Toxicodryas pulverulenta ( Fischer, 1856 )

Greenbaum, Eli, Allen, Kaitlin E., Vaughan, Eugene R., Pauwels, Olivier S. G., Wallach, Van, Kusamba, Chifundera, Muninga, Wandege M., Aris- Tote, Mwenebatu M., Mali, Franck M. M., Badjedjea, Gabriel, Penner, Johannes, Rödel, Mark-Oliver, Rivera, Jacqueline, Sterkhova, Viktoria, Johnson, Grant, Tapondjou, Walter P. & Brown, Rafe M., 2021, Night stalkers from above: A monograph of Toxicodryas tree snakes (Squamata Colubridae) with descriptions of two new cryptic species from Central Africa, Zootaxa 4965 (1), pp. 1-44 : 24-27

Toxicodryas pulverulenta ( Fischer, 1856)

( Table 2, Figs. 8 , 11 )

Dipsas pulverulenta: Fischer (1856:11) ; type locality: “ Edina , Grand Bassa County in Liberia (West-Afrika).”

Dipsadomorphus Boueti: Chabanaud (1917a:373); type locality: none provided, but subsequently clarified to “ Porto-Novo ” “ Dahomey ” [Porto-Novo, Benin] by Chabanaud (1917b:12).

As noted by Ceríaco et al. (2018), the description of this species was based on two specimens (only one syntype remains today according to Hallermann 1998 and Uetz et al. 2019), one of which was depicted in plate 4 of livraison 38 by Jan & Sordelli (1871). In a footnote to the nomenclatural history of Boiga (Toxicodryas) pulverulenta, Hughes & Barry (1969:1020) wrote “Dr. Ladiges [then curator at ZMH] tells us that the type is still in Hamburg and is from St. Thomé, not Edina, Grand Bassa County, Liberia as stated by Loveridge (1958:269).” The latter citation is in error ( Loveridge 1957). Ceríaco et al. (2018) deduced that the information from Ladiges was based on an old label associated with the presumed remaining type specimen. Because extensive fieldwork on the island of São Tomé over the last century failed to document this species, Ceríaco et al. (2018) concluded that it does not occur there, and the original type locality from Fischer (1856) “Edina, Grand Bassa County in Liberia (West-Afrika)” is correct. Moreover, the former authors determined that the pholidosis from this presumed type ( Ceríaco et al. 2018:fig. 1) is not consistent with the extensively detailed original description, and thus, it is not a type specimen (contra Uetz et al. 2019). Although we agree with this conclusion, an examination of this specimen (ZMH R04376) by J. Hallermann (pers. comm.) found some differences in the morphometric data provided by Ceríaco et al. (2018) (e.g., SVL = 635 mm, not 880 mm), and we used these updated data in our analyses of morphological data ( Table 2).

Chabanaud (1917a:375), convinced that the odd configuration of subcaudals (combination of single and double subcaudals near the vent) seen in one male and one female was unique to Colubridae , named the taxon Dipsadomorphus boueti from these specimens that were donated by “Dr Bouet,” who collected for the Paris Museum in Ivory Coast (1909) and Dahomey (1910–1913). Unfortunately no specific type locality was provided. Chabanaud (1917b) then clarified and corrected himself by stating that both types were males (the mistaken female was a juvenile), and they were collected from “Porto-Novo” in Dahomey, which is modern-day Porto-Novo, the capital city of Benin. Chabanaud (1917c) subsequently realized that his specimens of D. boueti represented T. pulverulenta individuals with abnormal subcaudals, and he synonymized the former taxon with the latter (as D. pulverulentus ). We agree with this taxonomic placement, because the types of D. boueti have subcaudal counts (106 and 116) and TL/SVL ratios (0.25 and 0.28) that are most consistent with T. pulverulenta ( Table 2).

The Porto-Novo locality is on the eastern edge of the Dahomey Gap (sensu Demenou et al. 2016:fig. 1), a renowned biogeographic barrier to at least some forest-specialist species in West Africa. Because T. pulverulenta does not seem to be a strict forest specialist (see Habitat below), and the Porto-Novo locality occurs on the eastern edge of the Dahomey Gap, it is likely that the Gap is not a barrier to dispersal for this species. We therefore hypothesize that the Niger Delta is the biogeographic barrier separating T. pulverulenta from its cryptic sister taxon T. adamanteus sp. nov.

Diagnosis. A species of Toxicodryas restricted to West Africa, west of the Niger Delta, defined by the following combination of characters: maximum SVL <1 meter (vs. maximum SVL> 1 meter in T. blandingii and T. vexator sp. nov.), DSRN 19–21 (vs. 23–25 in T. blandingii and 23–29 in T. vexator sp. nov.), DSRM 19–21 (vs. 21–25 in T. blandingii and T. vexator sp. nov.); cloacal plate undivided (vs. usually divided in T. blandingii , and divided or undivided in T. vexator sp. nov.); both sexes brown to pink with darker cross-bars that often enclose a whitish spot, and the dorsum and venter sprinkled with fine dark brown or black spots (vs. adult males glossy or velvety black with a yellow venter, and adult females light brown, gray, or yellowish-brown with light-brown or cream cross-bars on the flanks, with yellowish-brown venters in T. blandingii and T. vexator sp. nov.); hemipenis relatively long with long spines mid-way along the shaft that decrease in size towards the apex and base, with a domed apex (vs. hemipenis relatively short and massive [i.e., broad], proximal third covered with spines, distal two-thirds dimpled with a flattened apex in T. blandingii and T. vexator sp. nov.).

Variation. Morphometric variation of Toxicodryas pulverulenta is shown in Table 2. Chabanaud (1917a) first noted that some individuals (including the type of Dipsadomorphus boueti ) can have a few single subcaudals posterior to the cloacal plate. Bogert (1940) provided morphometric data, but he did not distinguish between populations from Liberia ( T. pulverulenta ) and former French Cameroon ( T. adamanteus sp. nov.), except that “the Liberia specimens are distinctly more reddish brown than the Cameroon specimens.” However, he listed the maximum total length of a male (1112 mm) and female (1050 mm) T. pulverulenta from Liberia. In snakes from West Africa (without noting sex), including Cameroon where T. adamanteus sp. nov. occurs, Angel (1933:146) noted temporal formula variation of 2 + 2 (rarely 2 + 3 or 3 + 2 or 1 +2), 236–276 ventrals, 96–132 subcaudals, and a maximum size of 1225 mm; nearly identical data were reported by Villiers (1950a), Doucet (1963), Stucki-Stirn (1979), and Chippaux (2006). Although all of our examined specimens and most literature records noted the 3 rd to 5 th supralabial in contact with the eye (e.g., Villiers 1950b), Chippaux (2006) documented individuals with the 4 th to 6 th supralabial in contact with the eye, and sometimes, only two scales in contact with the eye, but some of these specimens might be attributable to T. adamanteus sp. nov. Segniagbeto et al. (2011) reported snakes from Togo with 165–175 ventrals, which is undoubtedly erroneous.

Fischer (1856:83) noted his type specimen had seven maxillary teeth that were oriented nearly backwards, becoming larger posteriorly. These were followed by two larger teeth (i.e., fangs) that were furrowed in a “besonderen Hauttasche” [special skin pocket]. There were 10–12 mandibular teeth, which were slightly curved towards the back of the mouth, and increased in size posteriorly. Bogert (1940:61) remarked “ five specimens examined show variation from eleven to thirteen anterior subequal teeth followed after a very short diastema by two larger grooved fangs and a smaller fang, the total number of teeth being fourteen to eighteen.” Because only two of his examined specimens originated from former French Cameroon (attributable to T. adamanteus sp. nov.), at least three of these specimens were from Liberia, which are attributable to T. pulverulenta . In snakes from Ghana, Leeson (1950) noted 11–13 maxillary teeth, becoming slightly larger posteriorly, followed by 2 fangs, and sometimes a 3 rd, smaller fang; 14–16 palatine and pterygoid teeth, and 15 mandibular teeth with the anteriormost ones largest. Johnsen (1962) reported that his specimen from Liberia had 11 maxillary teeth on one side, and six on the other. Based on a specimen from Liberia, Malnate (1972) noted the species lacks posterior hypapophyses.

In his original description of the species, Fischer (1856:83) described the coloration in great detail as chocolate brown above, yellow below, finely dotted everywhere. On each side, near the back, there was a large number (60– 70) of pale red spots that lacked dark edging and extended over 4–6 scales. Usually the spots on one side alternated with those on the other; sometimes they also were opposite to each other and in this case were connected to weak “Querbinden” [cross-ties] by bright red connecting strips that extended over the back. Usually there was a small black spot under each of these spots on the outermost tip of the corresponding ventral shields. The innumerable fine black points, with which the whole body was sown, were grouped on the abdominal shields on each side at the point where they bent over to rise sideways, to form a black spot, which in their succession looked like a black longitudinal band, whereby the narrow belly appeared delimited from the flanks. Head was brown and without black lines. Upper lip, lower lip, throat yellow, dotted with black. Günther (1858:173) described the dorsum of two Nigerian specimens as “brown with a strong cast of purple” with elliptical transverse streaks, and at mid-body, these streaks had a small yellow spot in their center. In his description of Dipsadomorphus boueti, Chabanaud (1917a) noted the types were light brownish gray and dotted with brown, whereas the supralabials and venter were yellowish gray.

Leeson (1950) described animals from Ghana as brownish red on the dorsum, with “dull brown” heads, and “lightly coloured” patches on the flanks that had a black edge on the lower margins. There were more narrow light gray bands on the anterior third of the body that gradually diminished to form light gray patches on the posterior two-thirds of the body. The ventral surface of the head was white or cream, whereas the venter of the body was pinkish with numerous brown spots. Brown lines “commence”[ed] just before the middle of the body on each side of the ventrals, and continued along the edge of the ventrals to the tip of the tail. In his description of two specimens from Ivory Coast, Villiers (1950b) noted their color pattern was pale brownish gray, the dorsal scales dotted with black, the back with alternate dark brown diamond spots (some ocellated with white). Yellowish ventral surface with two black lateral lines. Doucet (1963) noted the dorsal coloration ranged from uniform reddish or yellowish or powdery brown, sometimes with dark bars, with ventral coloration ranging from yellowish to pinkish. Chippaux (2006) noted dorsal coloration as dark beige or reddish with occasional dark gray designs or crossbars; venter pinkish with two dark lateral lines. Based on photographs of an adult male from Guinea ( Fig. 11B ), the base of the tongue is orangish red, and the forked tip is silvery white with black edging. Our observations of live specimens suggest the dorsal scales have an almost satiny sheen, similar to the appearance of a spider web (MOR, pers. obs.).

Hemipenis. Bogert (1940) did not note whether his hemipenis description was based on specimens from Liberia ( T. pulverulenta ) or former French Cameroon ( T. adamanteus sp. nov.). Doucet (1963:301) described the hemipenis of a snake from Ivory Coast as very different from that of B. [ Toxicodryas ] blandingi . Quite elongated, thorny at the base and dimpled at the apex, it is not bifid. The spines on either side of the sperm groove are very long in the middle part and decrease in size towards the apex and the base. The apex is domed, not flattened.

Diet. Villiers (1950a) noted both species of Toxicodryas in West Africa feed mainly on birds. Cansdale (1954) reported an individual from Ghana with two young mice in its stomach. Johnsen (1962:121) reported an adult male from Liberia with “a small insect-eating bird” in its stomach. In their paper on snakes of Ghana, Leston & Hughes (1968:754) noted the presence of undigested hair and a 10-cm long rodent tail in the stomachs of two specimens, and that “this suggests the attraction of Cocoa is for its Rodent fauna.” Another specimen contained the foot and tail of an Agama sp. lizard (sensu Leaché et al. 2017).

Böhme (2000) noted the diet of snakes from Guinea included small mammals (shrews and rodents), adult and nestling birds, and lizards with well-developed limbs. Greene (1989) suggested that there is an ontogenetic shift in diet from mostly lizards in young individuals to mostly birds and/or mammals as adults, and some individuals can ingest a third of their body weight if they eat more than one prey item in a nest or roost.

Behavior. In a paper on Guinean snakes, Böhme (2000) classified the species as relatively common and nocturnal.

Reproduction. An adult female found in Ghana in early September contained eggs “about 8 mm maximum breadth and between 30 and 35 mm long” attached to the left and right ovaries ( Leston & Hughes 1968).

Habitat. Menzies (1966) documented several specimens from forest in Sierra Leone, but one animal found at Rokupr seemed to occur in a habitat labeled as mangrove and coastal savanna. Leston & Hughes (1968:754) noted that this species was very common in cocoa tree pods in Ghana. Hughes & Barry (1969) listed the habitat as forest. Leston (1970:143) encountered several snakes in Ghana in trees (including one in a rotten cocoa pod), “amidst old files on an office shelf,” on a 1.5-meter high cocoa tree in a greenhouse, and in savanna. Hughes (1988) noted the species only from rainforest in Ghana. Rödel & Mahsberg (2000) found snakes in Ivory Coast from thick undergrowth in a swamp bordered by fields and secondary forest, and swampy primary forest. Branch & Rödel (2003) captured a juvenile in a funnel trap on the ground in closed-canopy forest in Ivory Coast. In Togo, Segniagbeto et al. (2011) noted the species is most common in forest, but some specimens were found outside of it, presumably in savanna.

Geographic distribution and habitat. Based on molecular data from Allen et al. (in press) and patterns of our morphometric data ( Table 2), we hypothesize that this species occurs west of the Niger Delta from Guinea to Nigeria.

Venom. Venom composition and effects are unknown ( Weinstein et al. 2011).

Figures

FIGURE 8. Diversity of Toxicodryas hemipenes. (A) Toxicodryas blandingii from Ivory Coast, in lateral and “front” views, redrawn from figure 29 of Doucet (1963); scale bar = 1 cm, (B) T. pulverulenta from Ivory Coast, redrawn from photograph of Plate IX, photo K of Doucet (1963), who listed the hemipenis length as 16 mm. Drawings by J. Rivera, (C) Photograph in life of male T. vexator sp. nov. (field no. CRT 3890) from Kona, Democratic Republic of the Congo (DRC), showing everted hemipenis in ventrolateral view. Photo: Z. Nagy, (D) Photograph of preserved male T. adamanteus sp. nov. holotype (UTEP 22204) from DRC, showing everted hemipenis in ventrolateral view. Photo: E. Vaughan.

FIGURE 11. Photos of Toxicodryas pulverulenta in life. (A) adult female (ZMB 86384) from Mt. Yonon, Guinea, (B) adult male (ZMB 86410) near Yomou, Guinea, (C) adult female (ZMB 86412) from Mt. Yonon, Guinea, (D) unsexed individual near Dudwiokahn, Liberia. Photos: J. Penner.