Tamiops barbei ( Blyth, 1847 )

Hinckley, Arlo, Maldonado, Jesús E., Tamura, Noriko, Leonard, Jennifer A. & Hawkins, Melissa T. R., 2024, Lost in synonymy: Integrative species delimitation reveals two unrecognized species of Southern Asian tree squirrels (Rodentia: Sciuridae: Callosciurinae), Vertebrate Zoology 74, pp. 683-707 : 683-707

Tamiops barbei ( Blyth, 1847)

Sciurus barbei Blyth, 1847 , Journal of the Asiatic Society of Bengal 16: 875.

Tamias [sic] leucotis Temminck, 1853 , Esquisses zoologiques sur la côte de Guiné, Mammifères: 252.

Sciurus mcclellandi kongensis Bonhote, 1901 , Proceedings of the Zoological Society of London 1901: 55.

Sciurus novemlineatus Miller, 1903 b , Proceedings of the Biological Society of Washington 16: 147.

Tamiops inconstans Thomas, 1920 , Annals and Magazine of Natural History (Series 9) 5: 306.

Tamiops mcclellandi collinus Moore, 1958 , American Museum Novitates 1879: 1.

Holotype.

Two syntypes are housed in the National Zoological Collection of the Zoological Survey of India: ZSI 9482 and ZSI 9483. These represent two unsexed study skins and skulls collected by J. Barbe and have been previously cited by their former Indian Museum catalog numbers: c 2 and d 2. The third syntype described by Blyth could not be found in this collection ( Khajuria et al. 1977). These specimens could not be examined in this study but a topotype was examined ( NHMUK 1914.7 . 8.36).

Type locality.

Zami River, Ye Province, 100 miles south of Moulmein, Tenasserim, Burma [= c. 161 km south of Mawlamyine, Mon, Myanmar; ca. 16.21 ° N, 97.74 ° E].

Emended diagnosis.

A small-sized Tamiops [average HB = 107–114 mm (T. b. inconstans / T. b. barbei ), W = 47 g, GLS = 32 mm; Moore and Tate 1965; Liu et al. 2022] that can be distinguished from all other relatives by the combination of the following features: Outer light stripes are paler than inner light stripes and have a different width; rust / orange suffusion in venter but not in crown or nape; absence of yellow / orange hue in ear tufts; venter hairs have a very small extent of basal gray that is entirely covered by the colored hair tips, giving the venter a homogeneous and bright coloration; white / buff tipped tail hairs (Fig. 8 B, C, E ). It can also be discriminated based on one of the following combinations of characters, which correspond to its two subspecies. Tamiops barbei barbei : Strongly striped, with outer dark stripes as dark as inner dark stripe; wide outer pair of light stripes (maximum width: 6–9 mm), which are connected to a distinct light facial stripe; relatively small-sized baculum with shaft and blade, shaft has a small concavity where the blade is attached, blade is inserted in this concavity, blade attachment orientation is perpendicular to shaft orientation (Fig. 9 C, D ). Tamiops barbei inconstans : Faintly striped, with outer dark stripes less dark than inner dark stripe.

Comparisons.

In general terms, T. barbei is distinguished from its parapatric relative T. mcclellandii by its more colorful venter and paler tipped tail hairs, and at the turnover area between these species (west and central Indochina), by its strongly striped appearance and longer tail (Figs 8 , S 2 A). Since the dorsal pelage of T. barbei barbei and T. b. inconstans is quite different, and the latter is here considered a candidate species (see comments section), each of these subspecies will be compared separately with T. mcclellandii . Parapatric T. b. barbei and T. mcclellandii can be externally distinguished based on the following pelage features: outer dark stripes as black as inner dark stripe vs paler than inner dark stripe in T. mcclellandii during spring-summer; great vs little contrast between inner light and outer dark stripe pairs in T. mcclellandii ; outer pair of light stripes wide (maximum width: 6–9 mm) vs narrow (maximum width: 3–5 mm) in T. mcclellandii ; venter gray hair bases are short and entirely covered by the colored hair tips vs venter gray hair bases are long and not entirely covered by colored hair tips in T. mcclellandii , giving T. b. barbei a homogeneous bright yellow / orange ventral coloration vs yellow-buff mixed with gray / brown in T. mcclellandii ; white / buff vs golden / yellow tipped tail hairs in T. mcclellandii .

Allopatric T. b. inconstans and T. mcclellandii can be externally distinguished based on less pelage features: venter gray hair bases are short and entirely covered by the colored hair tips vs venter gray hair bases are long and not entirely covered by colored hair tips in T. mcclellandii , giving T. b. inconstans a homogeneous bright orange ventral coloration vs yellow-buff mixed with gray / brown in T. mcclellandii ; buff / pale yellow vs golden / yellow tipped tail hairs in T. mcclellandii .

It can also be distinguished from T. mcclellandii by its longer (106–163 mm) vs shorter (75–113 mm) tail in their distribution contact area (west and central Indochina; Fig. S 2 A). Similarly, cranium morphospace is also more distinct between parapatric T. b. barbei and T. mcclellandii , than between allopatric T. b. inconstans and T. mcclellandii (Figs 4 , S 2 B). More specifically, T. barbei has a deeper rostrum and broader interorbital constriction, but a more flattened braincase than T. mcclellandii (Figs 4 , S 2 B).

Finally, T. b. barbei can also be differentiated from T. mcclellandii through the following baculum characteristics: Presence vs absence of a small concavity where the blade is attached to shaft in T. mcclellandii ; blade attachment orientation is perpendicular vs tangent to shaft orientation in T. mcclellandii ; shorter (4.70–5.09 mm) vs longer (6.15–6.65 mm) shaft in T. mcclellandii (Fig. 9 ).

It is currently thought to have an allopatric distribution with its relatives Tamiops maritimus , T. mishanica and T. swinhoei (although T. barbei inconstans might have a sympatric / parapatric elevational distribution with T. swinhoei / maritimus in Yunnan and northern Vietnam) from which it can be externally distinguished based on its outer pair of light stripes, which are connected to the light facial stripe in T. barbei barbei (except in some T. barbei inconstans specimens), but just extend to the shoulder in the other species (except in T. swinhoei in which it is rarely connected with a faint line). Its pelage is also harsher, thinner, and shorter vs softer, denser and longer in T. swinhoei , and it lacks a yellow / orange hue in its ear tufts and reddish suffusion in crown while these features are frequently present in T. swinhoei . Its facial stripe is distinctive vs diffuse in T. minshanica , and its crown is characterized by a dull brown gray vs bright reddish-brown coloration in T. mishanica . It can be differentiated from parapatric T. rodolphii based on the following external features: outer light lines are thinner but more distinctive, contrasted and lighter than inner light lines, which are less conspicuous vs outer and inner light lines are of equal width and similar brightness, distinctiveness, and contrast with the dorsum in T. rodolphii ; outer dark lines’ coloration is homogeneous along the anterior-posterior axis vs outer dark lines generally grade posterior-anteriorly from black / dark brown to brown / reddish-brown in T. rodolphii ; absence of a thin pale brown line across the black mid-dorsal line vs presence of a thin pale brown line across the black mid-dorsal line in T. rodolphii (except in SE Thailand populations).

Finally, the glandes penis and bacula among T. minshanica , T. swinhoei , T. maritimus , T. barbei barbei , and T. barbei inconstans differ distinctly from each other ( Pocock 1923; Liu et al. 2022).

Distribution, habitat and natural history.

Distributed from the Irrawaddy River to the West to the Northwest provinces of Vietnam to the East (A. E. Balakirev pers. comm.), southern Yunnan ( China) ca. 23.5 º N to the North, and to Selangor ( Malaysia) to the South (Figs 2 , S 5). In Thailand, the Chao Phraya River Basin might constitute a barrier for this species and its eastern limit, since this species is replaced by T. rodolphii to the east of the Chao Phraya / Pa Sak River (Chon Buri and Chaiyaphum provinces). The only exceptions are several iNaturalist records from Khao Yai National Park, which is just to the East of this river, most of which seem to represent Tamiops barbei . Recorded from sea level to 2130 m a. s. l. (Table S 1).

Recorded feeding on cherry blossom flowers / nectar, Mudhuca floribunda , Ficus hirta , Musa acuminata , and Castanopsis acuminatissima (iNaturalist; Rueangket et al. 2019).

Conservation.

Recorded in Khao Sok, Khao Yai, Ko Tarutao, Thai Muang, Kaeng Krachan, Khoa Luang, Phu Suan Sai, Phu Kradueng, Thale Ban, Khao Pu-Khao Ya, Mae Ping, Si Satchanalai and Doi Luang, Doi Inthanon National Parks, Lentang Forest Reserve, Fraser’s Hill and Krau Wildlife Reserves, Chiang Dao, Phu Luang, and Huai Kha Khaeng Wildlife Sanctuaries (iNaturalist; Table S 1).

Comments.

The subspecies Tamiops barbei inconstans might merit species-level recognition. It is well differentiated from T. barbei barbei populations based on mitochondrial DNA, having divergerged ca. 3.54 million years ago with cyt b pairwise uncorrected genetic distances ca. 5 % ( Hinckley et al. 2023 a). Ecologically, it is adapted to subtropical forests instead of monsoon forests / rainforests. Morphologically, it exhibits a highly distinct dorsal pelage, a shorter tail than Indochinese T. b. barbei populations, and a somewhat overlapping but distinct craniodental morphospace. Its baculum also differs from that of nominotypical T. barbei populations ( Pocock 1923; Liu et al. 2022). Unfortunately, Hinckley et al. (2023 a) were limited by the sampling of only a single T. b. inconstans population and the absence of nuclear data. Future research should expand geographic and genetic sampling to more thoroughly assess whether this subspecies warrants full species recognition.

In T. barbei barbei , morphological sampling in Kra sensu lato complemented and supported the limited molecular evidence in this area of Hinckley et al. (2023 a), suggesting a phenotype transition / contact zone between Trang and Hat Sanuk (circa 7.5–12 ºN). Molecular evidence showed specimen FMNH 82879 from Tenasserim Town (west coast, 12 ºN) had south and north haplotypes for different markers. Additionally, FMNH 82879 and other specimens from this latitude and all the way south to Trang (west coast, 7.5 ºN) also showed an intermediate morphology among north and south groups in the PCA or measurement biplots. However, specimens from Chong Bueng (14.6 ºN) show most external measurements in the range of the north group (and T. m. kongensis pelage) while specimens from Nakhon Sri Thammarat and Surat Thani (east coast, circa 8–10 ºN) cluster with the south group.

Figures

Figure 2. Map of tropical East Asia indicating the localities of museum specimens examined in this study for Tamiops mcclellandii. Different subspecies are labeled with different symbols, while different colors illustrate the potential distribution of the two major genetic lineages described by Hinckley et al. (2023 a), inferred from pelage variation. Darker background shades correspond to higher elevations.

Figure 4. Morphometric variation in Tamiops mcclellandii. A First and second principal components from an analysis of 17 craniodental variables. B Second and third principal components of the same analysis. Samples are colored according to the two major lineages: Sundaland and Indochina (in blue and green), and Himalayas and Arakan Range (in orange). The former of which is further subdivided in two lineages shown here for the sake of comparison: NE Indochina (in green) and remaining Indochina and Sundaland (in blue). Different subspecies are labeled with different symbols.

Figure 8. Dorsal and ventral views of the skins of (A) Tamiops mcclellandii (NHMUK 79.11. 21.372, lectotype), (B) T. barbei barbei (NHMUK 1914.7. 8.36, topotype), and (C) T. barbei inconstans (NHMUK 12.7.25.31, holotype); live images of (D) T. mcclellandii taken by Lee Alloway in Kumarkata, Assam, India, and (E) T. barbei taken by Andaman Kaosung in Kaeng Krachan District, Thailand.

Figure 9. Baculum comparison between Tamiops barbei and T. mcclellandii. A Lateral (left) view of T. mcclellandii (USNM 564453); B ventrolateral view of T. mcclellandii (USNM 564453); C lateral (left) view of T. barbei (USNM 297043); D ventrolateral view of T. barbei (USNM 297043).