreen seasonal lowland forest (Stoorvogel, 1993) with average annual rainfall of 1942 mm (Buzzard, 2004; Korstjens, 2001). The forest is characterized by 2 wet seasons (September–November, March–May) and 2 dry seasons (December– February, June–August). Additional information on the study site is in Buzzard (2004), Korstjens (2001), and McGraw (1996).

Study Individuals and Observation Schedule Two habituated groups each of Cercopithecus campbelli, C. petaurist, and C. diana monkeys ranging from 7 to 26 individuals served as subjects. The groups contained 1 adult male for most of the study, 4–13 adult females, and associated immatures (Buzzard, 2004). I followed subjects from September 2000 through October 2001 except for January 2001. An assistant followed groups from September 2000 through January 2002. Separately, my assistant and I followed each group of Cercopithecus campbelli and C. petaurista for 3 9–11-h d/mo on average and each group of C. diana 2 d/mo on average. We followed or attempted to follow individual groups for 2 or 3 consecutive d; we attempted the follows again after 2 wk. On most observation days we followed groups from first contact (usually 0700– 0730 h) until the subjects stopped moving presumably in sleeping areas (ca. 1800 h). Occasionally, we followed the groups for half-days from 0700– 0730 h until 1230 h or 1200 h until ca. 1800 h. In seasonal analyses of home range size and home range use I used only 1 group per species so that seasonal intergroup comparisons involved similar sample sizes.

Home Range Area/Daily Travel During full-day and half-day group follows, I carried out 15-min scan samples on the individuals every 30 min (Buzzard, 2004). After each scan, an assistant or I estimated the center of mass of the group (Cords, 1987) in 0.25-ha quadrants aided by a system of trails with coordinates painted on

562

Buzzard

trees. I determined annual home range sizes via grid cell counts of 0.25-ha quadrants and minimum convex polygons (Olupot et al., 1994). Grid cell counts did not result in large lacunae related to topographic features. I used only grid cell counts to estimate seasonal home ranges. I analyzed home range sizes during 3-mo seasons that coincided with rainy and dry seasons and with fruit availability (Buzzard, unpublished): September–November 2000 (rainy season, fruit abundant); December 2000–February 2001 (dry, fruit abundant); March–May 2001 (minor rainy season, fruit intermediate); June–August 2001 (minor dry season, fruit scarce); September–November 2001 (rainy, fruit abundant). To calculate total home range sizes and overall average daily path lengths, I included data from 2 additional mo, December 2001 and January 2002. To facilitate comparisons with other studies I used only full-day follows (≥ 9 h) to analyze daily travel distances. I determined daily travel length by measuring the straight-line distance between successive centers of mass. I divided travel lengths by observation hours to determine travel rate (m/h). Because most of the subjects used the same ranges and spent the majority of time together in mixed-species associations (Buzzard, 2004), I sometimes was able to gather ranging data from >1 study group at a time. For example, during the day follows for Campbelli-1, Petaurista-1, or Diana2, I was often able to collect location records for any of the other groups because they often associated with each other during the 15-min scans. I used the additional location data only for home range area estimates; I did not use them to measure daily path lengths because they would have been biased toward time spent in association.

Home Range Use To determine the repeated use of areas used over time, I performed 2 analyses. First, I compared the frequency of quadrant use between species in each season. I considered 2 levels of intensity in quadrat use: 1) 0.25-ha quadrants that contained the centers of group mass in 1 and 14 nonterritorial populations had D < 1. Six nonterritorial populations also had indices >1, however, so an index >1 suggests that territoriality is economically feasible but not a necessary occurrence. Lowen and Dunbar (1994) tried to improve on the index of defensibility (D) by taking into account the length of territorial boundary, the detection distance of neighboring groups, and the number of foraging parties. Lowen and Dunbar (1994) developed the fractional monitoring rate, M, which more accurately classifies existing primate populations as territorial (or not) than Mitani and Rodman’s index of defensibility (D). Lowen and Dunbar (1994) identified a criterion M = 0.08, and found that 12 of 16 populations with M ≥ 0.08 were territorial and that 14 of 15 populations with M < 0.08 were nonterritorial. The fractional monitoring rate, M, is calculated as follows: M = N(sv/d2 ) where N = the number of foraging parties (n = 1 for the study species), s = the mean distance at which intruders can be detected, v = mean day journey length (km), d = the diameter of the circle equivalent in area to the home range.

564

Buzzard

Lowen and Dunbar (1994) used mean detection distances (s) of 0.05 km. I used the same value (0.05 km) for Cercopithecus campbelli, but 0.1 km for C. petaurista and C. diana. Greater detection distances seemed warranted for Cercopithecus petaurista and C. diana because their average group spreads exceed those of C. campbelli (Buzzard, 2004) and because they (especially C. diana) are more vocal than C. campbelli are (pers. obs.; ¨ Zuberbuhler, 2002), allowing acoustic as well as visual detection of neighboring groups. I also noted when groups visited home range boundaries at least once during a day or half-day follow. Home range borders were the outer edges of the annual home range areas; borders were not related to distinct topographical or habitat discontinuities. For Cercopithecus campbelli, I recorded boundary visits when the center of a group mass was ≤ 50 m of the border, and for C. petaurista and C. diana, I recorded boundary visits when the center of a group mass was ≤ 100 m of the border. Differences in average group spreads (Buzzard, 2004) accounted for the different criteria used to identify boundary visits.

RESULTS Home Range Area Petaurista-1 had the largest home ranges at the end of the 12-mo and entire study period (Table I). The larger size of Petaurista-1’s home range resulted from excursions of the group into the home range of Petaurista-2 and Diana-1 during the dry season (December 2000–February 2001). The home range of Campbelli-2 was the smallest; we encountered it less than any of the others because it seldom associated with another study group. We thus probably underestimated the home range of Cambelli-2. Home ranges asymptote for each species ca. 20 days (Fig. 1). All groups used between 62 and 99% of the total area in each season based on grid cell analysis (Table I). Mean 3-mo home range areas of Campbelli-1, Petaurista-1, and Diana-2 are 48 ha ± 6.9 (72% of total area), 49 ha ± 5.4 (67% of total area), and 49.7 ha ± 5.6 (85% of total area), respectively. The largest seasonal ranges were 1.3–1.4 times greater than the smallest seasonal ranges (Table I). None of the species had the largest seasonal range during the season of low fruit availability (short dry season, July–August). All 3 species had their largest seasonal range during the short wet season, March–April, a season of intermediate fruit availability


565

Table I. Seasonal and total home range sizes in hectares

Group Campbelli1 Campbelli2 Petaurista1 Petaurista2 Diana-1 Diana-2

Wet season (1) Sept–Nov 2000

Dry season Dec–Feb 2001

Minor wet Mar–May 2001

Minor dry Jun–Aug 2001

Wet season (2) Sept–Nov 2001

Entire study GCA, MCP

42.5 (33); 40.8 ± 1 —(8)

44.3 (31); 43.1 ± 1 —(10)

58.8 (37); 54.5 ± 1.1 —(10)

51.3 (27); 49.8 ± 1 —(8)

43.5 (24); 43.1 ± 0.5 —(12)

67, 80.5

46.5 (37); 44 ± 2 —(13)

45.5 (30); 43.5 ± 1 —(16)

58.8 (37); 55.5 ± 0.6 —(14)

47 (21); —

73.5, 97.75

—(12)

47.5 (22); 47.3 ± 0.5 —(9)

—(10) 48.3 (34); 45.8 ± 1.5

—(12) 42 (29); 41 ± 0.6

—(11) 57.8 (41); 54.3 ± 1.5

—(7) 50.5 (28); 49 ± 1

—(6) 49.8 (27); 48.3 ± 0.9

59.25, 77 58.5, 74.75

52, 64.25

64, 81

Note. I estimated seasonal home ranges via grid cell analysis (GCA) I combined annual home ranges over the study period and estimated them via GCA and minimum convex polygon (MCP). The number of days used for seasonal location records are in parentheses, and the seasonal values in bold are the largest. Standardized seasonal values based on 21-d samples follow the seasonal location records. To obtain standardized samples, I randomly removed days with location records from samples until 21 d remained to determine home range size. I repeated the process 100 times to determine the average standardized home range size and SD.

(Table I). After I standardized the season samples so that all samples included 21 d/season, standardized and raw samples were similar (Table I).

Daily Travel The daily path length for each group varied widely between days, and the mean daily path lengths did not differ significantly between groups of the same species (Buzzard, 2004). Interspecific differences were also small and not significant (Table II, Kruskal-Wallis H = 5.3 p > 0.05). Seasonal variation in daily path lengths for all 3 species is not significant either (Table II, Kruskal-Wallis H = 3.8, 6.3, 8.7 for Cercopithecus campbelli, C. petaurista, and C. diana, respectively, all p > 0.05).

Home Range Use I examined spatial patterns of range occupancy by comparing levels of quadrant use throughout the home ranges and showed that all groups did not concentrate their activities in particular quadrants; no quadrants

566

Buzzard

Fig. 1. Asymptote relationship between the number of day follows and the total number of ha by grid cell analysis for groups of C. campbelli (long dashes), C. petaurista (short dashes), and C. diana (line). Number of ha represents an average value of the 2 groups of each species.

were centers of the group’s mass in > 4% of scans, while subjects used most quadrants in < 1% of the scans (Table III). Groups had the largest areas of concentrated use in the wet seasons (Table III). The location of 1–4% areas of quadrant use varied across the seasons, but in general all groups had well-used quadrants spaced widely throughout their ranges in each season including boundary areas, and many such quadrants were noncontiguous (Buzzard, 2004). To evaluate the redundancy of ranging, I calculated C values from records of quadrant use I made on sequential days. Based on breaks she observed in her data, Kaplin (2001) viewed C ≤ 0.77 low corresponding to concentrated or redundant ranging patterns, and C ≥ 0.90 as high corresponding to long-distance ranging patterns with little redundancy of quadrant use from day to day. The low cutoff fit well with my data although I considered 0.88 as my high cutoff. I used 30, 37, and 4 pairs of sequential days for calculating C in Cercopithecus campbelli, petaurista, and diana, respectively. Groups of Cercopithecus campbelli, C. petaurista, and C. diana had C ≤ 0.77 in 10, 16, and 0% of paired sequential days, respectively. Groups of Cercopithecus campbelli had C ≥ 0.88 in 90% of the days while groups of C. petaurista had C ≥ 0.88


567

Table II. Average daily travel distances ± SD for subjects over the entire study period and over 3 mo seasons Cercopithecus campbelli Wet season (1) Dry season (1) Minor wet Minor dry Wet season (2) Study period

1261 ± 228 m (n = 15;737–1905 m) 1192 ± 303 m (n = 18;660–1586 m) 1105 ± 226 m (n = 22;711–1452 m) 993 ± 291 m (n = 12;607–1560 m) 1175 ± 362 m (n = 13;526–1685 m) 1155 ± 295 m (n = 85)

C. petaurist

C. diana

1046 ± 237 m (n = 16;703–1312 m) 1055 ± 322 m (n = 20;495–1754 m) 1140 ± 220 m (n = 15;842–1702 m) 951 ± 303 m (n = 11;654–1405 m) 940 ± 201 m (n = 10;673–1412 m) 1051 ± 263 m) (n = 77)

1234 ± 351 m (n = 8;602–1501 m) 965 ± 368 m (n = 8;532–1720 m) 1025 ± 394 m (n = 12;448–1997 m) 1008 ± 220 m (n = 11;597–1401 m) 1164 ± 374 m (n = 13;718–2082 m) 1152 ± 362 m (n = 58)

Note. Wet season (1) = Sept–Nov 2000; dry season (1) = Dec 2000–Feb 2001; minor wet season = Mar–May 2001; minor dry season = Jan–Aug 2001; wet season (2) = Sept–Nov 2001.

in only 76% of the pairs of days. The findings suggest that Cercopithecus petaurista had a more concentrated ranging pattern, while C. campbelli had a more long-distance ranging pattern. Despite the small sample, the 4 C for Cercopithecus diana > 0.86 also suggest a long-distance strategy, and to further demonstrate the adequacy of the sample for Cercopithecus diana, I randomly chose 4 C 100 times from the larger samples of C. campbelli and C. petaurista. The 4 values from Cercopithecus campbelli and C. petaurista averaged 0.94 ± 0.05 and 0.91 ± 0.06, respectively, well above the high cutoff of 0.88.

Table III. Group Campbelli-1 Petaurista-1 Diana-2

Seasonal areas (ha) that the centers of group mass in 1–4% of scans (see methods) Wet season (1) Dry season (1) 8 ha 8.75 10

5.75 5.75 7.75

Minor wet

Minor dry

Wet season (2)

4 4 3.25

4.25 5.25 8.25

7 6.5 6.5

Note. Largest values in bold. Wet season (1) = Sep–Nov 2000; dry season (1) = Dec 2000– Feb 2001; Minor wet season = Mar–May 2001; minor dry season = Jun–Aug 2001; wet season (2) = Sep–Nov 2001.

568

Buzzard

Ranging and Territoriality According to the defensibility index (D, Mitani and Rodman, 1979) and fractional monitoring rate (M, Lowen and Dunbar, 1994), it was economical for all study groups to be territorial. The defensibility index D for each group was > 0.98 (the suggested cutoff for territoriality, Lowen and Dunbar, 1994) when calculated with the home range sizes obtained from grid cell analysis. When larger home range sizes from minimum convex polygon were used in the calculations, all groups still had D values > 0.98 except for Petaurista-1 (D = 0.97). The suggested cutoff for territoriality with the fractional monitoring rate M is 0.08 (Lowen and Dunbar, 1994). M in groups of Cercopithecus petaurista and C. diana were > 0.08 when estimated home ranges via both grid cell analysis and minimum convex polygon methods. M values in Cercopithecus campbelli were just below 0.08 (0.071, 0.076 for Campbelli-1 and Campbelli-2, respectively). All groups made territorial border visits between 69% and 88% of full-day and half-day follows.

DISCUSSION Ranging variables were very similar among all the subjects and seasonality and degree of frugivory had little influence on ranging patterns. In principle, primates can use several strategies to cope with seasonal food scarcity (Oates, 1987). They may increase daily path length and monthly home range size (e.g., Saimiri oerstedi, S. sciurius, Terborgh, 1983). Alternatively, they can adopt a low-energy strategy by feeding on less preferred but more abundant resources and moving less (e.g., Cebus apella, Zhang, 1995). Many primates, however, maintain relatively consistent ranging patterns throughout the year (e.g., Lophocebus albigena, Olupot et al., 1997). The consistency in ranging patterns is accomplished in most cases by a farranging pattern that facilitates resource monitoring (Olupot et al., 1997), diet switching or both, (Indri indri, Pollock, 1977). Seasonal variations in fruit abundance did not seem to have a great effect on Ta¨ı guenon ranging including daily path lengths, seasonal home ranges, and patterns of habitat use. Most likely, a combination of diet switching and resource monitoring allowed the subjects to maintain consistent ranging patterns. Guenons are generally able to switch diets readily (Chapman et al., 2002; Lambert, 2002), and the diets changed for each study species during low fruit availability (Buzzard, unpublished). All 3 study species also used far-ranging strategies that are compatible with resource monitoring. Long daily path lengths in relation to home range size would


569

allow the guenons to collect and update information on the location and phenology of ephemeral feeding sites (Garber, 1993). Further, the guenons did not concentrate on any particular area within their territory for an extended time, and rarely reused quadrants on successive days as reflected by high C. The far-ranging strategy of Ta¨ı guenons may relate not only to resource monitoring but also to territorial defense, and the explanations are not mutually exclusive. Wrangham (1980) noted the evolutionary importance of territorial defense and proposed that territorial defense of resources is the mechanism behind female-bonded groups. The high defensibility indices suggest that territoriality is economically feasible for Ta¨ı guenons. Cercopithecus campbelli had fractional monitoring rates (M) slightly lower than 0.08. M is directly related to the detection distance, however, so that increasing the detection distance from 0.05 km to 0.1 km would result in M > 0.08 for Cercopithecus campbelli. The frequency of ¨ loud calls at Ta¨ı by all the study species (Zuberbuhler, 2002; pers. obs.) suggests that the mean detection distance of neighboring groups may be as high as 0.2–0.4 km at most times. Aggressive intergroup encounters and territoriality are typical of forest guenons and researchers have described them for many populations including the study species (Buzzard and Eckardt, in Press; Cords, 2002; Hill, 1994). The effect of territoriality on ranging behavior has not often been addressed in forest guenons. As an exception, Kaplin (2001) suggested thloat intergroup relationships may influence the long-distance ranging in another guenon, l’Hoest’s monkey (Cercopithecus lhoesti); groups of C. lhoesti may travel far not only to meet daily foraging requirements but also to limit other groups’ access to resources. Intense intergroup encounters that involved chasing lasted >1 h and occurred relatively often. Several field studies of other primates demonstrated relationships between intergroup interactions and ranging (Fashing, 2001). Further researchers have described territorial patrols in other primate species, including gibbons (Hylobates klossi, Whitten, 1982) and chimpanzees (Pan troglodytes, Goodall, 1986). Long-distance ranging in Cercopithecus diana especially may have developed in response to territorial maintenance. During daily follows for all species, subjects visited a territorial border on the majority of days. Cercopithecus diana occur at the highest population density (individuals/km2 ) and had the most intergroup encounters most of which were aggressive (Buzzard and Eckardt, in press). Researchers have found a negative relationship between the proportion of foliage in the diet and both daily path length and home range size in primates generally (Janson and Goldsmith, 1995). Although

570

Buzzard

Cercopithecus petaurista had more days with short daily path lengths and a more concentrated ranging pattern than those of C. campbelli or C. diana, the average daily path lengths of C. petaurista were comparably large and the majority of C-values for C. petaurista suggest a long-distance ranging strategy. In addition, Cercopithecus petaurista had the largest annual home ranges, contrary to expectations. Kaplin (2001) found a similar contradiction of theoretical expectations, with the more folivorous Cercopithecus lhoesti having larger home ranges than less folivorous but sympatric C. mitis in every month. Further Cercopithecus lhoesti has a less concentrated ranging strategy than that of C. mitis.

Community Comparisons Similarity among sympatric species in daily path length and home range size was greater in the study species at Ta¨ı than in other guenon communities (Table IV). At Nyungwe, the differences between the ranging patterns of Cercopithecus lhoesti and C. mitis are attributed to high terrestrial herb use by C. lhoesti because the terrestrial herbs may not be densely or predictably distributed (Malenky and Stiles, 1990). At Kibale and Kakamega, differences between the ranging patterns of Cercopithecus mitis and C. ascanius are best explained by different population densities. It is likely that the higher density groups of Cercopithecus ascanius at Kibale and higher density groups of C. mitis at Kakamega need to be compressed into smaller home ranges. An inverse relationship between density and home range size seems to characterize populations of Cercopithecus mitis over larger geographical areas (Butynski, 1990) as well as black-and-white colobus (Dunbar, 1987). Gautier-Hion et al. (1983) argued that the similarity in the ranging patterns of Cercopithecus pogonias and C. nictitans in Gabon is a result of high association rates that are best explained as antipredator strategies. In addition, both olive colobus (Procolobus verus) and red colobus (Procolobus badius) have similar ranging patterns with Cercopithecus diana at Ta¨ı, which some have attributed to high association rates resulting from the antipreda¨ 1997; Korstjens, 2001). tor strategies of the colobines (Bshary and Noe, High association rates of Cercopithecus campbelli and C. petaurista with C. diana are also most likely a result of antipredator strategies (Buzzard, 2004), which create similar rariging patterns in the species. The similarities in ranging patterns among Ta¨ı guenons compared to other guenon communities may result from a combination of higher predator risk at Ta¨ı and the role of Cercopithecus diana as a nuclear species that facilitates polyspecific ¨ association (Buzzard, 2004; Honer et al., 1997).


571

Table IV. Ranging parameters for various guenon communities (Cercopithecus spp.)

Study site Kakamega, Kenya

Species (groups)

C. mitis (n = 1) C. ascanius (n = 1) Kibale, C mitis Uganda (n = 1) C ascanius (n = 4) Nyungwe, C. mitis Rawanda (n = 1) C. lhoesti (n = 1) Makokou, C. nictitans Gabon (n = 1) C. pogonias (n = 1) C. cephus (n = 2) Ta¨ı, R.C.I C. campbelli (n = 2) C. petaurista (n = 2) C. diana (n = 2)

Home range area (ha)

Mean daily path lenth (m)

Density groups per km2

Density individuals per km2

Reference

38

1136

5.17

171

1

60

1543

5

115

2

51 ± 15

1216

1.7–2.9

32–56

3

24

1447

4–4.5

120–158

4

88

1307

—

—

5

117

2092

—

—

168

1903

—

—

168

1903

—

—

86

1638

—

—

59.5

1155

2.3

21

68.8

1051

2.4

27

58.9

1125

2.3

52

6

7

References: 1, Cords (1987); 2, Fashing and Cords (2000); 3, Struhsaker (1978); 4, Butynski (1990); 5, Kaplin (2001); 6, Gautier-Hion et al. (1983); 7, this study.

Researchers have described Cercopithecus diana as a nuclear species ¨ to which other satellite species are attracted (sensu Honer et al., 1997; Moynihan, 1962). In mixed-species flocks of birds, nuclear species promote the formation and maintenance of mixed flocks through the conspicuous nature of their calls, coloration, or behavior (Botero, 2002; Moynihan, 1962). Cercopithecus diana are much louder, more vividly colored, and more vocal than the other guenons. Further, researchers have demonstrated antipredator benefits for red and olive colobus associating with the highly vigilant ¨ 1997). Cercopithecus diana (Bshary and Noe,

ACKNOWLEDGMENTS I thank the minister of the environment and the forest, the minister of scientific research, the director of the center for ecological research ˆ d’Ivoire for permission to work at Ta¨ı at Ta¨ı and the PACPNT of Cote

572

Buzzard

National Park. I also thank the directors of the Ta¨ı Monkey Project (TMP), ¨ Klaus Zuberbuhler, ¨ Ronald Noe, Scott McGraw, and Johannes Refisch for the opportunity to study with the TMP. I thank my advisor, Marina Cords, members of my dissertation committee (John Oates, Don Melnick, Fred Koontz, and Cliff Jolly), and 2 anonymous reviewers for their comments and input toward the development of this article. The field work was possible through a dissertation improvement grant from Leakey foundation. REFERENCES Botero, P. (2002). Is the white-flanked antwren (Formicariidae: Myrmotherula axillaris) a nuclear species in mixed flocks? A field experiment. J. Field Ornithol. 73: 74–81. ¨ R. (1997). Red colobus and Diana monkeys provide mutual protection Bshary, R., and Noe, against predators. Anim. Behav. 54: 1461–1474. Butynski, T. (1990). Comparative ecology of blue monkeys (Cercopithecus mitis) in high and low density subpopulations. Ecol. Monogr. 60: 1–26. Buzzard, P. J. (2004). Interspecific Competition Among Cercopithecus campbelli, C. petaurista, ˆ d’Ivoire. Ph.D. dissertation, Columbia University, New and C. diana at Ta¨ı Forest, Cote York. ¨ R., Buzzard, P. J., and Eckardt, W. (in press). Social systems of the Ta¨ı guenons. In Noe, ¨ McGraw, W. S., and Zuberbuhler, K. (eds.) Monkeys of the Ta¨ı Forest: A African Primate Community, Cambridge University Press, Cambridge. Chapman, C. A., Chapman, L. J., Cords, M., Gathua, M., Gautier-Hion, A., Lambert, J. E., Rode, K., Tutin, C. E. G., and White, L. J. T. (2002). Variation in the diets of Cercopithecus species: Intraspecific differences within forests, among forests, and across species. In Glenn, M. E., and Cords, M. (eds.), The Guenons: Diversity and Adaptation in African Monkeys, Kluwer Academic, New York, pp. 325–350. Cords, M. (1987). Mixed species associations of Cercopithecus monkeys in the Kakamega Forest. Univ. Ca. Publ. Zoo. 117: 1–109. Cords, M. (2002). Friendship among adult blue monkeys (Cercopithecus mitis). Behaviour 139: 291–314. Demment, M. W., and Laca, E. A. (1991). Herbivory: The dilemma of foraging in a spatially heterogenous food environment. In Palo, R. T., and Robbins, C. T. (eds.), Plant Defenses Against Mammalian Herbivory, CRC Press, Boca Raton, FL, pp. 29–44. Dunbar, R. I. M. (1987). Habitat quality, population dynamics, and group composition in colobus monkeys (Colobus guereza). Int. J. Primatol. 8: 299–329. Fashing, P. J. (2001). Activity and ranging patterns of guereza. Int. J. Primatol. 22: 549–578. Fashing, P. J., and Cords, M. (2000). Diurnal primate densities and biomass in the Kakamega Forest: An evaluation of census methods and a comparison with other forests. Am. J. Primatol. 50: 139–152. Garber, P. A. (1993). Seasonal patterns of diet and ranging in two species of tamarin monkeys: Stability vs. variability. Int. J. Primatol. 14: 145–166. Gautier-Hion, A., Quris, R., and Gautier, J.-P. (1983). Monospecific vs. polyspecific life: A comparative sudy of foraging and antipredatory tactics in a community of Cercopithecus monkeys. Behav. Ecol. Sociobiol. 12: 325–335. Goodall, J. (1986). The Chimpanzees of Gombe: Patterns of Behavior, Harvard University Press, Cambridge. Hill, C. M. (1994). The role of female diana monkeys (Cercopithecus diana) in territorial defense. Anim. Behav. 47: 425–431. ¨ ¨ R. (1997). Dyadic associations of red colobus (Colobus Honer, O. P., Leymann, L., and Noe, badius) and the Diana monkey (Cercopithecus diana) groups in the Ta¨ı National Park, Ivory Coast. Primates 38(3): 281–291.


573

Janson, C. H., and Chapman, C. A. (1999). Resources and primate community structure. In Fleagle, J. G., Janson, C. H., and Reed, K. E. (eds.), Primate Communities, Cambridge University Press, Cambridge, pp. 237–261. Janson, C. H., and Goldsmith, M. L. (1995). Predicting group size in primates: Foraging costs and predation risks. Behav. Ecol. Sociobiol 6: 326–336. Kaplin, B. A. (2001). Ranging behavior of two species of guenons (Cercopithecus lhoesti and C. mitis doggetti) in the Nyungwe Forest Reserve, Rwanda. Int. J. Primatol. 22: 521–548. Korstjens, A. H. (2001). The Mob, the Secret Sorority, and the Phantoms: An Analysis of the Socio-ecological Strategies of the Three Colobines of Ta¨ı, Unpublished Ph.D. thesis Utrecht University, The Netherlands. Lambert, J. (2002). Resource switching and species coexistence in guenons: A community analysis of dietary flexibility. In Glenn, M. E., and Cords, M. (eds.), The Guenons: Diversity and Adaptation in African Monkeys, Kluwer Academic, New York, pp. 309–324. Lowen, C., and Dunbar, R. I. M. (1994). Territory size and defendability in primates. Behav. Ecol. Sociobiol. 35: 347–354. Malenky, R. K., and Stiles, E. W. (1990). Distribution of terrestrial herbaceous vegetation and its consumption by Pan paniscus in the Lomako Forest, Zaire. Am. J. Primatol. 23: 153– 169. McGraw, W. S. (1996). Positional Behavior and Habitat Use of Six Monkeys in the Ta¨ı Forest, Cote ˆ d’Ivoire, Unpublished Ph.D. dissertation, State University of New York, Stony Brook. Mitani, J. C., and Rodman, P. (1979). Territoriality: The relation of ranging patterns and home range size to defensability, with an analysis of territoriality among primate species. Behav. Ecol. Sociobiol. 5: 241–151. Moynihan, M. (1962). The organisation and probable evolution of some mixed species flocks of neotropical birds. Smithson. Misc. Coll. 143: 1–140. Oates, J. F. (1987). Food distribution and foraging behavior. In Smuts, B., Cheney, D., Seyfarth, R., Wrangham, R., and Struhsaker, T. (eds.), Primate Societies, University of Chicago Press, Chicago, pp. 197–209. Olupot, W., Chapman, C. A., Waser, P. M., and Isabirye-Basuta, G. (1997). Mangabey (Cercocebs albigena) ranging patterns in relation to fruit availability and the risk of parasite infection in Kibale National Park, Uganda. Am. J. Primatol. 43: 65–78. Pollock, J. I. (1977). The ecology and sociology of feeding in Indri indri. In Clutton-Brock, T. H. (ed.), Primate Ecology: Studies of Feeding and Ranging Behaviour in Lemurs, Monkeys and Apes, Academic Press, London, pp. 38–71. Reynolds, T. D., and Laundre, J. (1990). Time intervals for estimating pronghorn and coyote home ranges and daily movements. J. Wildl. Manage. 54: 316–322. Stanford, C. (1991). The capped langur in Bangladesh: Behavioral ecology and reproductive tactics. Contrib. Primatol. 26: 1–179. Stoorvogel, J. J. (1993). Gross Inputs and Outputs of Nutrients in Disturbed Forest, Ta¨ı Area Cote ˆ d’Ivoire, Veenman Drukkers, Wageningen, The Netherlands. Struhsaker, T. T. (1978). Food habits of five monkey species in the Kibale Forest, Uganda. In Chivers, D., and Herbert, J. (eds.), Recent Advances in Primatology. Vol. I: Behavior, Academic Press, London, pp. 225–248. Terborgh, J. (1983). Five New World Primates, Princeton University Press, Princeton. Whitten, A. J. (1982). Home range use by Kloss’ gibbon (Hylobates klossi) on Siberut island, Indonesia. Anim. Behav. 30: 182–198. Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour 75: 262–300. Zhang, S.-Y. (1995). Activity and ranging patterns in relation to fruit utilization by brown capuchins (Cebus apella) in French Guiana. Int. J. Primatol. 16: 489–507. ¨ Zuberbuhler, K. (2002). Effects of natural selection on the evolution of guenon loud calls. In Glenn, M. E., and Cords, M. (eds.), The Guenons: Diversity and Adaptation in African Monkeys, Kluwer Academic, New York, pp. 289–306.