Heliosciurus rufobrachium ( Waterhouse, 1842 )

Thomas, Howard H, Best, Troy L & Agwanda, Bernard, 2019, Heliosciurus rufobrachium (Rodentia: Sciuridae), Mammalian Species 51 (978), pp. 61-69 : 62-66

Heliosciurus rufobrachium ( Waterhouse, 1842)

Red-legged Sun Squirrel

Sc. [iurus] rufo-brachium Waterhouse, 1842:202. Type locality “brought from Fernando Po;” listed as “ Equatorial Guinea, Bioko” by Thorington and Hoffmann (2005:794)).

Sciurus rufo-brachiatus Waterhouse, 1843:128 . Incorrect subsequent spelling of Sc [iurus]. rufo-brachium Waterhouse, 1842.

Sciurus maculatus Temminck, 1853:130 . Type locality “La Guiné, sur les bords des rivières couverts de forêts;” listed as “ Gold Coast ” by Thomas (1923b:524).

Sciurus aubryi Milne-Edwards, 1867:228 . Type locality “Gaboon.”

Macroxus rufobrachiatus var. waterhousii Gray, 1867:328 . No type locality given; specified as “ Ashanti ” by Thomas 1923b:524.

Macroxus isabellinus Gray, 1867:329 . Type locality “West Africa;” stated as “probably the lower Niger ” by Rosevear 1969:69.

Sciurus (Heliosciurus) rufobrachiatus libericus Miller, 1900:633 . Type locality “Mount Coffee, Liberia, Africa.”

Sciurus nyansae Neumann, 1902a:56 . Type locality “Kwa Kitoto (Kavirondo).”

Sciurus aschantiensis Neumann, 1902b:175 . Type locality “ Ashanti.”

Sciurus keniae Neumann, 1902b:176 . Type locality “Westabhang des Kenia in 8000 Fuss Höhe.”

Sciurus rufobrachiatus pasha Schwann, 1904:72 . Type locality “Bellima, Mombutto,” Belgian Congo.

Sciurus rufobrachiatus semlikii Thomas, 1907:120 . Type locality “Beni, Semliki River. Alt. 3000 ′.”

Heliosciurus multicolor coenosus Thomas, 1909:104 . Type locality “Roman Catholic Mission situated at 19°30 ′ E, on the Ubanghi.”

Heliosciurus rufobrachiatus benga Cabrera, 1917:517 . Type locality “cabo San Juan ( Guinea Española).”

Heliosciurus rufobrachiatus arrhenii Lönnberg, 1917:68 . Type locality “Masisi near Kivu.”

Heliosciurus rufobrachium: Allen, 1922:45 . First use of current name combination.

Heliosciurus rufobrachium pasha: Allen, 1922:40 . Name combination.

Heliosciurus rufobrachium maculatus: Thomas, 1923b:524 . Name combination.

Heliosciurus rufobrachium acticola: Thomas, 1923b:525 . Name combination.

Heliosciurus rufobrachium isabellinus: Thomas, 1923b:525 . Name combination.

Heliosciurus rufobrachium arrhenii: Allen, 1939:297 . Name combination.

Heliosciurus rufobrachium aubryi: Allen, 1939:297 . Name combination.

Heliosciurus rufobrachium benga: Allen, 1939:297 . Name combination.

Heliosciurus rufobrachium keniae: Allen, 1939:297 . Name combination.

Heliosciurus rufobrachium nyansae: Allen, 1939:298 . Name combination.

Heliosciurus rufobrachium semlikii: Allen, 1939:298 . Name combination.

Heliosciurus multicolor occidentalis Monard, 1941:9 . Type locality “Cutia, Portuguese Guinea.”

Heliosciurus rufobrachium occidentalis: Rosevear, 1969:75 . Name combination.

[ Heliosciurus rufobrachium ] coenosus: Thorington and Hoffmann, 2005:794. Name combination.

CONTEXT AND CONTENT. Context as for genus. The species name is derived from the Latin rufu s, meaning red, and brachium, meaning forearm, referring to the reddish coloration of the front limb ( Rosevear 1969). Twenty-one subspecies of H. rufobrachium are recognized ( Thorington et al. 2012; Koprowski et al. 2016):

H. r. arrhenii ( Lönnberg, 1917:68) . See above.

H. r. aubryi ( Milne-Edwards, 1867:228) . See above.

H. r. benga ( Cabrera, 1917:517) . See above.

H. r. caurinus Thomas, 1923b:523 . Type locality “Gunnal; alt. 50 m,” Portuguese Guinea.

H. r. coenosus ( Thomas, 1909:104) . See above.

H. r. emissus Thomas, 1923a:520 . Type locality “Kumbo, about 6°50’N. and 10°50’E;” Southeast Nigeria.

H. r. hardyi Thomas, 1923a:519 . Type locality “ Béoumi, 250 miles north of Grand Bassam,” Ivory Coast.

H. r. isabellinus ( Gray, 1867:327) . See above.

H. r. keniae ( Neumann, 1902b:176) . See above.

H. r. leakyi Toschi, 1946:7 . Type locality “ Garissa, Chenia.”

H. r. leonensis Thomas, 1923b:523 . Type locality “Mano.”

H. r. lualabae Thomas, 1923a:520 . Type locality “Lodja, Upper Lukenye River,” Southern Congo.

H. r. maculatus ( Temminck, 1853:130) . See above ( aschantiensis Neumann , libericus Miller, and waterhousii Gray are synonyms).

H. r. medjianus J. A. Allen, 1922:48 . Type locality “Medje,

Belgian Congo.” H. r. nyansae ( Neumann, 1902a:56) . See above. H. r. obfuscatus Thomas, 1923b:526 . Type locality

“Ekkonnanakku. Alt. 200’,” Nigeria. H. r. occidentalis ( Monard, 1941:9) . See above. H. r. pasha ( Schwann, 1904:72) . See above. H. r. rubricatus J. A. Allen, 1922:50 . Type locality “near the

Lubila River, an affluent of the Tshopo River, about 50 miles southwest of Avakubi (south of the Ituri River), Belgian

Congo.” H. r. rufobrachium ( Waterhouse, 1842:202) . See above (acticola

Thomas and rufo -brachiatus Waterhouse are synonyms). H. r. semlikii ( Thomas, 1907:120) . See above.

NOMENCLATURAL NOTES. Waterhouse (1842) originally applied the name rufo-brachium for this taxon but then misspelled the name as rufo-brachiatus in his 1843 publication. Subsequent references to this taxon used the incorrect spelling, rufobrachiatus , until the error was identified by Allen (1922).

Currently, there are 21 recognized subspecies of Heliosciurus rufobrachium ( Koprowski et al. 2016) ; however, the number has varied from 22 ( Thorington and Hoffmann 2005) to 14 ( Emmons 2013) in recent publications. Considerable geographic variation in pelage color has been observed among populations of H. rufobrachium which has contributed to 27 taxa being recognized ( Hoffmann et al. 1993; Thorington and Hoffmann 2005). Amtmann (1975) allocated the taxa brauni, coenosus, emissus, and lualabae to H. gambianus but these taxa were retained in H. rufobrachium by Thorington and Hoffmann (2005). Thorington et al. (2012) did not recognize brauni (St. Leger, 1935), a taxon from Angolia, as a subspecies of H. rufobrachium and appear to have accepted the reallocation of this taxon to H. gambianus based on their map of the distribution of this species. However, the status of brauni remains unclear. Rosevear (1969) concluded that the affinities of keniae were with H. rufobrachium but Grubb (1982) and Kingdon (1974) pointed out phenetic affinities with H. gambianus . The inclusion of coenosus and emissus are uncertain, as emissus (Rosevear 1963, 1969) or both forms ( Amtmann 1975) were assigned as subspecies of H. gambianus . A thorough revision of the species is warranted to resolve both the phylogenetic content of H. rufobrachium and the number of subspecies present. Koprowski et al. (2016) pointed out that the precise distribution of subspecies coenosus, lualabae, medjianus, pasha, and rubricatus are unknown and that there may be some degree of distributional overlap.

DIAGNOSIS

Heliosciurus rufobrachium is sympatric or parapatric with the Gambian sun squirrel H. gambianus , small sun squirrel H. punctatus, Ruwenzori sun squirrel H. ruwenzorii , and Zanj sun squirrel H. undulatus . H. rufobrachium is distinguished from these four species by the distinctive red coloration of its legs ( Fig. 1 ) from which it gets its common name.

GENERAL CHARACTERS

Heliosciurus rufobrachium is a medium-sized African squirrel with moderately sized ears and large eyes ( Fig. 1 ). Mean external measurements (mm; n in parenthesis) for males and females, respectively, were: head–body length, 237.3 (12), 230.5 (8); tail length, 248 (12), 248 (8): length of hind foot, 47 (12), 49 (8— Emmons 2013). Average weight (g; ranges in parenthesis) of 12 males and seven females, respectively, were: 356 (300–420) and 351 (290–387— Emmons 2013). Dorsal fur is typically dark brown to gray while the similarly colored venter often has sparser hair coverage. Reddish fur is on the upper-side of the forelimbs and backs of the hind feet. This reddish color often extends on to the forearms, thighs, and inner surfaces of arms and legs. Portions of the muzzle also have a reddish color. Hairs on the body have three to five alternating bands of dark brown and buff. The long tail (about 195% of head–body length) is slender and black with numerous and often indistinct bands of pale yellow ( Fig. 1 ). Rather than being placed against the back, the long, thin tail, usually is held out straight behind the body, drooped over a branch ( Thorington et al. 2012), or curled around the body ( Rosevear 1969).

The head and skull are proportionately small compared to the body ( Thorington et al. 2012). Ears do not extend above crown of head ( Rosevear 1969). Postorbital processes are well developed, long, and pointed ( Fig. 2 ). Cranial measurements (mm; range in parenthesis) for five individuals were: greatest length of skull 52.8 (50.6–54.5), greatest width of skull 30.8 (29.1–31.8); P 4 -M 1 length 9.9 mm (9.4–10.4— Emmons 2013).

DISTRIBUTION

Heliosciurus rufobrachium occurs in Senegal, western Gambia, western Guinea Bissau, western Guinea, Sierra Leone, Liberia, southern Côte d’Ivoire, southern Ghana, southern Togo, Benin, southern Nigeria, Cameroon, Bioko and Rio Muni ( Equatorial Guinea), southwestern Central African Republic, southeastern Sudan, Uganda, Rwanda, Burundi, southwestern and eastern Kenya, and the Democratic Republic of the Congo ( Fig. 3 ) Although occurring as far east as Garissa, Garissa County, Kenya (type locality for H. r. leakyi ), the species does not inhabit coastal forests. Gathua (2000) reported H. rufobrachium as feeding in the Arabuko-Sokoke Forest of coastal Kenya but the only reference provided for the species identification is in the abstract and this identification cannot be verified. In the absence of voucher specimens from the Arabuko-Sokoke Forest and the range maps provided by Amtmann (1975), it is concluded that the squirrels studied by Gathua (2000) were H. undulatus , which has been documented in the coastal forests of Kenya and Tanzania ( Grubb 1982). Hoffmann et al. (1993) and Thorington and Hoffmann (2005) indicated H. rufobrachium as occurring in southeastern Kenya, whereas Thorington et al. (2012) showed the species distributed only as far east as Garissa, Garissa County, Kenya. Emmons (2013) presents a similar distribution but does not recognize H. r. leakyi . There are no known fossils of H. rufobrachium .

FORM AND FUNCTION

Form. —Mid-dorsal hairs of Heliosciurus rufobrachium are

21–25 mm long ( Rosevear 1969). Fur on underside is sparser than on back ( Rosevear 1969). On the tail, hairs are ≤ 50 mm long in the middle of the tail and are progressively shorter toward body and tip of tail ( Rosevear 1969). Thus, when hairs on tail are erected, the tail is somewhat bushy ( Rosevear 1969). H. rufobrachium is a non-glider ( Runestad and Ruff 1995).

Dental formula is i 1/1, c 0/0, p 1/1, m 3/3, total = 20 ( Rosevear 1969). Incisors are orange, broad, and robust, and upper incisors are smooth or slightly grooved ( Rosevear 1969). Upper cheek teeth are concave with strong transverse ridges and a prominent internal heel; lower cheek teeth are shallowly saucer-shaped, squarish, and have a prominent cusp at the corners ( Rosevear 1969). Females have three pairs of mammae; one pair thoracic, spaced widely apart, followed by a long gap then two abdominal pairs spaced close together ( Rosevear 1969).

Compared to a variety of other African sciurids, H. rufobrachium has a relatively small brain for its size: average (± SE) length of body (mm) and weight (g), respectively, of H. r. isabellinus , 213.2 ± 2.3 (n = 16), 280.9 ± 8.1 (n = 16); H. r. maculatus , 240.4 ± 2.7 (n = 32), 381.8 ± 9.6 (n = 29); and H. r. rufobrachium , 252.7 ± 9.0 (n = 3), 334.0 ± 35.0 (n = 4). Average (± SE) volume of braincase of 16 H. r. isabellinus , 32 H. r. maculatus , and four H. r. rufobrachium , respectively, was 5.08 ± 0.04, 6.01 ± 0.11, and 5.28 ± 0.11 cm 3 ( Roth and Thorington 1982).

Measurements of stomach, small intestine, cecum, and colon, respectively, of a 290 g male H. rufobrachium were: surface area, 51, 190, 48, and 63 cm 2; mass, 6, 4, 3, and 3 g; volume, 34, 25, 11, and 8 cm 3 ( Chivers and Hladik 1980). Multidimensional scaling of these measurements verified that H. rufobrachium has a gastrointestinal tract similar to other non-ruminant mammalian frugivores ( Chivers 1989).

Heliosciurus lacks cheek pouches. However, lateral retractor muscles are present, originate on the metacromion of scapula, and insert on the cheek ( Thorington et al. 1997). The jaw musculature of H. rufobrachium is similar to that of other soft-fruit eating tree squirrels ( Thorington and Darrow 1996). The origins and insertions of the superficial masseter, deep masseter, zygomaticomandibularis, and temporalis muscle groups of H. rufobrachium are either similar to or the same as Paraxerus and Protoxerus while medial pterygoid, lateral pterygoid, digastric, transverse, mandibular, mylohyoid, geniohyoid, stylohyoid, hyoglossus, styloglossus, and extrinsic tongue muscles showed little variation among the squirrels ( Thorington and Darrow 1996). Mean (± SD; n = 7) distance from middle of mandibular condyle to tip of mandibular incisor was 33.7 (± 1.2) mm. Values obtained by dividing this distance into other measurements of the mandible were: condyle to posterodorsal point of angular process, 0.36 (± 0.3); condyle to anteroventral point of angular process, 0.49 (± 0.2); condyle to anteriormost point of masseteric ridge, 0.65 (± 0.03); condyle to retro-molar pit, 0.39 (± 0.3); and condyle to tip of coronoid process, 0.16 (± 0.01— Thorington and Darrow 1996).

Forelimbs of H. rufobrachium are used in running, leaping, climbing, foraging, and other actions. The wrist includes distal ends of radius and ulna, which articulate with three proximal carpal bones to form the proximal carpal joints. Distally, these three bones articulate with five other carpals to form the midcarpal joints. Four of these distal carpals articulate with five metacarpals forming the carpo-metacarpal joints. On the palmar surface, the scapholunate articulates with the falciform bone. The origin of the radial radio-scapholunate, ventral radioscapholunate, dorso-ulno-triquetral, scapholunate-hamate, and triquetral-pisiform ligaments of H. rufobrachium is similar to those of a variety of squirrels ( Thorington and Darrow 2000). The radial radio-scapholunate ligament originates on the radial side of the styloid process, passes across the joint, and inserts on ventral side of scapholunate. The poorly defined ventral radio-scapholunate ligament forms part of the roof of the carpal tunnel between ventral surface of the radius and scapholunate. The hypothenar cartilage is incorporated into superficial forefoot fascia and tendon of the palmaris longus muscle and attaches onto the pisiform and falciform bones. Origin of the palmaris brevis muscle is from the transverse carpal ligament, falciform bone, and midline of the forefoot and insertion is on the hypothenar cartilage. Prominence of the hypothenar cartilage and palmaris brevis muscle in all tree and ground squirrels suggests these structures are used for grasping with forefeet. Pronation and supination, useful in manipulating food, is permitted by the radioulnar joint ( Thorington and Darrow 2000).

Musculature of the shoulder, arm, and forearm of H. rufobrachium is similar to other tree squirrels ( Thorington et al. 1997). Among tree squirrels, there was little variation of the origin and insertion of the following muscle groups: trapezius, extensor system of the arm, latissimus-subscapularis, deltoid, subscapularis, triceps, extensor group of the forearm, flexor system, flexor group of the arm, and flexor group of the forearm ( Thorington et al. 1997). H. rufobrachium possesses a distinct teres major fossa on the axillary edge of the scapulae that serves as the origin of the teres major muscle. This muscle helps produce retroflexion that is needed to overcome the force of gravity during scansorial movement.

Function. —Intra-vitreal injection of tritiated amino acids has been used to assess retinal projections of Heliosciurus rufobrachium . Following injection of anterograde tracer, the brain was sectioned and autoradiography revealed that retinal fibers were present in the basal telencephalon. Labeled fibers diverge from the dorsolateral margin of optic tract and chiasm, pass dorsally around the supraoptic nucleus, penetrate the diencephalic-telencephalic junction lateral to the hypothalamus, and, subsequently, continue rostrally and laterally within the basal telencephalon ( Cooper et al. 1994).

Mean metabolic rate (± SD) during the day at 29–30°C for a 230 g and a 312 g H. rufobrachium was 1.23 ± 0.29 and 1.34 ± 0.15 kcal/h, respectively. At night, under the same conditions, mean metabolic rate was 0.69 ± 0.06 and 0.98 ± 0.08 kcal/h, respectively ( Hildwein 1972). Based on these data, basal metabolism is 0.90 W ( Heusner 1991).

ONTOGENY AND REPRODUCTION

Little is known about reproduction and development of Heliosciurus rufobrachium . Females produce litters of one to two young with a mean of <1.5 in Gabon and Congo ( Rahm 1970, Emmons 1979). In Uganda, timing of reproduction is evidenced in males with the enlargement of two anal glands and an increase in size of testes ( Kingdon 1974). In captivity, H. rufobrachium has lived 8 years and 11 months ( Jones 1982).

Figures

Fig. 1.—An adult Heliosciurus rufobrachium in Kakamega Forest, Western Province, Kenya. Used with permission of the photographer Troy L. Best.

Fig. 2.—Dorsal, ventral, and lateral views of the skull and lateral view of the mandible of an adult male Heliosciurus rufobrachium from Kaimosi, Western Province, Kenya (USMN [United States National Museum of Natural History] #182754). Greatest length of skull is 51.4 mm. Used with permission of the photographers Scott A. Kincaid and Troy L. Best.

Fig. 3.—Distribution of Heliosciurus rufobrachium. Locations are the type localities of each subspecies. Subspecies: 1*, H. r. arrhenii; 2*, H. r. aubryi; 3, H. r. benga; 4*, H. r. caurinus; 5, H. r. coenosus; 6, H. r. emissus; 7*, H. r. hardyi; 8*, H. r. isabellinus; 9*, H. r. keniae; 10, H. r. leakyi; 11*, H. r. leonensis; 12, H. r. lualabae; 13*, H. r. maculatus; 14*, H. r. medjianus; 15*, H. r. nyansae; 16*, H. r. obfuscatus; 17, H. r. occidentalis; 18*, H. r. pasha; 19, H. r. rubricatus; 20*, H. r. rufobrachium; 21*, H. r. semlikii. Subspecies recognized by Emmons (2013) are designated with an asterisk. Map drawn by Jane Huang and Melissa Stepek.