Toxicocalamus atratus, Kraus & Kaiser & O’Shea, 2022

Kraus, Fred, Kaiser, Hinrich & O'Shea, Mark, 2022, Hidden diversity in semi-fossorial Melanesian forest snakes: A revision of the Toxicocalamus loriae complex (Squamata, Elapidae) from New Guinea, Vertebrate Zoology 72, pp. 997-1034 : 997

Toxicocalamus atratus sp. nov.

Figs 4M, N , 11E, F , 14 , 15

Toxicocalamus (Apistocalamus) loriae (part) - McDowell, 1969: 485.

Holotype.

MCZ R-84144, an adult female collected by Fred Parker at Kundiawa, 6.02°S, 144.97°E, elevation 1585 m, Chimbu Province, Papua New Guinea on 25 May 1964.

Paratypes (n = 90).

Papua New Guinea: Chimbu Prov-ince: along Wahgi River, 5.94°S, 144.80°E, elev. 1470 m, CAS 113665, 139564; Karimui, 6.50°S, 144.83°E, elev. 1170 m, CAS 118961-62; Kondiu, 5.98°S, 144.87°E, elev. 1600 m, AMNH R-75336-57; Kundiawa, 6.02°S, 144.97°E, elev. 1585 m, AMNH R-98495, R-98497, CAS 99916, 100069, 113670, 115986, 118948, 118960, 139584, 140043, MCZ R-83218, R-84026, R-111767, R-111788, R-115586, R-116774, R-116788, R-140818, R-145923, NMV 13421, USNM 166280; Kup, 5.95°S, 144.80°E, elev. 1500 m, AMNH R-72780-81; Mintima, 5.98°S, 144.91°E, elev. 1770 m, CAS 103374-75, 113663, 118957-59, MCZ R-116789-90, R-121547-48; Noru, 6.60°S, 144.63°E, elev. 1770 m, AMS R115365; Eastern Highlands Province: Agakamatasa, 6.72°S, 145.62°E, elev. 1720 m, MCZ R-121545; Lida Patrol Post, 6.32°S, 145.40°E, elev. 1800 m, CAS 139575; Lufa, Mt. Michael, 6.33°S, 145.25°E, elev. 1120 m, CAS 113666-67, MCZ R-121546; Nivi Unggai, 6.21°S, 145.31°E, elev. 2030 m, MCZ R-84142, R-116791 -92; Hela Province: Bobole, 6.23°S, 142.77°E, elev. 1145 m, AMS R122803, R122806; Halalinja, 6.15°S, 143.37°E, elev. 2140 m, BMNH 1976.92; Nipa, 6.10°S, 143.25°E, elev. 2070 m, UPNG 5811; Jiwaka Province: Banz, 5.78°S, 144.62°E, elev. 1650 m, AMNH R-85743, R-88060; Minj, 5.86°S, 144.87°E, elev. 1560 m, MCZ R-141849; Morobe Province: Kwaplalim, 12-13 km W Menyamya, 7.19°S, 145.97°E, elev. 1490 m, NMW 37670, UCM 51552-53; Southern Highlands Province: Mendi, 6.14°S, 143.66°E, elev. 1750 m, CAS 113664, MCZ R-121543-44; Moro Camp, Lake Kutubu, 6.36°S, 143.23°E, elev. 840 m, SAMA R69950; Western Highlands Province: Igindi, 6.19°S, 144.98°E, elev. 1630 m, AMNH R-98134; Kimil, 5.72°S, 144.53°E, elev. 1700 m, AMNH R-14783; Korn, Mt. Hagen, 5.84°S, 144.31°E, elev. 1630 m, AMNH R-14771, R-14773, R-14785-88.

Referred specimen.

Papua New Guinea: Morobe Prov-ince: S side Ekuti Divide, 7.42°S, 146.43°E, elev. 1050 m, BPBM 17423.

Etymology.

The species epithet is a masculine Latin adjective meaning "dressed in black," in recognition of the dark dorsal and ventral colouration of adults of this species.

Diagnosis.

A large member of the T. loriae Group (male SVL up to 655 mm, female SVL up to 682 mm) with the following unique combination of characters: sexual size dimorphism in SVL present (t 71 = 2.5689, p = 0.0062); two scales covering vent; posterior genials usually entirely separated (80%) but may be in anterior contact (20%) with each other; intergenial usually widest posteriorly (89%) or centrally (11%); preocular usually contacting nasal (77%), not contacting internasal; preocular rather short, less than twice as long as deep; postoculars two (one in 26%); posterior temporals two (58%) or three (42%); ventrals sexually dimorphic (t 85 = 7.400, p <0.00001), 177-206 in males, 187-218 in females; subcaudals sexually dimorphic with overlap (t 87 = -24.8814, p <0.00001), 40-47 in males, 26-41 in females; two scales covering vent; yellow nuchal collar and yellow markings on prefrontals present in juveniles, usually absent (but sometimes merely faded) in adults; tail spine paler than remainder of tail; and venter uniformly dark brown or dark brown with the posterior of each ventral paler brown or yellowish brown in adults, giving a banded appearance, black in life; venter yellow with a black spot on lateral margins of each ventral in juveniles.

Comparisons with other species.

Adult Toxicocalamus atratus is easily distinguished from all other members of the T. loriae species group except T. nymani in having a dark venter that is black or very dark brown in life and either uniformly brown or with each ventral banded dark brown in preservative. Other members of this complex have venters that are yellow ( T. lamingtoni , T. loennbergii , T. loriae , T. spilorhynchus , T. vertebralis ), grey ( T. nigrescens ), or yellow or pale grey with grey bands across each ventral ( T. mattisoni ). Toxicocalamus atratus can be distinguished from T. nymani by its juvenile ventral colour pattern (pale yellow with a black spot on the lateral edges of each ventral vs. uniformly black or dark brown but banded with dark brown in preservative in T. nymani ), larger size (males to 655 mm SVL, females to 682 mm SVL vs. 422 mm and 540 mm, respectively, in T. nymani ), and the greater number of ventrals with overlap in both sexes (males 177-206 vs. 178-198 in T. nymani ; t 65 = 5.0261, p <0.00001; females: 187-218 vs. 191-210 in T. nymani , t 62 = 4.3472, p = 0.000026). Although the venter of T. atratus is much darker, its banded pattern in most preserved specimens could perhaps be mistaken for the paler banded pattern seen in preserved T. nigrescens and T. mattisoni . Toxicocalamus atratus can be further distinguished from T. nigrescens in having a shorter preocular (preocular approximately squarish, slightly longer than tall in T. atratus vs. more than twice as long as tall in T. nigrescens ), and from T. mattisoni in having the preocular usually contacting nasal (vs. never in T. mattisoni ) and usually two postoculars (vs. one in T. mattisoni ).

Description of the holotype.

Adult female, 590 mm SVL + 72 mm TL = 662 mm TTL. Rostral broader than high, notched ventromedially; internasals angulate, semi-triangular, wider than long; prefrontals distinct from preoculars, approximately square but angled laterally and posteriorly, slightly wider than long (Fig. 14A, A '), bordered below by preocular and nasal; preoculars angulate, slightly longer than high, bordered anteriorly by nasal, below by second and third supralabials (Fig. 14B, B ', C, C’); frontal shield-shaped, lateral margins straight, not fused with supraoculars, anterior margin extending slightly anterior to remainder of scale medially; parietals approximately twice as long as wide. Nasals divided by large nares, with a short groove above and below along the posterior of naris. Postoculars single on each side, irregularly pentagonal in shape; one elongate anterior temporal above fifth and sixth supralabials, separating latter from parietal; two posterior temporals, subequal in size, lower abutting posterodorsal margin of sixth supralabial. Supralabials six on each side, third and fourth entering eye; infralabials six, first three in contact with anterior genial. Mental small, shallow, triangular, wider than deep, bordered behind by first supralabials; anterior genials slightly larger than posterior genials, in medial contact along entire length; posterior genials longer on left than right, completely separated by single elongate intergenial, which is widest posteriorly; seven gulars separate intergenial from first ventral in the midline; first sublabial separates posterior genial from fifth infralabial (Fig. 14D, D '). Eye relatively small; pupil round.

Dorsal scale rows 15-15-15, smooth, not notched posteriorly, without apical pits. Ventrals 207, each approximately four times wider than long; two scales covering vent; subcaudals 30, paired. Tail tipped by a pointed coni-cal spine.

In preservative (50 years after collection), dorsum dark brown dorsally, slightly paler laterally (Fig. 15A ). Venter dark brown, anterior ventrals dark brown, narrowly margined with paler brown posteriorly (Fig. 15B ), subcaudals dark brown. Supralabials yellow, dark brown on approximately dorsal half of each scale. Head dark brown with vague yellow blotch on each prefrontal just extending onto posterolateral corner of each internasal. No pale nuchal collar present. Chin and throat with pale straw yellow ground heavily suffused with brown throughout, imparting a largely brown impression overall. Tail spine white. Iris black.

Variation.

Preoculars contact nasals in most specimens but are separated by prefrontal contact with the second supralabial on both sides in 17 specimens and on one side in nine specimens; preoculars are invariably separated from contact with internasals. Postoculars one (25.5%) or two (74%), absent on left side of MCZ R-141849. Posterior temporals two (58%) or three (42%). Supralabials six, except five on right side of AMS R14788, CAS 118948, and MCZ R-84142, the left side of MCZ R-116790, and both sides of CAS 115986, 118962, and MCZ R-141849; third and fourth supralabials contacting eye, except third through fifth on right side of AMNH R-75344, and only third supralabial on right side of AMS R14788, CAS 118962, and MCZ R-84142. Infralabials invariably six. Posterior genials in small anterior contact (20% of specimens) or entirely separated (80%) by single intergenial (two small intergenials in AMNH R-72780-81 from Kup). Intergenials widest posteriorly (89% of specimens) but widest centrally in ten (11%).

Dorsal scale rows invariably 15-15-15. Ventrals 177-206 (196 ± 5) in 49 males, 187-218 (206 ± 7) in 43 females; subcaudals 40-47 (44 ± 2) in 48 males, 26-41 (31 ± 3) in 41 females. SCR 16.9-21.0% (18.3 ± 0.8%) in 48 males, 11.2-17.8% (12.9 ± 1.3%) in 41 females. Tail tipped by a blunt to pointed conical spine. Maximum male SVL = 655 mm, TLR in 38 adult males 12.9-19.4% (15.5 ± 1.7%); maximum female SVL = 682 mm, TLR in 33 adult females 6.7-18.7% (10.2 ± 2.2%); sexual size dimorphism present (t 71 = 2.5689, p = 0.0062). There appears to be an ontogenetic effect of tail length in juvenile males, whose tails are relatively shorter (mean TLR 12.5 ± 0.6; n = 10) than those of adult males (mean TLR 15.6 ± 1.7; n = 39). This difference is not present in females (mean TLR in eight juveniles 10.4 ± 1.4, in 32 adults 9.9 ± 1.7). The vent is typically covered by two scales, but this covering is incompletely formed in AMNH R-75355 and covered by a single scale in CAS 103774-75 and 139584.

Variation in colouration is largely ontogenetic, with adults being black or dark brown above and below, although these colours fade to brown in preservative, and often with each ventral appearing banded with dark and light brown as colouration fades in preservative. Small juveniles (SVL = 161-262 mm) are often paler than this, with a dark vertebral stripe often being present, but this seems to be lost as animals darken ontogenetically. Small juveniles also have a large yellow blotch on each prefrontal and an incomplete yellow nuchal collar whose sides are separated by two to four brown dorsal scale rows (Fig. 4M, N , 16 ). These markings usually disappear in adults but may be retained as vague markings. Furthermore, small juveniles have a yellow venter with each ventral marked on each lateral extremity with a black spot. Because the first row of dorsal scales is also yellow or pale brown, this imparts the impression of the venter having a row of black spots along each side. In a few small specimens (CAS 103374, 113666, MCZ R-116774), these yellow venters also have a few small brown flecks. The tail spine is white in most specimens but pale brown in two.

Colour in life.

Photographs of MCZ R-84026 (540 mm SVL) and R-111767 (480 mm SVL), both adult males, show uniformly black animals, with the venter of the latter also being black (Fig. 11E, F ). Photographs provided to us by Nick Baker of an uncollected juvenile from Southern Highlands Province, PNG, show an animal with a black dorsum (Fig. 16A ), yellow venter having a mid-ventral row of brown spots (Fig. 16B, C ), and yellow supralabials, a yellow spot on each prefrontal, and a very incomplete nuchal collar consisting of only two small yellow lateral spots (Fig. 16C, D ).

Fred Parker, the collector, took numerous field notes on this species in life. Colour patterns for adults were described by him as follows: "Black with pair of yellow spots on the snout, partial bars laterally on back of head." (MCZ R-121547, SVL = 360 mm); "Part grown, black above and below." (CAS 139564, SVL = 455 mm); "Olive-black above, a narrow darker vertebral line from behind head to tip of tail. Lips translucent pinkish marked grey. Ventrals greyish, paler than dorsum." (MCZ R-84142, SVL = 470 mm); "Uniform iridescent black on dorsal surfaces. Ventrally and laterally uniform black with no markings. Lips faintly yellowish. Spike on tail yellow with black tip." (MCZ R-84026, SVL = 540 mm). "Black above, brown laterally. Grey-brown underneath. Lips paler." (CAS 99916, SVL = 610 mm). "Black above and below. Head slightly paler with olive tinge. Highly iridescent." (AMNH R-98495, SVL = 515 mm).

He described the colour pattern for two juveniles as follows: "A juvenile with bright yellow bar across snout and short similar bars laterally on back of head from behind corner of jaw to posterior corners of large head shields but not meeting dorsally. Ventrally, translucent yellow, with a black spot at side of each ventral [scale]. Tail with yellow spike at tip, the spike with small brown tip. Whole of upper lips yellow. Some greyish markings under the head. A narrow dark vertebral stripe. Flanks paler than dorsum. Pair of anals marked grey." (MCZ R-83218, SVL = 211 mm); "Grey-brown above, whitish below, yellow bar on snout, lips yellow, part bars laterally at back of head." (AMNH R-98498, SVL = 299 mm). Finally, a neonate that hatched on 23 December 1964 was recorded as black above, translucent below, and with paler lips; we have been unable to locate this specimen in any museum catalogue.

Range.

Known from the Central Highlands of Papua New Guinea and extending as far east as the southern side of the Ekuti Dividing Range, Morobe Province, at elevations of 840-2140 m (Fig. 6B ).

Ecological notes.

Considered common at Kundiawa, Chimbu Province, PNG (Fred Parker, pers. comm.). For example, 88 animals were obtained in gardens on 3 December 1967. In general, most individuals of this species were collected during the day from under piles of vegetation in sweet potato gardens. In forested situations, only the occasional animal would be collected in or under logs during the day. Parker never observed the species active at night, which is consistent with the first author’s experience with other Toxicocalamus species. One specimen (MCZ R-111769, SVL = 437 mm) contained a large earthworm in its stomach.

Parker’s field notes also recorded that MCZ R-84144 (SVL = 590 mm) laid two eggs on 25 May 1964 and one on the following day; one of these hatched on 23 December, indicating a 7-month incubation period. MCZ R-111790 (SVL = 440 mm) was captured on 3 December 1967 and "laid four eggs after capture," CAS 115987 (SVL = 375 mm) was captured on 29 February 1969 when gravid with three eggs, CAS 115992 (SVL = 435 mm) and CAS 115996 (SVL = 625 mm) were captured on 11 March 1968 and noted to be gravid, and CAS 115997 (SVL = 480 mm) was captured on 19 April 1968 gravid with six eggs. All of these snakes were from Kundiawa, Chimbu Province. Thus, gravid females were captured during the months of February to April and eggs were laid in May and December, suggesting that reproduction in this species occurs year-round. The observed eggs were cylindrical, bluntly rounded at each end, and measured 35 × 12 mm, 35 × 12.5 mm, and 39 × 14 mm.

Remarks.

The primary feature distinguishing T. atratus from the very similar T. nymani is the ontogenetic change in ventral colour pattern, which is dramatic in T. atratus but absent in T. nymani . Some populations of T. nymani also retain the yellow nuchal collar and prefrontal spots into adulthood, which individuals of T. atratus never do. Furthermore, Lönnberg (1900: 579) described the dorsal colour of his freshly preserved specimens of T. nymani as "bronzy brown (almost blackish in the largest specimen)", whereas notes by Fred Parker recorded that a neonate and small juvenile of T. atratus were black above (see also Fig. 16 ). As noted in the Comparisons section above, T. atratus also differs from T. nymani by its larger maximum size and, statistically, by its greater mean count of ventral scales in both males and females. These differences are confirmed by post-hoc Tukey Tests in an ANOVA (p = 0.00551 and p = 0.04195 for males and females, respectively). Its lesser mean SCR in males also differs significantly from that seen in T. nymani . Each of these differences suggests that T. nymani and T. atratus are separate species, but scalational differences that would be useful to field observation are not obvious at this point. It will be useful to investigate this issue in greater detail once fresh specimens with tissues and colour notes become available for both species.

We refer the sole specimen from south of the Ekuti Divide (BPBM 17423) to this species on the basis of its ventral colour pattern, which indicates the lateral rows of brown spots on each ventral. However, the venter of this specimen is somewhat discoloured, and its collection locality is close to Wau, where T. nymani primarily resides, so confirmation of this assignment to T. atratus would be desirable once further specimens become available. This uncertainty leads us to exclude this specimen from the series of paratypes.

Figures

Figure 4. Dorsal and right lateral views of heads of juveniles of Toxicocalamus loriae Group snakes. A, B T. loriae (BPBM 10966), Agaun, Milne Bay Province, PNG. C, D T. nymani comb. nov., spotted form (BPBM 5442), Kalolo, Morobe Province, PNG. E, F T. nymani, dark form (BPBM 23699), Wau, Morobe Province, PNG. G, H T. lamingtoni comb. nov. (AMS R 9352), Mt. Lamington, Oro Province, PNG. I, J T. vertebralis sp. nov. (KU 129086), Wau, Morobe Province, PNG. K, L T. spilorhynchus sp. nov. (AMNH R- 107204), Garaina, Morobe Province, PNG. M, N T. atratus sp. nov. (CAS 118958), Mintima, Chimbu Province, PNG.

Figure 6. Type localities (stars) and other collection sites (circles) of Toxicocalamus loriae Group species. A Map of New Guinea and its satellite islands, showing the positions of the inset maps and the type locality of T. mintoni (magenta), an endemic of Sudest Island, Milne Bay Province, PNG. Scale = 500 km. B Papua New Guinea and adjacent areas of West New Guinea, Indonesia, with white lines demarcating provincial boundaries. Scale = 250 km. C West Papua Province, Indonesia (WP), showing the type locality of T. loennbergii comb. nov. (orange). Other species treated in this report are T. loriae (dark blue), T. lamingtoni comb. nov. (yellow), T. spilorhynchus sp. nov. (red), T. nymani comb. nov. (neon green), T. vertebralis sp. nov. (pink), and T. atratus sp. nov. (light blue). Additional related species in the T. loriae clade are T. goodenoughensis (brown), T. mattisoni (violet), T. nigrescens (black), T. pachysomus (dark green), and T. " Toxicocalamus loriae " Clade 4 (white). The type locality of the recently described dubious taxon T. longhagen (tan) is also indicated. Scale = 250 km. Provinces of PNG are Central (Ce), Chimbu (Ch; also spelled Simbu), Gulf (Gu), Hela (He; created in 2012), Eastern Highlands (EH), East Sepik (ES), Enga (En), Jiwaka (Ji; created in 2012), Madang (Ma), Milne Bay (MB), Morobe (Mo), National Capital District (NCD), Oro (Or; also known as Northern Province); Sandaun (Sa; formerly West Sepik), Southern Highlands (SH), Western (We), and Western Highlands (WH). Provinces of West New Guinea are Highland Papua (HP; created in 2022), Papua (Pa), and South Papua (SP; created in 2022). Sites of sympatry are Wau (W; neon green + pink) with two species and Garaina (G; neon green + red + yellow) with three species.

Figure 11. Toxicocalamus loriae Group species in live and perimortem photographs to show colour in life. A, B T. vertebralis sp. nov. (CAS 140042) from Kol, Jimi Valley, Jiwaka Province, PNG. C, D T. spilorhynchus sp. nov. (MCZ R- 152431) from Garaina, Morobe Province, PNG. E T. atratus sp. nov. (MCZ R- 84026) from Kundiawa, Wahgi Valley, Chimbu Province, PNG. F T. atratus (MCZ R- 111767) from Kundiawa, Wahgi Valley, Chimbu Province, PNG. Photographs by Fred Parker.

Figure 14. Head of the Toxicocalamus atratus sp. nov. holotype (MCZ R- 84144) from Kundiawa, Chimbu Province, PNG, in both photographic and line-drawing illustrations. A, A ' dorsal, B, B ' right lateral, C, C ' left lateral, and D, D ' ventral views.

Figure 15. A Dorsum and B venter of the Toxicocalamus atratus sp. nov. holotype (MCZ R- 84144) from Kundiawa, Chimbu Province, PNG.

Figure 16. Uncollected juvenile Toxicocalamus atratus sp. nov. from Kutubu area, 1760 m elevation, Southern Highlands Province, PNG, to show the colouration in life. Photographs by Nick Baker.