Callosciurus caniceps ( Gray, 1842 )

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

Callosciurus caniceps ( Gray, 1842)

Sciurus caniceps Gray, 1842 , Annals and Magazine of Natural History (Series 1) 10: 263.

Sciurus chrysonotus Blyth, 1847 , Journal of the Asiatic Society of Bengal 16: 873.

Sciurus bimaculatus Temminck, 1853 , Esquisses zoologiques sur la côte de Guiné, Mammifères: 251.

Sciurus epomophorus Bonhote, 1901 , Annals and Magazine of Natural History (Series 7) 7: 272.

Sciurus davisoni Bonhote, 1901 , Annals and Magazine of Natural History (Series 7) 7: 273.

Sciurus sullivanus Miller, 1903 a , Smithsonian Miscellaneous Collections 45: 17.

Sciurus domelicus Miller, 1903 a , Smithsonian Miscellaneous Collections 45: 18.

Sciurus bentincanus Miller, 1903 a , Smithsonian Miscellaneous Collections 45: 19.

Sciurus matthaeus Miller, 1903 a , Smithsonian Miscellaneous Collections 45: 19.

Sciurus casensis Miller, 1903 a , Smithsonian Miscellaneous Collections 45: 19.

Sciurus lucas Miller, 1903 a , Smithsonian Miscellaneous Collections 45: 20.

Sciurus altinsularis Miller, 1903 a , Smithsonian Miscellaneous Collections 45: 21.

Sciurus epomophorus milleri Robinson & Wroughton, 1911 , Journal of the Federated Malay States Museum 4: 233.

Sciurus concolor fallax Robinson & Kloss, 1914 , Annals and Magazine of Natural History (Series 8) 13: 225.

Sciurus concolor samuiensis Robinson & Kloss, 1914 , Annals and Magazine of Natural History (Series 8) 13: 226.

Sciurus epomophorus inexpectatus Kloss, 1916 , Journal of the Natural History Society of Siam 2: 178.

Sciurus helgei Gyldenstolpe, 1917 , Kungliga Svenska Vetenskapsakademiens Handlingar 57: 34.

Callosciurus epomophorus nakanus Thomas & Robinson, 1921 , Annals and Magazine of Natural History (Series 9) 7: 120.

Callosciurus epomophorus mapravis Thomas & Robinson, 1921 , Annals and Magazine of Natural History (Series 9) 7: 120.

Callosciurus epomophorus panjius Thomas & Robinson, 1921 , Annals and Magazine of Natural History (Series 9) 7: 119.

Sciurus caniceps helvus Shamel, 1930 , Journal of Mammalogy 11: 72.

Holotype.

Not specified in species description. Robinson and Kloss (1918) substitute the erroneous Bhutan type locality by North Tenasserim, and mention the “ type ” is at the “ British Museum ” ( NHMUK) but do not specify its catalog number. Moore and Tate (1965) and NHMUK staff suggest the following lectotype: NHMUK 41.1817, field number 213 a, an adult male prepared as a mounted skin with a damaged tail & cleaned damaged skull (Fig. 6 A ).

Type locality.

N Tenasserim, Burma [= Tanintharyi province, Myanmar].

Emended diagnosis.

A relatively large-sized Callosciurus (average HB = 228.6 mm, PL = 52.6 mm; Table S 6) distinguishable from all other relatives by a sharply marked black tail tip along with two alternative pelage combinations corresponding to its subspecies. In the northern part of its distribution, it displays a bright ochraceous / rufus orange on the flanks and dorsum during the dry season and agouti gray in the wet season. The bright orange fades into agouti gray as it approaches the venter, crown, and proximal one-tenth of the tail. The ears are agouti gray, generally with white hairs along the rim, occasionally resembling a tuft (C. c. caniceps ; Moore and Tate 1965). In the southern part of its distribution, “ the upper parts of the head, neck, all the back and the tail as far as the tip bear a … pelage regularly ringed with ashy and black … ” ( Temminck 1853), with a rusty reddish suffusion in the side of the neck, and frequently, in the flanks and upper part of the legs; venter coloration is whitish gray, with a red suffusion in the groin area in adult specimens (C. c. bimaculatus and C. c. helvus). Its baculum consists of a shaft and blade; shaft lacks a dorso-lateral expansion at its proximal end; blade base has a reduced lateral expansion at its posterior half, giving it a straight appearance from a lateral view, and a relatively triangular shaped appearance from a dorsal view (Fig. 7 ); mating call characterized by an average of 8.1 pulses, mean pulse interval of 0.195 seconds, and average frequency modulation of 493 Hz.

Comparisons.

A detailed comparison with its closest relative, C. concolor , has been included in the following account. Callosciurus caniceps can be distinguished from all parapatric / sympatric squirrels, including C. concolor , by the combination of gray ventral pelage, lack of a black band in the flank, presence of an abruptly marked black tail tip, and during the dry season, bright ochraceous / rufus orange in flanks and dorsum or rusty reddish suffusion on the side of the neck and groin.

Distribution, habitat, and natural history.

Distributed across mainland Thailand west to the Mekong and up to ca. 19 ºN latitude, covering the northern two thirds of peninsular Thailand, and southern Myanmar (Figs 1 , S 3; south of the Salween River; Moore and Tate 1965). Pelage and craniodental variation suggest its southern distribution limits are in Trang, Surat Thani, and Nakhon Si Thammarat provinces (Fig. S 3). However, these provinces were not included in the genetic sampling of Hinckley et al. (2023 a), which only included specimens north of 7.99 and south of 7.15 latitude. For a more detailed description of this species’ southern distribution extent, see the account and discussion for C. concolor .

Generalist species found in dry deciduous forest and dry evergreen forest, bamboo forest, secondary forest, parks, gardens, and coconut plantations ( Moore and Tate 1965; Kobayashi et al. 2020). In northern Thailand it is only common in bamboo-forests at rather high altitudes ( Gyldenstolpe 1914). In Sakaerat Biosphere Reserve in northeastern Thailand, C. caniceps frequently used the ground (34.7 %; Kobayashi et al. 2018), which contrasts with little ground use by its sister species’ (ca. 2 %; Abdullah et al. 2001; Tamura 1995). In support of this observation, there are 29 records of C. caniceps on the ground from iNaturalist, compared to just two for C. concolor . Further research is required to determine if these behavioral differences are consistent across both species’ ranges. Callosciurus caniceps is frequently found in sympatry with C. finlaysonii , with which it minimizes competition through diet preferences and / or vertical zonation segregation ( Kobayashi et al. 2018).

This species has been observed feeding on fruits of Terminalia catappa and Tamarindus indica , and flowers of Triplaris americana in Bangkok parks, and on ten species of plants including Ficus fruits, Sterculia pexa and Acasia seeds, or Mucuna macrocarpa nectar in Sakaerat Biosphere Reserve, and Musa acuminata in Kanchanaburi ( Marod et al. 2010; Sommung and Hawkesgood 2016; Kobayashi et al. 2018, 2019, 2020). Fruits and seeds accounted for 71.4 % of observed food items in a human-disturbed area of Sakaerat, while bark was the most common food item (ca. 33 %) in adjacent undisturbed forests, suggesting a flexible diet ( Kobayashi et al. 2018, 2020).

Reproductive information is scarce. A female collected on 11 March 1900 in the Mergui archipelago had two embryos (W. L. Abbott field notes, USNM Mammal Division Archives). No other reproductive information was easily obtained.

Conservation.

Recorded in several protected areas, including Doi Pha Hom Pok, Khao Yai, Kaeng Krachan, Erawan, Nam Tok Tham Sadet, Sirinat, Mu Ko Lanta, Khao Luang, and Hat Chao Mai National Parks, Sakaerat Biosphere Reserve, and Chiang Dao Wildlife Sanctuary (iNaturalist; Table S 1). Despite these records, the frequency of detection of C. caniceps was lower in areas with human activity compared to adjacent forests even when human activity and fragmentation impacts were minimal ( Kobayashi et al. 2020). This species (sensu lato) is currently considered of least concern. However little is known about its population density, and one study found it to be far less common than a congeneric species, Callosciurus finlaysonii ( Kobayashi et al. 2020) .

Comments.

The subspecies C. c. bimaculatus and C. c. caniceps represent two distinct but recently diverged mitochondrial clades, exhibiting limited nuclear differentiation ( Hinckley et al. 2023 a). Interestingly, both subspecies seem to be present in Koh Tao island. A single Koh Tao “ caniceps ” could be included in the craniodental PCA and this was clustered with the mainland populations while the two specimens resembling “ bimaculatus ” ( USNM 253434, 253438), actually representing the form “ helvus ”, showed a distinct morphospace due to their dwarf nature. Unfortunately, the only Koh Tao individuals sequenced in Hinckley et al. (2023 a) belonged to the “ caniceps ” form. Thus, given its distinct morphospace (Fig. 3 ) and pending molecular evidence, we here consider the pygmy Koh Tao population a valid subspecies: C. caniceps helvus . This subspecies was wrongly synonymized with nominotypical C. caniceps in Moore and Tate (1965) given that the holotype pelage resembles that of C. c. bimaculatus . Previously recognized island subspecies are here synonymized since these generally resemble the closest mainland populations but with slight variations such as a pale tail underside ( casensis , and fallax) or a darker ( domelicus , fallax) or paler ( altinsularis ) dorsum.

Figures

Figure 1. Map of tropical East Asia indicating the localities of museum specimens examined in this study for Callosciurus caniceps. 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 3. Morphometric variation in Callosciurus caniceps. First and second principal components from an analysis of 11 craniodental variables. Samples are colored according to the two main lineages from Indochina (in blue) and Sundaland (in orange), and the Koh Tao dwarf population (in pink). Different subspecies are labeled with different symbol-color combinations.

Figure 6. Dorsal and ventral views of the skins of (A) Callosciurus caniceps (NHMUK 41.1817, lectotype); live images of (B) C. caniceps caniceps taken by Natthaphat Chotjuckdikul (Te’) in Bangkok, Thailand; (C) C. caniceps bimaculatus taken by Pattaraporn Vangtal in Railay Bay Beach, Krabi, Thailand; and (D) C. concolor taken by Cheong Weng Chun in Fraser’s Hill, Pahang, Malaysia.

Figure 7. Baculum comparison between Callosciurus caniceps and C. concolor. A Lateral view of C. caniceps (USNM 296998). B Dorsal view of C. caniceps (USNM 296998). C Lateral view of C. concolor (USNM 283481). D Dorsal view of C. concolor (USNM 283481).