Black-Tufted Marmoset

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Black-tufted Marmoset, Callithrix penicillata (Geoffroy Saint-Hilaire, 1812), a new unwelcome addition to the fauna of Reserva Ecológica de Guapiaçu (Rio de Janeiro, Brazil).

Michael Patrikeev

28 Indian Harbour Road, Tobermory, Ontario N0H 2R0 Canada

On 28 September 2011, I observed and photographed a group of the Black-tufted Marmoset, Callithrix penicillata, near Rio Gato (22°23'57.98"S, 42°44'17.04"W; ca. 390 m asl.) in Reserva Ecológica de Guapiaçu or REGUA. REGUA is a private nature reserve located near the village of Guapiaçu in the municipality of Cachoeiras de Macacu, Rio de Janeiro, Brazil. The reserve protects ca. 6,500 ha of secondary and primary Atlantic forest in Serra dos Órgãos massif, extending attitudinally from 30 to 2,200 m; all areas above 400 m are included in the recently decreed Parque Estadual dos Três Picos (REGUA website: www.regua.co.uk, Pimentel and Olmos 2011). Prior to the reported C. penicillata observation, the only Callithrix species known from REGUA was the Common Marmoset, C. jacchus, (www.regua.co.uk, N. Locke, pers. comm.).

The Black-tufted Marmosets were detected by their vocalization in a mature secondary forest along “Green Trail”, and seven or eight of them were found eating small green fruit with white pulp, in trees ca. 10-12 m above the ground at ca. 15:45 hrs (Figure 1). The group contained at least one (or perhaps two) large young. The marmosets were not particularly wary, but soon moved away; all troop members following the same route over the branches. One adult lingered until the last member of the group, a large youngster, crossed over the trail, and then it joined the group. This species was not encountered during subsequent excursions to the area in early October 2011.

The marmosets observed along “Green Trail” conformed to the traits of C. penicillata (Nowak 1999, Rylands et al. 2008) by having black circumauricular tufts, crown and temples (Figure 2 and 3). C. jacchus has mostly white circumauricular tufts, blackish or brown forehead and temples (Figures 2 and 3). The Buffy-tufted Marmoset, C. aurita (not yet reported from REGUA), has small buff or ochre ear-tufts, black throat, head and cheeks (Nowak 1999, Rylands et al. 2008). Cristiane Hollanda Rangel (Projeto de Conservação da Fauna, Jardim Botânico do Rio de Janeiro), Fabio Olmos (Permian Brasil Serviços Ambientais, São Paulo) and Leonardo Pimentel (REGUA) examined my photographs, and confirmed that marmosets in the photos were indeed C. penicillata.

Neither C. penicillata nor C. jacchus is native to the state of Rio de Janeiro (Rocha et al. 2004, Ruiz- Miranda et al. 2011), although C. penicillata might have reached the Itatiaia National Park in the west of the state naturally (Coimbra-Filho 1984). C. penicillata is typical of the gallery and dry forest of Cerrado region in eastern Brazil, where it occurs in the states of Bahia, Minas Gerais, Goiás, Piauí, Maranhão and the north of São Paulo (Eisenberg and Redford 1999, Rylands et al. 2008), see Figure 4. C. jacchus is native to the scrub forest (Caatinga) and drier Atlantic forest of north-eastern Brazil, in the states of Alagoas, Pernambuco, Paraíba, Rio Grande do Norte, Ceará, Piauí, Maranhão, Bahia, and possibly

M. Patrikeev. 2011. Callithrix penicillata in Reserva Ecológica de Guapiaçu, Rio de Janeiro Page 1

Tocantins, Figure 4 (Bicca-Marques et al. 2006, Rylands et al. 2008). Both species are common within their natural range, IUCN Least Concern category (Rylands and Mendes 2008, Rylands et al. 2008).

C. jacchus and C. penicillata show a preference for disturbed and secondary forest, and fragmented habitats, and following the destruction of the Atlantic forest these species have expanded their natural range (Rylands and Faria 1993, Bicca-Marques et al. 2006). Both species were also widely introduced in other parts of eastern and south-eastern Brazil, from Sergipe to Santa Catarina (Olmos and Martuscelli 1995, Bicca-Marques et al. 2006, Rylands et al. 2008, Rylands and Mendes 2008, Ruiz-Miranda et al. 2011).

In the state of Rio de Janeiro, populations of the introduced Callithrix marmosets existed for decades, and presently they occur in at least 13% of the municipalities (Ruiz-Miranda et al. 2011). Juvenile and immature animals of both species are captured within their natural range and transported to large cities of the south-east to meet local and international demand. There some are released by owners in their gardens and fazendas, less desirable animals are liberated by traffickers, and seized marmosets are often freed by police at forest edges. Some owners admitted in releasing old or sick marmosets (Ruiz- Miranda et al. 2011).

International Union for Conservation of Nature recognizes invasion by alien species as one of the most significant threat to biological diversity, second only to habitat loss (IUCN 2007). In the case of C. jacchus and C. penicillata threat is in competition with native Callithrix and Leontopithecus (Ruiz-Miranda et al. 2011) and genetic swamping and eventual replacement of native Callithrix by the invaders. The issue is complicated by close relationship of species within the genus Callithrix. The six currently recognized species (aurita, flaviceps, geoffroyi, jacchus, kuhlii and penicillata) have mostly parapatric ranges (Eisenberg and Redford 1999, Coimbra-Filho et al. 2006, Rylands et al. 2008) and in the recent past were all considered subspecies of Callithrix jacchus (Hershkovitz 1977). Although all six were elevated to full species rank (Mittermeier et al. 1988; Coimbra-Filho et al. 2006; Rylands et al. 2008) genetic analysis of their taxonomic differences is inconclusive (see discussion in Coimbra-Filho et al. 2006). Natural hybrids occur in zones of contact (Rylands et al. 1993, Mendes 1997) and all species of Callithrix hybridize in captivity (Coimbra-Filho et al. 1993).

In the Rio de Janeiro state the majority of introduced marmosets are C. jacchus x C. penicillata hybrids, which tend to be larger than the parental species (Ruiz-Miranda et al. 2011). By the beginning of the 21st century C. jacchus, C. penicillata and their hybrids probably completely displaced native C. aurita at low elevations in the state through competition and hybridization, likely aided by deforestation and forest fragmentation (Coimbra-Filho 1991, Bicca-Marques et al. 2006, Rylands et al. 2008). Nowadays C. aurita is confined to higher elevations (500-1,200 m) within its former range (Rylands 1994, Olmos and Martuscelli 1995).

In Reserva Ecológica de Guapiaçu C. jacchus inhabits forests fragments, edges and recently reforested areas at low elevations, and probably does not extend into the forest interior (N. Locke, pers. comm. and pers. obs.). C. penicillata also prefers disturbed or fragmented forest and forest edges (Rylands and Faria 1993, Bicca-Marques et al. 2006), and perhaps my sighting of a breeding group of C. penicillata in

M. Patrikeev. 2011. Callithrix penicillata in Reserva Ecológica de Guapiaçu, Rio de Janeiro Page 2 mature forest is an isolated occurrence. However, this also may signal C. penicillata expansion into the interior forest and to higher elevations along Rio Gato corridor. Although C. aurita has not yet been reported from REGUA, it may occur in the higher, inaccessible parts of the reserve and adjacent parts of Parque Estadual dos Três Picos (the nearest population of C. aurita is only 25-30 km away, in Parque Nacional da Serra dos Órgãos, Rylands et al. 2008). Regardless of C. aurita presence in this area C. penicillata is not a welcome addition to the fauna of REGUA and Três Picos.

Ruiz-Miranda et al. (2011) discussed management of introduced Callithrix populations via removal or sterilization. A project to sterilize males (through vasectomy) was tested in the São João basin, and resulted in no new births in 4 out of 6 groups under observation (Ruiz-Miranda et al. 2011). However, to effectively control the introduced populations of marmosets Ruiz-Miranda et al. (2011) suggest sterilization of up to 80% of all males, making such undertaking costly and logistically difficult. Because of this, removal with possibly euthanasia of C. jacchus and C. penicillata is being considered in areas where these species and their hybrids pose immediate risk to the threatened C. auratus and Leontopithecus rosalia (C. Hollanda-Rangel, pers. comm.).

Acknowledgements

Nickolas and Raquel Locke, Jorge Bizzaro, Leonardo Pimentel, Fiona Reid, Regina Ribeiro, Cristiane Hollanda Rangel, Fabio Olmos, Jack Eitniear, Alan Martin, Lee Dingain, and InfoNatura.

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A B

Figure 1 Callithrix penicillata in Reserva Ecológica de Guapiaçu (A and C - adult of unknown gender, B - weaned young, and D – adult female). 28 September 2011. Photos by Michael Patrikeev.

M. Patrikeev. 2011. Callithrix penicillata in Reserva Ecológica de Guapiaçu, Rio de Janeiro Page 6

B A B A

C C

Figure 2 Callithrix penicillata and C. jacchus, side by side. C. penicillata has black circumauricular tufts (A), black crown and temples (B and C). C. jacchus has mostly white circumauricular tufts (A), blackish or brown forehead and temples (B and C). Photos by Michael Patrikeev (left) and Lee Dingain (right).

A B

Figure 3 Callithrix penicillata (A) in its natural range (Belo Horizonte, Minas Gerais); Callithrix jacchus (B) in Reserva Ecológica de Guapiaçu, Rio de Janeiro. Photos by Regina Ribeiro (left) and Alan Martin (right).

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Figure 4 Original distribution of the marmosets of genus Callithrix in eastern and south-eastern Brazil (shape files by InfoNatura http://www.natureserve.org/infonatura/).

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