Trimeresurus borneensis ( Peters, 1872 )

David, Patrick, Vogel, Gernot, Vijayakumar, S. P. & Vidal, Nicolas, 2006, A revision of the Trimeresurus puniceus-complex (Serpentes: Viperidae: Crotalinae) based on morphological and molecular data, Zootaxa 1293 (1), pp. 1-78 : 38-45

Trimeresurus borneensis ( Peters, 1872)

( Figs. 15–18 )

Atropophis borneensis Peters, 1872: 41 . Type locality. “ Sarawak auf Borneo” by implication, now Sarawak, Borneo Island , Federation of Malaysia. Syntypes. MSNG 8383a–b (2 specimens) and ZMB 7146 , according to Bauer et al. (1995: 80). Collected by G. Doria and P. Beccari, 1865–1868 ( MSNG8383 a–b) and Mr. Abendroth ( ZMB 7146 ) .

Bothrops sandakanensis Lidth de Jeude, 1893: 256 , 3 figures. Type locality. “in the neighnourhood of Sandakan Bay (N. Borneo)” by implication, now Sandakan, State of Sabah, Borneo Island, Federation of Malaysia. Syntypes. RMNH 4338 (2 specimens), according to Hoge & Romano (1974: 150), not traced according to McDiarmid et al. (1999: 330). Collected by Mr. J.C. Prakke.

Material (28 specimens). FEDERATION OF MALAYSIA. Borneo Island . State of Sabah . BMNH 94.6 .30.67, “Paitan, N. Borneo”, 6°22'60N, 117°22'0E ; BMNH 1968.847 (female), “Lundu, Sabah”, now Lundun (5°40'60N, 117°13'0E) ; FMNH 76324 (male), “Brantian River Estate, Tawau District, North Borneo”, a locality now near Kalabakan ; FMNH 240499 (male), “Area II, Tenom Purulon, Sabah”. State of Sarawak . BMNH 91.8 .29.38 , BMNH 92.6 .3.10 (2 males), “Mt. Dulit, North Borneo”, now Dulit Range ; BMNH 92.10 .7.16 (female) , BMNH 94.8 .3.7, “ Baram River, Sarawak ” ; BMNH 1911.1 .30.29 (female) , BMNH 1911.1 .30.30 (male), “Kidi Distr., Sarawak”, now Sungei Kudi, Kapit Division ; FMNH 128436 (female), “Pengkalan Lobang, 4 th Division, Sarawak”, now Pangkalan Labong, Niah National Park ; FMNH 129463 (female), “Niah, Kampong Tangap, 4 th Division, Sarawak”, a village on Tangap River, Niah National Park ; FMNH 131846 (male), Ulu Niah, 4 th Division ; FMNH 138662 (male) , FMNH 204307 (female), Nanga Tekalit Camp, Mengiong River, Kapit District, 3 rd Division ; FMNH 148828 (female), Labang Camp on Sungei Seran, Bintulu District, 4 th Division ; FMNH 158672 (female), Tubau Camp on Sungei Pesu, Bintulu District, 4 th Division ; FMNH 188499 (male), “Nanga Tekalit, Kapit District, 3 rd Division, Sarawak; SMF 21255–56 (2 females), “Baramfluss, Borneo”, Baram River ; ZMB 7146 , “Sarawak auf Borneo” (syntype) . INDONESIA. Borneo Island (Kalimantan). State of Kalimantan Barat . RMNH 8405 (1) (male) , RMNH 8405 (2) (female), southern foot of Gunung Kenepai, 00°42’N – 111°43’E ; RMNH 8407 (male), “Nanga Raoen, Borneo”, now Nanga Raun (0°37'60N, 113°10'60E) ; USNM 36277 (female), Kalimantan Barat. State of Kalimantan Timur . MNHN 1957.818 (female), “ Fl. Bahau, Borneo N.E”, now Berau River . No precise locality . MNHN 1975.116 , “Borneo ou Nord de Sumatra ”, here ascertained as a

Bornean specimen; ZMH R­06922 (female), “Borneo, Sumatra ”, here ascertained as a Bornean specimen.

Diagnosis. A species of the genus Trimeresurus , endemic to Borneo Island according to the present definition, characterized by the combination of the following characters: (1) an overall grey, brown or ochre pattern with 20–30 darker crossbands, distinctly related to the sex: in males, background colour in various shades of greyish­brown or yellowishgrey, with darker dorsolateral blotches, sometimes horizontally divided into two distinct blotches, separated darker areas and powdered with both cream and dark dots, giving a rather confused pattern; in females, pattern less contrasted, in shades of ochre or yellowhish­brown with more or less brown subrectangular dorsolateral blotches, often with broad darker edges and a wide lighter centre, producing a “saddle­like” pattern; males have a more complex pattern, but are especially much darker than females; (2) a distinctly projected and raised snout, strongly obliquely truncated when seen from the side, subrectangular seen from above; (3) internasals projected, strongly spatulate and bilobate, distinctly upturned; (4) 19 or usually 21 (rarely 20) DSR at midbody; (5) 1 st supralabial distinct from nasal; (6) 2 nd supralabials bordering the whole of the anterior margin of the loreal pit; (7) 1 to 3 moderate, narrow supraoculars, usually flat, rarely convex; (8) VEN: 149–166, SC: 41–67; (9) occipital and temporal scales distinctly keeled in both sexes in adults, less so in juvenile specimens; (10) IL of the first pair not in contact each with the other; (11) hemipenes short, reaching 11 th SC, entirely spinose; and (12) adult females usually light colored.

Description and variation. We did not identify morphological variation correlated to the geographical origin among our sample of 28 specimens.

The maximal confirmed total length known is 874 mm (SVL 768 mm, TaL 106 mm) (female; BMNH 92.10.7.16). The largest known male known to us is 567 mm long (SVL 460 mm, TaL 107 mm; FMNH 94.6.30.67). In our sample, females reach distinctly higher sizes than males.

Body rather slender in males, quite stout in large females. Head distinctly triangular, average, amounting (in adults above SVL 400 mm) for 5.5–6.6 % of SVL (x = 6.2 %) in males, 5.9–6.7 % of SVL (x = 6.4 %) in females, wide at its base, thick but flattened in males, very thick and swollen in females when seen from the side. Snout distinctly projected and raised anteriorly, strongly obliquely trunctated when seen from the side, with a distinct canthus rostralis, rectangular seen from above, with strongly spatulate and bilobated internasal scales, rather long, amounting (in adults) for 24.6–28.7 % (x = 25.7 %) of HL in males and 24.2–26.6 % (x = 25.6 %) of HL in females, or 1.7–2.2 (x = 2.0) times as long as diameter of eye in males, 2.2–3.0 (x = 2.5) times in females. Eye small or average, amounting for 0.8–1.0 (x = 0.9) times in males and 0.6–0.8 (x = 0.7) times in females of the distance eye–lip. Tail average, tapering progressively and strongly prehensile. Ratio TaL/TL: 0.121 –0.189, with a strong sexual dimorphism (see below).

DSR: 21–27 ­ (19)21 ­ 13–15, usually moderately keeled, always smooth on the first DSR in both sexes.

On a sample of 28 specimens, the number of MSR is 19 (4/28), 20 (1/28) and 21 (23/ 28). The number of PSR is 13 (1/ 28 specimens) and 15 (27/28).

VEN: 149–166 (plus 1–2 preventrals); SC: 41–67, paired; anal shield entire.

These values are drawn from our own data only, and are limited by the size of our sample. The literature is useless, as no author both explicitly restricted the specific nomen to Bornean specimens and provided variation of morphological characters of their available specimens.

Rostral not visible from above, about 1.3–1.6 times broader than high, triangular; nasals subrectangular, undivided; usually 2 (48/56 occurrences), rarely 1 (8/56) internasals on each side, enlarged, strongly projected, spatulate and strongly bilobate, raised and distinctly upturned; internasals or group of internasals separated by 1 (in 11/ 28 specimens) or 2 (in 17/28) small scales; 3–5 canthal scales, slightly larger than adjacent snout scales, bordering the canthus rostralis between the internasal and corresponding supraocular; 2 elongate subrectangular loreal scales between upper preocular and nasal in all examined specimens; two upper preoculars above the loreal pit, elongated and in contact with the loreal; lower preocular forming the lower margin of loreal pit; 2–3 small postoculars; 1–3 moderate, narrow supraoculars on each side (1: 31/56 occurrences, 2: 16/56, 3: 9/56; total number: 2–6; x = 3.2, s = 1.3), flat or rarely convex, not extending out of the margin of the head, never raised, in total 2.2–3.0 (x = 2.7) times as long as wide, 0.4–0.8 (x = 0.6) time as wide as the group of internasals, irregularly bordered on their inner margins by the upper head scales; 5–8 (x = 6.5, s = 0.8) slightly enlarged scales on upper snout surface on a line between the scale separating the internasals and a line connecting the anterior margins of eyes, smooth, juxtaposed, irregular in shape (6 in 12/28 and 7 in 11/ 28 specimens); 9–12 (x = 10.5, s = 0.8) cephalic scales on a line between supraoculars (10: 11/28; 11: 12/28), small, smooth, flat and juxtaposed; occipital scales larger than cephalic scales, moderately or strongly keeled in both males and females; temporal scales small, subequal, in 2 or 3 rows, usually moderately (11/ 13 specimens) or strongly keeled (2/13) in males, moderately (10/15) or smooth (5/10) in females; one thin, elongated, crescent­like subocular; 9–11 SL (x = 10.1, s = 0.6) (9: 7/56 occurrences; 10: 36/56; 11: 13/56, with most often the combinations 10–10 or 10–11 SL); 1 st SL, rather short, always separated from nasal; 2 nd SL tall, always bordering the anterior margin of the loreal pit, separated from nasal by 1 or usually 2 small scales; 3 rd SL longest and highest, 1.3–1.8 times as long as high (x = 1.5), separated from the subocular by usually 1 (48/56 occurences) or 2 (8/56) scales, without sexual dimorphism; 4 th SL as long as high, 0.7–0.8 (x = 0.75) time as low as 3 rd SL, separated from the subocular by 1 (11/56 occurrences) or 2 (43/56), rarely 3 (2/56) scales on each side; 5 th and posterior SL smaller than 4 th one, 5 th SL separated from subocular by 2 (in 47/56 occurrences) or 3 (9/56) scale rows of similar size, without clear sexual dimorphism; 12–14 (exceptionally 11 or 15) IL (11: 3/56 occurrences; 12: 13/56; 13: 22/56; 14: 13/56; 15: 5/56); scales of the 1 st pair not longitudinally in contact, being divided into two scales; first two pairs in contact with anterior chinshields; 8–10 rows of smooth gular scales; throat shields very irregularly arranged.

In life, the coloration pattern of Trimeresurus borneensis is also both quite variable and complex, and strongly related to the sex.

In males, the body background colour is greyish­brown, yellowish­grey, or pinkishgrey, with 20–30 dorsolateral dark brown, dark reddish­brown, dark purple brown or dark greyish­brown; between the blotches, the background colour is darker than on the sides of body, with scales usually heavily powdered with both cream irregular dots and minute dark grey or dark brown dots or marked with small, irregular, dark blotches, giving a rather confused pattern, but not especially “ashy” like in T. puniceus . The large dorsolateral blotches are irregular in shape, subrectangular or more or less constricted in their middle, or angulous, reaching down to the 2 nd or 3 rd DSR, or only the 6 th or 7 th DSR but vertically divided with below an irregular, elongated blotches of same colour, separated from the main blotch by a lighter coloration; the centre of the dorsolateral blotches is somewhat lighter, their edge more or less darker, often with white or cream; the blotches are usually separated at the level of their upper part; blotches of both sides of body may be either fused or alternate, with all intermediates between a perfect opposition and a total alternation; on the tips of ventrals and on the 1 st DSR, a series of small, dark, elongated ventrolateral blotches, more or less irregular. The tail surface is usually of the same colour than the dorsolateral blotches, usually dark brown or dark reddish­brown, with pale greyish­brown or yellowish­brown rings, often edged with cream; the last third or so of the tail is entirely paler reddish­brown or yellowish­brown.

As observed in T. puniceus , the pattern is much less complex in females of T. borneensis , but also less contrasted than in males; the body is yellow­ochre, fawn, greyishbrown or yellowish­brown, rather pale, with large, subrectangular, not constricted, dark brown, dark yellowish­brown, pinkish­brown, greyish­brown or greenish­brown blotches, in same number than in males; these blotches are usually separated one from the other on their sides, with broad darker edges and a wide lighter centre, producing the “saddle­like” pattern that Hoge & Romano (1974: 158) credited to T. puniceus ; blotches of both sides of body may be either fused or alternate, with all intermediates; the blotches are less distinct than in males, producing a more subdued pattern. The tail surface is as described in males, dark brown, chocolate or dark reddish­brown, with pale greyish­brown or reddish­brown rings, the last part being entirely reddish­brown or yellowish­brown.

In both sexes, the dorsal head surface and temporal regions are of the same colours as the dorsolateral blotches, not paler on the anterior supralabials; in males, the sides of the head are often irregularly colored, with a complex pattern of light markings with a mixing of different hues and scales heavily powdered with dark minute dots; the lower margin of supralabials is often much lighter or cream; in females, the sides of the head are more uniform, but heavily powdered with minute black dots; a more or less distinct, more or less wide orange­brown, pale pinkish­ or reddish­brown postocular streak extending on upper temporals from the eye to the corner of the mouth in widening progressively before vanishing in general body colour; the postocular streak is edged below with a dark streak of same colour than upper head surface, itself edged with a short area of paler hue below at the limit of the throat and the edge of the supralabials. Eyes are golden or brownish­grey, more or less dark.

Venter usually much darker than dorsal background coloration, usually dark reddishbrown, dark ochre­brown or chocolate, irregular in colour and hues, powdered with numerous minute black dots; tips of ventrals with irregular elongated blotches of same colour than dorsolateral blotches intermixed with white blotches, making a very irregular, broken ventrolateral stripe. The chin and throat are paler than upper head surface, with numerous black dots and cream or pale brown irregular markings.

In juveniles, the colour and pattern are basically identical, but background colour of females is lighter than in adults, most often in the hues of ochre, pale yellowish­brown or greyish­brown, with darker but rather subdued dorsolateral blotches, whereas males show a more contrasted pattern.

In alcohol, T. borneensis more or less shows the patterns described above. Males tend to be darker than females, with a more complex pattern with irregular hues, whereas it is not rare to encounter females with a pale, barely visible pattern.

Hemipenes. In situ, the hemipenes are bilobate, short, massive, reaching 11 th SC, forking opposite 5 th SC. They are smooth in the vicinity of the sulcus bifurcation point, with some short spines proximally, and entirely covered with with calyces distally.

Comparison with other species. Trimeresurus borneensis differs from T. puniceus and T. cf. puniceus by the general characters given above to separate these groups. Besides the differences between the puniceus ­ and borneensis ­groups cited above, Tables 7–8 show other morphological and meristic differences between T. puniceus sensu stricto and T. borneensis , such as the ratio TaL/TL in males, the number of cephalic scales (Cep), the number of supraoculars, and so on.

The differences between Trimeresurus borneensis and other members of the Trimeresurus borneensis group are detailed under their respective accounts. The main differences are summarized in Tables 2–3. The salient distinctive characters of Trimeresurus borneensis are (1) the projected snout, strongly bilobate and upturned; (2) the 2 nd supralabials entirely bordering the loreal pit; (3) large, distinct and usually flat supraoculars; and (4) the range now restricted to Borneo Island.

Sexual dimorphism. It is strongly marked in the relative length of the tail, in the number of ventrals and in the pattern:

(1) Difference in the ratio TaL/TL:

males: 0.166 –0.189 (x = 0.173, s = 0.007); females: 0.121 –0.154 (x = 0.136, s = 0.010)

(2) Difference in the average numbers of subcaudals, but with an overlap of values: 47–64 (x = 54.8, s = 4.6) in males vs. 41–67 (x = 46.9, s = 4.2) in females.

(3) Difference in the number of scales separating the 5 th SL from the subocular:

in males: 2 scales in 25/26 occurrences, 3 in 1/26, vs. 2 in 22/30 and 3 scales in 8/30 occurrences in females.

(4) Difference in the pattern. Males show a more complex and contrasted pattern than females, the latter ones being usually lighter in overall pattern when adult.

In our sample of 28 specimens, there is also a clear difference of size between males and females, but not in the numbers of ventral scales nor in other scalation characters.

Range ( Fig. 4 ). FEDERATION OF MALAYSIA. This species is endemic to Borneo Island. States of Sabah and Sarawak. This species is known from at least 30 localities ( Hoge & Romano, 1974; Stuebing, 1991, 1994; Stuebing & Inger, 1999; Malkmus et al., 2002; specimens listed above). BRUNEI DARUSSALAM. Recorded from Belalong ( Das, 1995). INDONESIA. This species is endemic to Borneo Island. States of Kalimantan Barat and Kalimantan Timur. In the Kalimantan part of Borneo, Trimeresurus borneensis has been recorded from a few localities ( Stuebing, 1991, 1994; Stuebing & Inger, 1999; Iskandar, 2004; specimens listed above). It is likely to be more widespread in highland wet forests.

Biology. According to Inger & Tan (1996), Stuebing & Inger (1999) and Malkmus et al. (2002), Trimeresurus borneensis inhabits mostly lowland rainforests and tropical wet forests up to about 750 m asl, but in the vicinity of Mt. Kinabalu it has been found in wet montane forests at 1200 m. It also inhabits swamps and plantations, often in damp places close to water. Juvenile specimens are more terrestrial than adults, living mostly on the forest floor, but they also climb into low vegetation. Adults are seen on shrubs trees, perched on tree trunks and in thick foliage up to two or three meters above the ground ( Stuebing & Inger, 1999). This species feeds on mammals, probably also on lizards and frogs. This species is oviparous, producing clutches of 7– 14 eggs. Little is known on its biology.

Comments. Trimeresurus borneensis has been depicted alive in colour pictures in Inger & Tan (1996: 52: Fig.89), Stuebing & Inger (1999: 225–226), Malkmus et al. (2002: 375: Fig. 362) and Gumprecht et al. (2004: 164, Figs. III & IV). Ink drawings of the dorsal patter appeared in Hoge & Romano (1974: 157: Fig.10 , 158: Figs. 13–14 ).

Figures

FIGURE 4. Map: distribution of the taxa recognized in the Trimeresurus puniceus­complex. Symbols: dots: Trimeresurus puniceus.—Squares: Trimeresurus cf. puniceus.—Triangles: Trimeresurus borneensis.—Inverted triangles: Trimeresurus wiroti.—Pentagons: Trimeresurus andalasensis.—Stars: Trimeresurus brongersmai.

FIGURE 10. Trimeresurus puniceus. Living male, from Sumatra. Photograph by Albert Halimi.

FIGURE 13. Trimeresurus cf. puniceus. Specimen from Anamba Island (USNM 26544). Lateral view of head, left side. Photograph by Gernot Vogel.

FIGURE 14. Trimeresurus cf. puniceus. Specimen from Anamba Island (USNM 26544). Dorsal view of head. Photograph by Gernot Vogel.

FIGURE 15. Trimeresurus borneensis. Syntype, ZMB 7146. General view. Photograph by Gernot Vogel.

FIGURE 16. Trimeresurus borneensis. Syntype, ZMB 7146. Lateral view of head. Photograph by Gernot Vogel.

FIGURE 17. Trimeresurus borneensis. Adult female from Poring Hot Spring. Photograph by Björn Lardner.

FIGURE 18. Trimeresurus borneensis. Young female from Poring Hot Spring. Photograph by Björn Lardner.