ORYX VOL 25 NO 2 APRIL 19E

Buffy-headed marmosets 10 years on

Stephen F. Ferrari and Sergio L. Mendes

The buffy-headed marmoset Callithrix flaviceps is among the rarest ofBrazil's Atlantic Forest primates and is potentially one of the mostendangered by habitat destruction. Rarely seen in captivity, little wasknown about the species until very recently. Studies carried out duringthe last 10 years have revealed that these marmosets are not only highlyadaptable but are also more widespread than was first thought. Therethus seems to be room for cautious optimism for the survival of thespecies as long as further habitat loss can be minimized.

Endemic to a small area of the Atlantic Forestof south-eastern Brazil (Figure 1), the buffy-headed marmoset Callithrix flaviceps may havethe smallest natural range of any SouthAmerican primate. Rare in the wild and virtu-ally unknown in captivity, even in Brazil, thespecies has a short history and faces an uncer-tain future. First described at the turn of thecentury (Thomas, 1903), C. flaviceps had beenrecorded only at a dozen localities in the stateof Espirito Santo (see Hershkovitz, 1977)before being discovered in eastern MinasGerais 10 years ago (Mittermeier et ah, 1980).The species may also occur in the very northof the state of Rio de Janeiro (Hershkovitz,1977), although this awaits confirmation.

Given its small geographic range anddependence on arboreal habitats, C. flaviceps isone of the primates most seriously affected bythe widespread destruction that has progres-sively decimated the Atlantic Forest duringthe course of this century (Mittermeier et al.,1982). C. flaviceps populations are now restrict-ed to relatively small, isolated remnants of theoriginal forest, the vast majority of which, likethat on the Fazenda Montes Claros in MinasGerais (now the Estac,ao Biologica deCaratinga (EBC), or Caratinga BiologicalStation), are privately owned. Mittermeier etal. (1980) were in fact only able to confirm thepresence of C. flaviceps in one officially protect-ed area, the Nova Lombardia BiologicalReserve in Espirito Santo.

The recent history of the species is more

promising. A great deal of information on itsbehaviour and ecology was collected during along-term field study carried out at MontesClaros, while a detailed survey has identifieda further four reserves in which C. flavicepsoccurs. Local residents are campaigning forthe preservation of other forest patches withinthe species's range and an environmental edu-cation programme is now well established ineastern Minas Gerais. The evidence from thefield studies indicates that this marmoset ishighly adaptable and that, as long as furtherhabitat destruction is minimized and someprovision is made for interchange between theremaining populations, there is room for opti-mism for the long-term survival of the species.

Callithrix flaviceps at Fazenda MontesClaros

Observations of C. flaviceps were begun atMontes Claros shortly after the discovery ofthe species at this site (Alves, 1986) and along-term study of the species's behaviouralecology was carried out over a 20-monthperiod between 1984 and 1986 (Ferrari, 1988,1989). Observations of the marmosets havecontinued intermittently up to the present dayand a further detailed behavioural study isnow under way.

The main study at Montes Claros was car-ried out in a hilly area of secondary forest atthe northern extreme of the forest reserve. The

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ORYX VOL 25 NO 2 APRIL 1991

_/EBC

_/MINAS GERAIS<-Mota do o

SossegoI? (\ /Capatao

•••.? i

K

Nova Lombardia^

S. Lourenco'°o ••'' /...-•- ' Sta.l

LNaSonai o P e d r a A-2ul

^ P g , ^ oForno Grande< ESP1RITO SANTO

< 42I,RIO DE JANEIRO 4 0 °

Figure 1. Geographic range of C. flaviceps in south-eastern Brazil and reserves mentioned in the text.

vegetation is typical of tropical secondary for-est, with marked concentrations of relativelyfew plant species (in comparison with primaryforest), many of which are extremely fast-growing. A plantation approximately 25 yearsago, the main area now boasts many nativetrees of well over 20 m in height.

Another characteristic of secondary forest,relative to undisturbed habitat, is a paucity offruit, especially at certain times of the year.This is a result of both the reduction in plantspecies and the time they require to reachreproductive age. In addition, as the seeds ofmany colonizing tree species are wind-dis-persed, their fruits are generally inappropriateas food for most primates. The monthly moni-toring of 1260 trees within the study areabetween July 1985 and August 1986 revealedthat only 222 (17.6 per cent) produced fruitduring this period, and that edible fruit wasgenerally scarce except during the wettestmonths of the rainy season (Ferrari, 1988).

While marmosets require a mixed diet ofplant and animal material, they are not depen-dent on fruit, being able to systematicallyexploit the edible gums that are produced bymany tropical trees and lianas. In addition totheir specialized lower incisors, which allowthem to gouge gum-producing holes in bark(Coimbra-Filho and Mittermeier, 1977), mar-mosets exhibit specializations of the digestivetract, which probably allow them to fermentthe carbohydrate content of the gum, permit-

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ting its efficient digestion (Coimbra-Filho etal., 1980).

These adaptations are essential to the sur-vival of marmosets in marginal or impover-ished forest habitats. The secondary forest atthe Montes Claros study site is dominated bytwo legume species, Acacia paniculata andAnadenanthera peregrina, both of which pro-duce edible gum and provide the monkeyswith an abundant source of plant material.Gum contributed as much as 88 per cent of therecords of C. flaviceps feeding behaviour dur-ing any one month, and accounted for morethan half of the feeding records in all monthsexcept January and February, when ediblefruit was abundant and partially replacedgum in the diet of the study animals.

Complementing their diet with arthropods,especially grasshoppers, and small verte-brates, the marmosets are able to thrive in anenvironment that appears to be relatively

« ,

Secondary forest in the C. flaviceps study area atMontes Claros. The large, open-crowned trees are allof a single species, Anadenanthera peregrina.

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BUFFY-HEADED MARMOSETS

inhospitable to other primates. More than 50muriquis Brachyteles arachnoides are present inthe reserve, for example, but have never beenobserved within the marmoset study area. C.flaviceps is the most abundant monkey in thispart of the forest, where it forms large, highlystable social groups. Recent observations alsoindicate that the marmoset population in thisarea has been expanding over the past 5 years.C. flaviceps appears to be least abundant in theprimary forest at Montes Claros. The total C.flaviceps population within the reserve atMontes Claros, whose area is approximately800 ha, was estimated at between 200 and 300individuals.

Callithrix flaviceps in Espirito Santo andMinas Gerais

C. flaviceps was registered in a further fourprotected areas in Espirito Santo: theBiological Stations of Sao Lourengo and SantaLucia (municipality of Santa Teresa), and inthe Forestry Reserves of Pedra Azul and FornoGrande (Figure 1). Local residents are alsoestablishing a research station at the Mata doSossego in Manhuacu, Minas Gerais, wherethe marmoset is known to occur. No evidencecould be found of the existence of the speciesin the Caparao National Park, however.

The survey of C. flaviceps distribution inEspirito Santo revealed that the species occursalongside the white-faced marmoset Callithrix

( 42<>'RI0 0E JANEIRO40°

Figure 2. Municipalities in which populations of C.flaviceps are known to exist.

Acacia paniculata is a dietary staple of the marmosetsat Montes Claros. Here a female C. flaviceps restsbetween feeding bouts in a typical acacia patch(Stephen F. Ferrari).

geoffroyi in at least three tracts of forest (SantaLucia and the Fazenda dos Irmaos Medanhain Santa Teresa, and Rio Bonito in SantaLeopoldina). While the two species are knownto hybridize in these areas, they are welldifferentiated ecologically and speciesintegrity has been maintained despite theisolation of these populations in relativelysmall tracts of forest. R. A. Mittermeier

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ORYX VOL 25 NO 2 APRIL 1991

(pers. comm.) also reports seeing greyish indi-viduals, possibly hybrids, in part of the NovaLombardia Reserve in 1980. Evidence ofhybridization between C. flaviceps and C. auri-ta was also found in the municipality ofCarangola, Minas Gerais. These sites are obvi-ously extremely important for the study ofecological and taxonomic relationshipsbetween these three marmoset species.

In addition to the major reserves, buffy-

Buffy-headed marmosets have keen vision and areconstantly attentive to their surroundings, alwayson the watch for signs of cryptic insects, especiallygrasshoppers, which balance the gum in their diet(Stephen F. Ferrari).

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headed marmosets are known to be present ina number of much smaller forest fragments inthe municipalities of Carangola, Caratinga,Ipanema, Lajinha and Manhuacu in MinasGerais (Figure 2), and of Iuna, SantaLeopoldina, Santa Maria do Jetiba and SantaTeresa in Espirito Santo, and it seems likelythat the species still occurs in other municipal-ities within the area of its geographical range.The adaptability of C. flaviceps was furtheremphasized during observations at Lajinha,where the marmosets were seen occupying aseries of small patches of secondary forest ofapproximately 1 ha, between which they trav-elled on open ground over distances of morethan 100 m.

10 years on

Having seen more than 95 per cent of theirunique Atlantic Forest ecosystem disappear,many Brazilians are becoming increasinglyconcerned with the preservation of the forest-ed areas that now remain. Conservation pro-jects, such as those involving the muriqui B,amchnoides and the golden lion tamarinLeontopithecus rosalia, have helped to raisepublic consciousness considerably (Dietz,1987) and for the preservation of the Atlanticforest, the project S.O.S. Mata Atlantica, isgaining support at all levels of Brazilian soci-ety.

While the national parks and other reservesof south-eastern Brazil obviously play animportant role in the conservation of thisecosystem and its numerous endemic species offauna and flora, the preservation of privatelyowned tracts of forest, however small or dis-turbed, may also be crucial for many species.As our studies have shown, buffy-headedmarmosets are extremely adaptable and areable to thrive under relatively harsh condi-tions in marginal and secondary forest patch-es. In the long term, the privately owned for-est remnants within the species's range maybe extremely important for the maintenancenot only of C. flaviceps numbers in the wild,but also of the genetic variability of a highlyfragmented population.

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BUFFY-HEADED MARMOSETS

,v

Like other marmosets, C. flaviceps prefer disturbedhabitats and forest edge, but are also wary of com-ing to the ground. This old male is resting on aPiptadenia gonocantha sapling in an abandonedbanana plantation, which borders the Montes Clarosstudy site (Stephen F. Ferrari).

Acknowledgments

Field studies at the Fazenda Montes Claros wereauthorized by the National Research Council(CNPq) and were supported by the MedicalResearch Council of Great Britain, the A. H. Schultz-Stiftung, the Central Research Fund of LondonUniversity, the Boise Fund and the Leakey Trust.Studies at other sites were supported by the Museude Biologia Mello Leitao, the WWF-US PrimateProgramme, FUNCAMP-MB and the A. H. Schultz-Stifrung. We would like to thank Cida Lopes Ferrariand Russ Mittermeier for their suggestions andAntonio Martins for Figures 1 and 2.

References

Alves, M.C. 1986. Observagoes sobre o Callithrixflaviceps (Thomas, 1903) na Estacao Ecologica deCaratinga—EBC/FBCN, MG (Callitrichidae,Primates). In A Primatologia no Bras;/—2 (ed. M. T.de Mello), pp. 205-206. Sociedade Brasileira dePrimatologia, Brasilia.

Coimbra-Filho, A.F. and Mittermeier, R.A. 1977.Tree-gouging, exudate-eating and the 'short-tusked' condition in Callithrix and Cebuella. In TheBiology and Conservation of the Callitrichidae (ed. D.G. Kleiman), pp. 105-115. Smithsonian InstitutePress, Washington DC.

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Dietz, L.A. 1987. Comparative analysis of species-targeted conservation education projects. Int. }.Primatol. 8,442.

Ferrari, S.F. 1988. The behaviour and ecology of thebuffy-headed marmoset, Callithrix flaviceps (O.Thomas, 1903). PhD Thesis, University CollegeLondon.

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Hershkovitz, P. 1977. Living New World Monkeys(Platyrrhini). Vol. 1. University of Chicago Press,London.

Mittermeier, R.A., Coimbra-Filho, A.F. andConstable, I.D. 1980. Range extension for anendangered marmoset. Oryx, 15,380-383.

Mittermeier, R.A., Coimbra-Filho, A.F., Constable,I.D., Rylands, A.B. and Valle, C.M.C. 1982.Conservation of primates in the Atlantic Forest ofeastern Brazil. Int. Zool. Yrbk, 22, 2-17.

Thomas, O. 1903. Notes on south American mon-keys, bats, carnivores and rodents, with descrip-tions of new species. Ann. Mag. Nat. Hist. 12,455-464.

Stephen F. Ferrari, Department of Anthropology,University College London and Departamento deZoologia, Museu Paraense Emilio Goeldi, CaixaPostal 399, 66.040 Belem, Para, Brazil.Sergio L. Mendes, Museu de Biologia Mello Leitao -FNPM, Santa Teresa, Espirito Santo and Instituto deBiologia, Unicamp, Campinas, Sao Paulo, Brazil.

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