Callosciurus concolor ( Blyth, 1855 )

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 concolor ( Blyth, 1855)

Sciurus concolor Blyth, 1855 , Journal of the Asiatic Society of Bengal 24: 474.

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

Sciurus lancavensis Miller, 1903 a , Smithsonian Miscellaneous Collections 45: 16.

Sciurus concolor terutavensis Thomas & Wroughton, 1909 , Annals and Magazine of Natural History (Series 8) 4: 535.

Callosciurus erubescens Cabrera, 1917 , Boletín de la Real Sociedad Española de Historia Natural 17: 518.

Callosciurus concolor telibius Thomas & Robinson, 1921 , Annals and Magazine of Natural History (Series 9) 7: 121.

Callosciurus moheius Thomas & Robinson, 1921 , Annals and Magazine of Natural History Annals and Magazine of Natural History (Series 9) 7: 122.

Callosciurus moheius mohillius Thomas & Robinson, 1921 , Annals and Magazine of Natural History (Series 9) 7: 122.

Holotype.

ZSI 9328. Skin and skull, collected or donated by G. Moxon in 1847. This specimen was not cited in the “ Annotated Catalogue of the Type Specimens of the Indian Museum ” ( Khajuria et al. 1977), but the skin is still housed in the National Zoological Collection of the Zoological Survey of India (Uttam Saikia pers. comm.). Other catalog numbers linked to this specimen are: Zoological Survey of India barcode number: ZSI 0000004087; Indian Museum of Kolkata catalog number: “ w ”.

Type locality.

From the vicinity of Malacca ” [Melaka, Malaysia].

Emended diagnosis.

A medium-sized Callosciurus (average HB = 218.3 mm, PL = 49.1 mm) that can be distinguished from all other relatives by the combination of the following morphological characters: “ reddish suffusion of color occurring on the mid dorsum [that usually extends to the proximal section of the tail] but not on the sides of the neck and body …; absence of a sharply marked off, quite black tip of the tail … [except in northern edge populations; see following sections], and a cool silvery gray color of the venter ” ( Moore and Tate 1965), that lacks a reddish suffusion in the groin area; cranium with relatively long postorbital processes ( LPOP: 3.8–5.8 mm), particularly proportionally to its least interorbital length ( LBO: 16.3–18.8 mm); baculum consists of a shaft and blade, shaft has a dorso-lateral (right) expansion at its proximal end, blade base has a large lateral expansion at its posterior half, giving it a sinuous appearance from a lateral view, and a relatively rounded / oval shaped appearance from a dorsal view (Fig. 7 ); mating call characterized by an average of 17.9 pulses, mean pulse interval of 0.098 seconds, and an average frequency modulation of 1476 Hz.

Comparisons.

Callosciurus concolor can be distinguished from its closest relative, C. caniceps , by its smaller size (average HB: 220 vs 235 mm; with the exception of the C. caniceps Koh Tao Island dwarf population, which is even smaller than C. concolor and excluded from this comparison). Additionally, this species exhibits relatively longer postorbital processes and a distinct distribution of ornamented pelage coloration. During the dry season, its dorsum has a reddish suffusion in the midline that generally extends to the most proximal side of the tail, while C. caniceps has a brighter, ochraceous / rufus orange in flanks and dorsum (C. c. caniceps ) or a rusty reddish suffusion in the side of the neck and groin, and frequently, in the flanks and upper part of the legs (C. c. bimaculatus ; Fig. 6 ). In the wet season, this reddish suffusion disappears or becomes less conspicuous in both species, but C. caniceps generally still retains a yellow / orange-brown hue. This hue can at least be noted in the side of the neck and groin in C. c. bimaculatus and in a few small patches throughout the dorsum in C. c. caniceps , which greatly contrast with the darker gray ash coloration in the latter. The venter of Callosciurus concolor is silvery gray distinct from the whitish gray (C. c. bimaculatus ) or agouti gray (C. c. caniceps ). Another diagnostic feature is the absence of a sharply marked off, black tail tip throughout most of C. concolor populations, whereas C. caniceps typically exhibits such feature. Notably, C. concolor populations in Langkawi, Adang, Terutao (⅛ specimens), and Songkhla have a black tail tip that is generally shorter and / or less intensely black than that of C. caniceps , resulting in a less pronounced contrast. However, in Trang, Surat Thani, and Nakhon Si Thammarat, the black tail tip of C. concolor is highly contrasted as in C. caniceps . Examined specimens from the latter two provinces, and all the rain-shade area until Singora have a washed dorsum coloration and possibly lack an ornamented dorsum midline during the breeding season. Thus, the absence of reddish suffusion in the groin area of C. concolor , compared to its presence in C. caniceps bimaculatus , along with the presence or absence of red suffusion on the side of the neck, appear to be the best diagnostic features for distinguishing these species in the contact areas of Surat Thani, Trang, and Nakhon Si Thammarat, and perhaps also in Satun, Phatthalung and Songkhla. However, juvenile and subadult specimens lack this reddish hue, suggesting this feature is diagnostic primarily in adults. The skull of C. concolor is smaller ( PL: 46–51.5 vs 49.7–56.2 mm) with a shorter rostrum ( SL: 18.0–21.2 vs 20.4–24.4 mm) and interorbital breadth ( LBO: 16.3–18.8 vs 18.3–21.7 mm; Fig. S 1 A), but relatively larger postorbital processes (average LPOP: 4.7 vs 4.8 mm; Fig. S 1 B) than C. caniceps . As mentioned, the allopatric dwarf population on Koh Tao island has a smaller size than C. concolor and was excluded from these comparisons, but it shows a distinct shape and its morphospace does not overlap with C. concolor , due to the combination of relatively larger postorbital processes and relatively shorter interorbital breadth of C. concolor with regard to the Koh Tao population (Figs 3 , S 1 A, B). Allometric size-controlled statistical analyses only supported significant differences in PL, DL, and MPL between C. concolor and C. caniceps (File S 1). Paradoxically, these measurements are the largest, perhaps suggesting an allometric size effect in the data, and that these sister species differ mainly in size, with little shape differentiation.

Baculum morphology provides additional distinguishing characteristics between C. concolor and C. caniceps : Presence vs absence of a dorso-lateral (right) expansion at shaft proximal end in C. caniceps ; presence vs absence of a large lateral expansion at blade base posterior half in C. caniceps , giving a sinuous ( C. concolor ) vs straight ( C. caniceps ) appearance from a lateral view, and a relatively rounded / oval ( C. concolor ) vs triangular ( C. caniceps ) shaped appearance from a dorsal view (Fig. 7 ).

Finally, C. concolor can be easily distinguished from its closest genetic relative, C. caniceps , by its generally distinct mating call (Fig. 5 A ; Table S 4, correct discrimination rate = 87 %). This is characterized by an average of 17.9 pulses, mean pulse interval of 0.098 seconds, and average frequency modulation of 1476 Hz vs an average of 8.1 pulses, mean pulse interval of 0.195 seconds, and average frequency modulation of 493 Hz in C. caniceps (Fig. 5 B – D ).

It can be easily distinguished from sympatric congeneric C. notatus and C. nigrovittatus by its lack of lateral stripes, and from C. erythraeus by its silvery gray venter, grayish head and limbs which contrast with the remaining dorsum, and darker tail tip vs reddish brown, reddish or agouti venter, homogeneously olive brown colored dorsum, including head, limbs and tail. It can be distinguished from sympatric Sundasciurus robinsoni , S. tahan , and S. tenuis by its larger size, grayish head and limbs, bushier dark-tipped tailed, and thinner and less contrasted pale eye ring, and from S. hippurus by its silvery gray venter coloration with just some black or dark gray / brown in the tail tip vs rusty red venter with entirely black tail in S. hippurus .

Distribution, habitat, and natural history.

Distributed across the Thai-Malay peninsula extending from Melaka to Trang province in the west coast and from central Pahang to Surat Thani in the east coast (Figs 1 , S 3). Habitat generalist recorded in lowland and hill primary and secondary dipterocarp forests recorded up to ca. 1135 m a. s. l., plantations, and urban / suburban areas ( Moore and Tate 1965; Tamura and Yong 1993; Abdullah et al. 2001; Saiful and Nordin 2004). In Ulu Gombak ( Malaysia), C. concolor preferred bushy areas with a larger number of small trees, in contrast with C. notatus that showed preference for the opposite ( Tamura and Yong 1993). In this reserve, the four species of squirrels use different levels of the habitat: L. insignis uses the ground, C. concolor lower levels, C. notatus middle levels, and C. nigrovittatus the highest levels of trees ( Tamura 1995). In the same site, it was shown to feed on 13 species of plants — on fruits (45 %), leaves (21 %), bark (17 %), and flowers (10 %) — with “ others ” comprising the rest of its diet. These consisted mainly of the fruits of Artocarpus elasticus , Piper adancum and Ficus spp. , and leaves of Bambusa vulgaris ( Abdullah et al. 2001) . Other studies in Malaysia based on stomach content examination instead of feeding observations showed that all specimens contained fruit and vegetable matter, and six contained insect remains (n = 9; Harrison 1954, 1961). In Ulu Gombak, the average size of home ranges of males was 2.65 and 3.73 ha, and that of females was 0.79 and 1.54 ha, and females ranges overlap, contrasting with the lack of overlap in other Callosciurus spp. ( Tamura 1993; Saiful et al. 2001). Mating bouts were observed from March to July in this site ( Tamura 1993). In Selangor, this species has been recorded in sympatry with C. nigrovittatus , C. notatus , C. erythraeus , Sundasciurus tenuis , Sundasciurus hippurus , Lariscus insignis , Rhinosciurus laticaudatus (R. Traub field notes; USNM Mammal Division archives).

Conservation.

Recorded in Labis and Ulu Gombak Forest Reserves, Hala Bala Wildlife Sanctuary, Perlis, Gunong Stong and Selangor State Parks, Tasik Bera Ramsar Site, and Taman Negara National Park ( Jayaraj et al. 2013; Ling et al. 2018; William-Dee et al. 2019; Munian et al. 2020; Fauzi et al. 2021; iNaturalist; USNM specimens). It was the most abundant Callosciurus species in a logged hill forest (8. l individuals / ha) but the least abundant one in a primary hill forest, perhaps suggesting a preference for secondary forests ( Tamura and Yong 1993; Saiful et al. 2001; Saiful and Nordin 2004). Similarly, it was not recorded in the primary forest of Krau Game Reserve but it was frequently seen in rubber plantations around the reserve ( Mackinnon 1978). This species is destructive in plantations of Artocarpus integrifolia and Cocos nucifera in various states of Malaysia ( Moore and Tate 1965).

Comments.

Northwestern edge populations from the islands of Langkawi (named form lancavensis ), Telibun [Ko Libong] (named form telibius), Adang (named form adangensis ) and Mohea, Nakhon Si Thammarat (named forms mehoeius / mohillius), have a pelage that is somewhat intermediate between C. concolor and C. caniceps bimaculatus , but more similar to the former (This study; Moore and Tate 1965). These have a more sharply marked-off, black tip of the tail than other C. concolor populations ( bimaculatus ); generally lack the red suffusion in the neck side ( concolor ), except a single specimen in Lankawi, Ko Terutao and Ko Libong which had some faint yellow C. c. bimaculatus ; lack a reddish suffusion in flanks and groin ( concolor ), and generally have a venter gray coloration that seems intermediate between concolor and bimaculatus (This study; Moore and Tate 1965). Specimens from Langkawi, Adang and Terutao islands were included in the craniodental PCA and are however clearly within the morphospace of C. concolor . Ko Libong museum specimens could not be examined but citizen science pictures suggest these are C. concolor , and / or potential hybrids (Table S 3). Remarkably, museum specimens ( USNM 83235) and pictures taken 3 km away, in the mainland (Prahmon, Yan Ta Khao District, Hat Chao Mai NP and Mot Tanoi Beach) show a C. caniceps skull and / or pelage. The mouth of the Trang and / or Palian River might represent the northwestern limit for this species at the west coast since a specimen from “ Trang ” ( USNM 86780), which must have been collected in a locality east of this river (according to W. L. Abbott’s field notes all localities sampled during the timeframe in which the specimen was collected were east of this river) and Kao Soi Dao (7.35, 99.86; USNM 258917–8), which is southeast of Trang River, showed C. concolor craniodental morphospace and / or pelage. Potential hybrid specimens are recorded at this river headwaters, in Lay Song Hong (7.83, 99.45; USNM 83495–7), while C. c. bimaculatus with a faintly ornamented pelage side are recorded in Khao Chong ( USNM 258916; 7.54, 99.79), at the foothills of the Nakhon Si Thammarat Range ( NSTR). This suggests that the Trang and / or Palian Rivers and NSTR might have constituted physical barriers to gene flow to some extent. Similarly, on the east coast, C. caniceps seems to have its southern limit around Surat Thani city and Ban Ta Yai (8.38, 99.87), potentially at the confluence of two major rivers: Ta Pi and Phum Duang. Tha Lo, which is SW of the city, has potential hybrids (Fig. S 4). The species C. caniceps seems to be distributed north of these rivers and west of NSTR (e. g., Ban Kok Klap, 8.88, 99.28; Robinson and Kloss 1915), while C. concolor seems to be found to the east of this range (Ban Ta Yai, Nakhon Si Thammarat; Figs 1 , S 3). Furthermore, specimens ( USNM 355078, 355079, 35580, 535161; Fig. S 4) collected in this mountain range or at its foothills (Doi Kaeo, Nam Tok Tha Phae, and Ban Tha Phae, at Lan Saka and Chawang districts) have a hybrid pelage (red infusion in mid-line but also in the sides, particularly on the neck, and groin area, or C. concolor venter with C. caniceps dorsum coloration). However, specimens from Ban Nam Tok, Ban Na and Thafa, unknown localities also at Chawang district ( USNM 535159, 535163–8), have C. caniceps pelage. Just at 30 km from the potential hybrid population of Nam Tok Tha Phae, and at the east side of NSTR, there is Ban Ta Yai (8.38, 99.87) which has C. concolor pelage. Craniodental data is quite consistent with pelage since localities from Nakhon Si Thammarat and Trang are intermingled with those of N and S groups in the PCA of Hayashida et al. (2007). However, localities from Prachuap Khiri Khan, Chumphon, Krabi and some from Mergui archipelago were also in between the morphospace of C. caniceps and C. concolor , but this study and / or Hinckley et al. (2023 a) craniodental, pelage and / or molecular evidence show these populations represent C. caniceps (Hayashida et al. 2006) . The addition of the diagnostic postorbital process length variable might have contributed to a better resolution in this study. Similarly, Hayashida et al. (2007) considered specimens with completed molar eruption as adults while this study was more conservative, considering specimens with deciduous or partially erupted premolars as subadults. According to molecular data, the southern limit of C. caniceps is between 6.5– 8 ° N, specimens sequenced further south in Hinckley et al. (2023 a) are from Phuket at east coast and Ko Tao at west coast, but sampling at Trang and Nakhon Si Thammarat provinces is lacking.

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 5. Variation in mating calls of Callosciurus species. A Principal Component Analysis highlighting mating call variation. B Univariate plot showing the number of pulses per call. C Univariate plot of pulse intervals, in seconds. D Univariate plot of frequency modulation, in Hz. Different taxa are represented by distinct symbols.

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).