Toxicocalamus loriae (Boulenger, 1898)

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 loriae (Boulenger, 1898)

Figs 1A, A ', 2A, A’, B, B’, 3A, A’, 4A, B, 5

Apistocalamus loriae Boulenger, 1898: 705.

Apistocalamus Pratti Boulenger, 1904: 451.

Apisthocalamus loriae - Boulenger, 1908: 249.

Apisthocalamus pratti - Boulenger, 1908: 249.

Apisthocalamus prattii - Barbour, 1912: 201.

Apistocalamus pratti - McDowell, 1967: 537.

Toxicocalamus (Apistocalamus) loriae - McDowell, 1969: 455.

Toxicocalamus loriae Clade 1 - Strickland et al., 2016: 671.

Holotype and collection.

MSNG 29141, an adult male from Haveri, British New Guinea (vicinity of 9.40°S, 147.60°E). The specimen was collected by the Italian anthropologist, ethnographer, explorer, and naturalist Lamberto Loria (1855-1913), who travelled in British New Guinea from 1889-1897 and sent a series of zoological specimens to the Museo Civico di Storia Naturale in Genoa, Italy. Based on Loria’s diary accounts of his travels (see Dimpflmeier 2014, 2019), the specimen was most likely collected during an excursion on 28 June 1893 to the southern versant of the Owen Stanley Range a point-to-point distance of 50 km east of Port Moresby. Thus, Boulenger’s (1898) estimate of 1889-1892 for the collection he described appears to have been at least a year short. The species was described in Series 2, Volume 18 of the Annali del Museo Civico di Storia Naturale di Genova, which is an 1897 volume that was published in March 1898 ( Poggi 2010).

Etymology.

Named by Boulenger (1898) for the collector of the holotype. The description was published in English.

Diagnosis.

A modestly sized member of the T. loriae Group (maximum SVL in males 490 mm, in females 440 mm) with the following unique combination of characters: two scales covering vent; three infralabials contacting anterior genial; posterior genials separated by two intergenials, one in front of the other; intergenials widest anteriorly. Elongate preocular, at least twice as long as wide, contacting nasal but not internasal; one (in 58% of specimens) or two (42%) postoculars; two (55%) or three (45%) posterior temporals; ventral scale count not sexually dimorphic, 162-197 ventrals in 15 males, 172-190 in four females; subcaudal scale count sexually dimorphic without overlap, 40-50 in males, 28-33 in females; SCR 17.1-21.5% in males, 12.5-16.1% in females; pale markings on prefrontals absent (67%), small or vaguely developed (28%), or present (5%), not obviously correlated with body size; tail spine white, paler than the rest of the tail; venter uniformly yellow, yellow with a mid-ventral row of brown spots on each ventral, with a few brown spots scattered down the venter, or with each spot expanded into a brown bar across the anterior of each ventral.

Comparisons with other species.

Toxicocalamus loriae is distinguished from all other members of the T. loriae Group in having the posterior genials separated by two intergenials that are aligned in the midline, one in front of the other, with each scale widest anteriorly. All other species are characterized by having the posterior genials separated by only a single intergenial that is widest posteriorly (typically) or centrally (occasionally). As noted above, in the other species there will rarely be two (or three in AMS R23069) intergenials, but the anterior one is either tiny or the two scales occur side-by-side at the posterior portion of the posterior genials; the rarity of these anomalous features suggests they are developmental oddities. Toxicocalamus loriae may be further distinguished from T. nigrescens by its smaller body size (maximum SVL in males 490 mm vs. 635 mm in T. nigrescens ), and yellow ventral colouration (grey in T. nigrescens ). It can be distinguished from T. mattisoni by preoculars that are in contact with the nasals (separated by prefrontal contact with second supralabial in T. mattisoni ) and its venter that is uniformly yellow or yellow with a mid-ventral row of brown spots or short bars (venter grey or yellow with each ventral scale barred anteriorly with darker grey in T. mattisoni ).

Redescription of the holotype.

An adult male, with tongue extending from right side of mouth; 490 mm SVL, tail tip missing but TL> 90 mm. Rostral, internasals, and anterior portions of nasals crossed by series of linear impressions, as if the snout had been pressed against a screen during preservation. Rostral wider than tall, notched ventromedially; internasals angulate, semi-triangular, wider than long. Prefrontals distinct from preoculars, approximately square but angled laterally and posteriorly, slightly longer than wide (Fig. 1A, A '), bordered below by preocular and nasal; preoculars elongate, narrower anteriorly, approximately twice as long as tall, bordered anteriorly by nasal, below by second and third supralabials (Fig. 2A, A ', B, B’). Nasal divided by large naris, with distinct groove above and below centre of naris on right side (region damaged on left side). Postoculars two, irregularly shaped, upper approximately four times larger than lower, combined they occupy approximately same area as eye. Frontal shield-shaped, not fused with supraoculars, its anterior margin may extend slightly forward medially from rest of scale; parietals approximately twice as long as wide. One elongate anterior temporal above fifth and sixth supralabials, separating latter from parietal; three posterior temporals, anteriormost smallest, followed posteriorly by a larger upper temporal and below it a smaller lower temporal, ventralmost temporal abutting posterodorsal margin of sixth supralabial. Supralabials six, third and fourth contacting eye; infralabials six, first three in contact with anterior genial. Mental small, shallow, triangular, wider than long, bordered posteriorly by first supralabials; anterior genials wider than posterior genials, in broad medial contact; posterior genials completely separated by two diamond-shaped intergenials, anterior of which is widest anteriorly, posterior of which is widest centrally; four gulars separate intergenials from first ventral in the midline; an elongate sublabial of a length equal to anterior genial separates posterior genial from fifth infralabial (Fig. 3A, A '). Eye relatively small; pupil round.

Dorsal scales smooth, not notched posteriorly, without apical pits, in 15-15-15 rows; ventrals 189, each approximately four times as wide as long, tail tip incomplete; two scales covering vent; subcaudals 44+, paired.

In preservative (122 years after collection), dorsum uniformly medium brown; venter yellow with a mid-ventral row of brown spots. Supralabials pale yellow ventrally, suffused with brown on upper portions of Supralabials 2-5 and on posterior portion of Supralabial 6; small amount of yellow colouration also present on the lower parts of the nasals. Chin and throat yellow, with small area of brown suffusion on posterior portions of infralabials, genials, intergenials, and gulars. Iris black.

Variation.

The anterior margin of the frontal may be almost straight but usually extends slightly forward of the rest of the scale in the midline of the head. The nasals usually have a distinct groove above and below the posterior margin of each naris; a sample from Mt. Obree has either very shallow grooves or lacks them entirely. One (58%) or two (42%) postoculars, both smaller than or occupying approximately the same area as an eye; two (55%) or three (45%) posterior temporals, positioned either as one larger scale above a smaller one, or with the smallest of three scales positioned anterior to the other two, followed posteriorly by a larger upper and a smaller lower temporal; in either configuration, the lowest temporal scale is abutting the posterodorsal margin of the sixth supralabial. Six (97.4%) or seven (2.6%) supralabials, the third and fourth (97.4%) or the third to fifth (2.6%) supralabials contacting eye; five (2.6%) or six (97.4%) infralabials, the first three (22%) or four (78%) in contact with the anterior genial. The anterior genials are wider than the posterior genials and approximately the same length or slightly longer; anterior genials in broad medial contact except in NMW 23783.1 and USNM 195619, where they are separated along most or all their length by an intergenial; posterior genials invariably separated by two diamond-shaped intergenials, whose anterior width is greatest.

Dorsal scales invariably in 15-15-15 rows. Ventrals not sexually dimorphic (t 14 = -0.2688, p = 0.3958), 162-197 (184 ± 10) in 15 males, 172-190 (179 ± 7) in four females; subcaudals sexually dimorphic without overlap, 40-50 in males, 28-33 in females; SCR sexually dimorphic without overlap, 17.1-21.5% (19.4 ± 1.4%) in males, 12.5-16.1% (14.6 ± 1.0%) in females. Tail tipped by a blunt to pointed conical spine. Maximum SVL 490 mm in males and 440 mm in females, adult TLR = 13.4-19.1% (16.6 ± 1.7%) and 10.8-17.5% (14.1 ± 3.3%), in males and females, respectively. The current dataset, with only two adult females, indicates that there is no statistically significant male-female difference in SVL (t = 0.3034, p = 0.3832). TLR in the two juvenile males (PNGM 23158, 24649b) is smaller (12.6% and 13.9%, respectively) than in adults, indicating that in this species, there may be an ontogenetic lengthening of the tail relative to SVL in males. In the four females, this trend appears to be reversed. Even though the sample size is very small, the two subadult females (BPBM 10966, 44892) display TLR values of 12.0% and 11.8%, respectively, with the adult individuals displaying slightly shorter tails relative to their SVLs.

In preservative, the dorsal colouration is uniformly medium brown (84%) or dark brown (11%) except that one specimen (BPBM 10967) is grey-brown mid-dorsally and laterally and has a dorsolateral stripe of medium brown extending the length of the body. The ventral colouration is uniformly pale yellow (37%), yellow with a mid-ventral row of brown spots (32%), yellow with some mid-ventral brown spots that are not present on each scale (11%), or yellow with a brown bar across the anterior portion of each ventral (16%) and with the brown colour more concentrated mid-ventrally into semi-circular spots; one specimen (NMW 27383.2) is uniformly pale brown ventrally, but this may be a discolouration artifact of an originally yellow venter inasmuch as the specimen was preserved in 1904-1906). Lower portions of the supralabials pale yellow, some or all suffused with brown on their upper portions. Yellow markings variably present on nasals, prefrontals, temporals, parietals, and in the nuchal area, virtually absent in the holotype and the sample from Mt. Obree; pale, invariably incomplete nuchal collar, usually limited to lateral markings but in some specimens with small, mid-dorsal yellow spots. Chin and throat pale yellow, usually with a small amount of brown suffusion on portions of the mental, the infralabials, and sometimes on the genials or the anterior intergenial. Conical tail spine with a white (95%) or brown or pale brown (5%) tip. Iris black. Juveniles (n = 4) have a brown head with a broken yellow nuchal band and yellow supralabials (Fig. 4A, B ). They may or may not have a small yellow spot on each prefrontal.

In life, field notes described BPBM 19502 as: "Dorsum dark slate-gray, changing to gray-brown laterally. No nuchal collar." BPBM 19503 was dark olive brown dorsally and slightly lighter dorsolaterally (Fig. 5A, B ), its venter and supralabials were bright lemon yellow, and its subcaudals were bright lemon yellow with grey margins (Fig. 5C ). The venter of BPBM 19502 was uniform yellow with a more orange cast than BPBM 19503 and featuring grey mid-ventral spots at the centre of ventrals in the posterior third of body; the subcaudals were lemon yellow, with dark grey margins (Fig. 5D ).

Range.

Known almost exclusively from the southern versant of the Owen Stanley Range of Papua New Guinea, from Tapini, Central Province, in the north to Mt. Dayman, Milne Bay Province, in the south, at elevations from 620-1530 m (Fig. 6B ). A single specimen (BPBM 44892) is known from Isurava, along the Kokoda Track, on the north side of the Owen Stanley Mountains in Oro Province.

Ecological notes.

Three individuals from Mt. Obree (elevation ca. 880 m) were obtained from local villagers, who presumably discovered the snakes while gardening. One specimen came from near a stream in primary rainforest (1570 m), and one more was found on the forest floor in primary rainforest on a ridge top (1680 m). At the time of collection, the understory on this ridge was not dense and contained a thick duff layer with a tight root network at the surface; the canopy was 25-30 m above the forest floor, with large emergent araucarians ( Araucaria sp., Araucariaceae ) reaching heights of 50 m. Farther downslope, near the stream, the forest had a much denser understory. These specimens were found active on the forest floor at 12:00 h and in mid-afternoon (~16:00 h), respectively.

Remarks.

We retain Apistocalamus pratti (BMNH 1946.1.17.53, Fig. 7 ) in the synonymy of Toxicocalamus loriae because the sole specimen shares with the holotype of the latter the two diagnostic features of having two intergenials separating the posterior genials and a yellow venter with a mid-ventral row of brown spots. It differs from the holotype of T. loriae in being smaller (330 vs. 490 mm SVL), having slightly fewer ventrals (186 vs. 189) and subcaudals (40 vs. 46), having a single postocular (vs. 2), and having a small, indistinctly defined yellow spot on each prefrontal. The last feature merely reflects variation seen in some of the smaller specimens of T. loriae. The other differences are trivial and not diagnostic.

Toxicocalamus loriae is unique among members of the T. loriae Group in having the posterior genials completely separated from contact with each other by two intervening intergenials aligned in the midline of the chin. This character state is among the more distinctive features that diagnose any of the T. loriae Group species. Furthermore, this feature occurs in only a small, contiguous portion of the entire geographical range occupied by the group. In our view, it provides compelling evidence for the unity of this species. However, we note that the sample size for this species is small (n = 19) and almost one-third of those specimens come from a single area (on the NW slope of Mt. Obree); all other localities are represented by only 1-3 specimens. Consequently, it is difficult to assess the importance of some of the morphological and geographic variation seen in this sample. We here consider four points in question that deserve further assessment once sufficiently large specimen series become available.

Ventral colour pattern.

This character is variable. Three specimens (AMNH R-59067, BMNH 1935.5.10.174, PNGM 23158) from Mafulu and from near Fane (9 km apart) show an expansion of brown pigment on each ventral that is not seen in any other specimens. In particular, the anterior edge of each ventral is adorned with a narrow bar of brown. Other specimens are either uniformly yellow ventrally (37%) or yellow with a row or scattering of brown dots mid-ventrally (42%); one specimen (NMW 27383.2) is uniformly pale brown ventrally, though we suspect this may be an artifact of preservation or storage. Of the three specimens from Mafulu and Fane, two still retain the central row of brown dots but the brown colouration extends laterally to these dots. Assuming these specimens are true T. loriae , this extends the range of colour-pattern variation seen in the species. We believe these are true T. loriae , both because they have the characteristic medial separation of the posterior genials by two intergenials as well as the fact that the medial brown dots are still evident in two of these three specimens. Furthermore, the sample of six specimens from Mt. Obree also makes clear that the degree of brown markings on the venter is variable within this species: one of these specimens has a yellow venter with a complete row of mid-ventral brown spots, two have yellow venters with some mid-ventral brown spotting, and three have uniformly yellow venters. Variation in degree of brown ventral spotting does not appear to be ontogenetic since the largest adults can be either uniformly yellow or have a complete series of brown spots.

Ventral counts.

Male ventral counts in our sample cover an unusually wide range (162-197) and might be thought to possibly reflect the presence of more than one species in our sample. However, these values seem to vary geographically, with two of the three highest counts (193, 194, 197) seen in the two northernmost samples (Fane, Mafulu) and the two lowest counts in the southernmost samples from Agaun, Milne Bay Province (162) and nearby Mt. Obree (169). Furthermore, the six males from Mt. Obree, Central Province, themselves show a range of variation (169-189) that encompasses 55% of the total variation seen in the entire sample of T. loriae , suggesting that considerable variation in male ventral counts does indeed characterize this species and may not in itself be evidence of multiple species. This interpretation could possibly change when larger sample sizes become available, but the overlap in counts seen in the Agaun and Mt. Obree samples, coupled with the broad variation seen in the latter, makes this seem unlikely.

Geography.

The large majority of specimens was collected on the southern versant of the central Owen Stanley Range. However, one specimen (BPBM 44892) came from the northern versant of these mountains in Oro Province. This is an unexpected locality for what appears to be a southern-versant species, for two reasons. Firstly, two other species of the T. loriae Group also occur in this general area of Oro Province (see below), and one of those is restricted to the northern versant. However, current evidence suggests that these species are segregated elevationally in this area, with the sole T. loriae specimen having been collected at an elevation of 1260 m, the second species occurring in hill forest from 100-940 m, and the third appearing to be a high-elevation form found at 1660-1850 m. Secondly, even if these species all segregate along elevational gradients, it remains uncertain how T. loriae would have crossed the formidable barrier presented by the Owen Stanley Range (elevation> 2000 m in this region). It could possibly have spread around these mountains from the south, through the low-elevation Musa Divide. If that is true, then additional surveys of this poorly explored region should reveal a more extensive presence of T. loriae at middle elevations of the Owen Stanley Range in Oro Province.

Provenance.

Two specimens (NMW 27383.1-2) are of ambiguous provenance. These were sent to Vienna by the anthropologist and explorer Rudolf Pöch (1870-1921), who worked in German New Guinea from 1904-06 ( Pöch 1907). The locality for these specimens ("Astrolabe Gebirge") can be interpreted as referring to the mountains visible from Astrolabe Bay (potentially either the Finisterre or Adelbert Mts.) in Madang Province, or to the Astrolabe Range south of the Owen Stanley Range in Central Province. The former interpretation is consistent with the fact that most of Pöch’s work was done in German New Guinea, including the area now contained within Madang Province. Against this is the fact that all Toxicocalamus in the T. loriae Group otherwise collected from this region are not T. loriae and do not match the NMW specimens. Contrarily, if the locality is interpreted to refer to the Astrolabe Range in Central Province, this would make geographical and morphological sense, because these specimens would then be from within 25 km of the type locality of T. loriae and are morphologically unremarkable T. loriae specimens. Pöch is known to have visited nearby Port Moresby for a few days before his departure from New Guinea, and it is possible that the specimens were on hand and given to him there by his hosts. In any event, these two specimens are morphologically and geographically consistent with their provenance being from the Astrolabe Range, Central Province. If they truly did come from somewhere in Madang Province, then they are morphologically unique for that region and would suggest that either T. loriae has a much wider range than currently evident (> 350 km from the nearest known locality for the species) or that a morphologically similar species occurs in the Madang region that has not been collected since Pöch’s time. Some specimens were indeed sent to Vienna from Port Moresby in the time frame under consideration, but there is no further information in the records of the Vienna Museum to determine what the shipment may have included. We tentatively adopt the position that these specimens came from Central Province, and we have included them in the diagnosis of T. loriae .

Figures

Figure 1. Dorsal views of heads of Toxicocalamus loriae Group snakes, presented as both photographic and line-drawing illustrations. A, A ' holotype of T. loriae (MSNG 29141), Haveri, Bartholomew Range, Central Province, PNG. B, B ' lectotype of T. nymani comb. nov. (UUMZ 290 / 2387), Sattelberg, Huon Peninsula, Morobe Province, PNG. C, C ' lectotype of T. loennbergii comb. nov. (BMNH 1946.1.18.24), Fakfak, Onin Peninsula, West Papua Province, Indonesia. D, D ' holotype of T. lamingtoni comb. nov. (AMS R 9351), Mount Lamington, Oro Province, PNG. Images not to scale. Scale abbreviations: anterior temporals (AT), frontal (F), internasals (IN), nasals (N), parietals (P), prefrontals (PF), postoculars (PO), preoculars (PR), posterior temporals (PT), rostral (R), supraoculars (SO).

Figure 2. Right and left lateral views of heads of Toxicocalamus loriae Group snakes, presented as both photographic and line-drawing illustrations. A, A ', B, B ' holotype of T. loriae (MSNG 29141). C, C ', D, D ' lectotype of T. nymani comb. nov. (UUMZ 290 / 2387). E, E ', F, F ' lectotype of T. loennbergii comb. nov. (BMNH 1946.1.18.24). and G, G ', H, H ' holotype of T. lamingtoni comb. nov. (AMS R 9351). Images not to scale. Scale abbreviations: anterior genial (AG), anterior temporal (AT), frontal (F), numbered infralabials (IN 1 - 6), internasal (IN), mental (M), nasal (N), parietal (P), posterior genial (PG), postocular (PO), preocular (PR), posterior temporals (PT), numbered supralabials (SL 1 - 6), supraocular (SO).

Figure 3. Ventral views of heads of Toxicocalamus loriae Group snakes, presented as both photographic and line-drawing illustrations. A, A ' holotype of T. loriae (MSNG 29141). B, B ' lectotype of T. nymani comb. nov. (UUMZ 290 / 2387). C, C ' lectotype of T. loennbergii comb. nov. (BMNH 1946.1.18.24). D, D ' holotype of T. lamingtoni comb. nov. (AMS R 9351). Images not to scale. Scale abbreviations: anterior genials (AG), intergenials (IG), numbered infralabials (IL 1 - 6), mental (M), posterior genials (PG), sublabials (Sb).

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 5. Portraits in life A, B and perimortem ventral views C, D of Toxicocalamus loriae BPBM 19503 A, B, C and BPBM 19502 D from NW side Mt. Obree, Central 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 7. Head of holotype of Apistocalamus pratti (BMNH 1946.1.17.53) from Dinawa, Central 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.