Sciurus aureogaster Cuvier, 1829

Koprowski, John L, Nieto-Montes de Oca, Adrián, Palmer, Geoffrey H, Ramos-Lara, Nicolás & Timm, Robert M., 2017, Sciurus aureogaster (Rodentia: Sciuridae), Mammalian Species 49 (951), pp. 81-92 : 81-84

Sciurus aureogaster Cuvier, 1829

Red-bellied Squirrel

[ Sciurus ?] aureogaster F. Cuvier , in É. Geffroy Saint-Hilaire and F. Cuvier, 1829:1. Type locality unknown; restricted to “Alta Mira [= Altamira], Tamaulipas ” by Nelson (1899:38).

Sciurus rafiventer Lichtenstein, 1830:116 . Type locality unknown.

Sciurus leucogaster F. Cuvier, 1831:300 . Type locality unknown.

Sciurus hypopyrrhus Wagler, 1831:510 . Type locality “ Mexico,” restricted to “Minatitlán, Veracruz ” by Nelson (1899:42).

Sciurus nigrescens Bennett, 1833:41 . Type locality unknown; restricted to “the high mountains south and southeast of the town of Aquixtla, in northern Puebla ” by Musser (1970:14).

Sciurus albipes Wagner, 1837:85 . Type locality unknown; stated as “probably from Cerro San Felipe, Oaxaca ” by Musser (1968:97).

Sciurus socialis Wagner, 1837:88 . Type locality unknown; stated as “near Tehuantepec, Oaxaca ” by Nelson (1899:36).

Sciurus mustelinus Audubon and Bachman, 1841:100 . Type locality “ California,” corrected to “lowlands of eastern

Sciurus ferruginiventris Audubon and Bachman, 1841:101 . Type locality “ California,” but corrected to “lowlands of central and southeastern Veracruz ” by Musser (1968:96).

Sciurus varius Wagner , in Schreber, 1843:168. A renaming of specimens originally reported by Wagner (1837) as S. albipes .

Sciurus ferrugineiventris Schinz, 1845:14 . Incorrect subsequent spelling of Sciurus ferruginiventris Audubon and Bachman, 1841 .

Sciurus hypoxanthus (Lichtenstein MS) I. Geoffroy SaintHilaire, 1855:158 . A renaming of specimens originally reported upon by I. Geoffroy Saint-Hilaire (1855).

Sciurus chrysogaster Giebel , in Schreber, 1855:650. An etymological substitute for aureogaster Cuvier, 1829 .

Sciurus hypopyrrhous Gray, 1867:424 . Incorrect subsequent spelling of Sciurus hypopyrrhu s Wagler, 1831.

Macroxus morio Gray, 1867:424 . Type locality unknown.

Macroxus maurus Gray, 1867:425 . Type locality, “ Mexico, Oaxaca.”

Macroxus griseoflavus Gray, 1867:427 . Type locality unknown; restricted to “Dueñas, Guatemala ” by Nelson (1899:67).

Macroxus leucopus Gray, 1867:427 . Type locality “ México, Oaxaca.”

Sciurus aureigaster J. A. Allen, 1877:750 . Incorrect subsequent spelling of aureogaster Cuvier, 1829 .

Sciurus affinis Alston, 1878:660 . Type locality unknown.

Sciurus rufiventris? Rovirosa, 1887:360 . Name applied to specimens from the Macuspana region of Tabasco.

Sciurus cervicalis J. A. Allen, 1890:183 . Type locality “Hacienda San Marcos, Volcán de Fuego, Tonila, Jalisco.”

Sciurus nelsoni Merriam, 1893:144 . Type locality “Huitzilac, Morelos.”

Sciurus wagneri J. A. Allen, 1898:453 . Renaming of occupied Sciurus albipes Wagner, 1837 and Sciurus varius Wagner, 1837 .

CONTEXT AND CONTENT. Order Rodentia , suborder Sciuromorpha , family Sciuridae , subfamily Sciurinae , tribe Sciurini , genus Sciurus , subgenus Sciurus . Two subspecies of S. aureogaster are recognized ( Musser 1968, 1970; Hall 1981; Hoffmann et al. 1993):

S. a. aureogaster Cuvier, 1829:59 . See above ( chrysogaster Giebel , ferruginiventris Audubon and Bachman , hypopyrrhus Wagler , hypoxanthus Lichtenstein , leucogaster F. Cuvier , maurus Gray , morio Gray , mustelinus Audubon and Bachman , rafiventer Lichtenstein , rufiventris Rovirosa are synonyms).

S. a. nigrescens Bennett, 1833:41 . See above ( affinis Alston , albipes Wagner , cervicalis J. A. Allen , chiapensis Nelson, cocos Nelson, colimensis Nelson, effugius Nelson, frumentor Nelson, griseoflavus Gray , hernandezi Nelson, hirtus Nelson, leucopus Gray , littoralis Nelson, nelsoni Merriam , nemoralis Nelson, perigrinator Nelson, poliopus Fitzinger, quercinus Nelson, rufipes Fitzinger, senex Nelson, socialis Wagner , tepicanus J. A. Allen, varius Wagner , wagneri J. A. Allen are synonyms).

NOMENCLATURAL NOTES. Hall (1981) following Musser (1968, 1970) treated Sciurus aureogaster as consisting of 2 subspecies:

S. a. aureogaster and S. a. nigrescens and we have followed their lead. Musser (1968, 1970) commented that because of the considerable variation in color across the geographic distribution of S. aureogaster , the recognition of additional subspecies might be warranted; however, given that more than 60 scientific names and combinations of names have been applied to specimens since the original species description, we concur with him in the recognition of only these 2 subspecies until additional systematic research is undertaken. We present a partial synonymy here that includes the major substantive names but does not include the numerous misspellings and typographical errors.

Sciurus is the Latin word for “squirrel” ( Jaeger 1955), and is derived from the Greek skia, meaning “shade,” and oura, meaning “tail” ( Borror 1960). The specific epithet aureogaster derives from the Latin aure, meaning “golden,” and gaster, meaning “venter” ( Borror 1960), and was presumably assigned in reference to the color of the venter in the type specimen. Other common names for S. aureogaster include: Mexican gray squirrel, Mexican red-bellied squirrel, ardilla, ardilla arbórea, ardilla arborícola, ardilla voladora ( Leopold 1959), ardilla negra, ardilla pinta (Hall and Dalquest 1963), chuch ( Barragán et al. 2007), and ardilla gris (Emmons and Feer 1997; Valdéz Alarcón and Téllez-Girón 2005, 2014).

DIAGNOSIS

Seven species of Sciurus may be sympatric with Sciurus aureogaster . Most congeners can be distinguished from S. aureogaster in areas of sympatry by pelage coloration and body size. In southeastern Mexico and Guatemala, S. aureogaster possesses prominent dorsal patches, whereas S. yucatanensis (Yucatan squirrel) has a generally unpatterned dorsum; complete melanism is common in S. aureogaster , but rare in S. yucatanensis ( Musser 1968) . External measurements in S. yucatanensis are at least 5–10% smaller than those in S. aureogaster (see “General Characters”), except for tail length, which is similar. Also, the cranium is always smaller and the sphenopalatine vacuities are closed more frequently and smaller in S. yucatanensis than in S. aureogaster ( Musser 1968) .

Sciurus aureogaster seems to be ecologically separated from S. variegatoides (variegated squirrel); however, where these 2 species may be sympatric, S. aureogaster possesses an orange or chestnut venter frequently spotted with black (rather than white as in S. variegatoides ) and slightly larger external measurements than S. variegatoides , except for tail length ( Musser 1968). S. colliaei (Collie’s squirrel), in the northwestern portion of the range of S. aureogaster , lacks the bright nape and rump patches present in the latter, possesses an orange tail (rather than gray as in S. aureogaster ), and has external measurements and cranial length that are 5–10% larger than those in S. aureogaster ( Musser 1968) . S. deppei (Deppe’s squirrel), in the eastern portion of the range of S. aureogaster , seems to be ecologically separated from the latter, has external measurements and cranial length 10–20% smaller than those of S. aureogaster , and a dark olive brown dorsum without bright patches (dorsum frosted pale to dark grizzled gray and dorsal patches present in S. aureogaster — Leopold 1959; Hall 1981). In the northern portion of its range, S. aureogaster may be sympatric with S. alleni (Allen’s squirrel), S. oculatus (Peter’s squirrel), and S. nayaritensis (Mexican fox squirrel), but the latter lacks the dorsal patches and peglike upper premolar (P3) present in S. aureogaster . S. aberti (Abert’s squirrel) also may be sympatric with S. aureogaster , but lacks the large dorsal patches present in the latter and possesses a dark dorsum, white venter, and pronounced ear tufts ( Leopold 1959; Hall 1981), whereas S. aureogaster lacks pronounced ear tufts and the dorsum is frosted, pale to dark grizzled gray, and the venter is white to orange to chestnut.

Morphometric analyses place S. aureogaster in a clade with S. colliae , S. variegatoides , and potentially Syntheosciurus brochus (Bang’s mountain squirrel—Villalobos and Cervantes-Reza 2007) or S. yucatanensis (Swiderski and Zelditch 2010) .

GENERAL CHARACTERS

Sciurus aureogaster is a medium-sized tree squirrel ( Fig. 1 ; Hayssen 2008). Measurement ranges (mm) for total length, tail length, and length of hind foot for adult animals collected throughout Mexico were: 418–573, 206–315, and 57–72, respectively ( Hall 1981). Ear length for 2 adults from Nuevo León and 5 adults from Michoacán range from 30 to 33 mm (Jiménez- Guzmán et al. 1999; N. Ramos-Lara and F. A. Cervantes, in litt.). Mean body mass of 7 specimens from Veracruz was 350 g (± 55 SD —Estrada and Coates-Estrada 1985). In Michoacán, mean body mass of adult males (n = 3) and females (n = 2) was 591.7 g (± 52.0 SD) and 562.5 g (± 17.7 SD), respectively (Ramos-Lara and Cervantes 2011). Individual and geographic variation in pattern and color of pelage in S. aureogaster is striking ( Musser 1968; Valdéz Alarcón and Téllez-Girón 2005, 2014). Upper parts are frosted pale to dark grizzled gray; patches of varying size and color may occur on the nape, shoulders, rump, and sides ( Hall 1981; Coates-Estrada and Estrada 1986). The venter ranges from white through orange to chestnut; the tail ranges from a variegated, grayish buff when underparts are pale to orange-red or chestnut when the venter is deep orange ( Hall 1981; CoatesEstrada and Estrada 1986). Partial and complete melanism are common ( Musser 1968). Sexual dimorphism in body size and coloration do not exist; however, dorsal patches appear brighter in adult than in the juvenile pelage ( Musser 1968).

The skull is relatively short with broad and expanded zygomata ( Fig. 2 ). The braincase is broad and depressed posteriorly. The mean brain mass estimated from brain case volume is 8.40 g ( Mace et al. 1981). The rostrum is compressed laterally; the frontal area is flattened. The auditory bullae are moderately inflated ( Musser 1968; Hall 1981). The range of mean cranial lengths for specimens from 51 localities across Mexico was 56.70–61.80 mm (n = 832— Musser 1968); mean values (mm) for other cranial measurements for specimens from the states of Jalisco, México, Michoacán, and Oaxaca (n = 19) were: greatest length of skull, 59.63; zygomatic breadth, 34.21; palatal length, 26.59; length of diastema, 13.80; least interorbital breadth, 18.51; length of nasals, 20.14; cranial height at vault of skull, 27.14; length of maxillary toothrow, 11.23 ( McGrath 1987). Mean lever arm lengths measured as distances (cm) from the posterior of the condyle to the following points were: tip of coronoid process, proximal end of temporalis insertion, 0.83; base of coronoid process, distal end of temporalis insertion, 1.96; posterolateral corner of angular process, posterior end of superficial masseter insertion, 1.32; medioventral corner of angular process, ventral end of superficial masseter insertion, 1.97; anterior end of the anterior deep masseter insertion, 2.72; tip of the incisor, 4.20; distal end of the 1st molar, 2.52 (Swiderski and Zelditch 2010). Relative to congeners, jaw centroid size and shape are larger in S. aureogaster (Swiderski and Zelditch 2010) .

DISTRIBUTION

Sciurus aureogaster is found on the western coastal plain of Mexico from Colima to Chiapas ( Álvarez 1968; Webb and Baker 1969; Webb et al. 1981; Álvarez et al. 1984; Íñiguez Dávalos and Santana C. 1993; Sánchez-Hernández et al. 2005) and on the eastern coastal plain from Nuevo León ( Guzmán 1961) and Tamaulipas (Baker and Webb 1966) to Tabasco, as well as in the mountains from the southern portion of the Mexican Plateau southward into the mountains of central and southwestern Guatemala ( Fig. 3 ; Hooper 1953; Musser 1968; Hall 1981; Valdéz Alarcón and Téllez-Girón 2005; Reid 2009; Thorington et al. 2012). In eastern Mexico, S. a. aureogaster is primarily found at elevations below 1,525 m, with the exception of a population at Pinal de Amoles in the mountains of northeastern Querétaro at about 2,440 m ( Musser 1968). On the Pacific coastal plain, S. a. nigrescens occurs into the mountains of central and southeastern Mexico, reaching elevations of about 3,965 m, and extending southward into the mountains of Guatemala ( Musser 1968). The subspecies seem to intergrade to the east and south ( Musser 1968).

Four S. aureogaster (2 males, 2 females; 1 melanistic, 3 redbellied) were introduced to Elliott Key, Dade County, Florida, in 1938 from eastern Mexico (Brown 1969). S. aureogaster was common across much of the 10.4 km 2 tropical island within 15 years and reached nearby Adams and Sands keys (Schwartz 1952; Brown and McGuire 1969, 1975; Brown 1969, 1997). Although Hurricane Andrew, a category 5 hurricane, submerged the island under a 6 m storm surge in 1992 ( Ogden 1992), squirrels survived the storm ( Koprowski et al. 2005) and spread to nearby Sands Key and Old Rhodes Key, but no longer occurred on Adams Key ( Palmer et al. 2014). An effort to remove this introduced population from the islands of south Florida began in 2008, and 49 individuals of both color morphs had been removed from Elliott Key and Sands Key by 2012 (Pernas and Clark 2011; Palmer 2012). No fossils are known.

FORM AND FUNCTION

The length of the baculum in specimens from Jalisco, Michoacán, and Oaxaca ranges from 10.1 to 13.8 mm (mean = 11.8 mm; n = 19). The baculum possesses an expanded head ranging from 2.6 to 3.2 mm (mean = 2.9 mm) in length and from 2.8 to 3.5 mm (mean = 3.2 mm) in height, which tapers immediately to a neck ( Burt 1960). The shaft of the baculum may possess a dorsal keel and widens gradually to a broad base (width ranging from 1.8 to 3.0 mm, mean = 2.5 mm; height ranging from 2.3 to 3.5 mm, mean = 3.0 mm). A spur is prominent on the ventral side; an anterior spur and a posterior tuberosity may be found on some bacula ( Burt 1960). The thyrohyals are between 4.0 and 6.0 mm and the ceratohyal is always> 5.0 mm (Hoffmeister and Hoffmeister 1991).

Geographic variation in morphological and pelage characteristics is complex and dependent on the character ( Kelson 1952; Musser 1968). The most evident variation seems to be related to temperature and humidity with relatively smooth gradation occurring across climatic gradients. In warm lowlands, tail length (relative to head and body length combined) is greater, overhairs are shorter (10–15 versus 20–25 mm), and underfur is sparser than in cool highlands. Juveniles molt directly into adult pelage with little change in color pattern, although colors are brighter in the adult pelage. Adults molt at least once each year, with pigmentation patterns of the pelage being similar in all seasons and in both sexes ( Musser 1968). The number of micronucleated erythrocytes found in peripheral blood decreases linearly with age (Zúñiga-González et al. 2000, 2001). Dental formula is i 1/1, c 0/0, p 2/1, m 3/3, total 22; P3 is small and peglike ( Musser 1968; Hall 1981).

ONTOGENY AND REPRODUCTION

Sciurus aureogaster reproduces throughout the year, with food availability apparently limiting reproduction (Brown and McGuire 1975; Ceballos and Galindo 1984). In Michoacán, mating chases occurred on 20–28 December, 12 March, 11 April, 17–18 July, 17 August, and 16 October (Ramos-Lara and Cervantes 2011). In the exotic population in Florida, mating chases were observed on 12 January and 24 May (Brown and McGuire 1975). Males with enlarged, scrotal testes were common (70–90% of adult males) throughout the year in Florida (Schwartz 1952; Brown and McGuire 1975). A male with scrotal testes was collected in Veracruz on 9 January (Hall and Dalquest 1963), whereas in Michoacán 1 male was observed on 18 January and 3 males were collected between 30 April and 2 May, all with fully scrotal testes (RamosLara and Cervantes 2011). Of several females collected in Tamaulipas from December–May, only 1 was pregnant, containing a single embryo (Alvarez 1963). A female with 2 nearly full-term embryos was collected on 3 March in Veracruz (Hall and Dalquest 1963). S. aureogaster produces 2–4 young/litter (Ceballos and Galindo 1984), after a gestation period of about 44 days (Valdéz Alarcón and TéllezGirón 2005, 2014). Litter size obtained in Florida nests was 1 (n = 3) or 2 (n = 1—Schwartz 1952; Brown and McGuire 1975). In Michoacán, a potential litter of 3 (2 gray individuals and 1 melanistic) was observed when 3 juveniles exited a nest (Ramos-Lara and Cervantes 2011). Lactation was observed throughout the year in Florida; the percentage of lactating females ranged from 12.5% in November to 50.1% in February (Brown and McGuire 1975). Lactating females in Michoacán were observed on 28 December and 15–19 January, whereas 1 lactating and 1 post-lactating females were collected between 30 April and 2 May (Ramos-Lara and Cervantes 2011). Body mass (mean ± SD) of 11 juveniles in captivity increased from 125.2 ± 33.8 g to 264.0 ± 54.1 g at 3 months to 342.8 ± 87.7 g at 6 months (Zúñiga-González et al. 2001).

Figures

Fig. 1.—Two adult Sciurus aureogaster from 30 km south of Soto La Marina, Tamaulipas, Mexico. Partial and complete melanism are common in both males and females of this species. Photograph courtesy of

Fig. 2.—Dorsal, ventral, and lateral views of the skull and lateral view of mandible of an adult male Sciurus aureogaster (KU [University of Kansas 17930]), from 3 km north of Tamazunchale, San Luis Potosí, Mexico. Greatest length of skull is 57.95 mm.

Fig. 3.—Geographic distribution of Sciurus aureogaster: subspecies are: 1, S. a. aureogaster; 2, S. a. nigrescens. Map redrawn from Hall (1981) with modifications. Map created by N. Ramos-Lara.