Callicebus miltoni, Dalponte & Silva & Silva Júnior, 2014

Dalponte, Julio César, Silva, Felipe Ennes & Silva Júnior, José de Sousa e, 2014, New species of titi monkey, genus Callicebus Thomas, 1903 (Primates, Pitheciidae), from Southern Amazonia, Brazil, Papéis Avulsos de Zoologia (São Paulo) 54 (32), pp. 457-472 : 462-469

Callicebus miltoni sp. nov.

Holotype

MPEG 42654 ( Figs. 1 , 2 A-D, 3A-B); Field number JD 550; Skin, skull and complete skeleton; Adult male; Collected by local hunter and then retrieved by J.C. Dalponte at the type locality. December 2010.

Paratypes

MPEG-42810; Field number FES 04 ; Adult male; Collected by Felipe Ennes Silva in secondary forest near the confluence of the Guariba and Aripuanã rivers (left bank of the Aripuanã River and right bank of the Guariba River : 07°42’42.10349”S, 60°35’31.47013”W), municipality of Novo Aripuanã, Amazonas, Brazil; January 27, 2013 .

MPEG-42811; Field number FES 05 ; Adult male; Collected by Felipe Ennes Silva in secondary forest near the confluence of the Guariba and Aripuanã rivers (left bank of the Aripuanã River and right bank of the Guariba River : 07°43’14.05081”S, 60°35’17.78161”W), municipality of Novo Aripuanã, Amazonas, Brazil; January 28, 2013 .

MPEG-42812; Field number FES 06 ; Adult female; Collected by Felipe Ennes Silva in secondary forest near the confluence of the Guariba and Aripuanã rivers (left bank of the Aripuanã River and right bank of the Guariba River : 07°43’04.16976”S, 60°35’14.70891”W), municipality of Novo Aripuanã, Amazonas, Brazil; January 28, 2013 .

MPEG 42991 ; Field number FES 12; Adult male; Collected by Felipe Ennes Silva and Raimundo Rodrigues da Silva in secondary forest in the left bank of the Aripuanã River , mouth of the Igarapé Jatuarana (07°44’12.24240”S, 60°31’16.16160”W), municipality of Novo Aripuanã, Amazonas, Brazil; August 23, 2013 .

MPEG 42992 ; Field number FES 13; Adult female; Collected by Felipe Ennes Silva and Raimundo Rodrigues da Silva in secondary forest in the left bank of the Aripuanã River , mouth of the Igarapé Jatuarana (07°44’12.24240”S, 60°31’16.16160”W), municipality of Novo Aripuanã, Amazonas, Brazil; August 23, 2013 .

MPEG 42993 ; Field number FES 14; Adult male; Collected by Felipe Ennes Silva and Raimundo Rodrigues da Silva in secondary forest in the left bank of the Aripuanã River , mouth of the Igarapé Jatuarana (07°44’11.17680”S, 60°30’54.83520”W), municipality of Novo Aripuanã, Amazonas, Brazil; August 24, 2013 .

Type locality

Curva do Cotovelo (08°59’45.21”S, 60°43’42.72”W), region of the mouth of the Pombal stream, Reserva Extrativista Guariba-Roosevelt , right bank of the upper Roosevelt River, municipality of Colniza, Mato Grosso, Brazil ( Fig. 4 ) .

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. 1 A-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. 2 A-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. 2 C-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 (orange-brown) 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 ), gray-white member extremities and light-gray stripe of the species group (modified from Gualda-Barros et al., 2012).

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 dark-ocher 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 in Material and Methods.

( Hymenaea intermedia ), roxinho ( Peltogyne catingue ), garapeira ( Apuleia molaris ), copaíba ( Copaifera spp. ), jutaí ( Dialium guianense ), sucupira-preta ( Diplotropis racemosa ), cumaru-champanhe ( Dipteryx odorata ), tento ( Ormosia nobilis ) and faveira ( Parkia sp. ), distributed openly. The undercanopy (average height 15 m) is marked by the occurrence of matamatámirim ( Eschweilera wachenheimii ), aquaricara ( Geissospermum urceolatum ), tachi ( Tachigali alba ), and the palms patauá ( Oenocarpus bataua ), sete-pernas (Sochratea exorrhiza) and açaí ( Euterpe precatoria ). The tree stratum is characterized by Miconia sp. and Psychotria sp. (average height 2 m), distributed openly. The shrub layer (average height 0.1-0.5 m) contains Olyra cf. latifolia , Selaginella conduplicata and Calthea altissima , distributed sparsely ( 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 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, 1981; Kinzey & 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). The species occurs in the Reserva Extrativista Guariba-Roosevelt, Mato Grosso (138,092 ha), but its presence is predicted in various conservation units that comprise the Apuí Mosaic: Parque Estadual Guariba, Amazonas (72,296.331 ha), Reserva Extrativista do Guariba, Amazonas (57,630 ha), Floresta Estadual do Aripuanã, Amazonas (336,040.065 ha), Floresta Estadual de Manicoré, Amazonas (83,381.039 ha), Reserva de Desenvolvimento Sustentável do Aripuanã, Amazonas (224,290.817 ha), in addition to the east side of Parque Nacional dos Campos Amazônicos, Amazonas / Mato Grosso (873,570 ha) and of the Estação Ecológica do Rio Flor do Prado, Mato Grosso (8,517 ha). A significant portion of the species’ distribution area is located within indigenous land (1,555.116 ha – 32%), represented by the Terra Indígena Arara do Rio Branco, Parque do Aripuanã, Kawahiva do Rio Pardo and Aripuanã. Therefore, approximately 57% (2,801.498 ha) of the distribution area of C miltoni is within protected areas, with the remaining 43% (2,120.044 ha) in private areas and/ or settlement areas.

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

FIGURE 1: Skin of the holotype of Callicebus miltoni sp. nov. (MPEG 42654). A) Dorsal view; B) ventral view; C) lateral (right side) view. Photos: Anderson Feijó.

FIGURE 2: Skin of the holotype of Callicebus miltoni sp. nov. (MPEG 42654): A) Dorsal view of the head; B) Lateral view (left side) of the head; C) Ventral view of the tail; D) Dorsal view of the tail. Photos: Anderson Feijó.

FIGURE 4: Geographic distribution of Callicebus miltoni sp. nov. Records numbered as in the Table 1.

FIGURE 5: Holotype of Callicebus miltoni sp. nov. before taxidermy, showing the whitish stripe of the forehead, dark-ocher sideburns and the orange tail. Photo: Jorge Lopes.

FIGURE 6: Callicebus miltoni sp. nov., compared to geographically neighboring species (C. bernhardi and C. cinerascens) belonging to the Callicebus moloch species group. Illustration by Stephen D. Nash.

FIGURE 9: Undercanopy of the ombrophilous alluvial forest, typical habitat of the Callicebus miltoni sp. nov. in the Roosevelt River region, Mato Grosso, Brazil. Photo: A. Gambarini.

FIGURE 10: Family group of Callicebus miltoni sp. nov. in the undercanopy of the ombrophilous forest at Panelas, right bank of the Roosevelt River, northwestern Mato Grosso, Brazil. Photo: A. Gambarini.

FIGURE 11: Adult Milton’s titi monkey eating Cecropia fruit while carrying a baby at Roosevelt River, Mato Grosso, Brazil. Photo: A. Gambarini.