New species of titi monkey, genus Callicebus Thomas, 1903 (Primates, Pitheciidae), from Southern Amazonia, Brazil

The genus Callicebus is one of the most diverse Neotropical primate groups, with 31 recognized species. However, large knowledge gaps still exist regarding the diversity of this genus. Such gaps are gradually being filled due to recent intensification of sampling efforts. Several geographic distributions have been better delimited, and six new species have been described in the last 15 years. The goal of the present study is to describe a new species of Callicebus belonging to the Callicebus moloch species group, recently discovered in an area previously considered to be part of the geographic distribution of C. cinerascens. Data collection was conducted through direct observations, specimen collection and interviews with local residents during four expeditions. Specimens were deposited in the mammalian collection of the Museu Paraense Emilio Goeldi.. For a comparative evaluation, we examined specimens of the other species of the Callicebus moloch species group, especially the geographically neighboring forms, C. bernhardi and C. cinerascens. We examined 10 chromatic characters of the fur. In addition to body mass, we verified the conventional external variables and 26 craniometric variables. The new species differs from all other Amazonian Callicebus by an exclusive combination of characters, being easily distinguished by the light gray line of the forehead, dark ocher sideburns and throat, dark gray portions of the torso and flanks, and uniformly orange tail. The geographic distribution of the new species is limited by the Roosevelt and Aripuana rivers, in the states of Mato Grosso and Amazonas, Brazil. Approximately 25% (1,246.382 ha) of this area falls within conservation areas, with five areas of sustainable use (746,818 ha) and three of integral protection (499,564 ha). Furthermore, a considerable portion of the distribution area is located within indigenous lands (1,555.116 ha - 32%). Therefore, 57% (2,801.498 ha) of the occurrence area of the new species falls within protected areas.

The genus Callicebus has a disjunct geographic distribution, occurring in most of the Amazon and Atlantic forest, in addition to several open vegetation areas adjacent to these biomes (Silva-Júnior et al., 2013). In Amazonia, the genus is absent from the areas north of the Amazon river, from the left margin of the Branco and left bank of the lower Negro rivers to the west until the Atlantic coast to the east, and also south of the Amazon river, in the region east of the Tocantins river. The distribution of the subgenus Torquatus is partially superimposed to that of the subgenus Callicebus (Callicebus cupreus species group). According to Roosmalen et al. (2002), the Amazonian distributions of Callicebus are always limited by the presence of rivers, and its occurs due to a combination of factors related to the animals' biology, such as the inability to swim and a preference for terra firme forests, which would hinder the passive population dispersal from one margin to another. Rylands et al. (2012) observed that there are still large gaps in our knowledge about the taxonomy of Callicebus, and also about their geographic distributions. Recently, such gaps are being systematically filled due to an intensification of field efforts, especially in Amazonia. Several geographic distributions are being better delimitated, including those of lesser known species such as C. modestus, C. olallae , C. dubius (Röhe & Silva-Júnior, 2010) and C. cinerascens (Noronha et al., 2007;Sampaio et al., 2012). In addition, six new species of the subgenus Callicebus were described in the last 15 years. Kobayashi & Langguth (1999) described C. coimbrai (Callicebus personatus species group) based on five specimens collected in three locations near the coast of the state of Sergipe, between the São Francisco and Real rivers in northeastern Brazil. Roosmalen et al. (2002) described two new species. The first, C. stephennashi (Callicebus cupreus species group), was based on five specimens of unknown origin, supposedly from the region between the Purus, Ipixuna and Madeira rivers. The second, C. bernhardi (Callicebus moloch species group), was based on three specimens from the region between the Madeira-Ji-Paraná and the Roosevelt-Aripuanã rivers. Wallace et al. (2006) described C. aureipalatti (Callicebus cupreus species group), discovered in the Madidi conservation area, located north of the Departmento de La Paz, northwestern Bolivia. The description was based on two specimens collected in the region of the Hondo River and on field observations. Defler et al. (2010) described C. caquetensis (Callicebus cupreus species group) based on two collected specimens, and on 13 social groups observed in the field. The new species was registered in 11 locations between the Orteguaza and Caquetá rivers, Colombia (Defler et al., 2010). Gualda-Barros et al. (2012) described C. vieirai (Callicebus moloch species group) based on four museum specimens and on two specimens observed in the field. The new species was found at three locations between the Iriri and Teles Pires rivers, in the states of Pará and Mato Grosso, Brazil. According to Rylands et al. (2012), there are still undescribed species of Callicebus, which should be discovered soon as field and laboratory research intensify.
The objective of the present study is to describe a new species of Callicebus recently discovered in the central-southern area of Brazilian Amazonia, a region previously considered as part of the geographic distribution of C. cinerascens. The new species is placed in Callicebus moloch species group (subgenus Callicebus), being very different from the other forms of the genus.

MATERIAL AND METHODS
We conducted four expeditions to the region of the Aripuanã, Roosevelt and Guariba rivers, states of Amazonas and Mato Grosso, Brazil. The first expedition was conducted from November 27 th to December 19 th , 2010, when we collected the holotype. The second expedition occurred in the region of the Guariba-Aripuanã from January 10 th to February 5 th , 2013. The third expedition occurred in the region of the Roosevelt-Aripuanã rivers from August 11 th to 30 th , 2013. On these occasions, we collected the six paratypes. The most recent expedition (November 9 th to 25 th , 2013) was conducted to add and confirm the information about the geographic distribution and limits of the new species.
Data collection in the field was conducted by walking on pre-existing trails, and in canoes on the banks of the Guariba River, near the Aripuanã River. We collected data using a combination of direct observations, collection of specimens and interviews with local residents. We used recordings of the vocalizations of Callicebus brunneus (present in Emmons et al., 1997) in order to locate animals by playback. This procedure has been used to locate other Callicebus species (Printes et al., 2011;Sampaio et al., 2012). In total we sampled at nine localities. Specimen collection was authorized by the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis -IBAMA, Sistema de Autorização e Informação em Biodiversidade -SISBIO (permanent collecting permit number 13507-1). For each collected specimen, we verified the age-sex class, reproductive state, body mass and biometric parameters. The specimens of the type series were deposited in the mammalian collection of the Museu Paraense Emílio Goeldi (MPEG), Belém, Pará, Brazil, representing the following voucher numbers: MPEG 42654, 42810-12, 42991-93.
For a comparative evaluation, we examined specimens of geographically neighboring species, C. bernhardi and C. cinerascens, deposited in the collections of the MPEG and of the Instituto Nacional de Pesquisas da Amazônia (INPA). This comparison also involved the examination of skins of the other forms in the Callicebus moloch species group, in order to verify chromatic similarities and differences. A list of the analyzed specimens is in the Appendix.

geographic distribution
The records of Callicebus miltoni sp. nov. occurred in the lowlands of the Roosevelt-Aripuanã Depression, an area previously considered by Roosmalen et al. (2002) and Veiga et al. (2008) as part of the distribution of C. cinerascens (Table 1; Fig. 4). The geographic distribution of the new species coincides with the interfluvial region of the Roosevelt and Aripuanã rivers, states of Mato Grosso and Amazonas, Brazil, and these rivers form the western (Roosevelt), eastern (Aripuanã) and northern limits of its distribution (Fig. 4). Callicebus miltoni was observed along the right bank of the Roosevelt River, replaced by C. bernhardi which occurs at the left bank of this river (FES, pers. observation). The series of hills resulting from the contact of the Dardanelos plateau and the Roosevelt-Aripuanã Dissected plateau whose declivity acts as an effective terrestrial barrier and represents the southern limit of the distribution of C. miltoni. These formations have abrupt contact with steep ledges, with the Roosevelt-Aripuanã Depression at its north face, and gradual contact with the Parecis plateau and part of the residual plateaus of Madeira-Roosevelt at the south (Brasil, 1980).

Description of the holotype
Dark-ocher (orange-brown) sideburns, with the individual hairs showing two colored stripes, one basal orange and one distal dark-ocher; forehead with a white (light gray) stripe contrasting with the dark agouti-gray crown; ears colored similarly to crown, but with white (light gray) edges and a discrete white (light gray) tuft; white vibrissae and beige eyelids (in natura); superior part of the body, flanks and external sides of members a uniform gray-agouti, which extends to approximately 1/10 th of the tail on the anterior-superior portion; white (light gray) hands and feet, in the same tone of the forehead stripe and ear edges, contrasting with the gray-agouti of the external parts of the members; throat in the same tone as sides of the face (dark-ocher); chest, belly and internal parts of the members light orange, visibly contrasting with the dark orange of the sideburns and throat; tail (except 1/10 th of the anterior-superior portion) uniformly light orange, though the individual hairs show two stripes, one basal light orange and one distal reddish-orange (Figs. 1A-C, 2A-D, 5).

Paratypes
The type series of C. miltoni sp. nov., composed of seven specimens, allowed for an initial evaluation of the intraspecific variation in fur color. The observed variation in the paratypes was small, showing the stability of the set of characters that define the chromatic pattern of the species, and the absence of sexual dichromatism. The gray coloration of the crown was lighter in specimens MPEG 42810, 42811, 42812 and 42991, with effects of the distinctness of the forehead stripe. MPEG 42810 showed a very diffuse stripe, almost imperceptible, and specimens MPEG 42811, 42812 and 42991 showed a less contrasting stripe with the crown than that observed in the holotype and in the other paratypes. Specimen MPEG 42993 showed darker sideburns, with a darkened tone, and MPEG 42812 showed lighter sideburns, slightly orange. Specimens MPEG 42811 and 42812 showed a slight brown tone in the gray color of the dorsum, and MPEG 42992 showed this same coloration only in the posterior part of the dorsum (saddle). Specimens MPEG 42812 and 42992 showed a whitish longitudinal stripe in the flanks. Specimen MPEG 42810 showed a more reddish color in the throat, chest and belly, and specimens MPEG 42812, 42991, 42992 and 42993 showed a darker coloration in these regions, less contrasting with that of the throat. Specimen MPEG 42810 had darker hands and feet, less contrasting with the color of the external surface of the members; specimen MPEG 42992 showed less contrasting hands, in addition to brownish fingers, and MPEG 42812 had ankles with brownish extremities. Specimen MPEG 42812 showed a lighter external surface of the members, contrasting with the dorsum, similarly to MPEG 42811 and 42992, but with less intense contrast. MPEG 42991 showed this same pattern only in the anterior members. Specimens MPEG 42812 and 42991 had darker internal surfaces of the members, similar to that of the sideburns; the same was true for MPEG 42992 and 42993, but only in the anterior members. MPEG 42810 had a blackish tone in 2/3 of the proximal portion of the tail (dorsal side), with the ventral side showing a small black portion separating the base from the remaining of the tail. Specimen MPEG 42811 showed some sparse whitish hairs along the tail. Specimens MPEG 42811, 42810 and 42991 had shorter tails, with shorter and less dense hairs and with the coloration of the basal stripe less contrasting with the distal stripe. MPEG 42991 had the basal part of the tail composed by two pairs of small stripes, alternating between golden-yellow and dark brown. MPEG 42992 showed uniformly colored ears, similar to the color of the crown.

Diagnosis
A species of titi monkey belonging to the Callicebus moloch species group, subgenus Callicebus (sensu Groves, 2005). Callicebus miltoni sp. nov. differs from all other Amazonian species of the genus Callicebus by an exclusive combination of characters. It is easily distinguished from species of the same group, particularly those with adjacent distributions, C. bernhardi and C. cinerascens, by the pattern of fur coloration, especially a contrasting gray stripe on the forehead ( Fig. 2A-B), orange-brown sideburns and throat, dark gray upper torso and flanks, and orange tail (except 1/10 th of the dorsal surface at the base of the tail) (Fig. 5, Fig. 6). The tail turned orange-brown after taxidermy in all specimens of the type series, but this remained an exclusive trait of C. miltoni (Fig. 2C-D).

Comparisons
Considering the species as a member of the Callicebus moloch species group (Table 2), C. miltoni differs from its closest geographically neighbor C. bernhardi (Fig. 6) by the dark-ocher tone of the sides of the face and throat, contrasting with the chest and belly, rather than the brilliant orange of the latter species; by the gray stripe on the forehead contrasting with the darker gray on top of the head, not apparent in C. bernhardi, and by the uniformly gray mid-dorsal region, without the reddish tone of C. bernhardi. Differs from its also closest geographically neighbor C. cinerascens (Fig. 6) in all characters, including the uniform gray pattern of the dorsal region, dark-ocher sides of the face and light gray extremities, rather than the general dark-gray pattern with reddish mid-dorsum and darker extremities of C. cinerascens. Differs from C. moloch by the dark-ocher sides of the face rather than the brilliant orange, and by the uniformly gray mid-dorsum, without the reddish tone of C. moloch. Differs from C. vieirai in all characters, including dark gray agouti forehead with whitish stripe contrasting with the crown (white or white-agouti in C. vieirai); dark ocher (orangebrown) sideburns (white in C. vieirai); ocher neck, orange-brown chest and light ocher (orange) belly (uniformly light yellow to light orange underparts in C. vieirai); and by the uniformly light ocher (orange) tail (agouti with gray base, blackish middle and whitish tip in C. vieirai). Differs from C. baptista by the gray pattern of the dorsum, flanks and external parts of members (dark gray in C. baptista), graywhite member extremities and light-gray stripe of the forehead (both darkened in C. baptista). Differs from C. brunneus in all traits, especially the gray pattern of the dorsum, flanks and external parts of the members (reddish-brown in C. brunneus), gray-white member extremities (darkened in C. brunneus), and light-gray stripe on the forehead (darkened in C. brunneus). Differs especially from C. hoffmannsi by the darkocher sides of the face and orange ventral parts, rather than the uniform yellowish-white of the latter.

Craniometric variables
The type series of C. miltoni is larger than that of other recently described Callicebus species, comprised of seven specimens. Despite this, the number remains low, hindering an analysis of intraspecific variation and interspecific comparisons of craniometric and external measures within the Callicebus moloch species group. Although all specimens are adults, the number of males (5) exceeds that of females (2). External and craniometric variables of the holotype and paratypes are presented in Table 3.

Natural history
The holotype of C. miltoni was collected in open ombrophilous alluvial forest, with high influence of the Roosevelt River, region of the mouth of the Pombal stream, known as "Curva do Cotovelo" (Fig. 7). In this area, the forest has four strata, with the highest stratum (average height 30 m) characterized by the occurrence of seringueira (Hevea spp.), jatobá  (Oliveira, 2011).
In the region of the Roosevelt River, C. miltoni was found in the high and medium strata of the ombrophilous forest. The first images of the new species (Fig. 8) were of an adult male in the undercanopy of the forest, above Panelas, right bank of the Roosevelt River (Fig. 9). In this region, two groups (composed of four and five individuals, respectively) comprising pairs of adults with juveniles ( Fig. 10) were seen feeding on fruits of ingá (Inga sp.), embaúba (Cecropia sp.; Fig. 11) and cacauí (Theobroma speciosum).
In the region of the mouth of the Guariba River, we located nine groups, most in the medium or high strata of the dense ombrophilous forest. The size of the groups varied between two and five individuals, but it was not possible to precisely estimate group sizes External measurements: HB = Head and body length (Bregma-Ischium) (mm); T = Tail length (mm); HF = Hind foot length (mm); E = Ear length (mm); W = Body mass (g).
Papéis Avulsos de Zoologia, 54(32), 2014 due to the monkeys' escape behavior upon detecting human presence. Some marked traits of the genus Callicebus include territoriality and long-call vocalizations (usually in the morning) as a way of maintaining intergroup distances (Robinson, 1979(Robinson, , 1981Kinzey & Robinson, 1983;Wright, 2013). However, during the rest of the day, their cryptic behavior makes it difficult to locate the animals (Ferrari et al., 2000;Vermeer et al., 2011). Callicebus miltoni also behaves in this way, judging by our field observations.
The vocalizations of C. miltoni groups were critical to locate the animals in the field, and occurred especially early in the morning and in the rainy season. In this season, three out of four observations were aided by the morning long-calls. On only one occasion, we used a playback to locate the groups. The recordings were used to stimulate the response of the animals once located, facilitating closer observation. In the dry season, morning calls were less intense. Therefore, the playbacks were essential to locate the groups, and contributed to the five observations made in this season.
The seasonality of C. miltoni vocalizations followed the pattern known for other Callicebus species, e.g., C. brunneus (Wright, 2013). In that study, morning calls during the time of highest fruit availability (rainy season) were related to territorial defense and access to resources.

Conservation
The geographic distribution of C. miltoni is approximately 4,921.540 ha, mostly located in the state of Mato Grosso (3,379.637 ha -69%). The remaining area is in the state of Amazonas (1,455.223 ha -29%), and a small portion (86,682 ha -2%) on the eastern edge of Rondônia.
Approximately 25% (1,246.382 ha) of the area of C miltoni is located in conservation units, five of those sustainable use preserves (746,818 ha) and three of those entirely protected (499,564 ha Landscape mapping, based on data from PRODES and DEGRAD-INPE (Irgang, 2011) to map the spatio-historical process of occupation of the conservation units of northwest Mato Grosso (Reserva Extrativista Guariba-Roosevelt, Parque Estadual Tucumã, Estação Ecológica do Rio Madeirinha and Estação Ecológica do Rio Roosevelt), shows that 86% of the deforestation occurs in the Reserva Extrativista Guariba-Roosevelt. In this area, which includes the type locality of C. miltoni, the greatest threats to the landscape are possible damning of the Roosevelt River, the deforestation of the Áreas de Proteção Permanente, and fire. Hunting does not appear to present a risk to the species in the region, although this may eventually happen, especially in indigenous territory. Capture of primate infants to be used as pets is frequent and common in traditional Amazonian communities. It is not uncommon for people to sell their pets to persons outside the community, and this is one of the potential conservation problems for the new species in the Reserva Extrativista Guariba-Roosevelt.
Starting from the accumulated deforestation by the year 2000 (83,021ha), we note that the occurrence area of C. miltoni was increasingly deforested until 2004, with 47,493 ha registered for that year. After this peak, the rates of deforestation diminished, although they are still high, with 2,775 ha recorded in 2013. The total deforested area calculated for the geographic distribution of C. miltoni is 231,680 ha (4,7% of the total area of occurrence of the species).

Etimology
The new species is named in honor of Dr. Milton Thiago de Mello in recognition of his contribution to development of Primatology. In particular, we note his essential participation in the creation of the Brazilian Primatology Society and of the Latin American Primatology Society, and in the education of most primatologists currently active in Brazil and abroad, among them one of the authors of this paper (JSSJ), through specialized Primatology programs that begun in the 1980s at the Universidade de Brasília.

Vernacular names
"Zogue-zogue" is the term used by the residents of the Reserva Extrativista Guariba-Roosevelt, as well as in all Brazilian Amazonia, to identify primates of the genus Callicebus. Initially, the new species was termed "Firetail titi monkey" due to its light orange tail, which distinguishes it from other Callicebus in Amazonia. After selection of the scientific name, the common name became "Milton's titi monkey".  Figures 1, 2 and 3. To Ayslaner Gallo for the immeasurable help in the field, for characterizing the landscape of the habitat of C. miltoni. We also thank Gustavo Irgang and Rosalvo Rosa and the staff at MapsMut. Adriano Gambarini provided professional images of C. miltoni in its natural habitat. Jamylle de Souza collaborated in data collection regarding the distribution limits of the new species during the Firetail Zogue-Zogue Expedition. We are grateful to Samuel Tararan, coordinator of the Amazonia Program of WWF-Brasil, for his tireless work to facilitate the expeditions that resulted in the discovery of the new species. To Luís Cláudio Barbosa from Conservation International Brasil and Eliane de Oliveira Neves from the GIS Laboratory from the IDSM that drawn the distribution maps of the new species. We also are indebt to Dr. Anita Stone for assistance with translating the manuscript to English, and Stephen D. Nash for the illustration of the new species.