Callicebus vieirai, Gualda-Barros & Nascimento & Amaral, 2012

Gualda-Barros, Juliana, Nascimento, Fabio Oliveira Do & Amaral, Marilia Kerr Do, 2012, A New Species Of Callicebus Thomas, 1903 (Primates, Pitheciidae) From The States Of Mato Grosso And Pará, Brazil, Papéis Avulsos de Zoologia (São Paulo) 52 (23), pp. 261-279 : 261-279

Callicebus vieirai sp. nov.

Holotype: MZUSP 34663 (field number PEV 747-748), skin and skull, adult male, collected by

Marília Kerr in the type locality on April 7 th, 1997 during an expedition conducted by Dr. Paulo Emílio Vanzolini; left coronoid process damaged.

Paratypes: MZUSP 25441 (field number JLSilvaFº 105), skin and skull, adult female, collected in November 22 nd, 1988, by J.L. Silva-Filho in the Largo do Souza , Rio Iriri, Pará, Brazil; the skull is very damaged, presenting only the nasals, the frontals, most part of parietals, part of the left orbit and a small part of the premaxilla, that support the upper left and right first incisors and the upper left second incisor; most part of the left side of the mandible is lost . MZUSP 25442 (field number JLSilvaFº 106), skin and skull, adult male collected in November 22 nd, 1988, by J.L. Silva-Filho in the Largo do Souza , Rio Iriri, Pará, Brazil; the skull is partially damaged, with the left side of the facial region lost . MZUSP 25443 (field number JLSilvaFº 107), skin and skull, adult male collected in November 22 nd, 1988, by J.L. Silva-Filho in the Largo do Souza , Rio Iriri, Pará, Brazil; the most part of the left side of skull is damaged, with the frontal, part of the parietal and squamosal bones, including the zygomatic arch, absent .

Type locality: Rio Renato , tributary of Rio Teles Pires (right bank), nearby the city of Cláudia, state of Mato Grosso, Brazil (11°33’00.15”S, 55°10’59.98”W; about 370 m above sea level) ( Fig. 1 ) .

Distribution: Known from three distant localities of the Brazilian states of Mato Grosso and Pará. In the state of Mato Grosso, the species occurs in the type locality, and a nearby Ribeirão Carmelita (tributary of Rio Azul) (11°01’00.15”S, 54°28’59.99”W) where two specimens were sighted by one of us (M.K.) but were not collected. Besides, the species possibly occurs in a third locality, Juína, in the northwestern Mato Grosso, where a male and a female were seized by Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis ( IBAMA) and further were led to the Parque Zoológico Municipal Quinzinho de Barros (Sorocaba, state of São Paulo; Rodrigo Teixeira, pers. comm.). However, there is not more information that indicates a more precise point in Juína region where the animals was caught. In the state of Pará, Callicebus vieirai occurs in Largo do Souza, Rio Iriri (04°00’S, 53°00’W), in Rio Xingu.

the white coloration present in the forehead, the crown and the beard, surrounding the dark face ( Figs. 2-4 , 7 ).

Measurements: see Table 1.

Description of holotype

External morphology and pelage ( Figs. 2-4 , Tables 1-3): Length of head and body smaller than length of tail, Habitat: The locality where the holotype was collect- ed may be described as a tropical evergreen rainforest, composed by medium-sized trees (20 meters high, but some them emerging up to 30-35 meters) with lianas and forming a discontinuous canopy. The understory is relatively dense and well stratified, and the forest floor is thick. Along the Rio Renato and nearby igarapés there are some conspicuous specimens of moriche palm ( Mauritia flexuosa ) in swampy soil. During the collection of the holotype, another individual, possible the partner, was sighted. Six days later (April 13, 1997), another individual was vocalizing at this place on a 10 m high tree. In the nearby Ribeirão Carmelita, in April 12 th, 1997, at 17:50 o’clock, two other individuals, apparently a couple, were seen in a narrow strip of forest along the river, each individual on a different bank.

Etymology: This new species is named to honor Dr. Carlos Octaviano da Cunha Vieira (1897-1958), mammalogist and Curator of the Mammal Collection at the Museu de Zoologia da Universidade de São Paulo ( MZUSP), Brazil, from 1941 to 1958. During this period, the efforts of Vieira contributed to the development of the Mammal Collection of the MZUSP and he also published several scientific articles that improved the knowledge on Brazilian mammals and birds.

Diagnosis: It is a medium-sized species of the C. moloch group, with overall coloration pale grayish brown agouti mainly in the crown, nape, dorsum, tail and the dorsal sides of the limbs; hands, feet and tip of tail white; belly and ventral sides of limbs orangish. Clearly distinct from other members of the species group by which is 60% of total length of the specimen. Forehead, sideburns and beard white, surrounding the blackish pigmented face; some white vibrissae present in the face around mouth and nostrils; between face and forehead there is a very narrow stripe of vibrissae with larger blackish bands alternating to narrower white bands. Crown and nape indistinct, pale grayish agouti, lighter than the dorsum, and showing shorter hairs (1 cm). Dorsum and flanks pale grayish-brown agouti with longer hairs (5 cm). Coloration of proximal outer surface of fore and hind limbs is indistinct from that of dorsum and flanks, but becomes gradually lighter and whitish on the distal portions; hands and feet (cheiridia) are whitish. Venter and inner sides of fore and hind limbs uniformly orangish, hairs not banded. Base of tail darker than dorsum, but in the middle region the pattern become similar to the dorsum, and the tip of tail is whitish. Face, ventral side of hands and feet, ears and genitals blackish.

Skull ( Fig. 5 , Tables 1, 2 and 4): the skull has an overall similarity to that others C. moloch group species. The squamosal portion of the zygomatic arch, in lateral view, is wide on the anterior region, becoming narrow towards to posterior region. The pterygoid has a small hamular process and the lateral lamina is well developed. The posteromedian palatine spine is absent. The pterygoid fossa is Ω-shaped and its anterior border is slightly convex. The supraorbital crests are well developed. The frontal bone is depressed behind the supraorbital ridges. The frontal sinus in the glabella is slightly inflated. One infraorbital foramen on the left and two on right side. Auditory bulla comparatively large, the first third is flattened and the other two thirds bilobated and more inflated. The jugular foramen is reniform, with the right one showing a small septum. The foramen hypoglossal is rounded, smaller than the jugular foramen and localized very next each other. The lambdoidal suture does not rise towards the sagital suture, remaining in a nearly horizontal plane. Mandibular body relatively high. The coronoid process long, hook-like shaped and extending above the condilar process.

Variation

External morphology and pelage ( Fig. 6 , Tables 1, 2 and 3): In the holotype ( Fig. 2 ), the white frame present in the forehead is wide and evident,

whereas in specimens from Rio Iriri it is narrow and less evident ( Fig. 6 ). The grayish-brown agouti coloration of the dorsum is darker in the paratypes, especially in MZUSP 25441 . Inner side of fore limbs is slightly more orangish in MZUSP 25441 and whitish in MZUSP 25442 . Hands and feet are grayish in MZUSP 25441 and MZUSP 25442 . Chest and venter slightly more orangish in MZUSP 22441 and MZUSP 22443 .

Skull ( Tables 1, 2 and 4): the upper border of orbits of all paratypes is less salient than the holotype. In MZUSP 25443 the infraorbital foramen is proportionally larger.The squamosal portion of the zygomatic arch in MZUSP 22442 , in lateral view, is narrower. In MZUSP 25443 the hypoglossal foramen is not visible while in MZUSP 25442 it is and it is also closer to the occipital condyle than to the jugular foramen, which is piriform in this specimen. The posterior portion of the auditory bulla is more inflated in MZUSP 22442 and slightly narrower in MZUSP 22443 . The anterior border of pterygoid fossa is slightly concave in MZUSP 22443 .

Comparisons

The species of the C. moloch group are distributed around the area of occurence of C. vieirai . Another species, C. pallescens , of the C. donacophilus group is distributed south to C. vieirai and has a similar coloration pattern.

C. vieirai is readily distinguished from C. moloch by the white beard and sideburns, the whitish agouti hands, feet and outer side of limbs, light orange throat, chest and belly, while in C. moloch the beard and sideburns are orange, the throat, chest and belly are dark orange, the hands and feet are buffy, and outer side of limbs are buffy or grayish to pale brown agouti ( Figs. 3 and 4 ).

C. vieirai is distinguished from C. cinerascens by the pale grayish-brown agouti coloration of dorsum, and crown, sideburns, beard, hands and feet are white or whitish, while C. cinerascens shows reddish brown agouti coloration in dorsum, and crown, sideburns, beard, hands and feet are grayish agouti.

C. vieirai is distinguished from C. baptista by white or whitish agouti forehead, white sideburns, pale grayish brown agouti dorsum, pale yellowish coloration in the throat, chest and belly, whitish agouti hands and feet, instead of a blackish to grayish agouti forehead, dark reddish brown sideburns, throat, chest and belly, blackish to grayish agouti dorsum, and blackish to grayish hands and feet.

C. vieirai differs from C. brunneus by the overall coloration of body a pale grayish brown agouti instead of dark brown agouti, and crown, sideburns, beard, hands and feet white or whitish instead dark brown.

C. vieirai differs from C. hoffmannsi by possessing a grayish tail instead of blackish, by the white sideburns and beard instead of yellowish or orangish, and hands and feet white or whitish instead dark grayish agouti.

C. vieirai differs from C. pallescens by the white or whitish agouti forehead instead pale grayish agouti or orangish agouti, and by the absence of a perceptible white ear tufs.

Table 3 summarizes the comparisons of color patterns in the studied species.

The species of the C. moloch group have great similarity in skull morphology and morphometrics ( Table 4), as well as a wide individual variation of skull characters. Thus, there are few skull characters that may be used to distinguish the species of group.

The chromatic fields of pelage coloration easily distinguish the species. The distinctive pattern of coloration of each species of Callicebus may be an adaptation to recognize conspecifics, and may operate like a mechanism of reproductive isolation, especially among sympatric species, avoiding or reducing the probability of hybridization. For example, in four marmoset species ( Callithrix kuhli , C. penicillata , C. jacchus , and C. geoffroyi ) the recognition behaviors related to facial color pattern may be interpreted as responsible for reproductive isolation mechanisms ( Cavalcanti & Langguth, 2008). These authors observed that intruders of the same species of resident individuals, recognized by the animals as potentially sexual competitors, were responsible to stimulate more responses than did intruders of different species bearing different facial color patterns, and this can be an indication of species level recognition. Further, Cavalcanti & Langguth (2008) also suggested that if a the intruder individual is not recognized as a potencial reproductive partner of the resident mate, showing low frequency of tuft flicking and genital display, then the matting and consequent hybridization among the species of Callithrix studied will be more difficult.

According to our data, C. vieirai has at least records from three separated geographical samples ( Fig. 1 ). Two of them are located in the State of Mato Grosso, nearby the city of Cláudia, including the Rio Renato, Ribeirão Carmelita and surrounding areas, and another in the region of Juína, while a third sample occurs in the Largo do Souza, Rio Iriri, center-northwestern Pará. The records from Cláudia and surroundings and from Largo do Souza occur within the area of distribution of C. moloch ( Fig. 1 ), suggesting the existence of an overlap in their respective geographic range. Nevertheless, the characters of C. vieirai are not within the variation observed in the specimens of C. moloch studied. The latter species shows a broader distribution, occupying the easternmost portion of general distribution of the group, occurring from the west bank of Rio Tocantins-Araguaia to the east bank of the Rio Tapajós in Pará, southwards to the headwaters of the Rios Araguaia, Xingu, and Tapajós in northern Mato Grosso and westwards to the eastern bank of the Rio Ji-Paraná in Rondônia and east bank of the Rio Aripuanã in Amazonas ( Fig. 1 ) ( de Vivo, 1985; de Vivo, unpublished data; Hershkovitz, 1990). On the other hand, according to Van Roosmalen et al. (2002) [and subsequently Pimenta & Silva Júnior (2005)], the southwestern limit of this species is the Rio Juruena, and the Juruena-Ji-Paraná interfluvium is inhabited by a new species, C. bernhardi , described by them and consequently the samples of Callicebus from this area can be assumed to belong to this species. According to Van Roosmalen et al. (2002), C. bernhardi is distinguished of C. moloch by its grayish forehead and crown, white ear tufts, and blackish tail with a distinct white pencil. However, our analysis and comparisons between the samples of Rondônia and other localities of C. moloch (e.g., Fordlândia) suggest that there are not significant differences in the variation of the chromatic fields and the same variations described for C. bernhardi are found in specimens from distinct localities. In other words, the sample of Rondônia is not different from the other C. moloch samples, which agrees with the results obtained by Auricchio (2010), who suggested that C. bernhardi is a junior synonym of C. moloch .

Furthermore, the Rio Ji-Paraná apparently is not an efficient barrier to C. moloch . Ferrari et al. (1996, 2000) recorded the presence of C. moloch in the left bank of the Rio Ji-Paraná and also in two localities far away, between the Serra dos Pacaás Novos, to the north, and the Chapada dos Parecis, to the south, where it shows evidence of a contact zone with C. brunneus . Considering the wide geographical range of C. moloch , we cannot reject the possibility sympatry between this species and C. cinerascens in the Rio Roosevelt – Rio Aripuanã interfluvium. Hershkovitz (1990) and de Vivo (unpublished data) suggested the occurrence of sympatry between these species in this region, however further studies in the field are necessary to confirm this hypothesis. Besides, Van Roosmalen et al. (2002) suggested that the region between the right bank of Rio Sucundurí and Rio Aripuanã and the left bank of the Rio Juruena might be inhabited either by C. hoffmannsi , which would extend its geographic range further southwards, or by a species not described yet. Within this region we recorded the specimens of C. vieirai from the Juína region, which is located in the left bank of the Rio Juruena.

Van Roosmalen et al. (2002) affirmed that the species of the cupreus and moloch groups are adapted to disturbed habitats and cannot occur sympatrically, due to them occupying the same ecological niche and therefore belonging to the same “ecospecies”. Further, the authors also argued that sympatry in Callicebus only occur between members of the moloch / cupreus groups and the torquatus group species, and that it is very common due to the fact that these species exhibit different habitat preferences, dietary requirements, and foraging behavior. However, the ecological niche is just another attribute of a species, not a defining attribute ( Groves, 2001), and as the evidences had previously shown, especially the sympatry between C. vieirai and C. moloch , they suggest a view contrary to Van Roosmalen et al. (2002).

According to Ferrari et al. (1996), the zoogeography of platyrrhines in southwestern Brazilian Amazonia is much more complex than it had been assumed previously. Herein, we also reinforce this affirmation and further expand it to the other regions, especially the southern and eastern parts of the Brazilian Amazonia. Additional studies, including the collection of specimens in order to suppress the geographic sample gaps, the meticulous identification of the taxa from these regions, and the application of phylogenetic studies using combined morphological, karyological and molecular data will improve the understanding of relationships among taxa of the same and different Callicebus species group, and also their respective evolutionary and biogeographic histories.

Conservation

In the last decades, the regions where Callicebus vieirai was recorded has suffered from constant human made changes, such as substitution of forested areas by cultivations of soybean, to raising livestock, explorative logging, and the construction of hydroelectric power plants along the main drainages of the region ( Alho & Martins, 1995; Pivello & Coutinho, 1996; Pavan 2001; 2007; Pivello, 2003; Klink & Machado, 2005). Some of these activities, especially livestock raising and logging, were observed on the vicinities of the type locality already in 1997. Callicebus vieirai has an unknown conservational status and further studies may reveal the real status for this species. Furthermore, the Parque Zoológico Municipal Quinzinho de Barros, Sorocaba, keeps live seven specimens of C. vieirai in exhibition ( Figure 7 ), that were mistakenly identified as Callicebus moloch donacophilus . As previously mentioned, the original couple is from the Juína region, in northwestern Mato Grosso.

Figures

FIGURE 1: Distribution of the specimens of Callicebus studied. Numbered points correspond to collection localities listed in the gazetteer (see Appendix 2).

FIGURE 2: Side view (above) and front view (bottom) of the head of the holotype of Callicebus vieirai (MZUSP 34663), showing the remarkable white circle around the face. Photographs by Fernando M. d’Horta.

FIGURE 3: Dorsal view of the skin of C. vieirai (MZUSP 34663; holotype) (left) and a male of C. moloch (MZUSP 10152) (right) from Itapoama, Pará, Brazil. Photographs by Mario de Vivo. Tail length modified due to process of preparation of skin.

FIGURE 4: Ventral view of the skin of C. vieirai (MZUSP 34663; holotype) (left) and a specimen of C. moloch (MZUSP 10152) from Itapoama, Pará, Brazil. Photographs by Mario de Vivo. Tail length modified due to process of preparation of skin.

FIGURE 5: Skull of the adult male holotype of C. vieirai (MZUSP 34663). The left coronoid process is damaged. Photographs by Marcus Vinícius Brandão.

FIGURE 6: Detail view of the head of C. vieirai paratypes (from Rio Iriri, Pará, Brazil), showing the variation color pattern in forehead: MZUSP 25441 (female) (left), MZUSP 25442 (male) (center) and MZUSP 25443 (male) (right). Photographs by Luciano Moreira Lima.

FIGURE 7: Specimens of C. vieirai kept in the Parque Zoológico Municipal Quinzinho de Barros, Sorocaba, Brazil. Photographs by Juliana Gualda-Barros.