The Atlantic Forest of the state of Rio de Janeiro was the habitat of six native primate species: Callithrix aurita, Leontopithecus rosalia, Alouatta guariba clamitans, Brachyteles arachnoides, Callicebus nigrifrons and Cebus nigritus; a seventh species, Brachteles hypoxanthus, possibly occurs in the state. In the literature, the number of non-native primate species for the state was less (three) than the native species (six or seven). Our study reviews the list of primate species, both native and non-native, within the state of Rio de Janeiro and discusses the possible impacts of the introduced primates on the native fauna. Using data from the literature, personal communication with experts, data from Brazilian Federal datasets (Linha Verde and CETAS), and specimens deposited in scientific collections of museums, we recorded 17 primate species with at least one record within the state of Rio de Janeiro. At least eight taxa can be considered non-native to the state. Conservation implications for native fauna may include food resource depletion and competition, hybridization, and disease transmission. Some of these effects were already recorded on the native fauna. We believe the removal of non-native primate species from the state is necessary in order to preserve native fauna regardless of political and ethical issues.
Introduction
Invasive species are a worldwide conservation problem, threatening species and ecosystems; after habitat loss, they are among the most important causes of species extinction or threat [1, 2]. Competition, predation and diseases are often considered the final causes for endangerment following invasions [3]. However, the effects of invasions are associated with more than one cause, mainly habitat disturbance [3]. Disturbance can be a key factor allowing the invasion of an environment by non-native species. Thus, in a fragmented landscape with altered natural habitats, biological invasions can have an additional negative effect on the native fauna [4].
The Atlantic Forest is one of the most biologically diverse and anthropogenically impacted biomes in the world, currently with only around 11–16% of its original cover [5]. The Atlantic Forest in the state of Rio de Janeiro was historically the habitat for six native primate species (Callithrix aurita, Leontopithecus rosalia, Alouatta guariba clamitans, Brachyteles arachnoides, Callicebus nigrifrons and Cebus nigritus), and contains today three additional non-native primate species (Callithrix jacchus, C. penicillata and Saimiri sciureus) with established populations within the state [6]. In addition, Cunha et al. [7] recently raised the possibility that the northern muriqui (Brachteles hypoxanthus) occurs in Itatiaia National Park (INP). Here we present an overview of the primate species in the state of Rio de Janeiro, reviewing the list of native and non-native species, and we discuss the possible impacts of the introduced species on the native primates.
Methods
Information about primate species' (native and non-native) occurrence in the state of Rio de Janeiro was collected from published literature [891011121314–15] of primates occurrence since the year 2000, from personal observations, and from specialists who worked in the state. In addition, we reviewed lists of primates present in the Centro de Triagem de Animais Silvestres CETAS/Rio de Janeiro (an animal rescue and rehabilitation center) and citizen phone complaints made on a state government phone line (Linha Verde) from 2003–2010. For the last two sources (CETAS and Linha Verde), the information on primates was at the genus level only in order to minimize misidentification of species. In our list, we did not use species recorded in captivity. We also used the IUCN red list website ( www.iucnredlist.org) [16, 17] and data from specimens deposited in the scientific collection of the Zoological Museum of São Paulo University (MZUSP) and from the National Museum of Rio de Janeiro (MNRJ).
Results
Based on our survey, we recorded 17 species of primates with at least one record in the state of Rio de Janeiro, including eight genera and four families (Appendix 1). At least eight species are known to be non-native to the state of Rio de Janeiro (Fig. 1). Six of the seven species considered native to the state were recorded in scientific collections, although an individual of buffy-headed marmoset (Callithrix flaviceps), not recorded previously for the state, was captured in 2011 in the municipality of Varre-e-Sai, state of Rio de Janeiro, and deposited in the National Museum of Rio de Janeiro.
From the literature we found four non-native species for the state of Rio de Janeiro. Cunha [12] reported the highest density of Cebus sp. a hybrid of introduced robust tufted capuchin (Cebus robustus) and the bearded capuchin (Cebus libidinosus) with the native black-horned capuchin (Cebus nigritus). The northern masked titi (Callicebus personatus) was reported to the state of Rio de Janeiro [8, 15, 17] although its occurrence needs to be confirmed. Another species is the golden-headed lion tamarin (Leontopithecus chrysomelas). The species was introduced accidently by a private collector and was seen for the first time in 2002 in a forest fragment, part of Serra da Titirica, municipality of Niteroi, state of Rio de Janeiro [14].
From specialists, in 1998, a biologist recorded an individual of black spider monkey (Ateles paniscus) in a forest fragment within the city of Rio de Janeiro (Isabela Deiss, personal communication). The most recent record of a non-native primate species within the state of Rio de Janeiro happened in November 2011. An adult male of black-and-gold howler monkey (Alouatta caraya) was captured on the west part of the municipality of Rio de Janeiro near the Pedra Branca State Park (Cristiane Rangel, personal communication).
Around 457 specimens were captured by or delivered to the CETAS while another 438 were recorded in citizen phone complaints (Linha Verde) from 2003 to 2010. Most of the records are of the genera Callithrix (363 and 415 records) and Cebus (86 and 17 records) respectively. However, other genera (Leontopithecus, Callicebus, Lagothrix and Alouatta) were also recorded.
Discussion
Our study shows that the number of primate species present in Rio de Janeiro is higher than reported on the previous list [6], with an additional five non-native and at least one native species to the state. However, not all recorded species have established populations within the state. For instance, the nonnative species from the genera Alouatta and Ateles are unlikely to harm the native primates since there have been no further records of their presence and are therefore unlikely to have formed established populations in the state.
On the other hand, the non-native species of the genera Callithrix and Saimiri have definitely established populations within the state of Rio de Janeiro [6], and golden-headed lion tamarins (L. chrysomelas) may have as well. The estimated number of golden-headed lion tamarins in 2009 was around 107 individuals [14]; however, this number may currently be higher because there have been four reproductive seasons since the survey and lion tamarins can produce twins in each reproductive season [18]. Also, the hybrids of the genus Cebus recorded by Cunha [12] have established populations mainly in the city of Rio de Janeiro. For these hybrids, a monitoring program of their progress outside the city of Rio de Janeiro and the evaluation of their current status within the state are necessary especially within the range of the native black-horned capuchin, C. nigritus.
The confirmation of the occurrence of the northern masked titi, C. personatus within the state of Rio de Janeiro, and therefore its classification as native or non-native, remains uncertain. The species has been suggested to occur in the Atlantic Forest of south-eastern Brazil in the states of Espírito Santo, northwestern Minas Gerais and northern Rio de Janeiro [8, 15, 17] but was not reported in Rocha et al. [6]. In their article, Roosmalen et al. [8] cited an expert personal communication and added the northern masked titi, C. personatus to the state of Rio de Janeiro, and Printes et al. [15], citing Roosmalen's et al. [11] work, also suggested the species to occur within the state of Rio de Janeiro. However, Grelle [19], evaluating the distribution of primate species endemic to the Atlantic Forest with records from scientific collections housed at MZUSP and MNRJ and from the literature, recorded only specimens of blackfronted titi, Callicebus nigrifrons at MZUSP. This information was recently confirmed (Carla C. Aquino, personal communication). We think that misinterpretation of the literature may cause this mismatching. The status of the buffy-headed marmoset, C. flaviceps, still needs to be confirmed. Its record in the municipality of Varre-e-Sai may represent an increase in its geographic distribution, as this portion of the state of Rio de Janeiro is inside the climatic and vegetational distribution of the species [20] and it is near the border of the species' geographical distribution [16, 21]. This could explain why it was not recorded previously in the state of Rio de Janeiro [6], but this assertion still needs to be confirmed as well.
Implications for conservation
It is widely accepted that a normal functioning ecosystem provides society with ecological services very important for human well-being [22]. Impoverished ecosystems, on the other hand, may function less efficiently as ecological processes are lost, and gradually lose their ability to deliver ecosystem services to human societies [22]. Thus, the problem of introduced primate species within the state of Rio de Janeiro requires attention, because the ecological costs of these outsiders may be the irretrievable loss of native species [23]. Although invasive species are a worldwide problem, in the state of Rio de Janeiro the problem is worse, as more non-native than native primate species were recorded within the state. Some of these species, such as the white-tufted-ear marmoset Callithrix jacchus and black-tufted-ear marmoset, Callithrix penicillata, have established populations in many parts of the state, and already threaten the native and endangered golden lion tamarin [24]. Also, the white-tufted-ear marmoset, C. jacchus as well as capuchin monkeys, Cebus sp. are known to prey on bird nestlings and eggs [25] which may have a strong negative effect on the restinga antwren (Formicivora littoralis), a critically endangered bird with very restricted geographical distribution [26] where white-tufted-ear marmoset, C. jacchus has already been recorded.
Inter-specific competition for food is expected among species with similar foraging behaviors like the con-generics of genera Cebus, Callithrix and Leontopithecus, and between the genera Callithrix and Leontopithecus due to similarities in their ecology and behavior. For instance, Ruiz-Miranda et al. [24] showed that white-tufted-ear marmoset (C. jacchus) and the black-tufted-ear marmoset (C. penicillata) compete for food with the golden-lion tamarin, L. rosalia. Both Callithrix species occur with the golden lion tamarin in many parts of the tamarin's geographical range [27].
Hybridization is probably the worst effect of these introductions. In general, con-generics can hybridize, and the hybrids may ultimately compete with the native species. Hybrids from the genus Callithrix were already recorded in the wild [28, 29]. Hybrids between the native buffy-tufted marmosets (C. aurita) with con-generics have been reported within Serra dos Orgãos National Park [30] where both white- tufted-ear marmoset (C. jacchus) and the black-tufted-ear marmoset (C. penicillata) also occur [10, 30]. The buffy-tufted marmosets, C. aurita is considered vulnerable by the IUCN due to the decline of its populations [29], and hybridization may be another serious risk to the species, mainly in protected areas such as Itatiaia National Park where the black-tufted-ear marmoset (C. penicillata) was also observed [31]. The high densities of hybrids between the black-horned capuchin (C. nigritus), the native species, robust tufted capuchin (C. robustus) and the bearded capuchin (C. libidinosus), recorded within the municipality of Rio de Janeiro [12] indicate that these hybrids are well adapted to the forested areas of the city. Specimens of Cebus with different phenotypes have been recorded in many parts of the state of Rio de Janeiro, suggesting that the hybrids may not be restricted to the city of Rio de Janeiro, implying another threat for the native the black-horned capuchin (C. nigritus). The presence of golden-headed lion tamarins (L. chrysomelas) within the geographic range of the native and endangered golden lion tamarin (L. rosalia) may represent another threat for the latter species [14]. In case of an encounter between the two species, the chances are high that the two species will hybridize [14] as has been observed in captivity [32]. There is also the risk that the golden-headed lion tamarins will introduce diseases previously absent from the region of the golden lion tamarin [14].
Fig. 1.
Introduced (and one native) primate species recorded in the state of Rio de Janeiro. From top right to left: Saimiri sciureus (Photo Gustavo Pedro de Paula), Callithrix jacchus (Photo Cristiane Rangel), Leontopithecus chrysomelas (Photo Leonardo Oliveira) and Callithrix penicillata (Photo Roberto Murta). These four species have established population within the state of Rio de Janeiro. From bottom left: Ateles paniscus (Photo Leonardo Oliveira), Alouatta caraya (Photo Roberto Murta) which are unlikely to form established population within the state, and Leontopithecus rosalia with a hybrid of C. penicillata and C. jacchus (Photo Leonardo Oliveira) within the range of the golden-lion tamarin.
Recommendations
It can be very difficult to control intentional and unintentional introductions that occur through diverse and unique means; therefore preventing new introductions is imperative [23]. Because hundreds of primates from different species were recorded as pets, we recommend an awareness campaign to prevent the use of primates as pets, showing the negative impacts of released primate species on the native fauna. Sterilization of the non-native species is an alternative to avoid population increase, spread and hybridization; although it would not halt ongoing negative effects on the native biodiversity and may be effective only for small populations [33], it nevertheless may be used as complementary action. The removal of introduced species is a difficult task in a large geographical range, but where achievable, removal is the best management option for dealing with invasive species where prevention has failed [23].
The first step in removing introduced species is to identify the areas where they occur. A monitoring program is necessary to determine the geographical range of the problem and to identify priority areas where removal of introduced primates is urgent, such as in protected areas and near endangered species. The National Action Plan for Endangered Mammals of Southeastern Brazil (PAN MAMAC), developed by Instituto Chico Mendes de Conservação da Biodiversidade-(ICMBio) in November 2010, includes as one of its recommendations the removal of all introduced primate species in the state of Rio de Janeiro [34]. Though this recommendation will likely cause political and social concern, it is the most appropriate action considering the potential effects on the native primate species as well as on the whole biodiversity of the state.
Acknowledgments
We thank Isabella Deiss for providing information about Ateles paniscus, Cristiane Rangel about Alouatta caraya, and Márcio Urselino for providing data from CETAS and Linha Verde. We thank Alcides Pissinati from the Rio de Janeiro Primate Center (CPRJ), Anthony Rylands, Fabiano Melo, and José de Souza Silva Junior for the identification of an individual of Callicebus and Carla C. Aquino for providing information about the specimens of Callicebus deposited on MUZUSP. We also thank James M. Dietz and Sara Zeigler for the English review. Leonardo C. Oliveira received a PNPD-CAPES fellowship and Carlos E V Grelle received grants by CNPq (productivity fellowship) and FAPERJ (Jovem Cientista do Estado).
