terrestrial activity in pitheciins (cacajao, chiropotes...

American Journal of Primatology 74:1106–1127 (2012)

RESEARCH ARTICLE

Terrestrial Activity in Pitheciins (Cacajao, Chiropotes, and Pithecia)ADRIAN A. BARNETT1,2∗, SARAH A. BOYLE3,4, MARILYN M. NORCONK5, SUZANNE PALMINTERI6, RICARDO R.SANTOS7, LIZA M. VEIGA8,9, THIAGO H.G. ALVIM10, MARK BOWLER11, JANICE CHISM12, ANTHONY DI FIORE13,EDUARDO FERNANDEZ-DUQUE14, ANA C. P. GUIMARAES8, AMY HARRISON-LEVINE15, TORBJØRNHAUGAASEN16, SHAWN LEHMAN17, KATHERINE C. MACKINNON18, FABIANO R. DE MELO10, LEANDRO S.MOREIRA10, VIVIANE S. MOURA10, CARSON R. PHILLIPS19, LILIAM P. PINTO20,21, MARCIO PORT-CARVALHO22,ELEONORE Z. F. SETZ23, CHRISTOPHER SHAFFER24, LIVIA RODRIGUES DA SILVA25, SULEIMA DO S. B. DASILVA26, RAFAELA F. SOARES8, CYNTHIA L. THOMPSON27, TATIANA M. VIEIRA8, ARIOENE VREEDZAAM28,SUZANNE E. WALKER-PACHECO29, WILSON R. SPIRONELLO2, ANN MACLARNON1, AND STEPHEN F. FERRARI301Centre for Research in Evolutionary and Environmental Anthropology, Roehampton University, London, England2Biodiversity Unit, National Institute for Amazonian Research, Manaus, Amazonas, Brazil3Department of Biology, Rhodes College, Memphis, Tennessee4Biological Dynamics of Forest Fragments Project, National Institute for Amazonian Research and Smithsonian TropicalResearch Institute, Manaus, Amazonas, Brazil5Department of Anthropology, Kent State University, Kent, Ohio6Centre for Evolution, Ecology and Conservation, School of Environmental Sciences, University of East Anglia, Norwich,Norfolk, United Kingdom7Centre of Agrarian and Environmental Sciences, Federal University of Maranhao, Chapadinha, Maranhao, Brazil8Post-graduate Program in Zoology, Museu Paraense Emilio Goeldi, Belem, Para, Brazil9Department of Zoology, Museu Paraense Emilio Goeldi, Belem, Para, Brazil10Research-Aid Foundation, Federal University of Goias, Goiania, Brazil11Department of Psychology, University of St. Andrews, St. Andrews, Scotland12Department of Biology, Winthrop University, Rock Hill, South Carolina13Department of Anthropology, University of Texas at Austin, Austin, Texas14Department of Anthropology, University of Pennsylvania, Philadelphia, Pennsylvania and Centre for Applied LitoralEcology (Conicet), Argentina15Department of Anthropology, University of Colorado – Boulder, Boulder, Colorado16Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, Norway17Department of Anthropology, University of Toronto, Toronto, Ontario, Canada18Department of Sociology and Criminal Justice, Saint Louis University, St. Louis, Missouri19School of Natural Resources and Environment, Florida Museum of Natural History, University of Florida, Gainesville,Florida20Postgraduate Ecology Course, Institute of Biology, Campinas State University, Campinas, Sao Paulo, Brazil21National Center for Amazonian Biodiversity Research and Conservation, Chico Institute for Biodiversity Conservation,Manaus, Amazonas, Brazil22Sao Paulo Forestry Institute, Bauru Experimental Station, Sao Paulo, Brazil23Animal Biology Dept., State University of Campinas, Campinas, Sao Paulo, Brazil24Department of Anthropology, Washington University in St. Louis, St. Louis, Missouri25Post-graduate School, Biology Department, Federal University of Amazonas, Manaus, Amazonas, Brazil26Wild Animal Reproduction Laboratory Institute of Biological Sciences, Federal University of Para, Para, Brazil27Department of Anatomy & Neurobiology, Northeast Ohio Medical University, Rootstown, Ohio28Advanced Teachers Training Institute of Suriname, Leysweg 5, University of Suriname Campus, Paramaribo, Surinameand Green Heritage Fund, Suriname29Department of Sociology and Anthropology, Missouri State University, Springfield, Missouri30Department of Biology, Federal University of Sergipe, Sao Cristovao, Sergipe, Brazil

Neotropical monkeys of the genera Cacajao, Chiropotes, and Pithecia (Pitheciidae) are considered tobe highly arboreal, spending most of their time feeding and traveling in the upper canopy. Until now,the use of terrestrial substrates has not been analyzed in detail in this group. Here, we review thefrequency of terrestrial use among pitheciin taxa to determine the ecological and social conditions thatmight lead to such behavior. We collated published and unpublished data from 14 taxa in the threegenera. Data were gleaned from 53 published studies (including five on multiple pitheciin genera)and personal communications of unpublished data distributed across 31 localities. Terrestrial activitywas reported in 61% of Pithecia field studies (11 of 18), in 34% of Chiropotes studies (10 of 29), and36% of Cacajao studies (4 of 11). Within Pithecia, terrestrial behavior was more frequently reported

∗Correspondence to: Adrian A. Barnett, Roehampton University–CREEA, Holybourne Avenue, London SW15 4JD, United Kingdom.E-mail: [email protected] 6 November 2011; revised 27 June 2012; revision accepted 2 July 2012

DOI 10.1002/ajp.22068Published online 28 August 2012 in Wiley Online Library(wileyonlinelibrary.com).

C© 2012 Wiley Periodicals, Inc.

Pitheciin Terrestriality / 1107

in smaller species (e.g. P. pithecia) that are vertical clingers and leapers and make extensive use ofthe understory than in in the larger bodied canopy dwellers of the western Amazon (e.g. P. irrorata).Terrestrial behavior in Pithecia also occurred more frequently and lasted longer than in Cacajaoor Chiropotes. An apparent association was found between flooded habitats and terrestrial activityand there is evidence of the development of a “local pattern” of terrestrial use in some populations.Seasonal fruit availability also may stimulate terrestrial behavior. Individuals also descended to theground when visiting mineral licks, escaping predators, and responding to accidents such as a droppedinfant. Overall, the results of this review emphasize that terrestrial use is rare among the pitheciinsin general and is usually associated with the exploitation of specific resources or habitat types. Am. J.Primatol. 74:1106–1127, 2012. C© 2012 Wiley Periodicals, Inc.

Key words: behavior; pitheciids; primates; terrestrial

INTRODUCTIONWhile some extinct New World primates may

have been exclusively, predominantly, or partiallyterrestrial [Rosenberger et al., 2009], all livingNeotropical species are highly adapted for an arbo-real lifestyle [Heymann, 1998]. Nevertheless, thereare examples of terrestrial use among severalplatyrrhines suggesting that coming to the ground isa response to specific local environmental factors. Po-tential causes for such interpopulational differencesinclude habitat fragmentation [Cebus olivaceus:Fragaszy, 1986], specialized foraging adaptations[Cebus apella: Haugaasen & Peres, 2009; Cebus li-bidinosus: Spagnoletti et al., 2009], use of minerallicks [e.g. Ateles belzebuth: Link et al., 2011a,b], co-foraging with other (primarily terrestrial) mammals[e.g. Cebus apella and Nasua nasua: Haugaasen &Peres, 2008], and the relaxation of predation pres-sure [Brachyteles hypoxanthus: Mourthe et al., 2007;Ateles spp.: Campbell et al., 2005].

In other Neotropical primate populations, terres-trial activity may be an established, but infrequentelement of the behavioral repertoire, and is almostinvariably related to the execution of three mainactivities—the retrieval of food items [Cebus apellaand Saimiri sciureus, Silva & Ferrari, 2009], move-ment between discontinuous substrates [Alouattacaraya, Bicca-Marques & Calegaro-Marques, 1995;Brachyteles arachnoides: Dib et al., 1997], and spe-cific social behaviors, such as play and resting[Brachyteles hypoxanthus: Tabacow et al., 2009]. Theuse of terrestrial mineral licks is a characteristic ofthe behavior of many Amazonian atelids, for exam-ple [Campbell et al., 2005; Link et al., 2011a,b], andthe retrieval of arthropod prey from the leaf litter isa typical behavior in callitrichids [e.g. Garber, 1992;Yoneda, 1984]. With the exception of retrieving fooditems and minerals from the ground, some terres-trial activities are associated with changes in habi-tat structure or plant community composition due tohuman activities. As a result, these changes may berelatively recent [see Tabacow et al., 2009].

The subfamily Pitheciinae encompasses threegenera of medium-sized platyrrhines (adult body

weight range 2–4.5 kg). Collectively known as“pitheciins,” these primates are extremely (Cacajaoand Chiropotes), or quite strongly (Pithecia), special-ized dentally for the predation of immature seeds[Kinzey, 1992; Norconk et al., 2009; Rosenberger,1992; Teaford & Runestad, 1992]. The larger-bodiedgenera, Cacajao (uacaris) and Chiropotes (beardedsakis or cuxius, hereafter “cuxius” giving preferenceto the local common name throughout much of thegeographic range of this genus: Barnett et al., inpress-a), tend to inhabit the middle to upper strata ofthe forest, through which they move using a mixtureof quadrupedal climbing and leaping along horizon-tal substrates [Walker, 1996, 2005]. A key differencebetween the genera is the occupation of flooded for-est ecosystems by many uacari populations, whichmay place additional limitations on the potentialfor terrestrial behavior. The smallest sakis (Pitheciapithecia) typically use lower to middle strata whentraveling, which may be related to their morpholog-ical specializations for vertical clinging and leaping[Walker, 2005]. Other Pithecia species (e.g. P. albi-cans, P. irrorata, P. monachus) occupy higher forestcanopy levels, are more quadrupedal, and more oftenleap and land horizontally (Janice Chism, unpub-lished data vide Swanson-Ward and Chism, 2003;Anthony Di Fiore and Eduardo Fernandez-Duque,unpublished data vide Di Fiore et al., 2007). With thepossible exception of P. irrorata, which may feed pre-dominantly on hard fruits [Palminteri, 2010], sakistend to have a more diverse diet that includes ahigher proportion of ripe fruit and young leaves thanuacaris and cuxius [Norconk, 2011].

In addition to their tendency to occupy the mid-dle and upper forest strata, the dietary preference ofpitheciins for immature seeds may also reduce theirpotential for terrestrial behavior, given that imma-ture fruit are much less likely to fall to the groundthan ripe fruit. Furthermore, a number of recentstudies have shown that pitheciins are more flexiblein both behavioral [Barnett, 2010; Boyle & Smith,2010; Thompson & Norconk, 2011; Veiga, 2006]and ecological terms [Boyle et al., 2009, 2012; Nor-conk, 1996; Port-Carvalho & Ferrari, 2004; Silva &

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1108 / Barnett et al.

Ferrari, 2009] than previously thought [e.g. Johns& Ayres, 1987]. As such, the exploitation of ter-restrial resources, and moving between fragmentedhabitats, may contribute to an increase in the prob-ability of terrestrial activity. It is therefore possi-ble that, within the studied genera, those who spendmore time in strata closer to the ground may be thosethat are also more terrestrially active.

While raptors appear to be the principal threat toplatyrrhines in trees [Barnett et al., 2011; Ferrari,2009; Hart, 2007], attacks by ground-based, scan-sorial, predators (e.g. ocelots, jaguars, tayras) havebeen documented [see Bezerra et al., 2011; Bianchi &Mendes, 2007; Olmos, 1994; Peetz et al., 1992]. Fur-thermore, Matsuda and Izawa [2008] witnessed pre-dation by jaguars on spider monkeys when they wereon the ground. Thus, risk of predation may reducethe incidence of coming to the ground for arborealplatyrrhines. Indeed, foraging [Ferrari, 2009; Stone,2007], diurnal resting [Wright, 1998], and frequencyof terrestrial play [Tabacow et al., 2009] have beenshown to be sensitive to the perceived level of pre-dation risk. Terrestrial activity may therefore be ex-pected to occur more often in areas where predatorsare either naturally infrequent, or reduced becauseof human impacts such as hunting or habitat modi-fication. Other limiting factors may include habitatstructure and the spatial distribution of resources.

Though specialists in immature seeds, pitheci-ins track the availability of food resources and mayswitch to other food classes as the availability of fruitfluctuates (e.g. flowers, insects, or leaves: Norconk,2011; Veiga & Ferrari, 2006]. In other primates, di-etary transitions are often accompanied by a shiftingto habitats that are not usually frequented or by pro-cessing foods differently [e.g. Furuichi et al., 2001;Marshall et al., 2009]. Such items are often termedfall-back foods [Lambert, 2010], and though not nec-essarily nutritionally poor [Hanya et al., 2006], aregenerally used when phenological gaps result in anabsence of more typical dietary items [Wranghamet al., 1998]. Marked temporal changes in food avail-ability are especially common in areas where rainfallis strongly seasonal. Since fallen fruit may persiston the ground long after it is available in trees [e.g.Forget, 1992], it is possible that terrestrial behaviorin pitheciins may peak in the dry season and/or whenfew other food resources are available.

Although terrestrial activity in pitheciines is fre-quently observed in captivity (Fig. 1), it is rarely ob-served in the wild. To investigate why, we extractedbehavioral data from pitheciine field studies to ob-tain an overview of the patterns of terrestrial be-havior in this platyrrhine group. On the basis of thearguments presented above, we predicted terrestrialbehavior would be:

(1) More common in species spending more time inthe lower strata of the forest canopy.

Fig. 1. Pitheciines can engage in terrestrial activity, but do sorarely in the wild (Photo: L.C. Marigo, Cacajao calvus rubicun-dus semicaptive at Amazon Ecopark, Manaus, Brazil).

(2) Observed more commonly in habitats with fewerpredators.

(3) Recorded more frequently during seasons whenthe availability of preferred or standard di-etary components (fruits and leaves on trees) isrestricted.

METHODSWe collated data on 14 pitheciin taxa from 31

study sites (Fig. 2), and grouped terrestrial activ-ities noted during these studies into the follow-ing categories: feeding, drinking, play, nonplay so-cial behavior, antipredator behavior, and dispersal.

Am. J. Primatol.


Fig. 2. Map of the 31 study sites represented in this review: (1) Yasunı National Park, Napo Province, Ecuador; (2) Pacaya SmiriaNational Reserve, Loreto Peru; (3) Quebrada Blanca Biological Station, Ucayali, Peru; (4) Tamshiyacu-Tahuayo Area of RegionalCommunal Conservation, Ucayali, Peru; (5) Lago Preto, Rıo Yavari, Ucayali, Peru; (6) Los Amigos Conservation Concession, Madre deDios, Peru; (7) Mosiro Itajura (Caparu) Biological Station, Rıo Apaporis, Vaupes, Colombia; (8) Rıo Pasimoni, Amazonas, Venezuela;(9) Bebador, Pico da Neblina National Park, Amazonas, Brazil; (10) Upper Urucu River, Amazonas, Brazil; (11) Teiu Lake, Mamiraua,Solimoes, Amazonas, Brazil; (12) Amana Lake, Amana Sustainable Reserve, Solimoes, Amazonas, Brazil; (13) Lago Guri, Bolıvar,Venezuela; (14) Barcelos region of middle Rio Negro, Amazonas, Brazil; (15) Uauacu Lake, Rio Purus, Brazil; (16) Rio Jau, JauNational Park, Amazonas, Brazil; (17) Biological Dynamics of Forest Fragments Project, Amazonas, Manaus, Brazil; (18) Bosque deCiencias and INPA campus, Manaus, Amazonas, Brazil; (19) Rio Aripuana, Tapajos, Para, Brazil; (20) Turtle Mountain, Iwokrama,Essequibo, Guyana; (21) Upper Essequibo Conservation Concession, Guyana; (22) Timehri District, Guyana; (23) Cristalino PrivateReserve, Brazil; (24) Raleighvallen-Voltzberg Nature Reserve, Sipaliwini District, Suriname; (25) Brownsberg Nature Park, Broko-pondo District, Suriname; (26) Saraca-Taquera National Forest, Para, Brazil; (27) Tapajos, Rio Tapajos National Forest, Para, Brazil;(28) Barrage de Petit-Saut, Sinnamary river basin, Saint-Elie, French Guiana; (29) Tucuruı Hydroelectric Dam Lake, Para, Brazil;(30) Fazenda Martirinho, Maranhao, Brazil; and (31) Gurupı Biological Reserve, Maranhao, and eastern Para, Brazil (a complex offive sites in the region).

Because many uacaris inhabit flooded forests, we in-cluded activities that involve contact with the sur-face of groundwater, such as the retrieval of floatingfruits and drinking while suspended pedally frombranches. Falling to the ground was not included be-cause it is not considered an intentional act.

As none of the studies focused specifically onterrestrial behavior, procedures varied considerably,which impeded statistical analysis. However, to al-low comparison among similar studies [i.e. Campbellet al., 2005], we calculated hourly rates of terrestrialbehavior whenever possible or appropriate. Whenexamining the likely factors responsible for the ob-served frequency of terrestrial activity at each site,we considered dry season intensity, hunting pres-sure, and level of habituation. However, these vari-ables had not always been quantified by the inves-tigators and, when they had, very different method-ologies had been used. In consequence, we relied on

qualitative estimates of these three factors made bythe researchers for each of their respective study lo-calities. Though clearly less desirable that quantifiedbases, we consider it an improvement on both no esti-mates and on collating post-hoc quantifications, thesecond of which would have provided only an illusorylevel of accuracy.

As terrestrial activity is rarely reported in pub-lished studies, the current review relies on a consid-erable amount of unpublished data collected duringstudies from which other results have already beenpublished. Such data are cited as “[unpublished data,vide Author’s name, year]”.

Taxonomic note: The Latin name for Cacajaospecies follows Hershkovitz [1987], since the pre-cise appellation for some members of the genusis currently disputed [vide Boubli et al., 2008;Ferrari et al., 2010]. The intrageneric taxonomy ofChiropotes is also in flux: though it is clear that there

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are different taxa east and west of the Rio Branco,Roraima State, Brazil, the correct names for themcontinue to be debated [compare Bonvicino et al.,2003 with Silva Jr. & Figueiredo, 2002 and Veiga etal., 2008]. Here, we denote populations west of theRio Branco with a dagger (†) in the text and tables,while populations east of the Rio Branco are markedwith an asterisk (*). This research adhered to theAmerican Society of Primatologists ethical principlesfor the study of primates.

RESULTSUacaris (Cacajao spp.)

Uacaris are unique among the platyrrhines intheir degree of preference for flooded forests, al-though many populations inhabit terra firme forestsseasonally or year round [see Heymann & Aquino,2010]. Despite this, available data (Table I) suggesta tendency for uacaris occupying terra firme foreststo be less terrestrial than those in seasonally floodedhabitats. Of these cases, six were observations of an-imals in contact with aquatic substrates.

The lack of published records of terrestrial usefor the Peruvian red uacari, Cacajao calvus ucay-alii (Table I) is reemphasized by personal commu-nications from Sara Bennett, Richard Bodmer, andPablo Puentes, who have all conducted many yearsof fieldwork within its range, and have never en-countered these animals on the ground, although R.Bodmer [personal communication] received a reportfrom a student who had observed an animal comingto the ground to escape an agonistic encounter witha conspecific. As if to further emphasize the lack ofterrestrial behavior in this species, Bowler and Bod-mer [2011] regularly observed Cebus albifrons andSaimiri sciureus—but never Cacajao c. ucayalii—descending to the ground at Lago Preto, Peru, toretrieve fallen Mauritia flexuosa (Arecaceae) fruits,even when the uacaris were part of the same mixed-species group. Nearby on the Rio Tahuayo, JaniceChism [unpublished data] also noted uacaris remain-ing in trees while syntopic Saimiri descended to theground to forage. Similarly, in an 18-month fieldstudy in igapo, terra firme, and caatinga habitatsthe Pico de Neblina region of northeastern BrazilianAmazonia, Jean-Philippe Boubli [unpublished data,vide Boubli, 1997] did not observe terrestrial activityby either uacaris or cuxius.

During the only long-term study of white uacari(Cacajao c. calvus), Ayres [1986] recorded monkeyscoming to the ground during periods of fruit scarcity(the low water season) to feed on germinating seeds.However, Helder Queiroz [personal communication]has conducted some 30 months of fieldwork in thesame area (Mamiraua), and has never witnessed ter-restrial behavior in these uacaris. Similarly, JoaoValsecchi and Nayara Cardoso have surveyed both

C. c. calvus and C. c. rubicundus extensively inMamiraua and neighboring areas since 2001 [e.g.Vieira et al., 2009], and have never observed terres-trial behavior, although most of these surveys wereconducted during high water, and on unhabituatedanimals.

In contrast, there are several records of ter-restrial behavior in the golden-backed uacari, Ca-cajao melanocephalus ouakary (Table I). Barnett[2010] observed the predation of germinated seedsof four tree species (Eschweilera tenuifolia, Lecythi-daceae; Leopoldinia pulcra, Areceae; Pouteria ele-gans, Pouteria sp., Sapotaceae) at low water, a be-havior apparently similar to that recorded by Ayres[1986]. Eschweilera tenuifolia, a high-ranked uacarifood [Barnett, 2010], was the most commonly eatendiet item. The uacaris were extremely wary when onthe ground, and almost invariably retired to perchon a branch or buttress root to process the food. De-fler [2004] has observed similar behavior in Colom-bia (Fig. 2). Barnett [2010] also observed uacarisretrieving Aldina heterophylla fruits from the sur-face of a river while suspended from overhangingbranches by their rear legs during periods of highwater. Bruna Bezerra [unpublished data, vide Bez-erra et al., 2011] observed uacaris drinking water inthe same fashion and, on another occasion, an an-imal was forced to swim to safety after the branchsupporting it broke. Marcela Oliveira [unpublisheddata, vide Barnett et al., in press-b] did observethis species briefly on the ground. Barnett [2005] re-ported that uacaris raid turtle nests at low water onthe Rio Negro. In summary, most references to ter-restrial use by uacaris are related to seasonal short-ages of arboreal foods (or possibly changes in foodpreferences?). There was only one observation of ter-restrial behavior related to social avoidance. Noneof the uacari studies took place on island habitatswhere predation pressure might be different frommainland habitats. The rate of terrestrial use in thesingle uacari study that directly recorded terrestrialuse was 0.102 events/hour.

Bearded Sakis or Cuxius (Chiropotes spp.)Records of systematic terrestrial behavior are

restricted to Chiropotes chiropotes*, Chiropotes sa-tanas, and Chiropotes utahickae (Table II ).

At Tucuruı, cuxius dispersed distances of up to400-m across land bridges during low water peri-ods [Liza M. Veiga, unpublished data, vide Veiga,2006], or moved terrestrially between trees on asmall island [Suleima Silva, unpublished data]. Chi-ropotes satanas also has been observed to descendhaltingly to the ground to retrieve fallen Attaleafruits [Marcio Port-Carvalho, unpublished data],and such terrestrial fruit collection also occurredrelatively frequently during polyspecific associationswith tufted capuchins (Cebus apella) and squirrel

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imal

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nt

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l(1)

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into

[200

8]

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hir

opot

es†

(wes

tof

the

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)

13:D

anto

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chad

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ri(V

enez

uel

a)

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rafi

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nd,

180

ha)

Non

e15

mon

ths

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ata,

vid

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,200

1]

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ri(V

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rafi

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st(r

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nd,

180

ha)

Non

e17

mon

ths

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(199

6)

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ri(V

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a)

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rafi

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nd,

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ths

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and

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zey

[199

4]

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tof

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iolo

gica

lD

ynam

ics

ofF

ores

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ents

Pro

ject

(Bra

zil)

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rafi

rme

fore

st(c

onti

nu

ous

and

frag

men

ts)

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imal

17m

onth

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e–

Boy

lean

dS

mit

h[2

010]

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gica

lD

ynam

ics

ofF

ores

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ents

Pro

ject

(Bra

zil)

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mar

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rra

firm

eco

nti

nu

ous

fore

st

Min

imal

12m

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zao

[199

2]

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urt

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tain

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e,G

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mar

yte

rra

firm

efo

rest

atre

serv

oir

Non

e11

mon

ths

2N

one

–W

righ

tet

al.[

2009

]

21:U

pper

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ibo

Con

serv

atio

nC

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ssio

n,

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yan

a

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mar

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ract

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s(3

);F

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[201

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ary

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man

[vid

eL

ehm

an,2

004a

,20

04b]

Am. J. Primatol.


TA

BL

EII

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onti

nu

ed.

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nti

ng

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onpr

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en

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rest

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uen

tor

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beh

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erve

rT

axon

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.2)

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itat

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)(n

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)n

oda

ta)

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eren

ce)

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ure

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(Su

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ure

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mon

ths

4F

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ing

(1),

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y(1

)–

Vre

edza

am[v

ide

Boi

nsk

iet

al.,

2005

]

24:R

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berg

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ure

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erve

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rin

ame)

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mar

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eco

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stM

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al28

mon

ths

1N

one

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nR

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etal

.[1

988]

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ure

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rin

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one

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and

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zey

[199

4]

25:B

row

nsb

erg

Nat

ure

Par

k(S

uri

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e)

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mar

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eco

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nu

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al13

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ths

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gory

[201

1]

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ure

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nu

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inim

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ths

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e4

Gre

gory

[200

6]

25:B

row

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ure

Par

k(S

uri

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e)

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eco

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nu

ous

fore

stM

inim

al12

wee

ks3.

5F

orag

ing

(1);

Oth

er(1

)4

Nor

con

ket

al.[

2006

]

26:S

arac

a-T

aqu

era

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ion

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ores

t(B

razi

l)

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mar

yte

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firm

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al11

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es(4

);F

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(1);

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isan

ce-

avoi

dan

ce(1

);U

nce

rtai

nca

use

(1)

3M

elo

etal

.[20

10]

C.s

atan

as29

:Bas

e4,

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razi

l)P

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11]

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va&

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rari

[200

9]

Am. J. Primatol.


TA

BL

EII

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onti

nu

ed.

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nti

ng

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seas

onpr

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rein

ten

sity

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erve

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ta)

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eren

ce)

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ase

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zil)

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firm

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rest

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,300

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2)3

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006]

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ase

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ucu

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(Bra

zil)

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mar

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firm

efo

rest

frag

men

t(1

,300

ha)

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imal

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anto

s[2

002]

29:J

oao

Isla

nd,

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curu

ı(B

razi

l)P

rim

ary

terr

afi

rme

fore

st(i

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d19

ha)

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imal

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onth

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pers

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ala

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nt

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6;V

eiga

&F

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ri,i

npr

ess]

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azen

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ho

Ter

rafi

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igh

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g(1

)3

M.P

ort-

Car

valh

o[v

ide

Por

t-C

arva

lho

&F

erra

ri,

2004

]31

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rupı

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logi

cal

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erve

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tern

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ing

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uen

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,200

0]

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l)

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9h

a)

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imal

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San

tos

[200

2]

aF

orcu

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orth

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eA

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onR

iver

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vaJr

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dF

igu

eire

do[2

002]

prop

osed

that

indi

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als

east

ofth

eR

ioB

ran

cosh

ould

beca

lled

Ch

irop

otes

sagu

latu

s(T

rail

l,18

21)a

nd

thos

eto

the

wes

tof

that

rive

r,C

.ch

irop

otes

,wh

ile

Bon

vici

no

etal

.[20

03]

sepa

rate

dth

emin

toC

.ch

irop

otes

and

C.i

srae

lita

,res

pect

ivel

y.D

espi

teth

eu

nce

rtai

nti

esov

erth

esp

ecie

sn

ame,

supp

orti

ng

evid

ence

show

sth

ere

are

two

dist

inct

popu

lati

ons

ofcu

xiu

sn

orth

ofth

eA

maz

onR

iver

:ata

wn

yto

brow

nba

cked

from

the

Rio

Bra

nco

toth

ew

est

(†)

and

are

ddis

hba

cked

from

the

Rio

Bra

nco

toth

eea

st(* )

.Bec

ause

ofth

is,w

eh

ave

dist

ingu

ish

edth

emin

this

tabl

e.

Am. J. Primatol.


monkeys, Saimiri sciureus [Guimaraes, 2011; Veiga& Ferrari, in press]. Vieira [2005] observed Chi-ropotes utahickae coming to the ground to re-trieve Endopleura uchi (Humiriaceae) and Annonatenuipes (Annonaceae) fruits, the latter sometimesoccurring during associations with capuchins andsquirrel monkeys. While retrieval of fruits accountedfor most of the observations of C. satanas and C.utahickae on the ground, both species also havebeen seen eating “geniparana” (Gustavia augusta:Lecythidaceae) and drinking lake water while sus-pended by their feet in a manner similar to thatobserved in Cacajao [Ricardo Santos, unpublisheddata, vide Santos, 2002; Suleima Silva, unpublisheddata, Liza Veiga, unpublished data, vide Veiga,2006]. At Saraca-Taquera National Park, Para, Thi-ago Alvim and colleagues [Melo et al., 2010] recordedseven instances of terrestrial activity in Chiropoteschiropotes*. During a foraging bout, a group of sevenadults (2M, 5F) and a juvenile were recorded for-aging on the ground for more than 15 min, for im-mature Duckesia verrucosa (Humiriaceae) fruits (themonkeys’ previous foraging activities in the parenttree having caused the fruit to fall to the forestfloor). The single-seeded fruits of D. verrucosa aresome 6-cm long and have seeds protected by a sclero-tized endocarp, implying extended processing timefor each fruit. During the 15-min terrestrial forag-ing bout, animals spent 10–20 sec selecting a fruitfrom the ground, retreating to a branch to processit, and then repeating the process. Three examplesof within-group aggression were also recorded: inone, a male and female chased another male to theground and proceeded to bite him for over a minute.The male ran 20 m along the ground with an openwound on his foot, being chased by the male and fe-male. The event lasted 6 min and 35 sec. In the sec-ond, the observer encountered two animals, clearlyin an aggressive interaction, running on the ground4 m apart. After the aggressor returned to the trees,the other 10 members of the subgroup descended towithin 2 m of the ground and vocally mobbed the ag-gressed animal (an adult female). Two other eventsinvolved a single animal running along the ground(for a distance of 10 m and 30 m) following aggressiveinteractions in the canopy. In a third event, an adultwas seen running along the ground for some 10 m:although the cause was unknown the many vocal-izations in the canopy indicated an aggressive inter-action may recently have occurred. During a 15-minintergroup encounter, two adult males attacked anadult female who ran 30 m along the ground beforeclimbing a tree. The seventh event involved a nestof bees that the group accidentally disturbed whileforaging. This generated many alarm calls and ani-mals could be seen manually fanning their faces toward off the insects. One individual avoided them byjumping to the ground and running there for some20 m.

At Cristalino Nature Private Reserve, MattoGrosso, Brazil, Rafaela Soares was observing a 9-strong group of C. albinasus (3 M/4 F/1 YF-youngfemale/1 FF-female with baby) feeding on seeds ofan understory Bignoniaceae, when two adult maleswho had been playing together fell from 5 m, sat onthe ground hugging each other for a few seconds andthen walked quickly along the ground for a minutebefore ascending a liana, rejoining the group andbeginning to feed [Soares, unpublished data; videSasaki et al., 2010; Soares, 2011]. This does notfit the definition of terrestrial activity used in thispaper. However, as the study area is strictly pro-tected, hunting unrecorded in recent times and theanimals highly habituated by dint of ecotourist activ-ity, this example is therefore included to show thattrue terrestrial activity in this species appears to begenuinely rare. That the population at Crisalino ap-pears to strongly avoid terrestrial activity is under-scored by observations that, while in mixed groupswith Cebus apella, red-nosed cuxius will use thelower strata of the forest, but a female C. albina-sus did not retrieve a fallen infant from the groundeven though it was barely yet capable of independentlocomotion.

At Brownsberg Nature Park, Suriname,Katherine MacKinnon [unpublished data, videNorconk et al., 2006] twice observed Chiropoteschiropotes* on the ground. Once four animals wereobserved eating fallen fruit, most likely naturallyByrsonima crassifolia (Malpighiaceae). On thesecond occasion, 2+ C. chiropotes were presenton the ground, but ran up a tree as soon as theyperceived the human observer. The animals on theground had been silent, and remained so as theyfled. Other troop members gave a whistle alarm call,and remained silent as they ascended. At nearbyRaleighvallen-Voltzberg Nature Reserve, CarsonPhillips [vide Phillips, 2008] observed two instancesof Chiropotes chiropotes* on the ground. This dryseason observation occurred while a lone male wastravelling with a group of Saimiri scuireus. Theassociation lasted for a week. As the S. scuireusforaged for insects in dry bamboo leaves the maleC. chiropotes was observed on two occasions toaccompany them, though it was not clear if he alsoforaged. As part of an extended study of Saimiriand Cebus at the same site [unpublished data, videEhmke, 2004; Kauffman, 2004], Arioene Vreedzaamencountered lone juvenile male Chiropotes chi-ropotes* who travelled with mixed S. scuireus-C.apella group (some 50 individuals of each species)for 2 days and accompanied them in their terrestrialactivities. Bouts of terrestrial activity up to 10-minlong were recorded. These included both foragingand play, in the latter case the young C. chiropotesattempted to engage even though it was some threetimes larger than the Saimiri. Diet items eaten bythe Chiropotes were not recorded, but, like C. apella

Am. J. Primatol.


and S. scuireus, C. chiropotes was seen to rummageamong dry fallen leaves.

At the Upper Essequibo Conservation Conces-sion, Guyana, Chris Shaffer [unpublished data, videShaffer, 2012] recorded 8 instances of terrestrial be-havior in C. chiropotes*. Three were quite brief (some10–15 sec) and occurred during agonistic interac-tions between two or three adult males of the samegroup. In these, one male was chased down the trunkof the tree onto the ground, and along the ground,and then up another tree. No physical contact wasobserved. In one case, a male intervened during acopulation between another male and a female, thenproceeded to chase the male who had been copulat-ing. Similar chasing was observed during an inter-group encounter. In this case, three males from onegroup chased a single male from another group. Thechasing lasted for more than 15 min, with repeatedbouts of terrestrial behavior. It was preceded byalarm calling as the groups approached each other.A fourth instance occurred during an attempted at-tack by a harpy eagle (H. harpyja). As the eagleswooped down, all of the cuxius jumped to lower ver-tical strata while alarm calling. Most group memberssettled into dense vegetation in the understory, re-maining there for 8 min before returning to canopy.

In all of the instances reported above, the indi-viduals appeared to go to the ground as a last re-sort, in an attempt to escape. However, Shaffer alsorecorded four cases where individuals appeared com-fortable on the ground. In one of these, a female andjuvenile playing in the lower canopy, ran down a treeto the ground some 3 m away from the observer, andcontinued playing on the ground for 6 min, before re-turning to the canopy. Three instances of terrestrialinsectivory also were observed. One of these involvednine individuals who searched through dead leavesand bark from fallen trees for 15 min. Another in-volved four individuals for 10 min, and the third twoindividuals for 5 min. In all cases, the terrestrialindividuals represented only a small portion of thegroup, almost all of whom were foraging for insects.Shaffer noted that the terrestrial animals appearedto use foraging techniques similar to those used bythe other individuals in the group who were foragingin the understory.

Martins et al. [2005] observed C. utahickae de-scending to the ground to avoid an attack by a harpyeagle, Harpia harpyja. The only terrestrial behaviorobserved in the other Chiropotes species was the re-trieval of an infant by its mother, seen once each inC. albinasus and C. satanas (Table II). This can beconsidered a random event, however, rather than asystematic behavior.

As in some uacari reports, cuxius at two siteshave been observed remaining in the trees eventhough capuchins and squirrel monkeys in thesame mixed-species groups retrieved fruits from theground (Attalea and Orbygnia) [Santos, 2002; Silva

& Ferrari, 2009], and these fruits represented a di-etary staple for cuxius. At a third site [Boyle &Smith, 2010], Chiropotes chiropotes* did not cometo the ground to forage or disperse, even thoughsympatric capuchins (Cebus apella) and tamarins(Saguinus midas) did so. On the rare occasions whenChiropotes has been observed coming to the groundto forage, the behavior involves extreme caution andalmost invariably, a rapid retreat to a higher perch.Overall, while terrestrial activity does occur in Chi-ropotes, it does not appear to have any major ecolog-ical role.

In summary, terrestrial activities in cuxiu wererelated to retrieving food and for purposes of disper-sal, with the proviso that both populations inhab-ited artificial islands or peninsulas in the Tucuruıreservoir. The cuxius were well habituated to hu-man observers, although Boyle’s study groups alsowere well habituated and some of her study groupsinhabited forest fragments. She, however, did notobserve terrestrial habitat use. Neither it was ob-served by Soares in her well-habituated group (evento the extent of not retrieving a fallen infant), nor itwas clearly very rare in Chiropotes at Raleighvallen.As in the case of uacaris, wild cuxius appear to bemore reticent to come to the ground for food than ca-puchins and squirrel monkeys; even where humanhunting is not known to occur (e.g. Shaffer’s site inGuyana). The rate of terrestrial use in cuxius studiesranged from 0.002 to 0.111 events per hour, with amean rate of 0.034 events per hour.

Sakis (Pithecia spp.)The data on sakis (Table III) indicate that ter-

restrial behavior was recorded in more than halfof the studies. Pithecia pithecia is clearly the best-studied pitheciin species, and the fact that a thirdof field studies failed to record terrestrial behav-ior suggests that the absence of records for somespecies (Table III) may be partly related to dura-tion of study, degree of habituation, and site-specificcharacteristics (e.g. mineral licks, insect eating, is-land habitats). Thus, while a long-term study of P.monachus [Soini, 1986] did not record terrestrial use(Table III), Happel [1982] observed P. monachus(identified in litt. as P. hirsuta) visiting a terrestrialmineral lick during her much briefer fieldwork.

Three studies [Di Fiore et al., 2005; Harrison,1998; Suzanne Palminteri, unpublished data] havereported terrestrial foraging for insects (Fig. 2). In P.aequatorialis [A. Di Fiore and E. Fernandez-Duque,unpublished data: vide Di Fiore et al., 2005], andP. irrorata (Fig. 3), the preys were army ants them-selves (Ectoninae) rather than any insects or smallvertebrates that the ants had disturbed. This con-trasts with the pattern typically reported in cal-litrichids [e.g. Rylands et al., 1989] and formicariidbirds [Willis & Oniki, 1978]. Di Fiore et al. [2005]

Am. J. Primatol.

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Am. J. Primatol.


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Am. J. Primatol.


Fig. 3. Terrestrial foraging by Pithecia irrorata, southern Ama-zonian Peru (Photos: Edgard Collado).

observed that insect-feeding bouts could last formore than an hour, with the sakis spending muchof their time close to the ground and making briefterrestrial forays to capture the ants. In P. pithecia[Harrison-Levine et al., 2003] the prey were largeacridid grasshoppers (Tropidacris spp.), and this be-havior represented the single most frequent recordof terrestrial behavior in the pitheciins, a total of 126events. The sakis spent an average of 8.8 sec on theground to capture each grasshopper, but invariablyascended to branches above 3 m from the ground toconsume their prey [Harrison-Levine et al., 2003].

Retrieval of fruits or seeds from the forest floorwas observed in a number of P. pithecia, studies,and, as in the other genera, the pattern of behav-ior was a rapid retreat to a high branch for pro-cessing. Walker [2005] observed P. pithecia feedingextensively on fallen Capparis muco (Cappariaceae)and Chrysophyllum (Sapotaceae) fruits, which con-tributed 2.5% of total feeding records. This speciesalso has been observed feeding extensively on fallenLicania (Chrysobalanaceae) discolor fruits at thesame site [Harrison, 1998; Norconk, 1996], and in

French Guiana [Vie et al., 2001]. The study sitesin Venezuela and French Guiana were islands sur-rounded by water, the result of inundation duringdam creation. In the Colosso forest fragment in theBDFFP (Biological Dynamics of Forest FragmentsProject) near Manaus, Brazil, Eleonore Setz [unpub-lished data, vide Setz, 1993] observed a male P. pithe-cia coming to the ground to retrieve a Duguetia lati-folia (Annonaceae) fruit dropped by the adult female.

Other isolated cases of terrestrial behavior inP. pithecia include locomotion between fragmentsof forest [Shawn Lehman, unpublished data, videLehman, 2004a, 2004b], drinking at the edge of areservoir [Harrison, 1998], the avoidance of an at-tack by a harpy eagle, and an agonistic encounterwith conspecifics [Vie et al., 2001]. In a long-termstudy on a small BDFFP fragment, E. Setz [unpub-lished data] observed juveniles falling to the groundon two occasions, while the mother watched, but didnot descend to assist. On a number of occasions,the same study group also crossed at least 300 m ofshrub-filled pasture to move between fragments. Ontwo other occasions, a juvenile, unable to cross a gapin the canopy by leaping, called for assistance and,when none arrived, descended to the ground to movebetween trees. A subadult male of this same groupwas observed following the group on the ground dur-ing two consecutive days [A.M. Calouro, personalcommunication], and was presumed to be sick or in-jured. It did not rejoin the group and presumablydied.

In P. albicans, one animal was observed brieflychasing another to the ground from the lower canopy,where further chasing and a brief fight occurredbefore both returned to the canopy [Torbjørn Hau-gaasen, unpublished data, vide Haugaasen & Peres,2005]. Chases in which individuals descended tothe ground (i.e. chased to the ground or fell froma tree and ran along the ground) during territo-rial encounters also were observed in P. pitheciain both Venezuela (Lago Guri) [Norconk, 2011] andSuriname (Brownsberg) [Norconk, unpublisheddata: vide Norconk et al., 2006].

Social interactions on or near the ground involv-ing play were documented in two P. pithecia studies.In P. pithecia, E. Setz [unpublished data: vide Setz,1993] recorded 106 play events—including chasingand slapping hands on the ground—during 500 hr ofmonitoring. At Brownsberg Nature Park, Suriname,8 of 30 bouts of juvenile play in 2007 occurred onthe ground [K. Talbot and M. Norconk, unpublisheddata]. Bouts lasted up to 33 min (mean 21 min) andwere significantly longer than the more numerousarboreal play bouts (mean 9.3 min). Cynthia Thomp-son [unpublished data, vide Thompson & Norconk,2011] also observed play in P. pithecia at this site.The play would entail locomoting and hopping onthe ground between small trees (where they clung ina posture typical of a Vertical Clinger and Leaper,

Am. J. Primatol.


sensu Napier, 1967), "pinning" their playmate tothe ground, and "wrestling" (for lack of better de-scriptors). Such bouts lasted between 5 and 20 min-utes. Thompson’s study group would regularly reuse-specific travel paths, and would predictably locomoteon the ground when crossing the same paths. In ad-dition, a juvenile was observed to take cover on theground under some brush when a hawk was sightedand alarm calls were given by other group members.On another occasion an adult male was seen runningon the ground from a predator threat, and two ter-restrial chasing events were seen as a result of inter-group encounters. Thompson twice observed feedingon the seeds of Vouacapoua americana (Fabaceae)the ground. Feeding on this species initially occurredin trees only, but appeared to switch to ground for-aging later in the feeding season when more of thefruits had dropped to the ground (and presumably,fewer where left still on the tree, though quantitativedata on this was not collected). Bouts involved theentire group and lasted some 10 minutes. Thomp-son also observed P. pithecia feeding on fruits andflowers of Passifloraceae vines located at or near theground.

In P. irrorata, Palminteri [unpublished data,vide Palminteri, 2010] recorded a single bout of ter-restrial play that lasted approximately 10 min. Thisis the only example of this behavior in any of theother four saki species.

At other sites, however, terrestrial use is ei-ther absent or so rare as to be unrecorded. For ex-ample, at Iwokrama International Centre, Guyana,where Alouatta maconnelli and Ateles paniscus haveboth been observed crossing open savannah betweenforested areas [B. and K. Wright, unpublished data,vide Wright et al., 2009], sympatric Pithecia havenever been seen on the ground.

In summary, among pitheciins, sakis providethe most extensive and diverse information on useof terrestrial habitats, with terrestrial activity re-ported most consistently in P. pithecia. Several char-acteristics of saki species and the habitats in whichthey live may have influenced terrestrial activities.First, among Pithecia species, P. pithecia uses thelowest strata of the forest extensively [Norconk,2011; Walker, 1996]. Second, two studies (Lago Guri,Venezuela, and a BDFFP fragment, Brazil) tookplace in small forest islands or fragments. The so-cial groups in these two studies were very well ha-bituated and were the subjects of long-term stud-ies. Third, the Lago Guri study took place in astrongly seasonal habitat that resulted in periodsof strong food- and water-shortage [Cunningham &Janson, 2007; Norconk, 1996]. Additionally, the ani-mals clearly could not easily leave the islands and somay have been forced to adopt other foraging strate-gies. The very sparse information from other Pithe-cia species, even when they are well habituated (e.g.Di Fiore and Palminteri studies), suggests that their

TABLE IV. Mean per Hour Rate of Terrestrial ActivityObserved

Mean per hourlySpecies Study observation ratea

Cacajao m. ouakary Barnett [2010] 0.102Chiropotes albinasus Pinto [2008] 0.002Ch. chiropotes Melo et al. [2010] 0.0072Ch. chiropotes Shaffer [2012] 0.014Ch. satanas Guimaraes

[2011], mainlandgroup

0.010

Ch. satanas Veiga [2006],mainland group

0.111

Ch. satanas Veiga [2006],island group

0.004

Ch. utahickae Vieira [2005] 0.008Pithecia irrorata Palminteri [2010] 0.003P. pithecia Thomson and

Norconk [2011]0.0046

P. pithecia Walker [2005] 0.058P. pithecia Norconk [vide

Norconk et al,2003]

0.062

P. pithecia Vie et al. [2001] 0.002P. pithecia Harrison [1998] 0.165P. pithecia Setz [vide Setz,

1993]0.220

aNumber of events divided by the number of observation hours.

preference for higher forest strata limits their ac-cess to (and possibly interest in) the ground. Fur-thermore, the finding of frequent play activities onthe ground in free-ranging sakis of Brownsberg Na-ture Park in Suriname (a continuous habitat), sug-gests that forest fragmentation is not a necessarycriterion for the observation of terrestrial behaviorin this species. Fourth, the rate of terrestrial use insaki studies ranges from 0.003 to 0.22 events/hour,average 0.0845 (Table IV). However, this figure doesnot take into account the fact that typical contactwith the ground is brief and entails picking up aninsect or a brief tussle during play.

Because of differing methods used by authors instudying pitheciin species, it was only possible to cal-culate hourly rates of terrestrial behavior for a smallsubset of the studies analyzed here (Table IV). As-suming a daily activity period of 12 hr, an hourly rateof 0.083 events would represent an average rate ofterrestrial behavior of once per day per group. This,value was surpassed in only four studies, suggest-ing that terrestrial behavior is neither a commonnor a regular occurrence in pitheciins. This is espe-cially so given that it was extremely rare for all groupmembers to be on the ground at the same time, andthat most bouts of terrestrial behavior were brief andhighly context specific.

Am. J. Primatol.


TABLE V. Concordance of Results and Predictions

Prediction Concordance

Terrestriality will be more common in speciesthat spend more time in the lower strata of theforest canopy.

Some firm support: High canopy sakis (e.g. P.irrorata) engaged in terrestrial activity, as didCacajao spp. and Chiropotes spp. However, thegreatest number of terrestrial behavior events wasrecorded for P. pithecia, the pitheciine that spendsmore time in lower strata than any other. In thisspecies there may be a predisposition to regard theground as a supplementary feeding source.

Terrestriality will be observed more commonlyin habitats where there were fewer predators.

Equivocal support: Terrestriality was regularlyobserved at sites where predator pressure waspresumed low (forest fragments, islands indam-created lakes), but actual predator densitieswere not quantified, so terrestriality may have beendue to other factors (e.g. food availability). Also,terrestrial behavior (including both foraging andplay) was recorded in primary habitats wherepredator densities expected to be high.

Terrestriality will be recorded more frequentlyin seasons when the availability of thestandard components of the diet were limited(effectively that terrestriality occurs whenspecies descend to the ground to accessfall-back foods).

Some firm support: It may be the case for Cacajaofeeding on germinating seedlings, and Pitheciafeeding on seeds from fallen fruits; however, thelatter was recorded most frequently in environments(such as artificially created islands) where foodavailability may be highly restricted in some monthsdue to the reduced tree diversity. Seasonality doesnot appear to explain the insectivory recorded inthree saki species. This foraging appears to bepurely opportunistic, taking advantage of a proteinsource whenever it occurs.

Meeting PredictionsWe found some support (Table V) for the predic-

tions that terrestriality will occur more frequentlyin: (1) species spending more time in lower foreststrata; (2) habitats with fewer predators; and (3) sea-sons when the availability of standard dietary com-ponents are limited.

DISCUSSIONTerrestrial behavior is rare in pitheciins, and

even when contact with the ground occurs, it is usu-ally brief. It has been recorded in all three genera,but not in all species, and in fewer than half the stud-ies analyzed here. Nevertheless, it seems reasonableto assume that the lack of records for some specieswas the result of relatively few, or short, studies,rather than systematic interspecific variation in be-havior. This observation is supported by the data onP. pithecia (Table III), in which terrestrial behaviorwas unusually common at some sites, but not ob-served at others, even under ostensibly similar eco-logical conditions.

Where terrestrial behavior was observed, moststudies recorded a very small number of events, sug-gesting that the probability of recording the behaviorin a given study was, to some degree, a chance event.

Certainly, the overall pattern was distinct from theone observed by Campbell et al. [2005] for Ateles, inwhich terrestrial behavior was recorded in all stud-ies, albeit at relatively low rates (0.01–0.05 eventsper hour). Hourly rates higher than those reportedfor spider monkeys were recorded in four pitheciins,whereas in all other studies for which it was possi-ble to calculate a rate, values were well below 0.02events/hour (Table IV).

Even when they did come to the ground, pitheci-ins normally spent a very limited amount of timethere. Even during the play bouts observed in someP. pithecia groups, individuals were on the groundfor only a matter of seconds. The aversion of pitheci-ins to terrestrial activity is emphasized by a numberof aspects of their foraging behavior, such as the re-moval of terrestrially retrieved items to perches forprocessing, accessing ground-level water by pedalsuspension, and a reluctance to accompany to theground the foraging primates with which they wereassociating. Similarly, while many Amazonian spi-der (Ateles), and howler (Alouatta) monkeys visit ter-restrial mineral licks regularly [Link et al., 2011a,b],pitheciins appear to prefer arboreal sources, such astermite nests [Ferrari et al., 2008; Setz et al., 1999;but see Happel, 1982]. Given the circumstances ofmost observations, it seems unlikely that the avoid-ance of terrestrial activity is a predator-avoidance

Am. J. Primatol.


strategy directed toward human observers [Gautieret al., 1999], although this may have been a factor insome cases [e.g. Peres, 1993].

In Cacajao and Chiropotes, terrestrial activi-ties other than dispersal were observed so infre-quently that it is inappropriate to infer causal rela-tionships from any inter-site differences in frequen-cies. In Pithecia, by contrast, terrestrial activity wasrecorded in more than half the study sites, withforaging being the most common behavior. For P.pithecia, terrestrial foraging was most commonly ob-served when the availability of ripe fruit and youngleaves was low (Table III). In this regard, ground-retrieved resources may be considered fallback foodsfor sakis [Marshall & Wrangham, 2007 for topic re-view]. Furthermore, sites where habituated Pitheciastudy groups terrestrial have not been observed toexhibit terrestrial behavior (e.g. Quebrada Blanca,and rios Tahuayo and Yavarı, Peru), have a very at-tenuated dry season [Goulding et al., 2003], whileat Guri Lake, and terrestrially active sakis studiedby Harrison-Levine, Norconk, and Walker-Pacheco,lived on islands that had a strong and prolongeddry season [Norconk, 1996] and a depauperate plantcommunity. However, seasonal food dearth is un-likely to be the sole explanation, since in Pitheciapopulations south of the Amazon, observed terres-trial behavior did not coincide with times of low fruitand young leaf availability (e.g. the ant feeding ob-served by S. Palminteri in P. irrorata [Fig. 3], andfor P. aequatorialis by A. Di Fiore et al. occurredat various times of the year, not just when fruitsand leaves were least available, Table III). In addi-tion, while the forests around Manaus have a pro-nounced dry season [Ribeiro et al., 1999], terrestrialforaging in by pitheciins there remains unreported.This is understandable for the urban P. pitheciastudied by Rodrigues da Silva [2007] because theirforests, which contained horticultural resources, al-lowed them to supplement their diet with non-native,dry-season fruiting species (e.g. bananas). However,studies in unmanaged nearby terra firme forests [e.g.Setz, 1993; E. Oliveira et al., 1985] did not record ter-restrial foraging. Thus, while there may be a causalconnection with duration and/or intensity of reduceddry season food availability for some populations, thelink is far from clear-cut and terrestrial use appearsto involve a number of factors.

A cautious overview of the data points suggestthat three factors underpin the observed pattern ofterrestrial behavior in the Pitheciinae: (1) the eco-logical division between the more dietary general-ist Pithecia and the more specialized seed predators,Cacajao and Chiropotes, (2) an apparent associationbetween flooded habitats and terrestrial activity, and(3) the development of a “local behavioral pattern’’ insome populations. Methodological variables, such asthe level of study population habituation, also maybe important.

In addition to the quantitative differences(Tables I–III), the sakis presented two behav-ioral patterns—insect foraging and play—only oncerecorded on the ground for the other pitheciins.Both behaviors are more typical of callitrichids thanpitheciins, and may represent specific local circum-stances (see below). Such differences between sakisand uacaris/cuxius may at least partly be accountedfor by the ecological divergences between the twogroups, in particular the preference of P. pitheciafor lower forest strata and a tolerance for more dis-turbed habitats [Norconk, 2011]. This explanationdoes not hold for such saki species as P. irrorata,which spends most of its time in high canopy [videPalminteri, 2010], and descends to lower layers onlyto practice myrmecophagy.

Overall, 13 of the 30 studies in which terres-trial behavior was recorded were conducted in thecontext of flooded habitats, although this parame-ter is inflated by the fact that nearly half of thesestudies took place at two sites, Tucuruı (Brazil) andGuri Lake (Venezuela), with recently created frag-ments. In the specific case of the uacaris, the abil-ity to exploit ground-based resources, in particu-lar, would likely be an important attribute for pop-ulations inhabiting seasonally flooded varzeas andigapos, where resource availability may show verystrong seasonal variation, with fruit being scarce forlong periods. In such circumstances, the only avail-able fruits may be on the ground. By contrast, noterrestrial behavior has been observed in studies ofCacajao c. ucayalii and Cacajao m. melanocephalusconducted primarily in unflooded habitats (Table I).A similar pattern can be observed in Chiropotes—only three events were recorded at sites other thanTucuruı, and one of these was the retrieval of aninfant, which is an extrematis event. This is consis-tent with observations of cuxius at most sites, wherethey tend to occupy the highest strata of terra firmeforests [Bobadilla & Ferrari, 2000; Norconk, 2011].Predation risk may also be important: in five for-est fragments studied by Port-Carvalho and Ferrari[2004], C. satanas was active on the ground at onlythose sites where Panthera onca and Puma concolorwere least likely to have occurred. In addition, hu-man hunting levels may be significant, since the onlysite at which Chiropotes were observed to both playand engage in protracted terrestrial insectivory wasat the Shaffer’s Essequibo site in Guyana, where thenearest village is 80 km away (and its animistic resi-dents of the Macushi and Wapishana tribal groups donot hunt monkeys). As noted above, even in an areawith no recently recorded hunting, a well-habituatedgroup of C. albinasus were not seen to forage orplay on the ground in over a year of field observa-tion (though the risk of higher predation from non-human predators at such a site is a consideration).At Raleighvallen, terrestrial activity (especiallyforaging) in Saimiri sciureus and in Cebus apella

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was so common as to be unremarkable [ErinEhmke, Laurie Kauffman, unpublished data: videEhmke, 2004; Kauffman, 2004; Phillips, 2008; Vath,2008], but any Chiropotes or Pithecia that wereassociating with them were never recorded asparticipating.

The evidence in Pithecia is less conclusive, andis more consistent with the greater propensity ofthis genus for terrestrial behavior, which, as arguedabove, may reflect the broader ecological differencesbetween the three genera. In this case, half of thestudies in which terrestrial behavior was recordedwere conducted at reservoir sites (Guri Lake and Pe-tit Saut). In addition, play was more frequent at non-reservoir sites (though insect foraging was well rep-resented at both reservoir and non-reservoir sites).

Considering the third possibility, the develop-ment of a “a locally occurring behavior pattern” [“a lo-cal tradition” sensu Huffman & Hirata, 2003] in somepopulations, it should be noted that in the case ofa Brachyteles hypoxanthus population in southeast-ern Brazil, the evolution of a terrestrial tradition ap-pears to have been reinforced by factors such as habi-tat fragmentation and reduced terrestrial predatorpressure (including human hunters) [Tabacow et al.,2009]. While habitat fragmentation is relatively ac-centuated at some of the analyzed sites, predationpressure is unlikely to have declined significantlyin any area. On the contrary, Camargo and Ferrari[2007] suggested that the high population densitiesand isolation of one site (Germoplasma Island in Tu-curui) might have contributed to increased vulnera-bility of the island’s primates to Eira barbara, a scan-sorial predator known to hunt terrestrially [Presley,2000]. In this context it is interesting to note that,for P. pithecia, I. Homburg [unpublished data, videHomburg, 1998] recorded no terrestrial activity infifteen months in 1991–1992 while working on ex-actly the same small island where Harrison [1998]and Harrison-Levine et al. [2003] later recorded sub-stantial terrestrial foraging activity in this species.The rise of a local tradition (or, at least, locale-specific patterns of behavior) at this site seems plau-sible (perhaps following increasing impoverishmentof food resources). However, it is possible (thoughdifficult to prove) that increased familiarity with ob-servers between 1992 and1998 resulted in Pitheciafeeling more confident in their presence and simplyexhibiting more frequently the already present high-risk behavior of terrestrial foraging.

Population specific behaviors (“local traditions”to some authors) may be a possible explanation forinterpopulational differences in other genera. While,for example, Cacajao m. ouakary was observed ex-ploiting germinating Eschweilera seeds at Jau [Bar-nett, 2010], it was not seen doing so at Amana, some150 km to the west, despite the availability of the re-source [M. Oliveira, personal communication], andthe near-identical nature of the habitats. Similarly,

while some cuxius groups at Tucuruı often came tothe ground to retrieve fruit, others were clearly re-luctant to do so [Santos, 2002; Silva & Ferrari, 2009;Veiga, 2006; Vieira, 2005], even though they inhab-ited areas with apparently identical resource pro-files. Terrestrial insect foraging and play are alsorisk-sensitive behaviors, which may require a learn-ing component. However, any such conclusions arespeculative, given the limited time scale of most ofthe available data.

Overall, data presented in this review suggeststhat pitheciins may be the least terrestrial of theplatyrrhines, but engage in this behavior in responseto the particular ecological contexts, for example re-trieval of specific high-yield resources, such as in-sects or germinating seeds. However, the rate andpersistence of this activity appears to differ greatlyamong populations and species. One question raisedby these data is that terrestrial behavior amongpitheciins may be increasing in response to anthro-pogenic disturbance that alters forest structure andmodifies resource availability, and may necessitatethat animals engage in relatively risky activities,such as terrestrial behavior. This may representan additional cause for concern for the long-termsurvival of impacted populations, especially if suchactions are combined with increased hunting (e.g.Peres, 2001). Hopefully this, and other aspects, willbe clarified as an expanded database is accumulatedthrough ongoing and future field studies. We also rec-ommend the use of more detailed sampling protocolsfor the study of terrestrial behavior in Neotropicalprimates.

ACKNOWLEDGMENTSThe following colleagues generously shared un-

published data indicating the absence of pitheciinterrestrial use in their primate study populations:Sara Bennett, Bruna Bezerra, Richard Bodmer,Jean-Philippe Boubli, Nayara Cardoso, Erin Ehmke,Eckhard Heyman, Tremaine Gregory, MarceloGordo, Ingo Homburg, Laurie Kauffman, MariaAparecida Lopes, Marcela Oliveira, Angela Peetz,Leila Porter, Pablo Puertas, Helder Queiroz, JoaoValsecchi, Carrie Vath, Robert Wallace, Barth W.Wright, and Kristin A. Wright. Elena Cunninghamprovided useful comments and Caroline Ross greatlyimproved an early draft of the manuscript. This isContribution No. 1 from the Pitheciine Action Group.

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