habitat partitioning among primates in maraca island, roraima, northern brazilian amazonia

International Journal of Primatology, Vol. 18, No. 2, 1997

Habitat Partitioning Among Primates in MaracaIsland, Roraima, Northern Brazilian Amazonia

Antonio Rossano Mendes Pontes1'2Received July 26, 1996; accepted November 14, 1996

I studied a primate community on a tropical rainforest island, in the northern-most area of the Brazilian Amazonia. While walking through six distincthabitats along a 12-km trail, running toward the center of the island—a remoteundisturbed area—I collected data on the use of the different forest types andforest strata by the primate community and the formation of either mixedgroups or species assemblages. Five species are present: Cebus olivaceus, C.apella, Saimiri sciureus, Ateles belzubuth, and Alouatta seniculus. Theyseemed to be habitat generalists, using most habitat types. The five speciesused the higher strata more significantly, probably because Maraca does notpresent well-defined forest floors, which could be a result of being located inthe transition between the great areas of savannah and the Amazonianseasonally dry forests. The five species all formed some polyspecificassociations, which involved sharing the available food resource. Mixed groupswere significantly more frequent and therefore possibly more important toSaimiri, which was not the case in relation to the other four species.Assemblages, defined as the presence in the same clumped resource, withoutcoordinated activity, of < 3 primate species, were recorded primarily in fruitingfig trees. I suggest that assemblages are impelled by food constraints, forcingcofeeding in large seasonal resources, highlighting the ecological importanceof figs to these primates. Linear regression models show that the number of

Wildlife Research Group, Department of Anatomy, The University of Cambridge, DowningStreet, Cambridge CB2 3DY, UK. e-mail: [email protected]

2Universidade Federal de Pernambuco (UFPE), Centro de Ciencias Biol6gicas (CCB),Departamento de Zoologia, Rua Prof. Moraes Rego 1235, Cidade Universitairia, Recife, PE,Brazil 50670-420.

131

0164-0291/97/0400-0131$12.50/0 © 1997 Plenum Publishing Corporation

132 Mendes Pontes

feeding bouts in each habitat type is positively related to the number of fruitingtrees exploited, but the density of these fruit trees, diversity of plant species,tree height, and total basal area of each habitat type have no relationship tofeeding.

KEY WORDS: primates; habitat partitioning; mixed groups; feeding assemblages; Amazonia.

INTRODUCTION

Primate communities in Amazonia, and in the Neotropics as a whole,tend to be very diverse, with some sites comprising < 14 sympatric primatespecies (Peres, 1991, 1988; Johns, 1985; Terborgh, 1983). Some localitiescan be relatively impoverished, with no more than three primate species(Peres, 1989). I recorded only five species. This apparent impoverishmentcan be caused by biogeographical, environmental, and other factors whichshould be considered when conservation priorities are assessed (Eisenberg,1980). As specific forest types are analyzed in greater detail, microhabitatdifferences become far more evident.

Habitat use can vary greatly, with the animals shifting their habitatexploitation according to season, structure of the forest, e.g., canopy con-tinuity, or being generalists in one area and specialists in others,consequently affecting primate species richness among forest types. For in-stance, Saimiri sciureus prefers riverine forests, seasonally entering highforest, far from riverine forest, depending on resource availability (Peres,1993; Terborgh, 1983; Ayres, 1981).

Many authors have explained the sympatry of different primate speciesby showing that they either use restricted minor habitats, which are in-cluded in broader types, or have marked differences in diet, use of foreststrata, or locomotor behavior (Fleagle and Mittermeier, 1981; Mittermeierand Van Roosmalen, 1981), thus exploiting the habitat in distinct ways.However, differential use of forest strata by primates, like those on Maracais not so remarkable. They could be compensated by other features, suchas differences in density and biomass (Mendes Pontes, in preparation),which need consideration in conservation planning.

The formation of polyspecific primate troops, either mixed groups(Terborgh, 1983) or feeding assemblages (Klein and Klein, 1973; Richard,1970), seem to be very important in habitat use because of the benefitsfrom these interactions, mainly an increase in foraging efficiency andpredator avoidance (Terborgh, 1990, 1983; Norconk, 1990a, b). As on Ma-raca, polyspecific associations can comprise up to three primate species

Primate Habitat Partitioning in Northern Amazonia 133

Fig. 1. Location of the study area, MaracS Ecological Station, State of Roraima, Brazil.

(Podolsky, 1990), which occur mostly in periods of minimum food avail-ability.

I conducted the study at Maraca Ecological Station, in the northernpart of the State of Roraima. My goal was to understand better habitatpartitioning among the five species of Cebidae that occur in the east ofthe island, where there are several forest types. This region of the islandhad not been studied previously.

134 Mendes Pontes

METHOD

The five primate species on Maraca are: Cebus olivaceus, Cebus apella,Saimiri sciureus, Ateles belzebuth, and Alouatta seniculus. Except for the twoCebus species, I refer to them by their generic names.

Maraca Island (3°15' to 3°35'N and 61°22' to 61°58'W) comprises 1013km2 of tropical rain forest (Ministerio de Interior, 1977). It is a fluvial is-land, formed by the bifurcation of the Uraricoera River and lies betweenthe Maraca Channel to the south and Santa Rosa to the north (Fig. 1).The island is situated at the junction between the Amazonian forest (Hylea)and the great areas of dry savannah, which lie to the south and east of themainland. At least 95% of the island is forested (Milliken and Ratter,1990).

Total precipitation during 1992 was 1222.5 mm. Temperature wascharacteristically high throughout the year, with a pronounced drop in thewet season. The highest maximum temperature (43°C) occurred once inOctober and once in November, and the lowest minimum temperature(20°C) occurred three times in January. Maraca presented a marked sea-sonality, with a dry season from September to March and a wet seasonfrom April to August. The driest month was September with no rain, andin all dry months but November, <5 mm of rain fell. This is typically avery dry period. The wettest month was July, with 293 mm of rain (Fig.2).

We identified vegetation types along a 12-km trail, following Millikenand Ratter (1990), who had previously identified them. They used thepoint-centered quarter (PCQ) transect method (Mueller-Dombois and El-lenberg, 1974), and we strictly followed their results and assistance to definethe limits of the same forests. Although most of the island consists of twomain forest types—terra firme forest and mixed forest—we note the fourless extensive habitat types in nonflooded forest.

(1) Terra Firme Forest is normally about 25-35 m in height, with emer-gents reaching 40 m. During the dry season some trees, including someemergents, lose their leaves. Milliken and Ratter (1990), with the additionof some new records (Nunes, 1992), recorded 160 species (of 115 generaand 41 families) of emergent, canopy, and larger understory trees in thisforest type. Total basal area, 182.7 ha; total forest area surveyed in thisstudy, 45.5 ha.

(2) Mixed forest which has a similar floristic composition and height,but with a higher species diversity, compared to terra firme. There is oneparticular species that does not occur in terra firme forest: Peltogyne gracili-pes (Leg. Caesalp.), the Pau-Roxo, which is particularly important due toits high density in some places. For mixed forest, the recorded species in-


Fig. 2. Minimum, mean and maximum temperature (lines), and rainfall (bars) inMaraca during 1992.

elude 160 from terra firme forest, plus 51 additional species (totaling 201species, of 131 genera and 43 families). Total basal area, 109.7 ha; totalforest area surveyed in this study, 66 ha.

(3) Pau-roxo forest occurs in two small patches, surrounded by mixedforest. It is characterized by a predominance of pau-roxo tree, with veryfew other plant species. It is considered to be almost a monodominant for-est and is one of the highest forest types, reaching 40 m (Milliken andRatter, 1990). It is possible to identify pau-roxo forest from the air, duringthe dry season when leaves are lost. It is usually very clear and sunny be-cause of its frequent canopy discontinuity. For this forest type we recorded26 species (of 23 genera and 14 families), excluding understory species.Total basal area, 52.2 ha; total forest area surveyed in this study, 2 ha

(4) Buritizal forest occurs along the streams which flood during the wetseason. The most common plant species is Mauritia flexuosa (Palmae), andthe trees normally reach 23 m in height, forming a rather discontinuouscanopy. For this forest type we recorded 19 species (of 19 genera and 16

136 Mendes Pontes

families) (Milliken and Ratter, 1990), excluding herbs, shrubs, trilets, andvines. Total basal area, 9 ha; total forest area surveyed in this study, 2 ha.

(5) Carrasco forest contains very small trees (about 4-5 m high) of veryshrubby, multitrunked form, which makes it almost impossible to penetrate.Some of the characteristic plant species are Desmoncus polycanthos andBactris maraja (Palmae). We recorded 34 species (23 genera and 22 fami-lies). Total basal area, 0.23 ha; total forest area surveyed in this study, 1ha.

(6) Low forest with dwarf pau roxo is the most open forest habitat andis comparable to pau-roxo forest, but the trees seldomly exceed 15 m inheight. Lianas are abundant and the soil is sandy. We saw no large mam-mals in this forest type, in which we recorded a total of 52 plant species(from 44 genera and 27 families). Total basal area, 2.53 ha; total forestarea surveyed in this study, 3.5 ha.

We censused the primates via the line transect method (Burnham etal., 1980) over 12 km. We marked trees numerically at 50-m intervals andconducted observations for 6 months, three times a week, every week, fromJuly to December 1992, including 2 months of the wet season (July andAugust) and 4 months of the dry season (September to December). Wecollected data on a replicated cumulative basis (e.g., in both directionsalong the trail), whenever we encountered groups.

I walked from 0545 to 1745 hr, at a speed of 2 km/hr, with stops ofsome seconds to search for animals within a preestablished effective stripwidth of 50 m to each side of the trail in all forest types. On most days Iwalked the entire 12 km of trail in both directions, totaling 24 km/day. Iplotted the location of a group as the center of the sighted animals beforethey fled (Whitesides et al., 1988). I recorded the following data: species,group size, sighting distance, exact location upon the trail, forest type andassumed direction of travel. I also recorded the date, start and finish time,and total distance walked each day [Burnham et al., 1980; National Re-search Council (NRC), 1981; Brockelman and Ali, 1987; Buckland et al.,1993]. The sightings provided data both about habitat partitioning and onanimal abundance (Mendes Pontes, unpublished data).

I recorded vertical stratification of each sighting in order to define theuse of forest levels for each of the studied species. When individuals werefeeding, I noted the item and plant species. The food categories are leaves(young and old), ripe or unripe fruit, flower, seeds and roots. I also col-lected samples of food plant species, then preserved them in 5%formaldehyde or dehydrated them. They are at the Herbarium Universi-dade Federal de Roraima. I collected feces containing seeds and preservedthem in 5% formaldehyde. Animals are feeding when handling, holding,licking, or chewing food items of plant origin or capturing, handling, or


ingesting animal matter. Samples were identified by botanists at the KewGardens, London.

A maximum of 15 min was established for each group observation,but most encounters lasted 5-10 min. There are height classes, accordingto Van Roosmalen (1985): understory, 0-15 m; lower canopy, 15-20 m;middle canopy, 20-25 m, high canopy, 25-30 m; and emergent trees, >30m. These classes were very difficult to define since the forests on Maracaare not clearly stratified. The stratum used by the group is that in whichI first sighted them. For the rare and very low forest types I estimated anapproximate height.

According to Peres (1991), Cords (1990), Norconk (1990a, b), Gatesand Whitesides (1990), Terborgh (1990, 1983), Mittermeier and Roosmalen(1981) and Klien and Klein (1973), there are two types of polyspecific as-sociations: mixed groups, which are relatively permanent, lasting from a fewhours up to days and characterized by traveling together (normally involv-ing only Cebus and Saimiri), and assemblages, which are ephemerousassemblages of different species, mainly feeding in a single tree during pe-riods of scarcity or when alarmed or resting. They do not mix, and theyinvolve at least one of the large-bodied species (Ateles or Alouatta).

I analyzed the relationships among number of feeding bouts densityof fruiting trees, forest tree diversity, fruiting trees diversity, forest height,and total basal area of each forest via a simple regression model and loga-rithmic transformation of data to fit a linear model (Sokal and Rohlf, 1981)

RESULTS

Habitat Use

I recorded 376 sightings of primates in five habitat types representing1806.2 km of total trail distance surveyed: 782 km in terra firme forest and1024.2 km in mixed forest, both including the other smaller habitat types—pau-roxo forest, buritizal, and carrasco forest. I have no sightings in dwarfpau-roxo forest.

Fitting a curvilinear regression model with number of sightings bykilometers walked in each of the six forest types shows that more sightingsthan expected were in the smaller habitat types—buritizal, pau-roxo andcarrasco forest—suggesting that the primates seem to use them less fre-quently than the other main ones (y = -19.68 + 1.03 x km - 0.00094 km2)and that the higher number of sightings recorded in the larger forests wasnot an artifact of the observer walking longer distances.

138 Mendes Pontes

The smaller-bodied species—Saimiri, Cebus apella and C. olivaceus—occurred most in terra firme forest, while the large-bodied ones—Atelesand Alouatta—were more frequent in mixed forest. Buritizal forest wasused most often by C. olivaceus and Ateles, where there is no sighting ofAlouatta. Pau-roxo forest appeared to be visited only by Ateles and Alouatta,and Carrasco forest, a very low, shrubby vegetation was visited only bySaimiri. No primates occurred in dwarf pau-roxo forest. In addition, Atelesoccurred once, C. olivaceus, twice, and Saimiri six times in a lower type ofterra firme forest. Alouatta and Ateles occurred once and Saimiri six timesin a lower variation of mixed forest (12-15 m high) (Fig. 3).

Use of Forest Strata

Different forest layers appeared to be used similarly by all species,which may be due to the structure of the habitats. For this reason, I dividedthe forest layers into two categories: lower strata, including understory,

Fig. 3. Overall occurrence of the five primates in the different forest types inMaracS (n = 376), TFF, terra firme forest (n = 228); MF, mixed forest (n =114); PRF, pau roxo forest (n = 6); BF, buritizal forest (n = 24); CF, carrascoforest (n = 4); DPF, dwarf pau-roxo forest (n = 0).


lower canopy, and middle canopy, and higher strata, which includes uppercanopy and emergents. All five species used the higher strata of the forestsignificantly more often (x2 = 34.9, df = 4, p < 0.001).

Fig. 4. Use of the forest strata by (a) Saimiri stiureus (n = 52); (b) Cebus apella(n = 24); (c) C. olivaceus (n = 157); (d) Alouatta (n = 38); (e) Ateles (n = 105).

140 Mendes Pontes

No primates were on the ground, and none entered the shrub layer.All primates but Saimiri visited the emergent trees more frequently thanthe other strata, and Saimiri and C. apella were most often in the understory(Fig. 4). Ateles and Alouatta were more frequently in the higher strata, be-ing recorded almost exclusively at this level.

Polyspecific Associations

All five species formed polyspecific associations. They contained eithertwo species (Saimiri and C. olivaceus or Saimiri and C. apella) or threespecies (Saimiri, Cebus, and Ateles or Saimiri, Cebus, and Alouatta).

Mixed Groups

Mixed groups were in both main forest types—terra firme forest andmixed forest—and also in the buritizal forest. They consisted of eitherSaimiri and C. olivaceus or Saimiri and C. apella (Table I). They stayed inclose proximity and moved as one group. In 66% of the sightings they wereeither feeding or foraging, and sightings of mixed groups were more fre-quent during October and November, at the beginning of the dry season.They used upper canopy and emergent trees of all the forest types morefrequently. A maximum of 52 monkeys was in one mixed group (the onlyfull count), and the minimum was five. In one sighting of a mixed groupthere was only one C. olivaceus.

Saimiri was twice as often in single groups versus mixed groups, thoughthe difference is not significant: 60% of the time (n = 31), they were insingle troops, 34.6% of the time in mixed groups (n = 18), and 5.4% ofthe time in feeding assemblages. Therefore, Saimiri was equally likely tobe in mixed groups or alone (x2 = 1.9, df 1, NS). Cebus apella were alonein 75% of sightings (n = 18) and 25% in mixed groups 25% of the time(n = 6). This difference is significant (x2 = 6, df 1, p < 0.05). They werenot in feeding assemblages, and formed mixed groups only in terra firmeforest. C. olivaceus was single groups 90% (n = 141) of the time, in mixedgroups 8% (n = 12), and in feeding assemblages only 2% of the time(n = 4). This suggests that C. olivaceus is least dependent on polyspecificassociations: this difference is highly significant (x2 = 99.5, df l,p < 0.005).

Mixed groups of Saimiri and C. olivaceus were in terra firme forest,buritizal forest, and mixed forest. Sightings in buritizal forest are generallylow for them when alone (Fig. 3). Thus, it appears that this forest type,comprising mostly individuals of Mauritia flexuosa (Palmae), the 'Buriti,'

142 Mendes Pontes

which fruits throughout the year, is exploited more frequently by mixedgroups.

Assemblages

Ephemeral parties containing a number of species also occurred,mostly as feeding assemblages in emergent trees. There was no mixing ofthe groups, was recorded and they stayed together for short periods, leavingthe tree in clearly different directions. Even if they followed the same route,the groups were distinct. Individuals kept in their own species groups, andwhen, for instance, an Alouatta approached Cebus, the Cebus would imme-diately retreat. Also, Alouatta would frequently advance toward a preferredsite in the tree, and Cebus would retreat.

These parties comprised either two species (Ateles and Alouatta orAteles and C. olivaceus) or three species (Alouatta, Ateles, and C. olivaceus;Saimiri, C. olivaceus, and Ateles; and Saimiri, C. olivaceus, and Alouatta).On one occasion a subgroup of Ateles joined a feeding bout with anothersubgroup, which had been at the site for some time, while a group ofSaimiri. was also present. Trispecific primate assemblages such as thatamong Saimiri, Cebus, and Ateles occurred only in two large emergent figtrees, in the second driest month of the scarcity period.

Assemblages of two or three species occurred only during the dry sea-son. Most were in emergent trees of terra firme forest, where parties hada maximum of 29 monkeys and a minimum of 4. Most of the sightingswere of fruit feeding (Table II). The term feeding assemblage was used,but assemblages of animals engaged in other activities, such as alarmingand resting, also recurred. During one alarm sighting an adult femalehowler was attacked and killed by a raptor, which did not carry it away.Both groups including the group from which the victim was killed and onegroup of Ateles, together called loudly and could be heard from about 500m away.

There were considerably more sightings of single groups of Alouattaand Ateles than polyspecific assemblages. For Ateles, only 6% (n = 6) ofsightings were mixed (n = 4 in terra firme forest and n = 2 in mixedforest), while 94% of sightings (n = 99) were in single troops. This differ-ence is highly significant (x2 = 82.3, df l,p < 0.001). Sightings of Alouattaare 13% (« = 5) in assemblages in terra firme forest (n = 3), and mixedforest (n = 2), while 87% (« = 3) of sightings are of single troops. Thedifference is also significant (%2 = 20.6, df 1, p < 0.001). There are twoobservations of mixed groups of Saimiri and C. olivaceus cofeeding in afruiting tree, once with Ateles and once with Alouatta (Table II).

144 Mendes Ponies

Diet

Ateles exploited 25 species (of 24 genera and 16 families) of plants.They ate either ripe or unripe fruits and young leaves, mostly of Moraceae.Eight species of eight genera and six families were used by Alouatta, eitheras ripe fruits, flower buds, or young leaves. Nine species (of 9 genera and5 families) were foods for C. apella, and 11 species (of 11 genera and sevenfamilies) for C. olivaceus, all consisting of either ripe or unripe fruits. Capella used mostly Palmae, while no trend is notable for C. olivaceus.Saimiri used the resources from nine species (of eight genera and six fami-lies) (Table III). Fruits made up the majority of the feeding bouts on plantmatter for all the primate species. Alouatta was the most folivorous (44%of all the feeding bouts), Saimiri fed almost exclusively on fruits (98.8% ofall the feeding records), and Ateles exhibited the most diverse feeding pat-tern (Figure 5). Six tree species appeared to be the focus of feeding records:Tetragastris panamensis (Burseraceae), Couratari oblongifolia and Lecythiscorrugata (Lecytithidaceae), Bagassa guianensis and Ficus mathewsii(Moraceae), and Mauritia flexuosa (Palmae). These species, with the ex-ception of M. flexuosa, occur in the two main forest types; consequentlybeing available to all primates. Mauritia flexuosa (Palmae), which occursexclusively in the buritizals (strips of forest along streams), is very con-spicuous and widely available. I recorded no other plant or animal matterduring feeding, possibly due to nonsystematic observations of the groups.

Frequency of Feeding Bouts in the Forests

There is a significant positive relationship between the number of feed-ing bouts and the number of fruiting species exploited in each forest type.The density of these fruiting species, as individuals per hectare, however,is unrelated to feeding bouts (Figs. 6a and b). Indeed, most trees that pro-vide food for the primate community do not appear to fruit at the sametime. For instance, Ficus mathewsii in terra firme forest, which made upthe bulk of the feeding bouts during the dry season, had only two indi-viduals fruiting in a 50-ha sample.

Plant species diversity in the forests is positively related to the numberof feeding bouts (Fig. 6c). The forest type in which monkeys exploited agreater number of fruiting species is terra firme forest. This type has alower overall species diversity than mixed forest, but contains more speciesthat provide fruits, such as Moraceae, Sapotaceae, Palmae, and Rubiaceae.Burseraceae was also highly exploited by the primates, but Milliken andRatter (1990) recorded a slightly higher absolute density in mixed forest.

146 Mendes Ponies

148 Mendes Pontes

Fig. S. The use of the different plant resources by the primates from MaracSIsland.

There is no sighting in dwarf pau-roxo forest, which has more species thansome other types, but other characteristics, such as the low height of theforest and discontinuity of the canopy, made it unsuitable for the primates.

There is no clear relationship between the height or total basal areaof the forest types and the number of feeding bouts (Figs. 6d and e), pre-sumably because these two parameters overall are not directly related tothe potential food richness in the forests, unless only fruiting trees are con-sidered.

DISCUSSION

Forest Use

Eastern Maraca Island provided a diversity of forest types and foodspecies for the primates, though all appeared to use habitat selectively. Allprimates were most frequently in the terra firme forest, and none used thedwarf pau-roxo forest. They appeared to use the terra firme forest pre-


Fig. 6. The relationship between the percentage of feeding bouts in the different forest typesand (a) fruiting species which were exploited, (b) absolute density of the exploited trees, (c)plant species diversity of the forests, (d) approximate height of the forest, and (e) total basalarea of each forest.

150 Mendes Pontes

dominantly, but each species had different preferences for the other foresttypes. Saimiri and Cebus were not in the pau-roxo forest, Alouatta was notin the buritizal forest, and only Saimiri was in carrasco forest.

Peres (1993) showed a clear distinction in habitat partitioning amongprimates in the Urucu River Basin, Amazonia, related to flooded and high-ground forest, where stable microsympatry occurred only in small subsetsof the whole community. Species restricted to flooded forest are habitatspecialists Ateles, Alouatta and Saimiri—though Saimiri also enter high for-est in periods of food scarcity (Terborgh, 1983). I analyzed only nonfloodedforest in great detail and identified the forest types within the broader cate-gory. For instance, C. apella used all the forest types and, consequently, isa habitat generalist. Ayres (1981) showed that Saimiri used seven (possiblyeight) habitat types, of nine; Cebus six, Alouatta three habitats, and Atelesonly one.

Thus, I suggest that Saimiri, which occurs in a variety of habitats(Ayres, 1981) and was in four of six forest types, is better classified as ageneralist, though it remains selective to a certain extent. (Ateles, referredto as a specialist by Ayres (1981) and by Peres (1993), is relatively flexible,occurring in four of the six habitat types. Green (1978) even recorded Atelesin secondary forest, though it appears unable to tolerate disturbed habitats(Branch, 1983).

The two species of Cebus were also restricted in their preferences forforest types, using only three of the six available. They appeared to avoidareas with low densities of fruiting trees (pau-roxo forest) and areas witha low canopy height (carrasco and dwarf pau-roxo). A comparison of nicheuse of the two Cebus species indicates considerable overlap in forest type,vertical strata and plant resources (Mendes Pontes, 1994).

My findings highlight three points. First, there may be large regionaldifferences in habitat preferences, with species being generalists in one areaand specialists in another depending on local microhabitat variation. Sec-ond, local environmental factors may promote habitat shifting underdifferent conditions. Third, the available area of the habitat type may in-fluence the extent of specialization. Broad categories such as terra firmeforest may include within them smaller microhabitats visited opportunisti-cally or, indeed, avoided. On Maraca Island the high-ground terra firmeforest contained within it five other forest types, and the primates tendedto exploit at least some of them. The observed selectivity may be more aconsequence of the avoidance of resource-poor areas when conditions areextreme, while the tendency for species to associate may be enhanced byresource scarcity.

A comparison of niche use by the two Cebus species shows that theyoverlap in both forest types and in vertical strata, and that they also fed


on the same plant resources (Mendes Pontes, 1994), though C. apella ex-ploited considerably more species of Palmae than C, olivaceus did.Interestingly, C. olivaceus is the more common species in eastern Maracaand C. apella the rarest, which is the opposite of what Mittermeier andVan Roosmalen (1981) found in the Voltzberg Reserve, Surinam. Spironelo(1991) showed that C. apella depends on Palmae to a great extent, espe-cially during periods of fruit scarcity. This, at least partially underlies theimportance of buritizal forest, which should be fairly important in definingforest use by this species. However, the occurrence of C. apella does notappear to be related to the absolute density of Palmae, since density isalso fairly high in the two main forests (Milliken and Ratter, 1990). It couldbe argued that Maraca lies at the northern limit of the distribution of C.apella (Emmons and Peer, 1990; Groves, 1993), and its niche overlaps thatof with C. olivaceus. This overlap may be the reason for its rarity, alongwith its higher dependence on palms.

C. apella and Saimiri used the same vertical strata with a differentfrequency. Contrarily, Fleagle and Mittermeier (1981) found that they useddifferent strata even when mixed. Furthermore, forest use overlapped interra firme and buritizal forest, and they appeared to exploit the same re-sources (Mendes Pontes, 1994).

I saw Alouatta in only three forest types, but they used them moreevenly than other primates, which were in a greater number of habitatsdid. This is probably because of their feeding habits, which enabled Alouattaalone to exploit leaves (for instance, in pau-roxo forest). They appearedto avoid areas with discontinuous canopy (Glanz, 1982; 1990). Their reli-ance on tall trees (Neville, 1972) was not marked on Maraca Island, wherethey used the same middle to upper vertical strata that Ateles did. System-atic observations would probably show important dietary differences, whichmake such overlap possible. This coexistence is probably due to forest struc-ture, for Maraca lies in the transitional area between the large savannahsof Roraima and the seasonally dry tropical forest, being in act an ecotone,whose forests do not present distinct strata. Maraca forms very open anddiscontinuous forests in most of the areas.

Polyspecific Associations

Polyspecific troops of Saimiri and C. olivaceus, and to a lesser extentC. apella, were on Maraca. Polyspecific associations have been recordedfor many primates in the Neotropics (Podolsky, 1990; Peres, 1988; Johns,1985; Mittermeier and Coimbra-Filho, 1982). The most important benefitof polyspecific associations may be to increase foraging and feeding effi-

152 Mendes Pontes

ciency, depending on food availability in the forest, survivorship, and mostimportantly predator avoidance (Terborgh, 1983; Cords, 1990; Norconk,1990a, b; Mittermeier and Coimbra-Filho, 1982; Garcia and Tarifa, 1988;Terborgh, 1990; Oates and Whitesides, 1990; Peres, 1991).

Mixed groups did not occur either in Mixed Forest (where Saimiri oc-curred once) or in carrasco forest (where only Saimiri occurs). Sometimesone mixed group could hare a feeding site with a third species in a mixedparty or assemblage. This suggests that not only mixed species groups, asin the case of Saimiri and Cebus, but also other species that would notnormally share the same site can exploit the same food source at the sametime without conflict. Again, it might depend upon food availability in thesite, with the species mixing more frequently during periods of minimumfruit abundance (Janson et al., 1981; Terborgh, 1983; Podolsky, 1990). Po-dolsky (1990) found that Saimiri visited proportionally more fruit treeswhen associated with Cebus, which benefited them by locating the fruittrees.

The observed feeding assemblages of three species took place duringOctober, a period of food scarcity with the lowest estimates of fruit avail-ability (Milliken and Ratter, 1990), and scarcity may have been especiallymarked during this study. It took place during a particularly dry year, withlower than average rainfall in the dry season (RADAMBRASIL, 1975) anda maximum monthly rainfall of only 293 mm, compared with the >400 mmrecorded by Nunes (1992). Peaks and troughs of rainfall also shifted, e.g.,the driest months were September and March, compared to February andApril in 1988/1989. In particular, two tree species fruit in the driest monthsas a function of water stress: Tetragastris panamensis (Burs.) and Lecythiscorrugata (Lecythidaceae.). Thus they can be a shifting, but reliable, sourceof fruit in years when few other species produce fruit, leading to a greaterdependence of the frugivores on them.

Trispecific troops are the rarest of the association types, and oc-curred only in fruiting fig trees, without aggression between group mem-bers. Terborgh (1983) states that clumped resources promote largeaggregations, which does not stimulate obligatory sociality, and I observedno social interaction between species when sharing the same food source.Indeed, species appeared to avoid close contact. Aggregations may thusbe better described as ephemeral assemblages impelled by food con-straints, and although no data on size of fruit patches are available, theseassociations occurred mainly in large fruiting trees. Polyspecific associa-tions are, however, crucial during lean periods, when animals crowd intothe rare fruiting fig trees, emphasizing the overwhelming ecological im-portance of this plant type.


Diet

Alouatta ate both leaves and fruits, as is typical of them elsewhere(Julliot and Sabatier, 1993; Gaulin and Gaulin, 1982). They ate the youngleaves of Peltogyne gracilipes (Leguginosae, Caesalpiniaceae), which occurat high densities in mixed forest and pau-roxo forest. In the latter forest,it is the dominant plant species and appears to be the one most adaptedto this almost monodominant forest.

Julliot and Sabatier (1993) found that Bagassa guianensis (Moraceae)alone comprises 10.2% of Alouatta total fruit diet. Nunes (1992) and Ifound that Bagassa guianensis is heavily exploited by Ateles, but we did notrecord it being eaten by Alouatta seniculus, probably due to the unsystem-atic observations of the groups.

Ateles fed primarily on the ripe or unripe fruits of Pradosia surinamen-sis (Sapotaceae), which also accounted for 28.9% of Nunes (1992) recordsof fruits and young leaves. They eat this fruit either ripe or unripe, duringOctober, November, and December. The second most exploited tree spe-cies is Tetragastris panamensis (Burseraceae), but only for fruit. While thisspecies was most available in terra firme forest, it was also in mixed forest.Spider monkey use of a wide range of Maraca forest habitats can be ex-plained by the density of these two plant species in the forests, and by thefact that they could also feed on leaves when fruits were not available.

Robinson (1986) recorded Rubiaceae, Moraceae, and Verbenaceae asthe most heavily exploited families by C. olivaceus, and did not record themusing Palmae. Cebus can depend on Palmae not only for different fruitparts, but also for seeds, pith, and other plant parts, as well as insects [(Ter-borgh, 1983) C. apella, (Freese and Oppenheimer, 1981) C. apella,(Mittermeier and Roosmalen, 1981) C. apella and C. olivaceus]. Accordingto Terborgh (1983), Palmae can account for up to 73% of the total feedingtime of C. apella, and the most heavily exploited families are Moraceae,Mimosaceae, and Palmae. Further, according to Terborgh (1983),Moraceae can account for 95% of the feeding time of Saimiri because ofthe exploitation of Ficus.

Groups in the mixed forest eat young leaves of Peltogyne gracilipes(Leguminocae, Caesalpiniaceae), which occurs at a high density in this for-est. In pau-roxo forest, this species has an even higher density, forming analmost monodominant forest, where the only primates were Ateles, whichare partially folivorous, and Alouatta which are mostly folivorous. This sug-gests that the high abundance of this species is a limiting factor definingthe absence of the smaller-bodied frugivorous monkeys: Cebus and Saimiri.

154 Mendes Pontes

Frequency of Feeding Bouts in the Forests

The most important feature of the forests that define habitats used bythe primate community are not only the number of existing plant speciesbut also the number of plant species that provide food throughout the year.Indeed, terra firme forest contained the highest number of families thatprovide fruit for primates, despite not being the most diverse forest in termsof plant species. The most diverse forest—mixed forest—has a high densityof Peltogyne gracilipes, which forms an almost monodominant forest in someplaces. Although the leaves of this species were eaten by Ateles andAlouatta, the fruits were not taken, which may explain the lower numberof sightings there.

Figs appear to be crucial to all six primates, despite being scattered,fruiting unpredictably, and at occurring densities as low as 2 individuals/50ha. Such large variation and widespread distribution appears typical of figs(Lambert and Marshall, 1991; Gautier-Hion and Michaloud, 1989) and con-firm that the density of fruiting species per hectare is not related to feedingbouts. The former found only three figs fruiting in a 74-ha phenologicalsample, and the latter, only five individuals with ripe fruits in a 100-hasample. Most of the multispecific feeding assemblages were in the twolarge, emergent trees. Not only were individuals of the three primate spe-cies observed together, but also other frugivorous mammals such asprocyonids, rodents, and birds (e.g., toucans), shared the food resource atthe same time totaling up to 70 animals. Borges (1993), Terborgh (1986),and Leighton and Leighton (1983), also found that figs, despite being scat-tered, and fruiting unpredictably, are very important for the frugivore guild,therefore being a keystone resource. The extent to which the frugivorousguild depends on figs and their classification as keystone plant species re-mains to be studied.

ACKNOWLEDGMENTS

Foremost I thank D. Chivers and P. Lee for their advice, Van Roos-malen for his consultancy during fieldwork, and M. Ayres for thepermission to carry out this study at Maraca, while at IBAMA-Brasilia. Ithank P. Furley for satellite images, Mascie-Taylor for advice in statistics,and J. Ratter and W. Milliken for their botanical expertise. B. Wells kindlyrevised the English. I am also indebted to the Vice-Governor of the Stateof Roraima in 1992, A. Dias for important support, Centro de EstudosEcologicos—UFRR for logistics, WWF-Brasilia, the Royal GeographicalSociety—London, and the British Council-Brasilia Headquarters for a


grant, AMBTEC Foundation—Roraima for logistics and financial support,and finally, IBAMA—Brasilia for straightforward decisions to make thiswork possible. The following professionals contributed with important sug-gestions: M. Galetti, C. Drews, A. Chiarello, M. Lehr, F. Ahsan, R.Laidlaw, A. Cuaron, L. Formiga, and S. Heard. I am also grateful to anony-mous reviewers for their useful comments.

REFERENCES

Ayres, J. M. (1981). Observances sobre a ecologia e o comportamento dos Cuxius (Chimpotealbinasus and Chimpotes satanas, Cebidae, Primates), Master thesis, Instituto Nacionalde Pesquisas da Amazonia (INPA), Manaus, Brazil.

Borges, R. M. (1993). Figs, Malabar giant squirrel, and fruit shortages within two tropicalIndian forests. Biotropica 25(2): 183-190.

Branch, L. C. (1983). Seasonal and habitat differences in the abundance of primates in theAmazon (Tapaj6s) National Park, Brazil. Primates 24(3): 424-431.

Brockelman, W. Y., and Ali, R. (1987). Methods of surveying and sampling forest primatepopulations. 2. In Marsh, C. W., and Mittermeier, R. A. (eds.), Primate Conservation inthe Tropical Rainforest, John Wiley and Sons, New York, pp. 23-62.

Buckland, S. T., Anderson, D. R., Burnham, K. P., and Laake, J. L. (1993). Distance Sampling.Estimating Abundance of Biological Populations, Chapman and Hall, London.

Burnham, K. P., Anderson, D. R., and Laake, J. L. (1980). Estimation of density from linetransect sampling of biological populations. Wildl. Monogr. 72: 1-202.

Cords, M. (1990). Mixed species association of East African Guenons: General patterns orspecific examples? Am. J. Primatol. 21: 101-114.

Eisenberg, J. F. (1980). The density and biomass of tropical mammals. In Scute, M., andWilcox, B. (eds.), Conservation Biology, Sinnaver Associates, Sunderland, MA, pp 35-55.

Emmons, L. H., and Peer, F. (1990). Neotropical Rainforest Mammals, a Field Guide, Universityof Chicago Press. Chicago.

Fleagle, J. G., and Mittermeier, R. A. (1981). Differential habitat use by Cebus apella andSaimiri sciureus in Central Surinam. Primates 22(3): 361-367.

Freese, C. H., and Oppenheimer, J. R. (1981). The capuchin monkey, genus Cebus. InCoimbra-Filho, A., and Mittermeier, R. A. (eds.), Ecology and Behaviour of NeotropicalPrimates, Academia Brasileira de Ciencias, Rio de Janeiro, pp. 331-390.

Galetti, M., and Peres. C. (1993). 'Plantas Chaves' em florestas tropicais. Ciencia Hoje 16:57-58.

Galtier-Hion, A., and Michaloud, G. (1989). Are figs always keystone resources for tropicalfrugivorous vertebrates? A test in Gabon. Ecology 70: 1826-1833.

Garcia, J. E., and Tarifa, T. (1988). Primate survey of the Estacao Ecologica Beni. PrimateConserv. 9: 97-100.

Gaulin, S. J., and Gaulin, C. K. (1982). Behavioural ecology of Alouatta seniculus in Andeancloud forest. Int. J. Primatol. 3(1): 1-32.

Glanz, W. E. (1982). The terrestrial mammal fauna of Barro Colorado Island: Censuses andlong-term changes. In Leith, E. G., Rand, A. S., and Windsor, D. M. (eds.), The Ecologyof a Tropical Forest: Seasonal Rhythms and Long Term Changes, Smithsonian InstitutionPress, Washington, DC, pp. 455-468.

Glanz, W. E. (1990). Neotropical mammal densities: How unusual is the community in BarroColorado Island, Panama? In Gentry, A. H. (ed.), Four Neotropical Rainforests, YaleUniversity Press, New Haven, CT, pp. 287-313.

Green, K. M. (1978). Primate censusing in Northern Colombia: A comparison of twotechniques. Primates 19(3): 537-550.

156 Mendes Pontes

Groves, C. P. (1993). Order Primates. In Wilson, D. E., and Reeder, D. M. (eds.), MammalSpecies of the World. A Taxonomic and Geographic Reference, Smithsonian InstitutionPress, Washington, DC, pp. 243-276.

Guillotin, M., Dubost, G., and Sabatier, D. (1994). Food choice and food competition amongthe three major primate species of French Guiana. J. Zoo/. Lond. 233(4): 551-579.

Janson, C. H., Terborgh, J., and Emmons, L. (1981). Non-flying mammals as pollinating agentsin the Amazonian Forest. Biotropica 13(2): 1-6.

Johns, A. D. (1985). Primates and forest exploitation at Tefe, Brazilian Amazonia. PrimateConserv. 6: 27-29.

Klein, L. L. and Klein, D. J. (1973). Observations on two types of Neotropical primateintertaxa association. Am. J. Phys. Anthropol. 38: 649-654.

Lambert, F. R., and Marshall, A. G. (1991). Keystone characteristics of bird-dispersed Ficusin a Malaysian lowland rain forest. J Ecol. 79: 793-809.

Leighton, M., and Leighton, D. R. (1983). Vertebrate responses to fruiting seasonably withina Bornean rain forest. In Sutton. S. L, Whitmore C. T., and Chadwick, A. C. (eds.),Tropical Rain Forest. Ecology and Management, Special Publication No. 2. BritishEcological Society, Blackwell Scientific, London, pp. 18)-196.

Mendes Pontes. A. R. (1994). Environmental Determinants of Primate Abundance in MaracdIsland. Roraima, Brazilian Amazonia, Unpublished M.Phil. thesis, University ofCambridge, Cambridge,

Milliken, W., and Ratter, J. (1990). The Vegetation of the. Ilha de Maracd, First Report of theVegetation Survey of the Maraca Rainforest Project, Royal Botanic Garden, Edinburgh.

Mills, L. C., Soul6, M. E., and Doak, D. F. (1993). The keystone-species concept in ecologyand conservation. Bioscience 43(4): 219-224.

Ministerio do Interior (1977). Secretaria Especial do Meio Ambiente. Programa das EstacoesEcol6gicas. S4r. Meio Ambiente 2: 1-39.

Mittermeier, R. A., and Coimbra-Filho, A. F. (1982). Primate conservation in BrazilianAmazonia. In Prince Rainier of Monaco and Bourne, G. H. (eds.), Primate Conservation,Academic Press, New York, pp. 117-166.

Mittermeier, R. A., and Van Roosmalen, M. G. M. (1981). Preliminary observations on habitatutilization and diet in eight Surinam monkeys. Fol. Primatol. 36: 1-36.

Mueller-Dombois, D., and Ellenberg, H. (1974). Aims and Methods of Vegetation Ecology, NewYork, John Wiley & Sons, New York.

National Research Council (NRC) (1981). Techniques for the Study of Primate PopulationEcology, National Academy of Sciences. National Academic Press, Washington, DC.

Neville, M. K. (1972). The population structure of red howler monkeys (Alouatta seniculus )in Trinidad and Venezuela. Folia Primatol, 17: 56-86.

Norconk, M.A. (1990a). Introductory remarks: Ecological and behavioral correlates ofpolyspecific primate troops. Am. J. Primatol. 21: 81-85.

Norconk, M. A. (1990b), Mechanisms promoting stability in mixed Saguinus mystax and 5.fuscicolis troops. Am. J. Primatol. 21: 159-170.

Nunes, A. P. (1992). Uso do Habitat, Comportamento Alimentar e Organizacao Social deAteles belzebuth belzebuth (Primates:Cebidae); Master thesis, Universidade Federal doParS, Museu Paraensi Emilio Goeldi, Para\

Gates, J. F., and Whitesides, G. H. (1990). Associations between olive colobus (Procolobusvents) and Diana Guenos (Cercopithecus diana) and other forest monkeys in Sierra Leone.Am. J. Primatol. 21: 129-146.

Peres, C. A. (1988). Primate community structure in Western Brazilian Amazonia PrimateConserv. 9: 83-87.

Peres, C. A. (1989). A survey of a Gallery Forest primate community, Maraj6 Island, ParaVida Silvestre Neotrop. 2(1): 32-37.

Peres, C. A. (1991). Ecology of Mixed-Species Groups of Tamarins in Amazonian Terra FirmsForests, Ph.D. dissertation, University of Cambridge, Cambridge.

Peres, C. A. (1993). Structural and spatial organization of an Amazonian terra firme forestprimate community. J. Trop. Ecol. 9: 259-276.


Podoisky, R. D. (1990). Effects of mixed-species association on resource use by Saimiri sciureusand Cebus apella. Am. J. Primatol. 21: 147-158.

RADAMBRASIL (1975). Projeto de Integragao Nacional, Minist6rio das Minas e Energia,Departamento Nacional de Produgao Mineral, Levantamento dos Recursos Naturais, Riode Janeiro.

Richard, A. (1970). A comparative study of the activity patterns and behaviour of Alouattavillosa and Ateles geoffroyi. Folia Primatol. 12: 241-263.

Sokal, R. R., and Rohlf, F. J. (1981). Biometry, Freeman, San Francisco.Spironelo, W. R. (1991). Importancia dos frutos de Palmeiras (Palmae) na dieta de urn grupo

de Cebus apella (Cebidae, Primate) na Amazonia Central. In Rylands, A. B. (ed.), Aprimatologia no Brasil—3, Universidade Federal de Minas Gerais, Belo Horizonte, pp.285-296.

Terborgh, J. (1983). Five New World Primates: A Study in Comparative Ecology, PrincetonUniversity Press, Princeton, NJ.

Terborgh, J. (1986). Keystone plant resources in the tropical rainforest. In Soule, M. (ed.),Conservation Biology: Science of Scarcity and Diversity, Sinauer Associates, Sunderland,MA, pp. 330-344.

Terborgh, J. (1990). Mixed flocks and polyspecific associations: costs and benefits of mixedgroups to birds and monkeys. Am. J. Primatol. 21: 87-100.

Van Roosmalen, M. G. M. (1985). Habitat preferences, diet, feeding strategy and socialorganization of the black spider monkey (Ateles paniscus paniscus Linnaeus 1758) inSurinam. Acta Amazon. (Supp.) 15(3/4): 1-238.

Waser, P. M. (1990). "Chance" and mixed-species associations. Behav. Ecol. Sociobiol. 15:197-202.

Whitesides, G. H., Oates, J. F., Green S. M., and Kluberdanz, R. P. (1988). Estimating primatedensities from transect in a West African rainforest: A comparison of techniques. J. Anim.Ecol. 57: 345-367.

habitat partitioning among primates in maraca island, roraima, northern brazilian amazonia

Documents