2007 primate group siye an cde caatinga

8/6/2019 2007 Primate Group Siye an cde Caatinga

1/19

Primate Group Size and Abundance

in the Caatinga Dry Forest, Northeastern Brazil

Antonio Christian De A. Moura

Received: 29 December 2005 /Revised: 14 June 2006 /Accepted: 10 October 2006 /

Published online: 20 November 2007#

Springer Science + Business Media, LLC 2007

Abstract The Caatinga dry forest poses a series of ecological challenges for mammals

in general and primates in particular. The erratic rainfall pattern impacts on plant

diversity and phenological patterns; from year to year there is marked variability in fruit

production and failure to fruit is common. The harshness apparently accounts for the

impoverished mammalian fauna. However, data on primate abundance, distribution,

and possible environmental effects on primate density are lacking in this type of dry

forest. I censused the primate community in 3 habitats of the Serra da Capivara National

Park, Piaui, NE Brazil, over a total distance of 318 km. Overall, the abundance ofprimates in the Caatinga dry forest is very low as a consequence of low abundance of

food resources both in space and time. Alouatta caraya (predominantly folivorous)

occurs at extremely low density, and during the dry season are apparently confined to

canyon areas, where trees retain their leaves. Callithrix jacchus has morphological

feeding specializations for gum-eating, and gum is an important resource during food

bottleneck periods. Nonetheless, Callithrix jacchus occurs at comparatively low

densities. Group sizes for howlers and marmosets in the Caatinga are significantly

smaller than in other forest types. Contrarily, Cebus apella libidinosus had an average

group size within the range reported for Amazonian and Atlantic forests. Researchersconsider the generalized diet of capuchins as the explanation for their similar

abundance in different habitats, indicating relative independence from ecological

constraints. However, I suggest that capuchin foraging style and cognitive abilities are

important factors accounting for their unreduced group size and density even under

extreme conditions.

Int J Primatol (2007) 28:12791297

DOI 10.1007/s10764-007-9223-8

A. C. De A. Moura (*)

Darwin College and Department of Biological Anthropology, Cambridge University,

Silver Street, Cambridge CB3 9EU, U.K.

e-mail: [email protected]

A. C. De A. Moura

Laboratrio Tropical de Primatologia, Departamento Sistemtica e Ecologia CCEN,

Universidade Federal da Paraiba, Joo Pessoa PB. 58059900, Brazil

Present address:


2/19

Keywords cognitive foraging skills . conservation . feeding adaptations .

primate density

Introduction

The Caatinga is the third largest biome in Brazil. It is a complex mosaic of different

vegetation types locally determined by rainfall patterns, soil conditions, and history

of human disturbance (Andrade-Lima 1981; Moura 2004). Most of the vegetation is

secondary seasonal dry forest, which originated from human disturbance; in the past

the Caatinga was taller and not so strikingly dry (Coimbra-filho and Cmara 1996;

Webb 1974). The Caatinga biome extends over ca. 1 million km2 and the climate is

characterized by a low and extremely irregular rainfall pattern, with an average

yearly precipitation of 800 mm (Reis 1976; Sampaio 1995). The harsh ecologicalcondition of the habitat is a difficult challenge for the mammalian community in

general, particularly for primates.

Tropical dry forests normally have a much lower diversity and a lower net

primary productivity than those of rain forests (Murphy and Lugo 1986), and periods

of fruit scarcity are much longer than in tropical rain forests (van Schaik et al. 1993).

The features affect the vertebrate community, which tends to be characterized by a

small number of species at low abundance; the Caatinga has one of the lowest

diversities of vertebrates among neotropical dry forests (Ceballos 1995). Mammalian

fauna, in particular, is one of the poorest faunas in the tropics and has the lowestdensity of small terrestrial mammals (rodents) among tropical arid and semiarid

environments (Mares et al. 1985; cf. Freitas et al. 2005). Fruit-eating specialists are

particularly scarce, probably because of the highly seasonal and often unpredictable

availability of fruit (Machado et al. 1997; Moura and McConkey 2007).

In recent years there has been a growing interest in the Caatinga biodiversity and

conservation, and some studies have revealed an unsuspected high biodiversity in

insects, birds, and plants (Leal et al. 2005). The dearth of information on abundance

and distribution and the general ecology of Caatinga mammals is surprising because

such data are an essential requirement for conservation planning. Past study of

mammalian densities and abundance in the Caatinga are limited to small rodents and

marsupials. Studies are still lacking on the density and abundance of primates in the

Caatinga.

Factors Affecting Mammal Distribution in Tropical Forests: Implications for Primate

Abundance in Caatinga Dry Forest

Researchers have long linked the distribution of animals in the tropical forests to

environmental factors (Janzen and Schoener 1968), which explains differences in the

abundance of mammals among areas. The most commonly cited factor is food

availability (Mendes Pontes 1999; Peres 1997b), linked to soil fertility. Emmons

(1984) considered soil type differences as one of the most important environmental

factors explaining differences in mammalian abundance across the Amazon basin.

She also suggested that competitive interactions over food resources can influence

mammalian abundance.

1280 A. C. de A. Moura


3/19

Forest structure also could account for variable mammalian abundance; forests

with a higher structural complexity, mainly a dense undergrowth, have higher

mammalian abundance (Emmons 1984). Natural disasters are another factor

influencing abundance. For example, a severe drought in a dry forest of Madagascar

had a negative impact on the population of Lemur catta, leading to a 31% decrease 2yr after the drought (Gould et al. 1999). The decline of vital food resources over

time is another type of natural disaster that can lead to considerable reduction in

population size or even extinction like one of Cercopithecus aethiops (Lee and

Hauser 1998).

For fruit-eating primates, one of the most important variables affecting density is

the availability of fruits (Janson and Chapman 1999). Robinson and Redford (1986)

suggested that the density of capuchins is linked to fruit production. Sorensen and

Fedigan (2000) found that, in Costa Rican dry forests (Santa Rosa National Park),

the density of Cebus capucinus is higher in areas with more fruit abundance, andStevenson (2001) found that primate biomass in the neotropics is significantly

associated with fruit production. Consequently, in the Caatinga, higher primate

abundance can be predicted in habitats with higher fruit productivity.

The Serra da Capivara National Park (SCNP) has 3 distinct major habitats, each of

which represent a particular forest type: canyons, plateau and cliffs facing the plains.

The canyons are wetter than the cliffs and plateau. Accordingly, their forest is taller and

has a higher density of trees producing fruits eaten by mammals (Moura 2004). Thus,

one can expect a higher abundance of primates in the canyons than in cliffs and plateau.

However, one cannot explain primate abundance via environmental factors alone.Morphological feeding specializations can be a crucial element in determining the

density of primates in different habitats (Peres 1997b). For example, Callithrix jacchus

(360380 g; Smith and Jungers 1997), is one of the primate species with the highest

density in the Neotropics (Robinson and Redford 1986). The high density of marmosets

is probably a consequence of their morphological adaptations that allow extensive use of

exudates, mainly during lean fruit-food times (Stevenson and Rylands 1988). The

adaptation is associated with a smaller home range than that of similar-sized

callitrichines and causes a more packed distribution. Moreover, marmosets can attain

high abundance in secondary growth vegetation and in disturbed habitats (Rylands

1996). Thus, they are expected to be the most common primates in SCNP. Because the

habitat along the cliffs has a high density of exudate sources for marmosets

( Anadenanthera colubrina, Croton sonderianus, and Copaifera langsdorfii; Moura

2004) I suggest they will be much more abundant there.

During the dry season in the Caatinga forest, >70% of trees are leafless and there

is a marked drop in resource availability (Moura 2004). In seasonal dry forests, leaf

quality, viz., nutrient contents and palatability, is higher than in evergreen forests;

consequently, folivorous primates such as howlers attain higher densities (Peres

1997b). Yet, in the Caatinga, extreme droughts lasting for 1 yr are common

(Sampaio 1995), with potential drastic effect on the primates populations. Though

Peres (1997b) suggested that the abundance of folivores should not be drastically

affected by intense dry seasons, studies are lacking on the abundance and density of

howlers and other primates in harsh habitat like the Caatinga dry forest.

I provide estimates of the primate populations in SCNP from transect counts and

determine the distribution of primate species across habitat types. I show that each of

Primates in Caatinga Dry Forest 1281


4/19

the sampled habitats has an individual pattern of primate abundance, and that

environmental features are the main factor explaining their abundance. However, the

expected link between fruit productivity and primate abundance proved elusive. I

explain this apparent inconsistency based on peculiarities of the different forest types

sampled. Finally, I compare primate abundance and group size in Caatinga dry forestwith other forest types, such as the Atlantic forest and the Amazonian forest, where

food shortage is not as drastic.

Methods

Study Site

The Serra da Capivara National Park, located on the coordinates of 80

26

to 80

54

Sand 42019 to 4245 W, covers an area of 129.953 ha. Emperaire (1984), in a

detailed analysis of the geomorphology and associated vegetation, recognized 8

different types of habitat encompassed by the park, each with characteristic

vegetation types. However, 3 main habitat types can be easily distinguished in the

southwest area of the park where I conducted most of the study; they are also the

main habitats in the rest of the park. They are defined as:

& A sandstone plateau (ca. 500 m above sea level), with a peculiar low stature

deciduous vegetation (canopy height at 57 m). The majority of the park lies on

the plateau.& Canyons of varying length and width dissecting the plateau on its border,

accounting for about 15% of the park area. The vegetation inside the canyons is a

semideciduous forest with trees reaching 25 m. The canyons are wetter and

most of them have permanent or temporary waterholes.

& Cliffs (or cuesta, the slope of the plateau) separating the plateau from the

interplanaltic depression (plains); the vegetation on the cliffs is tall, with trees

22 m, and with characteristic species such as Tabebuia impetiginosa,

Anadenanthera colubrina, and Prockia crucis. This habitat occupies about

10% of the area of the park.

Plains are an extensive and important element of the regional landscape, but they

accounts for


5/19

to 154.8%. During the dry season, >70% of trees are leafless (Moura 2004). The

average annual temperature is 27C. The soils in the park are typically acidic (pH 5)

(Emperaire 1984).

Estimating Abundance

I followed established procedures of line-transect methods (Buckland et al. 2001;

Peres 1999) for surveying mammals. For the census, I used 6 transects of different

lengths in the 3 habitats of the park (Table 1).

Altogether, the transects had a total extension of 12.5 km, and I censused a total

of 318.6 km over 12 mo. However, the censuses did not start at the same time. For

example, census in the plateau started in November 2000, while those along the

cliffs started in April 2001. For about 3 mo (AprilJune 2001), 2 field assistants

helped with the mammalian census. Though the use of different observers

conducting the line transect censuses can give biased results (Mitani et al. 2000),

it is a normal practice to do so after training (Peres 1999). I completed 84.8% of the

total km surveyed.

0

50

100

150

200

250

300

Jan. Feb. Mar Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec.

Precipitation(m

m)

2001

Mean (1995-2001)

Fig. 1 Annual rainfall in the area and the average for 7 yr.

Table 1 Details of the transects censused

Place Habitat type Transect length (km) No of months censused Total km walked

Baixa Grande Cliffs 1 12 22.3Jurubeba 1 Cliffs 0.45 4 4.5

Jurubeba 2 Cliffs 0.7 9 13

Baixao da Vaca Canyon 1.4 10 33.6

Esperacanca Canyon 1.65 12 66

Zabele Plateau 7.3 11 179.2

Note that the plateau and canyons had a higher survey effort.



6/19

A reliable estimate of density is based on the number of sightings (minimum

n = 40), which depends on transect length and sampling effort. Generally transects

in most surveys of primates have a standard length of ca. 34 km (Peres 1999),

but owing to the topography of my study area, with a rugged terrain and canyons

of different sizes and shapes, it was unfeasible to have long transects except inthe more level sandstone plateau. Owing to limited time for censusing each

existing transect every month, I could not establish multiple transects in each

habitat type.

I placed transects at random, except for ones inside the canyons. I tried to

optimize the sampling effort and time spent in the field by choosing the longest

canyons (Esperanca at ca. 2 km and Baixao da Vaca at ca. 1.5 km), and proximity

to each other. In Esperanca Canyon there was an old cattle trail (ca. 700 m), part of

which I used for the census. In the Baixao da Vaca Canyon there is a relatively

straight trail entering it. Park guides and tourists occasionally used it; consequent-ly, some mammalian species were more habituated there, e.g., the rodent Kerodon

rupestris, but there was no provisioning in the area. In both canyons the trails

followed their contour and at some points there were deviations of >40 from a

straight compass bearing.

The Baixa Grande trail ran parallel to the cliffs at distances ranging from 30 m to

250 m. The Jurubeba 1 trail cuts perpendicularly to the cliffs and at its end there is a

parallel trail running just by the cliffs. I also used the parallel trail for the census

(Jurubeba 2 trail). Both Jurubeba trails are ca. 6 km distant from the Baixa Grande

trail. The trails followed a straight line whenever possible.In the sandstone plateau I used an old trail ca. 20 km long, located almost in the

middle of the park, bisecting the plateau from east to west. It was made >80 yr ago

and had been used by hunters and old inhabitants of a small village (around 200

people) inside the park, who left >4 yr previously. Another researcher used the trail to

study carnivores in the park ca. 6 mo before I started the census. I established the

beginning of the census transect 2 km from the start of the trail, where I detected no

sign of past human activity. The plateau trail is relatively straight, ca. 1 m and at some

points 1.5 m wide.

I marked each trail at 50-m intervals with yellow plastic flags, to enable observers

to record the transect distance when they saw an individual and as a point to stop and

listen for animals. We walked the trail slowly at a pace of ca. 11.5 km/h and

surveyed both sides. We walked transects 1 times per mo in the morning (from

0600 h) and in the afternoon (from 1400 h) to avoid bias in sampling individuals that

could be more active then.

During the census, I noted specific identity, group size, and activity and sex of the

individuals, as well as their locations relative to the transect line, distance to observer,

and angle in relation to the trail.

I set up vegetation plots along the trails and in other areas and identified all

the trees with DBH (diameter at breast height) 3.8 cm (n =2786) within a total

area of 2.5 ha (7 belt transects and 8 plots spread over the 3 main habitats,

including 5 canyons). I also collected phenological data from the trees. In addition,

I set up 60 pitfall traps and a series of nest traps (for solitary bees and wasps) in the

different habitats. Full details on methods to sample food availability are in Moura

(2004).



7/19

Analyses

The most common estimator used to assess the density of animals, particularly

mammal density from line-transect surveys, is the distance sampling method, as

Buckland et al. (2001) delineated via DISTANCE. The method requires a substantialsample size of >40 sightings, or 20 sightings (Peres 1999), to produce reliable

estimates of density. Frequently in tropical forests the number of sightings is below

the minimum for reliable estimates of densities, which seems to be common for

primates (Chapman and Chapman 1999). Moreover, to obtain 20 sightings of

primate groups in a habitat such as the Caatinga, one would probably have to walk

the transects for several thousand km, which was not practical.

I used the number of sightings per 10 km walked to estimate primate abundance.

Encounter rate is a useful way to estimate mammalian abundance in diverse habitat

types, and many researchers studying mammalian abundance, mainly of primates,have used encounter rates for comparisons between different habitats (Carrilo et al.

2000; Chiarello 1999; Emmons 1984; Lopes and Ferrari 2000) or to control for

differential sampling effort in different areas (Peres 1997a).

Though encounter rate is often used to compare primate abundance across habitats, it

can be misleading when used to compare abundance of primates living in habitats that

present drastic differences in availability of food. For example, low food abundance can

have a negative impact on group size by increasing mortality (Gould et al. 1999), yet

the number of groups encountered in a census could remain unaffected. Therefore, I

compare the group size of primate species encountered in the Caatinga with the groupsize of the same species living in forest with a higher availability of resources. The

data could demonstrate how the harsh Caatinga environment affects the primates.

However, it was not always possible to count group sizes accurately during the

censuses because the interindividual distance among group members was usually

high, and foliage or large outcrops concealed part of the group, which was often the

case for capuchins. Thus, group size estimates were improved with data collected

outside the censuses from the period of October 2000 to March 2002. Group size

estimates based on that data are more reliable because I could count the number of

individuals without staying on the transect line or having a 10-min limit for observing

them, as determined by the transect guidelines (Peres 1999).

Because many previous studies of neotropical primates provided both density

(individuals/km2) and encounter rates (groups/10 km walked), I regressed the

published data forCebus apella to estimate their density in the park. Unfortunately,

comparable density data were unavailable for Callithrix jacchus and Alouatta

caraya. For fitting the regression line, I used only data from studies that used

DISTANCE to estimate density because the statistics behind the program are

robust and thus can provide fairly accurate estimates of density (Buckland et al.

2001).

I tested the distribution of group size for each species via the Kolmogorov-Smirnov

1-sample test. Group size followed a normal distribution (p>0.3). For the comparisons

of primate group sizes in the Caatinga with those from different forest types, I used the

Student t-test if variance were equal (checked with the Levenes test for equality of

variance). If variances were unequal I used the unequal variance t-test. All tests are

2-tailed and I use the standard value of p=0.05.



8/19

Results

Line-transect Census

Among primates, Cebus apella libidinosus occurs at higher abundance along thecliffs, while howlers and marmosets occur more frequently inside the canyons

(Table 2). However, the higher frequency of marmosets in the canyons was

apparently due to a repetitive count of a single group living in secondary vegetation

along the cattle trail in Esperanca Canyon.

Primate Group Size and Occurrence in the Different Habitats

During the line transect census I saw a total of 8 groups of capuchins, with an

average group size of 4.8 individuals (range 1

9). When I incorporated the groupsize counts obtained outside the census, the average group size increased ( SD) to

8.8 4.3 individuals (n=40, maximum group size= 16; mode= 13 individuals).

However, on many occasions, I was unable to determine if I had sighted the same

or a different group because the home ranges of capuchins in the area overlapped

extensively. For instance, in the Oitenta area, where I followed a focal group of

capuchins (Moura and Lee 2004), 3 different groups passed through the area. A

group from Baixa Grande area sometimes traveled >5 km, passing by Oitenta area

moving in the direction toward Caldeirao do Gato Canyon, which another capuchin

group frequented. Nonetheless, the group sizes are within the reported range forcapuchins. During the censuses, I observed capuchins 6 times along the cliffs and

twice in the canyons (Table 2).

The average group size of Cebus apella in the Caatinga is within the range

reported for the Amazonian and Atlantic forests (Table 3). Indeed, there is no

significant difference in group size in the Caatinga versus those in wet forests (t=

0.87; df=63; p=0.38). In the dry Cerrado vegetation, Schaller (1983) reported an

average group size of ca. 8 individuals (n=24 groups).

Marmosets are the most widespread primate in the area, occurring in more

degraded areas, in shrub vegetation of the plains, and even on the plateau, where I

saw a small group of ca. 4 individuals. The area the marmosets seemed to be using

was ca. 2 km away from the transect trail; the vegetation was taller than that of the

plateau and had species such as Acacia cf. paniculata and Croton sonderianus from

which they can exploit exudate. However, when censusing the trail on the plateau, I

never saw or heard calls of marmosets. Overall, during the census I saw a total of 11

Table 2 Encounter rate, groups/10 km walked

Species Encounter rate

Cliffs Canyons Plateau Average

Alouatta caraya 0.4 (4) 0.13

Callithrix jacchus 1.0 (4) 0.7 (7) 0.57

Cebus apella 1.5 (6) 0.2 (2) 0.57

Values inside () represent number of sightings.



9/19

marmoset groups, but 6 sightings seemed to be of the same group, with similar

composition and in the same area. In the Esperanca Canyon, I always observed

marmosets in the forest along the cattle trail; the area has a recovering vegetation and

higher density of Acacia cf paniculata, which can be exploited for exudate.

Marmosets had a smaller mean group size than that of capuchins, with an average

( SD) of 2.9 1.67 individuals/group (n=30 including observation out of the

censuses, maximum group size=7, mode=2). Marmoset mean group size seems to

be adversely affected in the Caatinga dry forest. It is significantly lower than that of

Callithrix jacchus (Koenig 1995; Lazaro-Perea et al. 1999) living in different areas

of the Northeastern Atlantic forest (unequal variance, t=8.3; df=35.2; p


10/19

The mean group size for Alouatta caraya in the Caatinga is significantly lower

than groups sizes in Northern Argentina (t=4.61; df=19; p


11/19

Nevertheless, the density I estimated in the Caatinga area of 7.111.2

individuals/km2 is within the range reported for Cebus apella (Table 4) in the

Amazonian forest (2.955.7 individuals/km2) and in the Atlantic forest (range 6.25

25.75 individuals/km2).

Discussion

Primates are one of the most common mammals in the park, and they are present in

much of the Caatinga region, though howlers and capuchins have become extinct in

some localities due to habitat alteration ( pers. obs.; Coimbra-Filho and Camara

1996). The primates in the dry forest are not hunted by people, at least in the study

area; they are relatively easy to spot and their relative abundance (encounter rate)

could be determined.

Table 4 Encounter rate (groups/10 km) and density of Cebus apella in different types of habitats within

their geographical range

Forest type Encounter rate Density

individuals /km2Density

estimator

Source

Am: terra firme 0.2 2.9 DS Peres (1997a)

Am: terra firme 0.6 9 DS Peres (1997a)

Am: terra firme 1 15.7 DS Peres (1997a)



Am: terra firme 3 49.6 DS Peres (1997a)




Am: terra firme 1.3 21 DS Peres (1997a)


Am: terra firme 0.7 12.7 DS Peres (1997a)Am: Vrzea 1.1 17.4 DS Peres (1997a)

Am: Vrzea 2.9 55.7 DS Peres (1997a)




Am: Guyanan shield 0.17 Lehman (2000)

Am: terra firme 1.06 14.1 DS Wallace et al. (1998)

At: semideciduous 1.24 10.93* DS Cullen et al. (2001)

At: semideciduous? 2.47 25.76 DS Chiarello (1999)

At: semideciduous? 1.51 15.8 DS Chiarello (1999

At: semideciduous? 1.05 11.01 DS Chiarello (1999)At: semideciduous? 0.6 6.25 DS Chiarello (1999)



At: semideciduous? 0.905 10.2 OT Pinto et al. (1993)

Atl: semideciduous? 1.13 22 OT Price et al. (2002)

aThe density is the average density from the values provided by the authors.

Am = Amazonian Forest; At = Atlantic Forest; DS = Distance sampling program; OT = Kings, Leopolds

method or other type of density estimator.



12/19

Primate Abundance and Use of Different Habitats

Capuchins and marmosets are the most common primates in the area, while howlers had

the lowest abundance, being effectively restricted to the canyon habitat. Capuchins

predominated along the cliffs, being by far the most abundant primate there, though theyhad a somewhat more restricted distribution generally throughout the park than

marmosets did. Several factors might explain the absence of primates on the plateau.

Among the different areas surveyed, the plateau is the most inhospitable. During the

height of the dry season, the forest there became almost leafless (Moura 2004), and

shade and protection from heat are minimal. The availability of water is negligible and

restricted to a few temporary trunk holes. The lower height of the forest (mean 4 m) in

the plateau could also account for the absence of primates, facilitating predation by

terrestrial predators such as ocelots, pumas, and jaguars. Nevertheless, I observed

capuchins venturing into the plateau by the cliffs 14 times. The fact that I collecteddung of howlers with seeds of Byrsonima cf gardneriana, a species exclusive to the

plateau, suggests that they were also using the plateau at least in the rainy season,

perhaps as a shortcut between canyons (Moura and McConkey 2007). Apparently all

primates species were capable of using the plateau area, but only around the borders of

the plateau/cliffs.

The most puzzling result was that primates were most abundant along the cliffs,

the habitat with the lowest density of trees producing zoochoric fruits. Ecological

factors can play an important role in determining the abundance of primates, and

food supply is supposed to be a critical factor determining the abundance of primates(Brugiere et al. 2002; Chapman and Chapman 1999; Mendes-Pontes 1999; Peres

1997b). Indeed, Stevenson (2001) found that, in neotropical primate communities,

fruit productivity is the best predictor for primate biomass and abundance. In the dry

forests of Costa Rica, the density of Cebus capucinus is directly linked to fruit

abundance (Sorensen and Fedigan 2000). Thus, one would expect the highest relative

abundance of capuchins and other monkeys inside the canyons, where trees producing

fruit eaten by the primates have significantly higher densities, and where fruit

productivity seems to be much higher. Further, the most probable place to find water

holes or small water ponds during the dry season is in the canyons. Yet, primate

abundance there was particularly low. One possible explanation for the discrepancy is to

think of the canyons as islands with distinct flora, but with a small area and limited food

resources that could be depleted quickly. Perhaps the high abundance of primates,

mainly capuchins, along the cliff might be a consequence of moving between canyons,

but, if so, the encounter rate in the canyons should have been much higher because this

habitat was censused more often than the cliffs.

However, an important confounding factor was that the park management had put a

small number of feeding stations in some areas, provisioned with corn and manihot

tubers, at distances 400 m3 km from the cliffs. The feeding stations were established to

improve the recovery of gray brocket deer, collared peccary, and agouti populations.

Obviously, for capuchins it was a prime opportunity for food. For example, the group of

capuchins I followed spent >50% of their time around the provisioning area (Moura

2004). Howlers and marmosets did not eat the provisions. In the Baixa Grande area,

the feeding station was ca. 1.3 km from the census trail and in the Jurubeba area it was

300 m from the trail (Jurubeba 1). Clearly, the placement of the feeding stations might



13/19

affect the distribution of capuchins in the area, but there are 2 crucial elements of the

cliff habitat that minimizes or removes the possible association of the feeding stations

with the higher encounter rate of capuchins. First, the habitat along the cliffs is very

heterogeneous in terms of forest structure and geology, human disturbance, and

vegetation age. Moreover, in some areas with more shade and perhaps higherunderground water availability the vegetation is similar to that of the canyons. This

kind of mosaic habitat increases the diversity and availability of food resources and

consequently could support a large population of primates. In a primate community in

a rain forest in Gabon, populations of cercopithecines and colobines benefit from a

more heterogeneous habitat, and live at high density as a result (Brugiere et al. 2002).

Likewise, a more heterogeneous habitat increases the densities of neotropical primates

such as callitrichids and howlers (Emmons 1984; Michalski and Peres 2005).

The second point is related to a biological aspect of the vegetation along the cliffs.

About 70% of cliff trees are leafless during the dry season. Trees that lose theirleaves seasonally might contain a lower concentration of chemical protection against

herbivores (Coley and Barone 1996); thus they would harbor a more diverse and

abundant community of primary consumers. Leaves with a short lifetime, i.e.,


14/19

sampling effort because Dvoskin et al. (2004) surveyed 48 km, while I surveyed ca.

140 km (canyons and cliffs).

Interestingly, capuchins and marmosets had the same average encounter rate (0.57

groups/10 km). Though marmosets were more widespread throughout the area, I

expected them to be much more frequent because they can use disturbed areas andhave a small body size and home range. The similar relative abundance of

marmosets and capuchins in the Caatinga is perplexing because along the cliffs, an

important source of exudate for the marmosets, Anadenanthera colubrina was the

second most common tree (Moura2004). Exudates are a rich source of carbohydrate

and minerals for many species of Callitrichinae, particularly Callithrix and Cebuella,

and are available all year round (Lacher et al. 1984). If invertebrate diversity and

abundance are higher along the Cliffs and there is a higher abundance of food

resources, i.e., exudate trees, then why were marmosets found less frequently than

capuchins in the censuses? Perhaps it could be a consequence of habitat partitioningdue to feeding competition. Emmons (1984) emphasized that, in the more

unfavourable habitats of the Amazon basin, smaller mammalian species became

rare, while the larger ones maintained their densities. She suggested that direct

competitive interactions over food sources, mainly during periods of food scarcity,

put small mammals at a disadvantage. For primates, she cites cases in Cosha Cashu,

Per, where troops of Cebus apella displaced small primate species or prevented

them from having access to fruit sources. Though this is a plausible explanation for

the low abundance of marmosets along the cliffs, it is insufficient because

marmosets had access to exudate, a resource other primates did not exploit.Another explanation could be linked to the generalist diet of capuchins, allowing

them to use a greater number of resources in the cliff habitats than the marmosets

could. Cebus apella is generally widely distributed, inhabiting a wide variety of forest

types, and their success is associated mainly with a generalized and flexible diet

(Brown and Zunino 1990; Fragaszy et al. 1990). For instance Wallace et al. (1998)

noted no difference in group size and abundance of Cebus apella in 2 different

habitats, while Ateles was much more sensitive to habitat type. They explained the

almost ubiquitous presence of capuchins as due to their very generalized diet.

However, the same reasoning could apply to the marmosets. Marmoset diet is

generalized (Stevenson and Rylands 1988) and they can live in areas so modified and

degraded that no other neotropical primate can endure there (Moura, unpub. data).

Perhaps the similarity in relative abundance between marmosets and capuchins in the

cliff habitat was just a quirk of chance. Comparing the group size of primates in the

Caatinga with those from habitats not so severe and with a high availability of

resources, such as the Amazonian and Atlantic forest, could provide more meaningful

results and demonstrate how the harsh Caatinga environment affects the primates.

Capuchins, Marmosets, and Howlers: Generalists in the Caatinga Dry Forest

and the Ill fate of a Quasi-herbivorous Primate

Apparently the harsh condition of the Caatinga had a more deleterious effect on the

group size of howlers and marmosets than on capuchins.

Dvoskin et al. (2004) reported Alouatta caraya, with an average group size of 5.7

individuals in the Argentinean Chaco, while Zunino et al. (2001), in a more detailed



15/19

analysis in northern Argentina, found an average group size ranging from 3.5 to 12.4

individuals (n=61 groups). The values are far above those in the Caatinga (2.8

individuals/group).

One can generally explain the low group size of howlers in the Caatinga in terms

of availability of resources. Though howlers exhibit great flexibility in feedingstrategy (Chapman 1987), the leaves in the Caatinga forest, their main food resource,

are available only for a short period of time most trees are leafless in the dry

season and fruit production is low and practically limited to the rainy season.

Despite evidence suggesting that howlers can attain high densities in dry and highly

seasonal forest (Peres 1997b), in the Caatinga the erratic rainfall and long dry season

seem to play important roles in limiting their density. It is also possible that

interspecific competition with capuchins is responsible for their unusually small

group size. For instance, Zunino et al. (2001) observed the smallest average group

size for howlers in a forest that also contained Cebus apella and suggested thatinterspecific competition could be an important variable explaining low abundance

of howlers there. For the Caatinga, it is likely that a series of factors, i.e., low

availability of resources, habitat alteration, and perhaps competition with capuchins

contributed to the low density and small group sizes of howlers.

The small group size of marmosets in the Caatinga is more difficult to elucidate. It

is possible that their population had suffered a decline in the more recent past as a

result of a long period of drought (Gould et al. 1999), which is relatively common in

the Caatinga, leading to a prolonged crash in fruit production that caused mortalities.

Their small size may prevent them from moving to more favorable areas whenresources become scarce, as do many primates during food bottlenecks (Peres 1994),

and thus they are out-competed by capuchins. Their population is also under a strong

pressure by different predators, not only snakes and wild cats but also by capuchins.

To date, researchers have observed all species of capuchins preying on a range of

vertebrate species except other primates (Fedigan 1990; Rose 1997), but there is

anecdotal or indirect evidence that Cebus apella and Cebus capucinus might prey on

other primate species (Baldwin and Baldwin, 1977; Freese and Oppenheimer 1981;

Sampaio and Ferrari 2005). In an environment like the Caatinga it is possible that

capuchins could prey on marmosets, which fall in the body mass category (1 kg) of

typical mammalian prey of capuchins (Janson and Boinski 1992). Though I

observed no predation event, or found any remains of marmosets in 77 dung

samples from 6 different groups of capuchins, I noted that marmosets were always

nervous and fled in silence if a group of capuchins approached. All the factors could

lead to both local group extinctions and small group sizes, resulting in the overall

low density observed.

Researchers have linked variation in primate abundance among different types of

habitats to interspecific competition, predation, differences in plant composition and

structural heterogeneity of the habitat, hunting pressure, quality of food resources, and

historical factors (Butynski 1990; Brugiere et al. 2002; Cullen et al. 1999; Emmons

1984; Janson and Chapman 1999; Lopes and Ferrari 2000; Peres 1997a, b). However,

when a primate species such as Cebus apella exhibits similar abundance across a

series of habitats, even with great variability in forest structure and food availability,

invariably the most plausible explanation invoked is the litany of generalist food

habits (Bennet et al. 2001; Fragaszy et al. 1990; Wallace et al. 1998).



16/19

While one may use a generalized diet to explain abundance, it may not be the best

justification for similarity in group sizes of Cebus apella across habitats. Some

authors suggested that the use of palm nuts during periods of food scarcity is an

important factor sustaining capuchins in general, and particularly for Cebus apella

(Janson and Boinski 1992; Peres 1994; Spironello 1983, 2001; Terborgh 1983).However, SCNP was practically devoid of palm trees. In >5000 ha I noted only 3

palm trees (Copernicia sp.).

Further, though the density of capuchins for the area is low, it is nonetheless

similar to densities in some areas of the Atlantic forest and Amazonia (Chiarello

1999, 2000; Cullen et al. 2001; Peres 1997a). Why do capuchins in the harsh area

occur at a relatively similar density to those in areas of rain forest and why is their

group size unaffected by the low availability of food? Which strategies allow them to

survive there? It is likely that their capability to thrive in the Caatinga dry forest is a

consequence of their destructive foraging technique (Moura 2004) and also afunction of their cognitive abilities reflected in intensive use of tools to obtain

different types of food (Moura and Lee 2004).

Acknowledgments I thank Dr. P. C. Lee and 2 anonymous reviewers for helpful comments on the

manuscript and Rebecca C. Coles for a few suggestions. I thank Hilvaro M. Moreira and Felipe Alessio

for their assistance and companionship during the censuses. I also thank Niede Guidon for logistical

support that made this work possible and the Brazilian Research Council (CNPq) for the Ph.D.

scholarship.

References

Andrade-Lima, D. (1981). The Caatinga dominium. Revista Brasileira de Botnica, 4, 149153.

Baldwin, J. D., & Baldwin, J. I. (1977). Observations on Cebus capucinus in Southwestern Panama.

Primates, 18, 937941.

Bennett, C. L., Leonard, S., & Carter, S. (2001). Abundance, diversity and patterns of distribution of

primates on the Tapiche river in Amazonian Peru. American Journal of Primatology, 54, 119126.

Brown, A. D., & Zunino, G. E. (1990). Dietary variability in Cebus apella in extreme habitats: Evidence

for adaptability. Folia Primatologica, 54, 187195.Brugiere, D., Gautier, J.-P., Moungazi, A., & Gautier-Hion, A. (2002). Primate diet and biomass in relation

to vegetation composition and fruiting phenology in a rain forest in Gabon. International Journal of

Primatology, 23, 9991022.

Buckland, S. T., Anderson, D. R., Burnham, K. P., Laake, J. L., Borchers, D. L., & Thomas, L. (2001).

Introduction to distance sampling: Estimating abundance of biological populations. Oxford: Oxford

University Press.

Butynski, T. M. (1990). Comparative ecology of blue monkeys (Cercopithecus mitis) in high- and low-

density subpopulations. Ecological Monographs, 60, 126.

Carrillo, E., Wong, G., & Cuaron, A. D. (2000). Monitoring mammal populations in Costa Rican protected

areas under different hunting restrictions. Conservation Biology, 14, 15801591.

Ceballos, G. (1995). Vertebrate diversity, ecology, and conservation in neotropical dry forests.Seasonally

dry tropical forests pp. 195220. Cambridge: Cambridge University Press.

Chapman, C. A. (1987). Flexibility in diets of three species of Costa Rican Primates. Folia Primatologica,

49, 90105.

Chapman, C. A. (1990). Ecological constraint on group size in three species of neotropical primates. Folia

Primatologica, 55, 19.

Chapman, C. A., & Chapman, L. A. (1999). Implications of small scale variation in ecological conditions

for the diet and density of red colobus monkeys. Primates, 40, 215231.



17/19

Chiarello, A. G. (1997). Mammalian Community and Forest Structure of Atlantic Forest Fragments in

South-eastern Brazil. PhD. thesis, Cambridge, U.K. University of Cambridge.

Chiarello, A. G. (1999). Effects of fragmentation of the Atlantic forest on mammal communities in south-

eastern Brazil. Biological Conservation, 87, 7182.

Chiarello, A. G. (2000). Density and population size of mammals in remnants of Brazilian Atlantic forest.

Conservation Biology, 14, 1649

1657.Coimbra-Filho, A. F., and Camara, I. de G. (1996). Os limites originais do bioma Mata Atlntica na

regio Nordeste do Brasil. Rio de Janeiro: FBCN.

Coley, P. D., & Barone, J. A. (1996). Herbivory and plant defenses in tropical forests. Annual Review of

Ecology and Systematics, 27, 305335.

Cullen, L., Bodmer, E. R., & Valladares-Padua, C. (2001). Ecological consequences of hunting in Atlantic

forest patches, Sao Paulo, Brazil. Oryx, 35, 137144.

Defler, T. R. (1982). A comparison of inter-group behaviour in Cebus albifrons and C. apella. Primates,

23, 385392.

Dvoskin, R., Juarez, C. P., & Fernandez-Duque, E. (2004). Population density of black howlers (Alouatta

caraya) in the gallery forests of the Argentinean Chaco: A preliminary assessment. Folia

Primatologica, 75, 9396.

Emmons, L. H. (1984). Geographic variation in densities and diversities of non-flying mammals inAmazonia. Biotropica, 16, 210222.

Emperaire, L. (1984). A regiao da Serra da Capivara (sudeste do Piaui) e sua Vegetacao. Brasil Flor, 60,

421.

Fedigan, L. M. (1990). Vertebrate predation in Cebus capucinus: Meat eating in a Neotropical monkey.

Folia Primatologica, 54, 196205.

Fragaszy, D. M., Visalberghi, E., & Robinson, J. G. (1990). Variability and adaptability in the genus

Cebus. Folia Primatologica, 54, 114118.

Freese, C. H., & Oppenheimer, J. R. (1981). The capuchin monkeys, genus Cebus. Ecology and behavior

of neotropical primates, Vol. 1 pp. 331390. Rio de Janeiro: Academia Brasileira de Cincias.

Freitas, R. R., Rocha, P. L. B. da., & Simoes-Lopes, P. C. (2005). Habitat structure and small mammals

abundances in one semiarid landscape in the Brazilian Caatinga. Revista Brasileira de Zoologia, 22,119129.

FUMDHAM. (1998). Parque Nacional da Serra da Capivara. Fundao Museu do Homem Americano,

So Raimundo Nonato.

Gould, L., Sussman, R. W., & Sauther, M. L. (1999). Natural disasters and primate populations: The

effects of a 2-year drought on a naturally occurring population of ring-tailed lemurs (Lemur catta) in

Southwestern Madagascar. International Journal of Primatology, 20, 6984.

Izar, P. (2004). Female social relationships of Cebus apella nigritus in a southeastern Atlantic Forest: An

analysis through ecological models of primate social evolution. Behaviour, 141, 7199.

Izawa, K. (1980). Social behaviour of the wild black-capped capuchin (Cebus apella). Primates, 21,

443467.

Janson, C. H. (1984). Female choice and mating system of the brown capuchin monkey Cebus apella

(Primates: Cebidae). Zeitschrift fr Tierpsychologie, 65, 177200.Janson, C. H., & Boinski, S. (1992). Morphological and behavioral adaptations for foraging in generalist

primates: The case of the cebines. American Journal of Physical Anthropology, 88, 483498.

Janson, C. H., & Chapman, C. A. (1999). Resources and primate community structure.Primate

communities pp. 237267. Cambridge: Cambridge University Press.

Janson, C. H., & Di Bitetti, M. S. (1997). Experimental analyses of food detection in capuchin monkeys:

Effects of distance, travel speed and resource size. Behavioral Ecology and Sociobiology, 41, 1724.

Janzen, D. H., & Schoener, T. W. (1968). Differences in insect abundance and diversity between wetter

and drier sites during a tropical dry season. Ecology, 49, 96110.

Koenig, A. (1995). Group size, composition, and reproductive success in wild common marmosets

(Callithrix jacchus). American Journal of Primatology, 35, 311317.

Lacher, T. E., Fonseca, G. A. B. da, Alves, C., & Magalhaes-Castro, B. (1984). Parasitism of trees by

marmoset in a central Brazilian gallery forest. Biotropica, 16, 202209.

Lazaro-Perea, C., Snowdon, C. T., & Arruda, M. D. (1999). Scent-marking behavior in wild groups of

common marmosets (Callithrix jacchus). Behavioral Ecology and Sociobiology, 46, 313324.

Leal, I. R., Silva, J. M. C. da, Tabarelli, M., & Lacher, T. E. (2005). Changing the course of biodiversity

conservation in the Caatinga of northeastern Brazil. Conservation Biology, 19, 701706.

Lee, P. C., & Hauser, M. D. (1998). Long-term consequences of changes in territory quality on feeding

and reproductive strategies of vervet monkeys. Journal of Animal Ecology, 67, 3347358.



18/19

Lehman, S. M. (2000). Primate community structure in Guyana: A biogeographic analysis. International

Journal of Primatology, 21, 333351.

Lopes, M. A., & Ferrari, S. F. (2000). Effects of human colonization on the abundance and diversity of

mammals in eastern Brazilian Amazonia. Conservation Biology, 14, 16581665.

Machado, I. C. S., Barros, L. M., & Sampaio, E. V. S. B. (1997). Phenology of caatinga species at Serra

Talhada, PE, Northeastern Brazil. Biotropica, 29, 57

68.Mares, M. A., Willig, M. R., & Lacher, T. E. (1985). The Brazilian Caatinga in South American

zoogeography: Tropical mammals in a dry region. Journal of Biogeography, 12, 5769.

Mendes Pontes, A. R. (1999). Environmental determinants of primate abundance in Maraca island,

Roraima, Brazilian Amazonia. Journal of Zoology (London), 247, 189199.

Mendes Pontes, A. R., Normande, I. C., Fernandes, A. C. A., Ribeiro, P. F. R., & Soares, M. L. (2007).

Fragmentation causes rarity in common marmosets in the Atlantic forest of northeastern Brazil.

Biodiversity and Conservation, 16, 11751182.

Michalski, F., & Peres, C. A. (2005). Anthropogenic determinants of primate and carnivore local

extinctions in a fragmented forest landscape of southern Amazonia. Biological Conservation, 124,

383396.

Mitani, J. C., Struhsaker, T. T., & Lwanga, J. S. (2000). Primate community dynamics in old growth forest

over 23.5 years at Ngogo, Kibale National Park, Uganda: Implications for conservation and censusmethods. International Journal of Primatology, 21, 269286.

Moura, A. C. de A. (2004). The Capuchin Monkey and the Caatinga Dry Forest: A Hard Life in a Harsh

Habitat. Ph.D. thesis, Cambridge: Cambridge University.

Moura, A. C. de A., & Lee, P. C. (2004). Capuchin stone tool use in Caatinga dry forest. Science, 306, 1909.

Moura, A. C. D. A., & McConkey, K. R. (2007). The capuchin, the howler and the Caatinga forest: Seed

dispersal by monkeys in a threatened Brazilian biome. American Journal of Primatology, 60,

220226.

Murphy, P. G., & Lugo, A. E. (1986). Ecology of tropical dry forests. Annual Review of Ecology and

Systematics, 17, 6788.

Peres, C. A. (1988). Primate community structure in western Brazilian Amazonia. Primate Conservation,

9, 83

86.Peres, C. A. (1993). Structure and spatial-organization of an Amazonian terra-firma forest primate

community. Journal of Tropical Ecology, 9, 259276.

Peres, C. A. (1994). Primate response to phenological changes in an Amazonian terra firme forest.

Biotropica, 26, 98112.

Peres, C. A. (1997a). Primate community structure at twenty western Amazonia flooded and unflooded

forests. Journal of Tropical Ecology, 13, 381405.

Peres, C. A. (1997b). Effects of habitat quality and hunting pressure on arboreal folivore densities in neotropical

forests: A case study of howler monkeys (Alouatta spp.). Folia Primatologica, 68, 199222.

Peres, C. A. (1999). General guidelines for standardizing line transect surveys of tropical forest primates.

Neotropical Primates, 7, 1116.

Pinto, L. P. S., Costa, C. M. R., Strier, K. B., & Fonseca, G. A. (1993). Habitat, density and group size of

primates in a Brazilian tropical forest. Folia Primatologica, 61, 135143.Price, E. C., Piedade, H. M., & Wormell, D. (2002). Population densities of Primates in a Brazilian

Atlantic forest. Folia Primatologica, 73, 5456.

Reis, A. C. de S. (1976). Clima da Caatinga. Anais da Academia Brasileira de Cincias, 48, 325335.

Robinson, J. G., & Redford, K. H. (1986). Body size, diet, and population density of neotropical forest

mammals. American Naturalist, 128, 665680.

Rose, L. M. (1997). Vertebrate predation and food-sharing in Cebus and Pan. International Journal of

Primatology, 18, 727765.

Rylands, A. B. (1996). Habitat and the evolution of social and reproductive behavior in Callitrichidae.

American Journal of Primatology, 38, 518.

Sampaio, D. T., & Ferrari, S. F. (2005). Predation of an infant titi monkey (Callicebus moloch) by a tufted

capuchin (Cebus apella). Folia Primatologica, 76, 113115.

Sampaio, E. V. S. (1995). Overview of the Brazilian Caatinga. Seasonally dry tropical forests (pp. 3563).

Cambridge, U.K.: Cambridge University Press.

Schaller, G. B. (1983). Mammals and their biomass on a Brazilian ranch. Archivos de Zoologia, 31, 136.

Smith, R. J., & Jungers, W. (1997). Body mass in comparative primatology. Journal of Human Evolution,

32, 523559.

Sorensen, T. C., & Fedigan, L. M. (2000). Distribution of three monkey species along a gradient of

regenerating tropical dry forest. Biological Conservation, 92, 227240.



19/19

Spironello, W. R. (1983). Importancia dos frutos de palmeiras (Palmae) na dieta de um grupo de Cebus

apella (Cebidae, Primates) na Amazonia Central. A primatologia no Brasil, Vol. 3 (pp. 285296).

Belo Horizonte: Fundacao Biodiversitas.

Spironello, W. R. (2001). The brown capuchin monkey (Cebus apella): Ecology and home range

requirements in Central Amazonia. Lessons from Amazonia: The ecology and conservation of a

fragmented forest(pp. 271

283). New Haven, CT: Yale University Press.Stevenson, M. F., & Rylands, A. B. (1988). The marmosets, genus Callithrix. Ecology and Behaviour of

Neotropical Primates, Vol. 2 (pp. 79129). Washington: World Wildlife Fund.

Stevenson, P. R. (2001). The relationship between fruit production and primate abundance in neotropical

communities. Biological Journal of the Linnean Society, 72, 161178.

Terborgh, J. (1983). Five new world primates: A study in comparative ecology. Princeton, NJ: Princeton

University Press.

Thorington, R. W., Ruiz, J. C., & Eisenberg, J. F. A. (1984). A study of a black howling monkey (Alouatta

caraya) population in northern Argentina. American Journal of Primatology, 6, 357366.

van Schaik, C. P., Terborgh, J. W., & Wright, S. J. (1993). The phenology of tropical forests: Adaptive

significance and consequences for primary consumers. Annual Review of Ecology and Systematics,

24, 353377.

van Schaik, C. P., & van Noordwijk, M. A. (1989). The special role of male Cebus monkeys in predationavoidance and its effect on group composition. Behavioral Ecology and Sociobiology, 24, 265276.

Wallace, R. B., Painter, L. E., & Taber, A. B. (1998). Primate diversity, habitat preferences, and population

density estimates in Noel Kempff Mercado National Park, Santa Cruz Department, Bolivia. American

Journal of Primatology, 46, 197211.

Webb, K. E. (1974). The Changing Face of Northeast Brazil. New York: Columbia University Press.

Zhang, S. (1995). Sleeping habits of brown capuchin monkeys (Cebus apella) in French Guiana.

American Journal of Primatology, 36, 327335.

Zunino, G. E., Gonzalez, V., Kowalewski, M. M., & Bravo, S. P. (2001). Alouatta caraya: Relations

among habitat, density and social organization. Primate Report, 61, 3746.


2007 primate group siye an cde caatinga

Documents