Saguinus mystax ( Spix, 1823 )

Heymann, Eckhard W, 2022, Saguinus mystax (Primates: Callitrichidae), Mammalian Species 54 (1024), pp. 1-14 : 1-5

Saguinus mystax ( Spix, 1823)

Mustached Tamarin

Midas mystax Spix, 1823:29 . Type locality “in sylvis flumina inter Solimöens et Iça [= in forests between Rio Solimões and Rio Icá];” restricted to the south bank of the Rio Solimões near São Paulo de Olivença by Hershkovitz (1977:698).

Midas pileatus I. Geoffroy Saint-Hilaire and Deville, 1848:499 . Type locality “ Brésil, sur le Rio-Javary [= Brazil, on the Javary River];” redetermined as Lago de Tefé by Hershkovitz (1977:699; see “Nomenclatural Notes”).

Hapale pileata : Gervais, 1854:152. Name combination.

H [apale] mystax : Wagner, 1855:129. Name combination.

Jacchus mystax : Gerrard, 1862:29. Name combination.

Hapale (Midas) mystax : Trouessart, 1878:138. Name combination.

Midas pileatus juruanus von Ihering, 1904:416 . Type locality “Juruá River,” Brazil.

L [eontocebus]. mystax : Cabrera, 1912:29. Name combination.

Leontocebus pileatus : Elliott, 1913:197. Name combination.

[ Mystax ] mystax : Pocock, 1917:256. Name combination.

Hapale (Leontocebus) mystax : Lampert, 1926:611. Name combination.

Mystax pluto Lönnberg, 1926 . Type locality “Ayapuá [Lago], Rio Purus,” Brazil.

Tamarin mystax : Cruz Lima, 1945:220. Name combination.

Tamarin pileatus : Cruz Lima, 1945:228. Name combination.

Tamarin pluto : Cruz Lima, 1945:238. Name combination.

Marikina mystax : Hershkovitz, 1949:412. Name combination.

Marikina pluto : Hershkovitz, 1949:413. Name combination.

Marikina pileata pileata : Hershkovitz, 1949:413. Name combination.

Marikina pileata juruana : Hershkovitz, 1949:413. Name combination

Tamarinus mystax : Hill, 1957:115. Name combination.

Tamarinus pluto : Hill, 1957:218. Name combination.

Tamarinus pileatus : Hill, 1957:218. Name combination.

Saguinus mystax : J. B. Deinhardt, Devine, Possovoy, Pohlmann, and F. Deinhardt, 1967:13. First use of current name combination (see “Nomenclatural Notes”).

Saguinus (Saguinus) mystax : Napier and Napier, 1967:299. Name combination.

Saguinus pluto : Napier and Napier, 1967:299. Name combination.

Saguinus pileatus : Napier and Napier, 1967:299. Name combination.

Saguinus (Tamarinus) mystax : Egozcue, Perkins, and Hagemenas, 1968:82. Name combination.

Saguinus mystax mystax : Hershkovitz, 1968:563. Name combination.

Saguinus mystax pluto : Hershkovitz, 1968:563. Name combination.

Saguinus mystax pileatus : Hershkovitz, 1968:563. Name combination.

Saguinus mistax D’Alessandro, Eberhard, de Hincapie, and Halstead, 1986:285 . Incorrect subsequent spelling of Midas mystax Spix, 1823 .

CONTEXT AND CONTENT. Order Primates , suborder Haplorrhini , infraorder Simiiformes , parvorder Platyrrhini , family Callitrichidae . Saguinus mystax currently has three subspecies ( Hershkovitz 1977; Rylands and Mittermeier 2013):

S. m. mystax ( Spix, 1823) . See above.

S. m. pileatus (I. Geoffroy Saint-Hilaire and Deville, 1848) . See above.

S. m. pluto ( Lönnberg, 1926) . See above.

NOMENCLATURAL NOTES. The list of synonyms for Saguinus mystax is adopted from Hershkovitz (1977). He quoted Anderson et al. (1967) for the first use of the current name; however, he apparently was not aware of the paper by Deinhardt et al. (1967) that was published in the same issue of Laboratory Animal Care but ahead (pp. 11–29) of Anderson et al. (pp. 30–40) and should, therefore, be given precedence.

Napier and Napier (1967) listed mystax , pileatus , and pluto as distinct species. Groves (2001) considered S. m. pileatus (redcap mustached tamarin) sufficiently distinct from S. m. mystax (Spix’s mustached tamarin) and S. m. pluto (white-rump mustached tamarin) to justify its status as S. pileatus . This, however, isolated the distribution of S. m. pluto from S. m. mystax , which would be biogeographically implausible. Genetic analyses might result in elevating all three subspecies to species rank.

DIAGNOSIS

Saguinus mystax has a broad white mustache (hence the common name “mustached tamarin”; Fig. 1 ) and generally blackish brown fur on the entire back and underparts. This distinguishes it from the closely related Saguinus labiatus (redbellied tamarin) that has a much narrower mustache with red underparts and Saguinus imperator (emperor tamarin) that has a strongly lengthened mustache with grayish or brownish agouti fur. The broad white mustache and blackish brown fur distinguish S. mystax from sympatric tamarins in the genus Leontocebus (saddle-back tamarins) where the area around the mouth is grizzled and fur on the upper back (“mantle” or “saddle”) is generally different from the lower back (which gave rise to the common name “saddle-back tamarin”). Saguinus mystax is also larger than sympatric species of Leontocebus : mean head– body length of S. mystax (subspecies combined) 235–280 mm and Geoffroy’s saddle-back tamarin Leontocebus nigrifrons 190–236 mm ( Hershkovitz 1977). Saguinus m. pileatus is distinguished from the nominate form by its rusty red forehead and crown and from S. m. pluto by whitish hairs of the perineum and ventral tail base.

GENERAL CHARACTERS

All three subspecies of Saguinus mystax have blackish, black, or brown hairs on the body and limbs. Depending on the subspecies and body part, hairs are ticked orange or buffy ( Fig. 1 ). Skin around the mouth and nostrils is unpigmented and covered with white hair, except for black hair in the midline of the chin.

With a body mass of 450–650 g, S. mystax is among the largest members of the genus. Females are slightly heavier than males, and populations of S. m. mystax vary in body mass ( Table 1). Few data for S. m. pileatus suggest a similar range of body mass; no body mass data are available for S. m. pluto . Hershkovitz (1977) gave 257 mm (range 235–280, n = 22) as mean head–body length and 390 mm (365–424 mm, n = 22) as mean tail length for subspecies and sexes combined. For a population of S. m. mystax at Río Manití ( Peru), mean head–body length and tail length (± SD) were 242 ± 8 mm (n = 75) and 382 ± 18 mm (n = 72) for adult males and 246 ± 11 mm (n = 60) and 387 ± 21 mm (n = 57) for adult females, respectively ( Soini and de Soini 1990a; SD calculated from SE and sample size provided in this reference).

Mean skull dimensions (mm; subspecies and sexes combined) were: greatest skull length 54.0 (range 51.1–55.7, n = 46), condylobasal length 42.1 (40.0–43.9, n = 22), braincase length 45.6 (43.1–47.4, n = 28), braincase width 28.7 (27.1– 30.1, n = 28), zygomatic breadth 34.7 (30.6–36.9, n = 45), mandible length 32.5 (31.0–33.7, n = 22), mandible height 19.4 (18.3–20.9, n = 22), and length of upper postcanine toothrow 12.7 (12.0–13.4, n = 22— Hershkovitz 1977).

External genitalia are generally unpigmented; however, black pigment spots can be present on the scrotum, and their number and relative position can be used to identify individuals in the field ( Löttker et al. 2004a). Testicle volume varies among populations (Río Tapiche: 671 ± 114 mm ³, n = 58; Río Tahuayo: 711 ± 148 mm ³, n = 35; Río Manití: 830 ± 258 mm ³, n = 74; means from Soini and de Soini 1990a, SD calculated from SE and sample size in this reference) and seasons, being largest during the breeding season ( Soini and de Soini 1990a; Garber et al. 1996). Garber et al. (1996) reported smaller testicles (564 ± 270 mm ³) for S. mystax on Padre Isla (29 males) and at Quebrada Blanco (17 males), with variation of testicle volume between males residing in the same group. Perhaps due to their large size, testicles are often positioned asymmetrically, which can also be used for individual identification.

The vulva is large and usually ellipsoid but can also form a rounded triangle or be almost round. Mean vulva size (measured as the sum of length and maximum width) varies among populations (Rio Tapiche: 30.4 ± 4.3 mm, n = 52; Río Tahuayo: 34.8 ± 4.7 mm, n = 35; 38.5 ± 6.9 mm, n = 59; Soini and de Soini 1990a, SD calculated from SE and sample size in this reference). The vulva is often swollen during receptive periods ( Soini and de Soini 1990a).

Females have a conspicuous prominent suprapubic gland that becomes fully developed at about 1.5 years old or later ( Soini and de Soini 1990a); it is 8.5 ± 2.9 mm wide (range 4–15 mm, n = 127; Soini P., personal communication, 31 March 1997) and can vary in size parallel to variation of vulva size ( Soini and de Soini 1990a). The suprapubic gland is hardly developed in males ( Soini and de Soini 1990a; Garber et al. 1996).

DISTRIBUTION

Saguinus mystax is distributed in the western Amazonian lowland rainforests of Peru and Brazil ( Fig. 2 ; Hershkovitz 1977; Rylands et al. 1993). Throughout its distribution, it is sympatric with saddle-back tamarins ( Leontocebus cruzlimai [Cruz Lima’s saddle-back tamarin], Leontocebus fuscicollis avilapiresi [Ávila Pires’ saddle-back tamarin], Leontocebus fuscicollis fuscicollis [Spix’s saddle-back tamarin], Leontocebus nigrifrons , and Leontocebus weddelli melanoleucus [white saddle-back tamarin]).

The nominate S. m. mystax occurs in Peru south of Rio Amazonas, west to Río Ucayali and Río Tapiche ( Soini and de Soini 1990a; Aquino and Encarnación 1994). There is discrepant information concerning its southern limit. Hershkovitz (1977) identified the southern boundary to be Río Urubamba and Río Inuya, based on a single specimen from the upper Río Ucayali (locality 110 in Hershkovitz 1977:684). Aquino and Encarnación (1994) stated Río Inuya, and R. Aquino (personal communication, Universidad Nacional Mayor San Marcos, Lima, 7 February 2022) confirmed that he saw S. m. mystax only on the right (north) bank and S. imperator subgrisescens on the left (south) bank of this river. Hershkovitz (1977) also included the area between Río Huallaga and Río Ucayali as part of the distribution of S. m. mystax , based on a specimen collected by H. Bluntschli in 1927 (locality 96 in Hershkovitz 1977:684). Nevertheless, despite many years of research in the basins of Río Pacaya and Río Samiria, S. m. mystax has not been encountered in this area ( Soini and de Soini 1990a).

In Brazil, S. m. mystax is distributed south of Rio Solimões and largely restricted to the west of Rio Juruá ( Hershkovitz 1977). Peres (1990) reported S. m. mystax from Jaraqui on the east bank of the lower Rio Juruá, and Johns (1985) encountered S. m. mystax on the west bank of Rio Tefé (east of the lower Juruá), being replaced by S. m. pileatus on the east bank of Rio Tefé.

Saguinus mystax pileatus is endemic to Brazil, where it occurs south of Rio Solimões, west of Rio Purus ( Hershkovitz 1977). Although Hershkovitz (1977) indicated that it occurred west to the lower Rio Juruá, Johns (1985) found that Rio Tefé (the type locality) represented its western limit. A specimen from “Juruá (Rio), Amazonas” (locality 174b in Hershkovitz 1977:684) suggested that S. m. pileatus extended west to Rio Juruá above the headwaters of Rio Tefé. The southern limit is not well defined, but it extends to the south of Rio Pauini and Rio Inauini where S. m. pileatus seems to occur in parapatry or sympatry with S. i. subgrisescens ( Sampaio et al. 2018).

Distribution of S. m. pluto is not yet well defined. According to Rylands et al. (1993), it is delimited by Rio Purus in the east, Rio Coarí in the west, and Rio Tapauá in the south. Hershkovitz (1968, 1977) considered the area between Rio Solimões, Rio Purus, and Rio Madeira, south to at least 7° or 8° latitude as its distribution, which would make it sympatric with S. labiatus ; however, this is unlikely given the ecological similarity between the two species ( Rylands et al. 1993). Haugaasen and Peres (2005) reported a “black-capped” mustached tamarin from Lago Uauaçú, west of Rio Purus, and emphasized its phenotypic difference from S. m. pileatus and similarity to S. m. mystax , making it likely that they saw S. m. pluto (although they used S. m. pileatus in their table 2:250). Presence of S. m. pluto in the Pando Department of Bolivia, as reported by Izawa and Bejarano (1981), remains doubtful because it has not been verified by other studies in that area ( Cameron and Buchanan-Smith 1991; Buchanan-Smith et al. 2000).

FORM AND FUNCTION

Saguinus mystax possesses the dental formula typical for all callitrichids except Goeldi’s monkey Callimico goeldii : i 2/2, c 1/1, p 3/3, m 2/2, total 32 ( Hershkovitz 1977). Lower incisors of S. mystax are low-crowned compared with canines ( Fig. 3 ), creating the so-called “long-tusked” condition ( Napier and Napier 1967). Canines are used to open fruit husks, particularly hard or leathery pods of legumes from the genera Parkia and Inga (Heymann E.W., personal observation). An isolated population of S. m. mystax has high levels of dental variation ( Tornow et al. 2006).

Saguinus mystax has a broad spectrum of locomotor behaviors, but quadrupedal walking and leaping, mainly between horizontal substrates, are most frequently used ( Norconk 1986; Garber 1991; Garber and Pruetz 1995; Berles et al. 2022). In contrast to sympatric Leontocebus nigrifrons , it rarely leaps between vertical substrates. The long tail is used for balancing, particularly while moving on narrow substrates and during leaps wave lengths, located on the X-chromosome, comes in three alleles, coding for opsins with maximum sensitivity at 425 nm, 543 nm, and 563 nm ( Surridge and Mundy 2002; Smith et al. 2012). Field observations and captive experiments support the notion that the color vision polymorphism is maintained through a heterozygote advantage and frequency-dependent selection on the different color vision phenotypes ( Smith et al. 2003, 2012).

(Heymann E.W., personal observation). Gait sequence patterns are influenced by substrate size and inclination, with symmetrical gaits used at a higher rate on small supports, diagonal sequences predominantly used on inclines, and lateral sequences on declining substrates ( Nyakatura and Heymann 2010).

Like all other Neotropical primates except for Alouatta , S. mystax has a polymorphic color vision system, where all males and one-third of females are dichromats and two-thirds of females are trichromats. The opsin gene for long and middle

ONTOGENY AND REPRODUCTION

Ontogeny. —Infants are born with the mustache. They are nursed during the first 3 months of life; thereafter, attempts to suckle are rejected by the mother. The order of eruption of permanent teeth in Saguinus mystax is M1-I1-I2-M2-P3-P2-P1-C and m1-i1-i2-m2-p3-p1-p2-c; eruption starts at about 4 months and is completed at about 11 months ( Soini and de Soini 1990b). Adult body size is reached at about 12 months, but genitals and the suprapubic gland remain smaller than in fully adult individuals (>18 months— Soini and de Soini 1990a).

From birth onward, infants are mainly carried by adult males and other adult and subadult group members ( Fig. 4 ; Garber 1997; Huck et al. 2004a). Infants are carried on the back and make their first excursions off their carrier at about 3 weeks of age. They start to eat solid food, begging from other group members, at 4–5 weeks of age ( Huck et al. 2004c). Begging behavior can continue until the end of the first year of life, particularly for foods that are difficult to handle for infants and juveniles ( Heymann 1996; Huck et al. 2004c), and is associated with specific vocalizations.

Reproduction. —Length of the ovarian cycle has not been determined for Saguinus mystax , but it is about 23 days in S. oedipus (cotton-topped tamarin— Brand 1981; French et al. 1983; Heistermann et al. 1989). Based on captive observations, Sicchar and Heymann (1992) suggested slight changes in vulva coloration as external signs of estrus, but this was not substantiated by observations in the wild ( Löttker et al. 2004b). Gestation lengths have been estimated at 150–160 days in S. mystax ( Löttker et al. 2004b) and 160 days in S. bicolor (pied tamarin— Heistermann et al. 1987) but 184 days in S. oedipus ( Ziegler et al. 1987) .

Births are somewhat seasonal. Forty of 51 births (=78%) of S. m. mystax were recorded in November–February ( Soini and de Soini 1990a), corresponding with the early to mid-rainy season in northeastern Peruvian Amazonia. Ten of 14 births of S. m. pileatus took place in June to early October (dry season), the others in December–January (early rainy season— Peres 1991). Interbirth intervals are mostly 11–12 months (range 8–14 months; Soini and de Soini 1990a); in two females monitored over 3 years, mean interbirth interval was 334 days (254–369 days; Löttker et al. 2004b). No evidence of postpartum estrus was found in wild S. mystax ( Löttker et al. 2004b) .

Modal litter size is two ( Soini and de Soini 1990b). As for other callitrichids, twins are likely to be dizygotic and exhibit various levels of chimerism ( Benirschke and Brownhill 1962). Garber et al. (1993) reported one of two adult females> 12 years of age was still reproductive. Two males (father and son) were>13 and 11 years old when they disappeared (Heymann E.W., in litt.).

Figures

Fig. 1.—A wild young adult female Saguinus mystax mystax at the Estación Biológica Quebrada Blanco, a field research site in northeastern Peru (Heymann and Tirado Herrera 2021; Heymann et al. 2021). Used with permission of photographer Caroline Elisabeth Haas.

Fig. 2.—Distribution of Saguinus mystax based on maps and information in Hershkovitz (1977), Soini and de Soini (1990a), Rylands et al. (1993), Sampaio et al. (2018), and Rowe and Myers (2017). Base map by Mark Denil, Conservation International; map drawn by Stephen D. Nash, IUCN SSC Primate Specialist Group.

Fig. 3.—Dorsal, lateral, and ventral views of skull, and lateral view of mandible of an adult female Saguinus mystax pluto (Museum für Naturkunde Berlin, ZMB_Mam_35797). Greatest skull length is 55 mm. Copyright Hwa Ja Götz (MfN).

Fig. 4.—An adult male Saguinus mystax mystax carrying about 2-month-old twins in tierra firma rainforest at the Estación Biológica Quebrada Blanco, Peru. Used with permission of photographer Mojca Stojan-Dolar.