Paraxerus cepapi (A. Smith, 1836 )

Banotai, Chris M., Mazzamuto, Maria Vittoria & KOPROwSKI, John L., 2023, Paraxerus cepapi (Rodentia: Sciuridae), Mammalian Species 55 (1030), pp. 1-11 : 1-6

Paraxerus cepapi (A. Smith, 1836)

Smith’s Bush Squirrel

Sciurus cepapi A. Smith, 1836:43 . Type locality “ Inhabits the banks of the Marikwa [= Marico River],” North West [province], South Africa.

S [ciurus]. cepate Gray, 1843:140. Incorrect subsequent spelling of S. cepapi A. Smith, 1836 .

Paraxerus cepapi : Major, 1893:189. First use of current name combination.

Funisciurus cepapi : Thomas, 1897:933. Name combination.

Funisciurus yulei Thomas, 1902:120 . Type locality “Muezo, near Lake Mweru [ Zambia];” restricted to Mwenzo , Zambia by Swynnerton and Hayman (1951:308).

Paraxerus cepapi maunensis Roberts, 1932:9 . Type locality “ Maun , Ngamiland [= North-West District],” Botswana.

Paraxerus cepapi kalaharicus Roberts, 1932:10 . Type locality “Mabeleapudi,” south of Laka Ngami , northern Botswana.

CONTEXT AND CONTENT. Order Rodentia , suborder Sciuromorpha , family Sciuridae , subfamily Xerinae , tribe Protoxerini , genus Paraxerus . Ten subspecies are recognized ( Thorington et al. 2012; Burgin et al. 2020):

P. c. bororensis Roberts, 1946:317. Type locality “ Namabieda , Boror, Mozambique.”

P. c. carpi Lundholm, 1955:294. Type locality “junction of the Mussenguez and Zambesi Rivers (south bank) m Southern Rhodesia [ Zimbabwe].”

P. c. cepapi ( Smith, 1836:43) . See above.

P. c. cepapoides Roberts, 1946:316. Type locality “Zimbiti, near Beira.”

P. c. chobiensis Roberts, 1932:9. Type locality “ Kabulabula , Chobe River,” Namibia.

P. c. phalaena Thomas, 1926:296. Type locality “the forest between Ukuambi and Ondongwa,” Ovamboland , Namibia.

P. c. quotus Wroughton, 1909:516. Type locality “ Katanga Dist., Congo State ,” Democratic Republic of the Congo.

P. c. sindi Thomas and Wroughton, 1908:543, Type locality “ Tette [= Tete, Mozambique].”

P. c. soccatus Wroughton, 1909:515. Type locality “Vwaza, Hewe R;” stated as Malawi by Skead (1973:245). Ansell and Dowsett (1988) proposed soccatus to be a synonym of yulei .

P. c. yulei ( Thomas, 1902:120) . See above.

NOMENCLATURAL NOTES. The name Paraxerus was derived from Greek, with para, a prefix denoting near and xerus from xeres, denoting dry or arid because this genus is found in dry areas ( De Graaff 1981). Other common names include bush squirrel, mopane squirrel, yellow-footed squirrel (English), geellpooteekhoring, boomeekhoring (Afrikaans), uBusinti, uBuhlula, isiKhale (Ndebele), sehlora (Sepedi), setlhora, sepêpê (Setswana), tsindi (Shona), xindzi, maxidyani, sindyane (Tsonga), tshithura (Venda), unomatse (Xhosa), intshidane, ingwejeje, yasezihlahleni (Zulu), and kampanda (Kibemba— Malaisse and Parent 1982; Power and Child 2016).

DIAGNOSIS

The only tree squirrel species sympatric with Paraxerus cepapi is Paraxerus palliatus (red bush squirrel) in Mozambique and Malawi; this overlap occurs in evergreen and coastal forests in Zululand ( Viljoen 1977c). Paraxerus cepapi and P. palliatus can be differentiated in the following ways. The ventral area and tail of P. palliatus are more reddish compared with the yellow or golden coloration of P. cepapi ( Fig. 1 ). Beyond color, P. cepapi has a shorter head length (39–45 mm) than P. palliatus (45–52 mm — Skinner and Chimimba 2005). Paraxerus cepapi is generally larger (total length of 277–578 mm, ¯x = 360 mm, n = 67 in males and 290–425 mm, ¯x = 351, n = 61 in females) than P. palliatus (total length of ¯x = 404 mm, n = 23, in males), with females having head–body lengths of ¯x = 225 (n = 12) and tail lengths of ¯x = 205 (n = 24), although P. palliatus has a longer tail (¯x = 204 mm, n = 23 in males and ¯x = 205 mm, n = 24 in females) than P. cepapi (¯x = 169 mm, n = 65 in males and ¯x = 169 mm, n = 61 in females— Skinner and Chimimba 2005). Paraxerus cepapi has a lower body mass (¯x = 190 g, n = 28 in males and ¯x = 195 g, n = 24 in females) than P. palliatus (¯x = 275 g, n = 14 in males and ¯x = 378.9 g, n = 42 in females— Skinner and Chimimba 2005). Ears of P. cepapi are slightly smaller (¯x = 19 mm, n = 66 in males and ¯x = 20 mm, n = 61 in females) than P. palliatus (¯x = 21 mm, n = 23 in males and ¯x = 21 mm, n = 32 in females— Skinner and Chimimba 2005). Finally, P. cepapi has shorter feet (¯x = 43 mm, n = 67 in males and ¯x = 43 mm, n = 61 in females).

GENERAL CHARACTERS

Although pelage and body size vary considerably throughout its geographic distribution ( De Graaff 1981; Skinner and Chimimba 2005), Paraxerus cepapi generally has a grizzled, gray-yellow appearance, with black tips on individual hairs, and fur is short and soft ( De Graaff 1981). Limbs are often a more richly colored buffy-yellow ( De Graaff 1981). Eyebrows, sides of face, chin, throat, breast, and inner surfaces of legs are white, and the rest of the ventral surface is a duller white ( De Graaff 1981). Backsides of ears are brown; tail is shorter than head– body length, bushy, and distinctly barred with narrow, transverse, buffy bands ( De Graaff 1981).

Geographical variations in coat color include a whiter ventral region (P. c. sindi), rustier dorsum (P. c. cepapoides), or pale gray dorsum (P. c. phalaena — De Graaff 1981). Smithers (1971) described three distinct color groups in Botswana: darker individuals in the northwest in contrast to buffy-yellow individuals in the southern part of the eastern region and buffy gray individuals in the eastern Okavango. Albinism has been reported in Kruger National Park, South Africa ( Pienaar et al. 1980) and melanism in Kyle Recreational Park, Zimbabwe ( Monks 1998).

Mean measurements (mm or g; parenthetical range and n; males and females, respectively) for P. c. kalaharicus from northwestern Botswana were: head–body length, 167 (10) and 166 (12); tail length, 162 (130–180, 10) and 163 (range 135– 181, 12); length of hind foot, 44 (36–47, 11) and 44 (40–47, 12); ear length, 20 (19–21, 11) and 19 (16–22, 10); and body mass, 170 (117–200, 7) and 147 (108–200, 10— Smithers 1971). Mean measurements (mm or g; parenthetical n; males and females, respectively) for P. c. cepapi in the Transvaal, South Africa were: head–body length, 195 (10) and 192 (8); tail length193 (9) and 186 (6); length of hind foot 47 (9) and 47 (8); ear length, 19 (8) and 17 (7); and body mass of 182 for one male ( Rautenbach 1978). In a separate sample from the Transvaal, mean measurements (mm or g; parenthetical n; males and females, respectively) for P. c. cepapi were: head–body length 191 (67) and 182 (61); tail length 169 (65) and 169 (61); length of hind foot 43 (67) and 43 (61); ear length 19 (66) and 20 (61), and body mass, 190 (28) and 195 (24— Rautenbach 1982). Mean measurements (mm or g; parenthetical n; males and females, respectively) for P. c. maunensis in the Okavango Delta, Botswana were: head–body length 176 (13) and 181 (13); tail length 169 (13) and 162 (13), length of hind foot; 45 (13) and 44 (13); and ear length, 19 (12) and 19 (14— Rautenbach 1982). Mean body mass for P. cepapi in Mookgophong, South Africa was 223 g (n = 69— Viljoen 1986).

DISTRIBUTION

Paraxerus cepapi is the most abundant and widely distributed arboreal tree squirrel in southern Africa ( De Graaff 1981). It occurs in Tanzania, Democratic Republic of Congo, Angola, Zambia, Malawi, and Mozambique ( Fig. 2 ; Skinner and Chimimba 2005). In the southern African subregion, it is found from the extreme northeastern parts of Namibia with the Southwest Arid subregion as its western boundary ( Davis 1974); northern, northeastern, and eastern parts of Botswana; Zimbabwe; Mozambique south of the Zambezi River, excluding the extreme southern parts of the country; North West Province, South Africa, from the Zeerust district eastward; widely in Limpopo Province; and narrowly in northern and eastern Mpumalanga. Paraxerus cepapi does not occur further south than 26°S ( Skinner and Chimimba 2005). The only other tree squirrel species with an overlapping distribution is Paraxerus palliatus in Mozambique and Malawi; this overlap occurs in evergreen and coastal forests in Zululand ( Viljoen 1977c). No fossils are known.

FORM AND FUNCTION

Form.— Dental formula of Paraxerus cepapi is i 1/1, c 0/0, p 2/1, m 3/3, total 22 ( Fig. 3 ; Viljoen 1977a; De Graaff 1981). Premolars in maxilla were absent in a few older individuals collected in the southern locality of Rustenburg, South Africa; this was considered an abnormal regional difference ( Viljoen 1977a). P3 is small and peg-like, and P4 shows no prominent anterior cusp ( De Graaff 1981). Three clear depressions are present on M1 and M2, and M3 shows only two depressions, with the second being broad ( De Graaff 1981). Lower molars are ridged transversely, with their three depressions separated by four ridges ( De Graaff 1981). As P. cepapi ages, molars become two-lobed structures. Incisors tend toward pro-odonty ( De Graaff 1981). Lower incisors are consistently longer (¯x = 10.8 mm in adults and ¯x = 8.4 mm in young [molars not erupted]) than upper incisors (¯x = 7.0 mm in adults and ¯x = 4.9 mm in young— Viljoen 1977a).

Paraxerus cepapi has a palatal fold formula of 2 + 6 = 8, with the first antemolar fold very close to incisors and intermolar palatal folds beginning at the first or between the first and second premolar, the first fold is continuous followed by the distal five folds which are divided in the middle ( Eisentraut 1975).

Skull size of P. cepapi varies by locality and subspecies ( De Graaff 1981). Bony palate extends as far as the back surface of the third molar ( Fig. 3 ). Anterior palatine formina are short and set forward ( De Graaff 1981). Nasal width varies geographically but is typically narrowest at the middle ( De Graaff 1981). Paraxerus cepapi does not have an elongated rostrum. There are 1–2 transverse bony septa in the auditory bulla ( De Graaff 1981). There is a sharp edge on the rostrum formed by the anterolateral edge of the zygomatic arch. The arch terminates before the premaxilla and does not rise above the lower edge of the lachrymal ( Moore 1959). Anterolateral part of the nasal extends beyond the nasal process of the premaxilla, and the premaxila makes an indentation in the lateral margin of the nasal ( De Graaff 1981).

Based on tooth eruption and wear, 76 P. cepapi from South Africa were assigned to six age-classes that were grouped into three categories (juveniles, subadults, and adults— Viljoen 1977a). Young animals without full eruption of all molars were considered juveniles. Subadults were assigned to one of two classes. The youngest of these contained individuals with all molars present and premolars worn but not yet replaced, whereas older subadults exhibited all premolars replaced, M1–3 already with some wear, but dentin not yet visible. The three adult age-classes ranged from dentin visible on all molars but not on premolars which showed no wear and enamel still clearly visible on M1–3 on the youngest adults to the oldest adults with no pattern left on smoothly worn molars, with M3 sometimes broken in two. Mean skull measurements (mm) in those three age categories, juveniles, subadults, and adults, respectively, were: condylobasal length 38.8, 41.8–42.6, and 43.2–43.7; zygomatic breadth 23, 25.2–25.5, and 25.8–26.2; braincase breadth 18, 18.4–19.0, and 19.1–19.4; minimum interorbital constriction 10.5, 11.8–12.2, and 12.8–13.2; nasal length 10.7, 12.2–12.6, 12.5–12.8; and nasal breadth 5.7, 6.4–6.6, and 6.7–7.0 ( Viljoen 1977a:93, table 2). In all cases, lengths increased with age.

Brain size of P. cepapi is relatively large compared with other small mammals of southern Africa, which might be attributed to arboreality and phylogeny ( Bernard and Nurton 1993); however, Roth and Thorington (1982) found relative brain case volume to be no different among African ground and tree squirrels. Braincase volume (± SE) of P. cepapi was 3.38 + 0.05 ml ( Roth and Thorington 1982); braincase volume (± SD) was 1.6 ± 0.1 ml, and brain mass (± SD) was 192.5 ± 3.5 g (Bernad and Nurton 1993). Sensitivity of semicircular canals is comparable to that of other arboreal squirrels ( Pfaff et al. 2015). Eye lenses continue to grow from juvenile stages into adulthood with mean mass (mg; parenthetical range) of 6.14 (5.8–8.2) at 1.5 months, 8.78 (7.6–11.0) at 3.5 months, 10.35 (9.3–12.0) at 9 months, and no growth beyond 12 months of age ( Viljoen 1977a).

The bony penis of P. cepapi is divided into a crest, baculum, and cartilage. Posterodorsal curvature of the two crest halves is closed by the bone extension of each half. In some individuals, cartilage can be seen clearly in the tip anterior to the pear-shaped baculum and in the portion enclosed by the crest. Range of bacular measurements (mm) of 12 adult P. cepapi collected in South Africa were: baculum length 1.272 –1.372, crest length 2.896 –2.852, baculum proximal width 0.684 –0.772, and total length of everted part 4.560 –4.760 ( Viljoen 1977b).

Function.— Paraxerus cepapi molts twice annually, with spring molt starting in September and autumn molt in January ( Viljoen 1977c). Both molts move from anterior to posterior over the body ( De Graaff 1981). First molt occurs at about 41 days of age and is completed at 110–120 days of age ( De Graaff 1981).

Paraxerus cepapi is arboreal and spends most of its time in trees, running and jumping adeptly from branch to branch, but it also descends to the ground to forage ( Viljoen 1986; Thorington et al. 2012). Its resting metabolic rate is 0.65 ml O 2 /g/h at a thermoneutral zone of 34°C. When temperature increases from 34°C to 36°C, oxygen consumption increment is 15.58%. From 12°C to 32°C, body temperature is maintained at 38.8°C and increases to 39.67°C when ambient temperature clumped to a large extent ( Viljoen 1985). It has little to no salivation ( Viljoen 1985). Energetic and nutritional values of 100 g of muscle were 497 KJ, 74.3 g H 2 O, 21.0 g protein, 3.2 g fat, 1.5 g ash, 230 mg Ca, 250 mg P, and 5 mg Fe ( Malaisse and Parent 1982).

rises to 38°C ( Viljoen 1985). Paraxerus cepapi thermoregulates by pulmonary evaporative cooling, but it also has sudoriferous glands on soles of its feet ( Viljoen 1985). Low resting metabolic rate, body temperature, and low activity level allow P. cepapi to conserve energy especially in an environment where resources are only seasonally abundant (harsh, dry winter) and

ONTOGENY AND REPRODUCTION

Litters of Paraxerus cepapi have 2–4 young ( De Graaff 1981). Reproduction can take place year-round and peaks in warm and wet months of October–April ( Smithers 1971; Rautenbach 1982; Skinner and Chimimba 2005); however, under poor veld conditions such as drought, breeding is reduced ( Viljoen 1981). Because P. cepapi is uniquely social among tree squirrels, it possesses a unique ability to synchronize breeding within a group, triggered by female estrus call or male-specific call. It is possible that breeding synchronization could have a group acceptance function (e.g., avoid cannibalism— Viljoen 1977e). For example, it is hypothesized that when more than one litter is born in a single nest to different females, young have a greater chance of survival if they are all equally matched in age, weight, and consequently strength at inevitable food fights ( Viljoen 1977e). Testicular regression occurs January–June ( Viljoen 1975; Skinner and Smithers 1990), but De Villiers (1986) found exceptions to this, observing P. cepapi males with descendent testes in May.

Mating activity consists of much vocalization, chasing, and mounting and is observed most often in the early morning ( Viljoen 1977e). Female estrus is indicated by a distinct and highly excited version of the usual alarm rattle: this vocalization tends to undulate more on the upper notes that are more evident than lower notes, attracting males from afar causing them to follow and chase a female ( Viljoen 1977e). Females vocalize for 2–15 min at a time (up to 48 sequences/min) after which they pause, either while being chased or while autogrooming; after this pause, they often begin vocalizing again ( Viljoen 1977c). Females in estrus can be pursued by 3– 5 males, some of which might be strangers ( Viljoen 1977c). The high excitement of mating bouts can cause clicking and tail-flicking by females and males ( Viljoen 1977c). The tail of a female sometimes flicks while a male is thrusting, which might enable deeper penetration ( Viljoen 1977c).

Estrus, judged by five mating bouts in captivity, lasts about 4 h and ends at midday ( Viljoen 1977e). Calculated from four litters of captive P. cepapi , mean gestation from the day on which the female is in estrus to birth was 56.5 days (range 56–58 days— Viljoen 1977e). Ovaries from visibly pregnant P. cepapi contained well-developed vesicular follicles that increased in diameter as the term approached, suggesting that ovulation and estrus might occur at parturition ( Viljoen 1977e). Litters are born in constructed dreys or tree cavity nests. Dreys are made of natural materials such as leaves and sticks, whereas tree cavities, high enough to avoid terrestrial predators and fires, are lined with leaves and grass ( Viljoen 1986; Skinner and Chimimba 2005). After release from live traps, individuals often immediately returned to tree cavities ( Fleming and Loveridge 2003).

Young are altricial at birth, weigh about 10 g, and are sparsely haired; eyes are closed and do not open until about 8 days of age ( Skinner and Chimimba 2005). Females have six nipples (0 + 1 + 1 + 1—Pappas and Thorington 2013). Young leave the nest for the first time at about 20 days old, remaining on the trunk and branches near the entrance hole and staying close to the adult female until they are about 5 weeks old, by which time they are weaned ( Skinner and Chimimba 2005). When young become fully mobile, they follow their parents until about 10 months of age when they become sexually mature ( Skinner and Chimimba 2005). Food collected and brought to the nest is reserved for the parents; young are prevented from eating it; after young are weaned, they are responsible for finding their own food, which they learn by observing their parents ( Viljoen 1977c).

Females are very attentive to the needs of their young, remaining in the nest with them for 2–3 days postbirth, only emerging for short periods, and fastidiously grooming them upon returning to the nest ( Viljoen 1977c). Both parents groom young, but only females carry them ( Skinner and Chimimba 2005). When nests need to be relined, females move their young temporarily, carrying them to another temporary location by the hind leg as they cling to her neck with limbs and tail ( Viljoen 1977c). Males continue chasing strangers from the nest area during these events, even when young are not present ( Viljoen 1977c). Although males consistently protect their offspring, De Villiers (1986) observed an adult male killing juveniles ( Skinner and Chimimba 2005), perhaps a male reproductive strategy ( Weissenbacher 1987).

Figures

Fig. 1.—Paraxerus cepapi alert while foraging, Olifants Rest Camp, Kruger National Park, South Africa, 14 July 2012. Photograph by JLK.

Fig. 2.—Distribution of Paraxerus cepapi in southern Africa. Although distributions of the 10 subspecies are unknown, localities of their type specimens provide some insight: 1, P. c. cepapi; 2, P. c. bororensis; 3, P. c. carpi; 4, P. c. cepapoides; 5, P. c. hobiensis; 6, P. c. phalaena; 7, P. c. quotus; 8, P. c. sindi; 9, P. c. soccatus; and 10, P. c. yulei.

Fig. 3.—Dorsal, ventral, and lateral views of skull and lateral view of mandible of an adult female Paraxerus cepapi (FMNH [Field Museum of Natural History] 95160) collected at Humani Ranch, Sabi River, Victoria, Zimbabwe, on 6 September 1961.