flexibilidade comport a mental de macacos-prego

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Braz. J. Biol., 68(4): 685-693, 2008 685

Behavioral fexibility o a group o bearded capuchin monkeys

(Cebus libidinosus) in the National Park o Brasília (Brazil):

consequences o cohabitation with visitors

Sabbatini, G.a,b , Stammati, M.a,b , Tavares, MCH.c , and Visalberghi, E.b*

aDipartimento di Biologia Animale e dell’Uomo, Università di Roma “La Sapienza”,Viale dell’Università 32, 00185, Rome, Italy

bUnità di Primatologia Cognitiva, Istituto di Scienze e Tecnologie della Cognizione,Consiglio Nazionale delle Ricerche, Via Ulisse Aldrovandi 16/B, 00197, Rome, Italy

cLaboratório de Neurociências e Comportamento, Departamento de Ciências Fisiológicas – CFS,Instituto de Biologia – IB, Universidade de Brasilia – UnB,

CEP 70910-900, Brasilia, DF, Brazil

*e-mail: [email protected]

Received August 1, 2006 – Accepted February 16, 2007 – Distributed November 30, 2008

(With 4 gures)

Abstract

Increasing urbanization and deorestation have enhanced the opportunities o contact between humans and monkeysand the impact o human activities on primate behavior is receiving growing attention. This study explores whetheractivity budgets and diet o a group o capuchin monkeys (Cebus libidinosus) inhabiting the area o the swimmingpools o the National Park o Brasília is aected by the presence o visitors providing ood to them. During one year,both in the dry and the wet seasons, we scored capuchins’ behavior via scan sampling every ten minutes. Resultsshowed that this group spent less time oraging or wild oods than other comparable groups living in similar habitats.Moreover, capuchins relied more on human ood during the dry season, when pulpy ruits were less available, than inthe wet season. Our ndings conrm other studies on dierent monkey species that have shown that access to human

ood decreases the time spent oraging or wild ood and the home range size. They also show that capuchins are ableto modiy their diet, to exploit alternative ood sources, and to change their activity budget in response to the avail-ability o new ood opportunities and to seasonal ood availability.

Keywords: Cebus libidinosus, activity budgets, diet, human ood, seasonality.

Flexibilidade comportamental de um grupo de macacos-prego (Cebus libidinosus) no

Parque Nacional de Brasília (Brasil): conseqüências da convivência com os visitantes

Resumo

Recentemente, o impacto de atividades humanas sobre o comportamento de primatas tem recebido maior importânciadado o crescente desmatamento e urbanização, que têm avorecido o aumento do contato entre humanos e macacos.O presente estudo descreve os padrões de atividade e a dieta de um grupo de macacos-prego (Cebus libidinosus) quevive no Parque Nacional de Brasília. O Parque é reqüentado diariamente por visitantes, de modo que os animaisestão habituados à presença humana, bem como ao consumo de itens de sua dieta. Observações comportamentaisdo grupo oram realizadas ao longo de um ano, compreendendo a estação seca e a chuvosa, utilizando-se registro devarredura a cada 10 minutos. Resultados obtidos indicaram que o grupo despendeu menos tempo orrageando itensnaturais do que outros grupos vivendo em habitats similares. Além disso, durante a estação seca, quando há menordisponibilidade dos rutos de polpa, os macacos-prego alimentaram-se mais de itens da dieta humana como uma ontealternativa de recurso. Como demonstrado em estudos anteriores realizados com outras espécies de macacos, a ali-mentação baseada em itens da dieta humana pareceu diminuir a motivação dos animais para orragear no seu habitatnatural, assim como promoveu a redução do tempo gasto no orrageamento e a redução de sua área de uso. Nossosresultados indicaram ainda que o consumo de comida humana refete o caráter adaptável dos animais em explorarontes alternativas de recurso, bem como a sua habilidade em modicar a sua dieta e padrões de comportamento aceàs mudanças ambientais.

Palavras-chave: Cebus libidinosus, padrões de atividade, dieta, comida humana, sazonalidade.

ECOLOGY



Sabbatini, G. et al.

Braz. J. Biol., 68(4): 685-693, 2008686

included the area o the swimming pools o the Park andthe monkeys were used to visitors’ presence and to eatthe ood brought by visitors into the Park.

The rst aim o this study was to assess whether sea-sonal dierences in the availability o wild ood, 1 andwhether the presence and abundance o human ood (We

reer to the ood the monkeys nd in the orest as wildood, and to the ood brought by visitors to the Park, orbought by them into the Park, as human ood), aectedthe monkeys’ activity budgets and diet. To do so, we com-pared the diet and activity budgets in the dry and the wetseason and on the days in which human ood was scarce(when there were ew visitors) and days on which humanood was abundant (since there were many visitors).

The second aim was to examine whether relyingon human ood altered their activity budgets, diet andsubstrate use o our subjects. To do so we compared our

ndings with those reported in the literature or capuchinmonkeys living in similar habitats and acing compara-ble seasonal dierences in ood abundance, but that can-not rely on human ood as an alternative resource.

2. Material and Methods

2.1. Study area

The study was conducted in the Parque Nacional deBrasília, Brazil (15° 35’-15° 45’ S and 48° 05’-47° 53’ W).The Park has an area o 30,000 hectares, constituted o

typical scrub savanna (cerrado) and gallery orests, andis characterized by a tropical climate with two distinctseasons (Koppen’s Aw), the wet season (October toApril) and the dry season (May to September). Duringthe study period mean temperature was 21.9 °C (vary-ing rom 11.7 and 30.3 °C) and annual precipitation was1587.6 mm (1524.3 mm in the wet season and 63.3 mmin the dry season; data rom the Climatologic Station o the IBGE-RECOR Ecological Reserve, Brasília). ThePark is visited by almost 260,000 people per year (on-line IBAMA database). In particular, our study tookplace in an area where two natural swimming pools aresurrounded by semi-deciduous orest and paths; this areais requented by large groups o visitors or sports andleisure.

2.2. Subjects and data collection

Observations were made on a group o capuchinmonkeys that requented the area o the two swimmingpools (especially one) all year round. The group was ha-bituated to visitors’ presence and to eating human oodby obtaining it directly rom visitors, taking their leto-vers, or stealing it (Sabbatini et al., 2006). During the

study period, group size varied between 6 and 8 animalsdue to two births. Based on estimated age, subjects wereassigned to the ollowing age classes: inants (0-1 years),young (1-5 years) and adults (>5 years). The group con-sisted o one adult male, two adult emales, two youngmales, one young emale and two inants.

1. Introduction

The neotropical primate species Cebus libidinosus, ormerly considered a subspecies o Cebus apella, be-longs to the Cebidae amily, Platirrhinae inraorder(Groves, 2001). Cebus libidinosus is distributed in

Bolivia, northwestern Argentina, central and north-east Brazil, the Pantanal o Mato Grosso, and easternParaguay (Fragaszy et al., 2004). Capuchin monkeys livein a great variety o habitats. They are present in almostall tropical orest habitats, both rain orest and deciduousorest (Janson, 1985); capuchins can also live in limitedor secondary orest ragments, and do not excessively re-sent human presence (Hawkes et al., 1982). Capuchinsare omnivorous; their diet is constituted principally o ruits, but they also eat fowers, buds, roots, arthropods,small amphibians and reptiles, eggs, nestling birds andsmall mammals (Fragaszy et al., 2004). Capuchins’ eed-

ing techniques, that include complex and unusual ma-nipulative skills, allow them to exploit ood sources thatare not easily accessible to other primate species.

Behavioral fexibility is adaptive or coping withenvironmental change (Lee, 1991) and primates’ toler-ance to environmental change lies in the ability to locate,consume, and process adequate ood (Chivers, 1991).During periods o low resource availability, most specieso capuchins living in seasonal habitats modiy their diet,switching to alternative resources, and/or adopt behavio-ral strategies to enhance ood acquisition and reduce en-

ergy expenditure (e.g., Brown and Zunino, 1990; Peres,1994; Terborgh, 1983), and/or modiy group dimensionand individual distribution when oraging. When oodpatches are depleted or ood is scarce, capuchins ormsub-groups, which enable a better use o a large numbero dispersed small ood patches, and minimize travelcost and eeding competition (e.g., Phillips, 1995; Izar,2004), or exploit alternative ood types (e.g., Chapmanand Fedigan, 1990; Robinson, 1986).

Human ood, such as cultivated plants and garbage,can become part o monkeys’ diet (Lee et al., 1986;Richard et al., 1989) and aect their activity patterns

(Fa, 1986; Forthman Quick, 1986; Saj et al., 1999).Whereas the vast majority o the studies on the impact o human activities concern Old World monkeys, recentlythe capuchin monkeys’ behavior has received grow-ing attention in this respect (Galetti and Pedroni, 1994;Mikich, 2005; Siemers, 2000). In act, the development,urbanization and deorestation o South American coun-tries has enhanced the opportunities o contact betweenhumans and monkeys and aggressive interactions arebecoming common, especially with capuchins (Fragaszyet al., 2004; Mendes et al., 2005).

In this sense, we investigated the activity budgetsand diet o a group o wild capuchin monkeys living in asemi-deciduous orest in the National Park o Brasília. Inthis habitat, the amount o ood, especially ruit, changesthroughout the year, being less abundant in the dry sea-son than in the wet season. The capuchins’ home range



Behavioral fexibility o Cebus libidinosus

Braz. J. Biol., 68(4): 685-693, 2008 687

The data were collected between August 2003 andJuly 2004. Preliminary observations were made to ha-bituate the group to human observers and to ensure inter-observer reliability in identiying individuals and scoringbehaviors. Behavioral data were collected via 10 minutesscan sampling (Altmann, 1974) and samples were taken

in two dierent daytime blocks: one block was rom6:30 AM to 1:00 PM, the other rom 1:00 PM to dusk(6:00-6:30 PM). Sampling eorts in the two time blockswere uniormly distributed. Out o the 100 days in whichwe tried to track the group, 72 days resulted in group ol-lowing, or a total o 254 hours and 6,594 scan samples.Observers collected data on each individual’s location(in the orest or the swimming pool), ood types eaten,substrate height (height classes: 0 m; 0-5 m; 5-10 m;10-15 m; 15-20 m; >20 m) and behavior. The behavioralcategories scored were: Rest - animal stopped, lying orsitting down; Move: any spatial movement o the ani-mal; Feeding - the individual chews or swallows ood;Foraging - the individual holds, visually explores, snis,manipulates (digs, breaks, pounds, rips, rubs, peels), orbites a potential ood source; Social behavior - the in-dividual grooms, plays, perorms aliative/aggressivebehaviors; Human-capuchin interaction - the individualapproaches, contacts, or threatens a human being andvice versa.

Once a week, or one day, the swimming pool wasemptied or cleaning and the number o visitors andthe human ood potentially available to the monkeys

decreased dramatically. Observations were made bothwhen the swimming pool was ull o water (72.65%o scans) and when the pool was empty (23.35% o scans). The number o visitors present in the area wasestimated 2-3 times per day by two observers standingby the swimming pool that counted independently thenumber o visitors present in the swimming pool area.The two counts, that never diered more than 1-2 units,were successively averaged. The daily number o visitorswas calculated by averaging the 2-3 counts perormedduring the day. The number o visitors was closely re-

lated to the amount o human ood available or the mon-keys (Sabbatini and Stammati, pers. obs.), or the morevisitors were at the swimming pool the more ood waspresent in the garbage bins, or given to the monkeys, orcould potentially be stolen. Thereore, we will reer tothe days in which there were ew visitors as “scarce hu-man ood days” and to those in which they were many as“abundant human ood days”.

2.3. Data analysis

Proportions o scans devoted to the dierent activi-ties were calculated or each subject. Inants’ behavior

was considered only rom February 2004, when the new-borns were about six months old and began to behaveindependently rom their mothers.

To determine activity budgets we calculated the sumo the dierent activities or each individual by season(dry/wet) and according to whether the human ood

was abundant or scarce and then divided it by the totalnumber o scans recorded or each individual in the pe-riod considered. To assess dierences between activitybudgets and substrate height used in the wet and dry sea-sons, and when human ood was scarce or abundant, weused the Wilcoxon matched pairs test. To assess whether

time spent by capuchins in the orest and in the swim-ming pool area diered when human ood was scarceor abundant we perormed the χ2 test. Sex and age di-erences were analyzed by means o the Mann-WhitneyU test. To assess similarity between capuchins’ diet (interms o wild and human ood) during dry and wet sea-sons, and when human ood was scarce or abundant, weused Schoener’s index (1970) o diet overlap, that evalu-ates the percentage o diet similarity between periods ormonths.

3. Results

3.1. Visitor presence

During the dry season the mean number o visitorsper day was 178.28 (±20.95) and during the wet sea-son 95.93 (±23.02); these values were not statisticallydierent (N

1= 17; N

2= 81; t

96= 0.78; ns). When the

swimming pool was empty the mean number o visitorsper day was 15.47 (±0.49), while when the swimmingpool was ull, the mean number o visitors per day was128.80 (±26.05); these values were statistically dierent(N

1= 9; N

2= 89; t

96 = –2.37; p < 0.01).

3.2. Activity budgets, orest strata use and seasonality

Overall, as shown in Figure 1, or most o the time,capuchins moved (41%) and rested (15%). Foraging andeeding on wild and human ood (pooled) accounted ora total o 34% o scans, the majority o which concernedwild ood. Capuchins interacted with humans or 2%o scans and this value remained constant between sea-sons. Age dierences were evident or resting behavior:throughout the study period, adults rested signicantly

0

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45

S c a n s ( % )

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a n f o o d

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a n f o o d

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h a v i o u r

H u m a n - c a p u c h i n

i n t e r a c t i o n

Figure 1. Capuchins’ activity budgets throughout the studyperiod, as percent o 10 minutes scans.




Braz. J. Biol., 68(4): 685-693, 2008688

more than juveniles (Mann-Whitney test, U = 0; N1

= 3;N

2= 5; p < 0.05).During the wet season capuchins ate more wild ood

(Wilcoxon test, Z = 2.10; T = 3; N = 8; p < 0.05; seeFigure 2), while the opposite is true or human ood,that was eaten signicantly more during the dry season

(Wilcoxon test, Z = 2.38; T = 1; N = 8; p < 0.01). Duringthe wet season juveniles oraged signicantly morethan adults (Mann-Whitney test, U = 0; N

1= 3; N

2= 5;

p < 0.05) whereas during the dry season they sociallyinteracted more than adults (Mann-Whitney test, U = 0;N

1= 3; N

2= 5; p < 0.05).

Overall, as shown in Figure 3, capuchins spent most o their time between ground level and 5 m (51.86%) and dur-ing the dry season they used the substrates comprised be-tween 15 and 20 m signicantly more than during the wetseason (Wilcoxon test, Z = 1.99; T = 1; N = 8; p < 0.05).Sex and age did not infuence substrate height use.

3.3. Diet and seasonality

We observed capuchins eating 47 identied plantspecies, belonging to 29 dierent amilies (Table 1) anda variety o human oods, ranging rom ruits to sweetsand junk ood (Table 2). They devoted more time eatingwild than human ood (64.85% and 35.15% respectively;

1101 scans). Throughout the year capuchins ate inver-tebrates (grasshoppers, ants, spiders, butterfies, balmcrickets, larvae inside branches, etc.) and small verte-brates such as lizards, geckos, rogs, nestlings and bats.Sex and age did not aect time spent eating wild andhuman ood.

Season aected the type o ood eaten. Capuchinsate more human ood and seeds during the dry season(Wilcoxon test, Z = 2.38; T = 1; N = 8; p < 0.05 andZ = 2.20; T = 0; N = 8; p < 0.05, respectively) and ate moreruit and invertebrates during the wet season (Wilcoxon

test, Z = 2.38; T = 1; N = 8; p < 0.05 and Z = 2.20; T = 0;N = 8; p < 0.05, respectively). The most consumed wildoods during the dry season were fowers and ruits o Inga ingoides, the seeds o Luehea divaricata, the ruitso Copaiera langsdori, and o Ficus spp., and duringthe wet season the inforescences and inructescenceso Piper spp., the ruits o Zanthoxylum rhoiolium, o Psidium guajava, and o Ocotea sp., and invertebrates.Schoener’s diet overlap index between dry and wet sea-son was 46.89%.

3.4. Human ood and capuchins’ behavior

When human ood was scarce capuchins spent moretime in the orest than when human ood was abundant(χ2 with Yates’ correction = 16.04; d = 1; p < 0.001).In particular, the standardized residuals showed thatwhen human ood was scarce capuchins spent less timeby the swimming pool (standardized residuals = –2.20)and more time in the orest than expected (standard-ized residuals = 2.69). Thereore it is not surprising thatcapuchins ate signicantly more wild ood when humanood was scarce (Wilcoxon test, Z = 2.38; T = 1; N = 8;p < 0.05; see Figure 4).

When human ood was abundant, adults restedmore than juveniles (Mann-Whitney test, U = 0; N1

= 3;N

2= 5; p < 0.05) and were less involved in social interac-

tions than juveniles (Mann-Whitney test, U = 0; N1

= 3;N

2= 5; p < 0.05). When human ood was scarce, juveniles

oraged more on wild oods than adults (Mann-Whitneytest, U = 0; N

1= 3; N

2= 5; p < 0.05). Schoener’s diet

overlap index between the days in which human oodwas scarce and abundant was 69.59%.

4. Discussion

Seasonality o behavior and diet is common in wildcapuchins (Fragaszy et al., 2004). Our study extendedthese ndings by investigating how capuchins succeedin exploiting ood sources only recently introduced intotheir habitat, and that are not among those typically eatenby the species. The ability to incorporate human ood

Dry Wet

02550

75100125150175200225250275300

0 m 0-5 m 5-10 m 10-15 m 15-20 m > 20 m

N u m b e r o f s c a n s

*

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250

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e r o s

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**

*

Figure 2. Capuchins’ activity budgets during dry season(grey bars) and wet season (black bars), expressed as meannumber o scans (±standard error) in which each behaviorwas recorded. *p < 0.05; **p < 0.01.

Figure 3. Capuchins’ use o the orest strata during the dryseason (grey bars) and the wet season (black bars), expressedas average number o scans (±standard error). *p < 0.05.




Braz. J. Biol., 68(4): 685-693, 2008 689

Table 1. Natural oods eaten/oraged by the study group (data rom scan and ad libitum sampling).

Species Part

eaten*

Month** Density***

(ind.ha–1)

Percentage o

eeding records

Percentage

o oraging

records

ANACARDIACEAE

Mangiera indica Fr Nov., Jan.-Feb.W

- 0.36 0.56Tapirira guianensis Fr Sep.-Nov., Jan.B 196.80 1.82 -

ANNONACEAE

Xylopia sp. Fr Aug.D - - -unid. species Se Jan.-Feb.W - - -

BROMELIACEAE

Bromelia laciniosa Sp, Le Aug.-Sept., Apr.B - 1.0 0.65

Tillandsia sp. Le July, Mar.B - - -BURSERACEAE

Protium sp. Fr Aug.D

- - -CAESALPINACEAE

Bauhinia rua Se Sept.D 424.20 - -Copaiera langsdori Fr July-Aug.D 65.30 3.54 -

CECROPIACEAE

unid. species Le - - - -CLUSIACEAE

Calophyllum brasiliense Fr Jan.W 36.90 - -CYPERACEAE

Cyperus haspan Fr Jan.W

- - -HIPPOCRATACEAE

Cheiloclinium cognatum Fr Aug.D - - -LAURACEAE

Ocotea sp. - Nov.W - 1.82 0.09

Persea americana Fr Feb.W - - -LECYTHIDACEAE

Cariniana estrellensis Se July-Sept.D 147.70 0.36 8.53LEGUMINOSAE

Andira sp. Fr Aug.D

- - - Hymenea courbaril Fr Sept.D - - -unid. species Fl Apr.W - - -

MAGNOLIACEAE

Talauma ovata Se July-Aug., Jan.,Mar.-Apr., JuneB

65.30 0.82 2.22

MALPIGHIACEAE

Byrsonima laxifora Fr Sept.-Jan.B - 0.64 -MELASTOMATACEAE

Miconia chartacea Fr Sept.-Oct.B - 0.73 -MELIACEAE

Guarea sp. Fr Aug.D - - -MIMOSACEAE

Inga cylindrica Fr Nov.W 36.90 - -




Braz. J. Biol., 68(4): 685-693, 2008690

Species Part

eaten*

Month** Density***

(ind.ha–1)

Percentage o

eeding records

Percentage

o oraging

records

Inga heterophylla Fr Sept.-Nov.B - 1.18 0.09

Inga ingoides Fl, Fr July-Sept.,Nov.-Dec.B - 6.9 0.09

Inga sp. Fr Sept.D - - -MORACEAE

Ficus sp. 1 Fr Aug.-Sept.D 32.60 2.45 0.09Ficus sp. 2 Fr Apr.W 32.60 0.45 -

MYRSIANCEAE

Rapanea guianensis Fr Nov.W 65.30 1.36 -MYRTACEAE

Myrcia rostrata Fl Dec.W 163.20 0.09 - Myrcia tomentosa Fr, Fl Sept., Nov.-Jan.B 456.90 0.09 -Psidium guajava Fr Nov.-Mar.W - 5.63 1.30

Syzygium jambolana Fr Jan.W - 0.27 -PALMAE/ARECACEAE

Acrocomia aculeata Fr Aug.-Sept., Apr.B - - 0.09

Syagrus romanzoana Fr Aug.D - - -PASSIFLORACEAE

Passifora sp. 1 - Nov.W - 0.36 0.28

Passifora sp. 2 - Feb.W - - 0.19

PIPERACEAE

Piper sp. 1 Inf, Inr Aug.-Apr.B 65.30 4.54 1.48Piper sp. 2 Inf, Inr Aug.-Apr.B - 1.82 -

POACEAE

Olyra latiolia Le, Pi July-Sept., Dec.-Jan., Mar.-Apr.B

- 1.36 0.83

unid. species Le Mar.W - 0.18 -RUTACEAE

Zanthoxylum rhoiolium Fr Feb.-Mar.W 32.60 5.54 1.85SAPOTACEAE

Chrysophyllum

marginatum

Fr Aug.-Oct.B 163.20 0.73 -

SOPHOREAE

Ormosia paraensis Se July-Aug.D - - 0.19

TILIACEAE

Luehea divaricata Se, Fl Aug.-Sept.,Mar.-Apr.B

- 3.81 0.37

VOCHYSIACEAE

Vochysia tucanorum Fr Aug.D - - -

Invertebrates - Aug.-JulyB

- 5.00 52.27Vertebrates - Oct., Jan.-Apr.W - 0.54 0.56

Unid. natural ood 11.35 6.67

*Fr = ruit, Se = seed, Fl = fower, Inf = inforescence, Inr = inrutescence, Le = lea, Sp = sprout, Pi = pith; **W = wetseason, D = dry season, B = both seasons; and ***Data rom Ramos (1995).

Table 1. Continued...




Braz. J. Biol., 68(4): 685-693, 2008 691

into the diet is evidence o behavioral fexibility sinceit requires overcoming the initial avoidance response(Visalberghi et al., 2003).

Seasonality as well as human ood aected the dietand activity budget o the group o bearded capuchinmonkeys living in the Brasília National Park. Duringthe dry season capuchins ate more human ood, fowersand seeds than in the wet season, during which they atemore ruits and invertebrates. In act, in semi-deciduousorests pulpy ruits are less abundant than in wet or-ests (Morellato and Leitão-Filho, 1992) and this lowerood availability prompts capuchins to nd alternativestrategies to ulll their energy requirements. Galettiand Pedroni (1994) also ound seasonal dierences inthe diet o capuchins living in a semi-deciduous orestin South-Eastern Brazil. Recently, Moura (2004) arguedthat Cebus libidinosus living in the very dry caatinga

overcame ood shortage using tools to eat tubers andpalm nuts; the alternative strategy developed by ourcapuchins was to exploit human ood.

The use o the dierent orest strata is aected bythe vegetation structure and by the availability o oodat dierent heights. Capuchins are described as main-

ly arboreal monkeys using the medium and low oreststrata (Fleagle et al. 1981; Terborgh 1983), but theysometimes show a wide use o the orest foor (Siemers,2000; Moura, 2004). In particular, Siemers (2000) re-ported that the main actor that avored the presence o

capuchins in the orest foor during the dry season wasthe higher availability o ood dropped by humans on theground. During the dry season, our capuchins used thelowest height classes more than in the wet season alsoin the area o the swimming pools, since by staying atthose heights, they enhanced the opportunities to obtainhuman ood. Our results also showed that during thedry season they used the substrates comprised between15 and 20 m signicantly more. An explanation or thiscould be that during the dry season capuchins oragedat 15-20 m on trees o Cariniana estrellensis, a species

whose very hard and thick pericarps are morphologicaladaptations to protect their atty and protein-rich seedsrom predators. Capuchins overcame the seed protec-tion mechanism using very hard substrates to bang theruits on. Capuchins not only banged the ruit against thetree as reported by Peres (1991), but requently took thealready allen ruits, that they banged on articial sub-strates, such as concrete sidewalks. The latter type o ood processing increased the time that capuchins spenton the ground in the dry season.

Table 3 reports the activity budgets o capuchinso the National Park o Brasília and those o other wildCebus libidinosus groups reported in the literature. Thepercentage o time devoted to the dierent activities arerather similar across study sites, with the exception o oraging: our capuchins oraged and ed on wild oodto a lesser extent than other wild capuchins living in theother sites where human disturbance was lower, or non-existent. In particular, the percentage dedicated to orag-ing by our group is smaller than reported or the group o similar dimension studied by Vilela (2003) in a protectedsemi-deciduous orest area near Brasília. Since the majorecological dierence between these groups is the pres-

ence o visitors and visitors’ ood, this nding stronglysupports the idea that human ood aects capuchins’ ac-tivity budget.

Our ndings conrm those already reported or oth-er monkey species relying on human ood as a resource(Forthman Quick, 1986; Lee et al., 1986; O’Leary and

Table 2. Articial oods eaten/oraged by the study group

Food type Percentage o eeding records Percentage o oraging records

Fruit juice/sot drinks 1.91 2.13

Sweets (candy, cookies, cakes) 3.91 1.67

Fruit 11.08 3.61

Milk and by-products 1.82 0.37Corn, sugar cane 3.27 1.02

Cooked oods, sauces, snacks 8.63 2.41

unid. human ood 4.45 10.29

R e s t

M o v e

F e e d w i l d f o o d

F e e d h u m a n f o o d


F o r a g e h u m a n f o o d

S o c i a l b e h a v i o u r



0

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90

S c a n s ( % )

Scarce human food days

Abundant human food days

**

Figure 4. Capuchins’ activity budgets during days in which

visitors and their ood were scarce (grey bars) and in whichvisitors and their ood were abundant (black bars), expressedas mean percent o scans (±standard error) in which each be-havior was recorded. * p < 0.05.




Braz. J. Biol., 68(4): 685-693, 2008692

Table 3. Activity budgets o wild groups o Cebus libidinosus.

Species Habitat Group

size

Move

(%)

Rest

(%)

Feeding

(%)

Foraging

(%)

Social

behavior

(%)

Source

Cebus libidinosus Semi-deciduoustropical orest

8 41 15 17* 17* 8 Present study

Cebus libidinosus Semi-deciduoustropical orest

7 38 14.5 18 29.5 - Vilela (2003)

Cebus libidinosus Dry tropicalorest

10 37.1 ~5.5 19.6 22.3 ~ 6.5 Moura (2004)

*Data on eeding and oraging behaviors reers to human and wild ood pooled.Although Vilela (2003) and Moura (2004) labelled the species studied Cebus apella libidinosus, according to a new taxo-nomy, capuchins living in those areas are considered Cebus libidinosus.

Fa, 1993; Saj et al., 1999). In act, our results showedthat capuchins decreased the time spent oraging andmodied the target o their ood searches mostly whenthe visitors were present and the possibility o eatingtheir ood arose. Since the majority o the interactionsinvolved the presence o ood (Sabbatini et al., 2006), weargue that the time spent interacting with visitors by thecapuchins (2%) can be considered a sort o oraging.

Another actor aecting capuchins’ behavior is thenumber o visitors: capuchins spent more time in the or-est and ate more natural oods when human ood wasscarce than when it was abundant. In act, when therewere less visitors and less human ood available, our

group o capuchins ed more on natural ood sources andinteracted less with humans.In conclusion, the consumption o human ood we

documented refects the adaptability o capuchins to ex-ploit alternative concentrated and abundant ood sources(Terborgh, 1983) and their ability to modiy their diet andbehavioral patterns in response to changing environmen-tal conditions. As Forthman Quick (1986) suggested, thenature o costs and benets, spatial and temporal distri-bution, seasonality, age composition are all actors con-tributing to alterations in activity patterns. In our case,the ood provided more or less directly by visitors was

preerred because o being easy to obtain and digest, andwas very likely with a higher caloric content than mostnatural ood. Although chemical analyses o wild and ar-ticial ood eaten by our capuchins were not carried out,human ood has been reported to be more energetic thanwild ood eaten by monkeys (e.g., Lee et al., 1986; Fa,1986; Saj et al., 1999; Muruthi et al, 1991). Moreover,human ood represents a staple ood source during pe-riods o natural ood shortage, its spatial concentrationand the abundance in the swimming pool area modiedactivity budgets and possibly restricted the ranging pat-

tern. Research contributing to knowledge o the impacto humans’ presence on animal behavior should be takeninto account by Park administration when allowing peo-ple to visit and enjoy natural environments.

Acknowledgements — We thank the National Park o Brasíliaand, in particular, the director Dr E. M. da Silva Jr or permission

to conduct eldwork and to use the Park’s accommodation.We thank the Universidade de Brasília and all the people atthe Laboratorio de Neurociências e Comportamento or theircollaboration. We are grateul and indebted to P. Pinha, I. Wagaand R. T. Souza or their help in the eld observations anddata collection, and to Pro. L. M. Breyer (Depto de Botânica,Instituto de Biologia, UnB) and Dr E. S. G. Guarino (Deptode Zoologia, Instituto de Biologia, UnB) or the help withbotanical species identication. A special thanks to Pro. P.Izar and an anonymous reviewer or their useul comments onearly versions o the manuscript. G. Sabbatini received nancialsupport orm the Università “La Sapienza” di Roma and romthe Centro Studi Etologici-Ethoikos (LIBCSE 01/2004), M.Stammati received nancial support rom the Università “La

Sapienza” di Roma. Research Fund was granted by UnB/IBEdital Royalties 2003 and FINATEC.

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