Psammodynastes pulverulentus occurs widely and is moderately abundant in the forests of Myanmar. The species shows morphological uniformity throughout its distribution from Kachin-Sagaing to Tanintharyi. Although there are no size differences among adult females (mean = 326, 253–436 mm SVL) and males (322, 222–471 mm SVL), a few morphological features are sexually dimorphic: adult females have shorter tails than adult males (TailL/TotL means ♀♀ 17%, ♂♂ 20%) and relative head width and eye diameter are slightly larger in males. The number of ventral and subcaudal scales are only slightly different between females and males (median ventral, ♀♀ 158.5, ♂♂ 159; subcaudals, 54, 59.5, although significantly different). Our smaller Thai sample displayed the same pattern of variation in measurements and scalation as the Burmese sample. We developed a coding scheme for coloration and qualitatively demonstrate dimorphism in the Burmese sample; females are darker ventrally than males but females and males are the same dorsally. Other coloration traits are also dimorphic. In our Burmese sample, the number of adult males (n = 21) outnumbered females (18). Adult females were most abundant in the 251–300 mm SVL size class, males of near equal abundance in 201–250, 251–300, and 301–350 mm size classes. Relative to other Burmese snakes, P. pulverulentus ranked eighth in abundance, nearly equal number in frequency of occurrence with Dendrelaphis pictus. Our reproductive data do not clearly define reproductive periodicity and, based on large vitellogenic follicles, a likely clutch/litter size of 4 to 7. Although only 30% of our sample contained identifiable prey (frogs, lizards), most (67%) had digestive boluses in the lower half of the intestinal tract. Skinks were the dominant lizard prey and Limnonectes the dominant anurans. Uniformity or at least low differentiation between our Burmese and Thai samples and the results of Rasmussen (1975) advocate for the continued acceptance of the pan-Asian species concept for Psammodynastes pulverulentus.
The Asian Common Mockviper is a moderately common snake in the forests of tropical Asia. It has a surprising broad distribution from peninsular India to Taiwan and southward through the Sundas to the Philippines (Fig. 1). It and its more-limited distribution cousin, P. pictus, are fascinating and enigmatic snakes, fascinating because of their unique dentition and venomous bite, and enigmatic because this dentition and other aspects of their morphology and even genetics have made them incredibly difficult to classify.
The Common Mockviper was described in 1827 (H. Boie, 1827:547) as Psammophis pulverulentus in the family Dendrelaphidae. Its familial placement has remained uncertain, and even a recent molecular study (Pyron et al. 2011) did not resolve its placement other than it was not closely related to any other colubroid snake species. Subsequently, Pyron and colleagues (2013) placed Psammodynastes in the Pseudaspidinae, Lamprophiidae.
Rasmussen (1975), in one of the most comprehensive reviews of an Asian snake species, examined the morphology of over 700 specimens from throughout the entire range of P. pulverulentus. He noted considerable variation in ventrals and maxillary teeth; however, he did not identify any concordant pattern of morphological variation among the multiple populations and traits sampled. The absence of concordance led him to the conclusion that the widely distributed populations represented a single species. Subsequently Zhao (1995) examined eastern China populations and interpreted the ventral and subcaudal variation in the Taiwanese population to denote subspecific differentiation (Psammodynastes pulverulentus papenfussi Zhao).
Our goal has been to re-examine the morphology (external) of the Burmese populations of P. pulverulentus, to test the morphological uniformity of Burmese populations, and to compare and contrast our results with those of Rasmussen (1975) who had a much smaller sample (n = 10) from Myanmar and widely dispersed therein. His distribution-wide study enables us to compare the variation observed in Myanmar with that of other Asian populations. Our broader in-country (Myanmar) geographic comparison is possible owing to the decade-long survey by the Myanmar Herpetology Survey (MHS) teams' fieldwork from late 1997 to early 2010 (see Acknowledgment section for details on the Survey). Additionally we took the opportunity to examine aspects of feeding and reproductive biology while examining the specimens' morphology.
Materials and Methods
Our emphasis focuses on Burmese specimens (n = 63), although we include a few specimens (n = 25) from adjacent Thailand for comparative purposes as a geographically near population. Specimens examined are identified in Appendix 1. Statistical test were performed in SYSTAT version 12.
Our characters consist of mensural ones, scalation, and coloration. Detailed definitions of the characters and their various states are presented in Appendix 2. For measurements, we used Vernier calipers and measured to 0.1 mm accuracy. We performed a repeat-measurement test (Hayek & Heyer 2001) to determine the consistency or accuracy of our measurements. Measurements were taken on the right side for all bilateral characters. We recorded nine mensural characters: snout-vent length (SVL), tail length (TailL), head length (HeadL), head width (HeadW), snout to eye distance (SnEye), snout to naris distance (SnNar), orbital diameter (OrbD), interorbital distance (Interorb), and internarial distance (SnW).
Our scalation (meristic) character set included 13 traits (all counts): supralabials (Suplab), infralabials (Inflab), loreals (Loreal), preoculars (Preoc), postoculars (Postoc), anterior temporals (TempAnt), posterior temporals (TempPost), anterior dorsal scale rows (DorsAnt), midbody dorsal rows (DorsMidb), posterior dorsal rows (DorsPost), ventrals (Vntl), subcaudals (Subcaud), and entire or divided precloacal scale (Precl).
Coloration (color and pattern) is typically presented textually and totally lacking enumeration. Textual presentation, aside from being subjective, does not allow a statistical evaluation of similarities and differences. To quantify coloration, we created a set of characters, each with two or more states. Binary states were assigned 0 and 1, multistates 0, 1, 2 and so forth. We identified 10 coloration characters, which we determined by a trial run that we could record consistently in preserved specimens. Further, we recognized that we could score the characters and their states more accurately by a joint examination of each specimen. The ten characters are: Dorsal trunk markings, DorsTrnk; General dorsal color, GenColor; Head, middorsal color pattern, HedDors; Nape stripe, NapeStrp; Postorbital stripe, Postorb; Supralabial color, SuplabC; Temporal color, TempC; Ventral chin stripe, VntChinSt; Ventral color, chin and throat, VntChinTh; Ventral color, background, VntTrnk. Characters and character state definitions are in Appendix 2. These characters were scored in all individuals whose current condition permitted us to score all ten characters. Subsequently, we compared differentiation between the sexes separately in the adult and juveniles samples by π2 tests.
Determination of a specimen's gender and reproductive state (maturity) was determined by dissection. GRZ is of the opinion that accurate sex determination in amphibians and reptiles is possible only with the examination of the gonads. Similarity maturity can be assessed only with such examination (He performed this task for all specimens examined herein.). Even with viewing the condition of the gonads, determination of maturity remains difficult in many individuals. Visible embryos, large yolking (vitellogenic) follicles, oviducal eggs or enlarged/stretched oviducts unquestionable identify mature females. Similarly enlarged testes with enlarged seminiferous tubules and enlarged and strongly pleated ductus deferens identifies a mature male. These criteria were not available for many of our specimens, hence evaluation of maturity becomes arbitrary. These criteria and the difficulties, as well as the discoveries, are described in the results section on reproductive behavior.
Our examination of the reproductive tract indicated that some specimens contained prey and boluses (Fig. 2) of digested meals and offered an opportunity to expand the known diet of these species. We used x-ray examination to identify the presence of prey in the stomachs and upper portion of the intestine of specimens. If a specimen held prey with visible skeletal structure, the prey item was removed, noting its orientation, and identified.
Distribution and abundance
Our sample included individuals from all Burmese political units except Bago, Mon, Shan, Kayah, Kayin, and Mon. The mockviper's absence from these area, we believe, reflects the absence of our team's field work in Kayah and Kayin, and their limited activity in the other four areas. Although the team surveyed a number of forested sites in Bago, the relative time spent in this Division and the randomness of snake sightings/captures argue against its absence there. Additionally, we regularly found P. pulverulentus in the Hlawga Wildlife Park (Yangon Division). This forested area represents the southern terminus of the Bago Yoma and is now isolated from the main mountain range by about 100 km of agricultural lands. Our map of specimens examined (Fig. 3) shows this species' broad distribution in Myanmar and also highlights the presence of its forest habitat. All MHS specimens were captured in forest, secondary and primary.
The MHS surveys were not conducted to obtain data on abundance; however, the frequency of vouchering different snake species offers an estimate of relative abundance. Using the number of individuals from a variety of snake species, which the MHS captured and now cataloged in the CAS and USNM herpetological collection, provides a measure of snake abundance (Fig. 4). The most abundant snake seen and captured by the MHS teams was the Checkered Keelback, Xenochrophis piscator. Its relative abundance is nearly double that of next most abundant snakes (Ahaetulla nasuta, Amphiesma stolatum, and Trimeresurus albolabris). The third abundance ranking includes Ahaetulla prasina, Lycodon aulicus, and Rhabdophis subminiatus. P. pulverulentus and Dendrelaphis pictus are in the fourth rank, about 30% as frequently captured as X. piscator.
The MHS survey sample can provide an estimate of seasonal activity. Using adults only, the Survey found 3 individuals in January, none in February, 2 March, 2 April, 5 May, 2 June, 6 July, 7 August, 4 September, 13 October, 6 November, and 3 in December. Interpretation of these data are complicated by the absence of actual time spent in forested habitats in the different months and the combination of survey samples from different localities. Nevertheless, a general pattern emerges suggesting lower abundance/activity during the Burmese cool and dry seasons (December to April) with increasing abundance through the monsoon (May–June to September–October).
Sex, maturity, and reproduction
Sex determination in Psammodynastes pulverulentus of all sizes is easy; determination of sexual maturity is not. A ventral incision at the 28th to 32th ventrals anterior to the vent reveals sexual ducts and often the left testis of males. The posterior end of the left ovary lies further forward, in the vicinity of the 38th to 40th ventrals. The testes of mature males are long (>15 mm, left side), broad, and with a ribbed appearance created by enlarged seminiferous tubules; the ductus deferens is also large and strongly convoluted. In specimens with smaller testes and modestly convoluted ductus deferens, the testes appear granular, and the seminiferous tubules are not evident, and these males are considered immature. Females with oviducal eggs or developing fetuses are obviously mature. Females with enlarged stretched oviducts are considered to have previously been pregnant even if the ovaries now contain small, early vitellogenic follicles. If vitellogenic follicles are 10 mm long and the oviduct beginning to enlarge and fold, the female is considered a maturing subadult and labeled as mature for estimating the size (SVL) of mature females. Females with less developed follicles and strap-like or small oviducts are immature.
Based on the preceding criteria, the smallest mature (adult) female is 253 mm SVL, smallest mature male 222 mm SVL (Table 2). There are immature individuals exceeding these “minimum” sizes. The large immature females (n = 8) range from 249 to 333 mm SVL, large immature males (n =10) from 212 mm to 306 mm SVL. Even owing to the difficulties of determining maturity, we are confident of these specimens' immaturity. We are, however, less confident on the accuracy of our lower size limit for mature females and males. Our Thai sample has similar minimums for adult females (282 mm SVL) and males (217 mm SVL), although the Thai sample (Table 2) lacks the larger sized individual seen in the Burmese sample.
Vitellogenesis begins early (i.e., at a small size) in P. pulverulentus. Vitellogenic follicles occur in females of 253 mm SV and larger. Usually these females have two or three larger (≥3 mm), equivalent sized follicles in each ovary and a few smaller one that are not yolking as yet, i.e., shiny white in color compared to darker yellow of the vitellogenic ones. We found only two Burmese female (one each in July and October) with large (≥8 mm) preovulatory follicles, one (December) with oviducal eggs (∼6 mm), and none with fetuses; the only female carrying a fetus was a Thai specimen without collecting data. Burmese males with enlarged epididymides had testes lengths of 12 to 20 mm SVL. Assuming these males were in reproductive readiness, they suggest an extended reproductive season: January, May, July, August, September, October, and December.
The Burmese sample contained 19 snakes with identifiable prey in the upper digestive tract (Table 1). Most snakes with prey contain a single identifiable prey item, but two snakes each contained two prey, recently capture owing to the limited digestion of the anterior most prey and beginning digestion of the posterior-most one. The most common prey item were skinks (n = 9; 50% of total prey), specifically Sphenomorphus, Eutrophis, and Lygosoma. The Sphenomorphus (6) are unidentifiable to the specific level; however, one of two Eutrophis is E. multifasciatus. A Lygosoma (CAS 240982) was the prey of a Kachin mockviper; it appears to represent either a new country record of L. haroldyoungi or most likely a new species as it appears morphologically distinct from all lygosomines known from Myanmar and elsewhere in Southeast Asia (Miller & Zug 2016). One agamid, a juvenile Calotes “versicolor,” and two geckos, Hemidactylus, were also identifiable prey. One of the latter was H. tenkatei and nearly undigested as it was the second or last prey. No snakes were discovered, although mockvipers are known to occasionally consume non-venomous colubrid snakes (Greene 1989). Six frogs were extracted from our Psammodynastes, three unidentifiable to genus level due to digestive disintegration The other three frogs were dicroglossids (Limnonectes or Fejervara) and again unidentifiable to species owing to digestion leaving only the hindlimb skeleton and skin only on the ankles and feet.
Even though the sample is small, there is a suggestion that females may eat more lizards than frogs (2 frogs: 9 lizards) in comparison to males (4:3, frogs:lizards). Prey selection by snake's body size is not suggested by the frequency of frogs and lizards in different snake body size classes: frogs:lizards in snakes <300 mm SVL 4:7, 301–400 mm 2:4, and >401 mm 0:2. Lizards are more numerous in all size classes. While our data are suggestive of sexual dimorphism in diet, we suspect that data simply reflects the randomness of snake-prey encounters.
Predator success is high for the mockviper. About a third (30%) of our Burmese samples had partially digested prey in the upper portion of digestive tract, and two-thirds (67%) of the sample contained digestive bolus in the posterior part of the intestine. A cursory examination of a few of the boluses revealed scale fragment and other miscellanea, proving that they represent at least one feeding bout.
Another aspect revealed by prey examination was the apparent rapidity and focus of digestion. Most prey were swallowed head first (Table 1), and as they move through the gut, the anterior end of the prey dissolves completely with a striking delineation between a narrow digestion zone on the prey and an unaltered posterior portion of the prey (see Miller & Zug 2016: fig. 2). There also is a striking difference in the rate of digestion of lizards and frogs, that is frog remains were largely confined to the hindlimbs, usually mid-thigh and distally.
The mockviper is regularly reported as an aggressive snake and actively striking when disturbed. This aggressive behavior contradicts GRZ's experience with this snake in Myanmar and David McLeod (pers. comm.) in Thailand where it is an alert and relatively docile snake. The explanation for this difference in temperament is well stated by Kuntz (1963):
“It is easily excited, moderately aggressive in captivity, does not hesitate to strike and will attempt to bite.”
The important difference in observations appears to be captivity.
To test the accuracy of our data-gathering for measurements, we independently measured a single specimen multiple times (USNM 587230, n = 10, AHM; USNM 587233, n = 10, GRZ). Each of us recorded all ten measurements. Our accuracy can be gauged by the range of the coefficients of variation (V). AHM, who subsequently measured all P. pulverulentus specimens, had a range of 0.3 to 16.5% V for the ten measurements, and GRZ's range was 0.5–6.5%. Strikingly the least variable measurement for both of us was SVL; OrbD and SnW were the most variable for AHM and SnEye and SnW for GRZ. The coefficient ranges indicate a reliable and consistency of data collection.
Another feature that required testing prior to an evaluation of the variation within the individual measurement traits (Table 2) is the presence or absence of sexual dimorphism. We used Student's t tests to compare the means of adult females and males. The Thai adult specimens (♀ n = 5. ♂ n = 8) are statistically different (p ≤ 0.05) for two traits, SVL (p = 0.023; ♀ = 325.7 mm, ♂ = 271.8 mm) and HeadL (p = 0.036; ♀ = 16.4 mm, ♂ = 15.3 mm). In the adult Burmese sample (♀ n = 26. ♂ n = 31), only TailL is statistically significant between females (TailL mean = 68.4 mm) and males (80.8 mm).
We also generated a set of proportions (TailL/SVL, TailL/TotL, HeadL/SVL, HeadW/HeadL, SnEye/HeadL, NarEye/HeadL, EyeD/HeadL, Interorb/HeadL, SnW/HeadL) and tested them for sexual dimorphism. The same pattern of sexual dimorphism was displayed in both the Burmese and Thai sample with TailL/SVL, TailL/TotL, and Interorb/HeadL significantly different (p ≤ 0.05) between the sexes. Males have proportionately longer tails (Burmese ♀♀ vs. ♂♂ means TailL/TotL 17.3 & 19.9%, TailL/SVL 21 & 25%, Student's t p <0.001; Thai ♀♀ vs. ♂♂ TailL/TotL 18.2 & 20.3%, 22 & 25%, p = 0.01) and broader heads (35 & 37%, p = 0.01; 33 & 36%, p = 0.09) than females. The means for the other proportions are similar among Burmese (n = 40) and Thai (n = 13) adults: HeadL/SVL 5.3%, 4.9%; HeadW/HeadL 46, 46%; SnW/HeadL 23, 26%; NarEye/HeadL 18, 20%; SnW/HeadL 15.1,17.7%; OrbD/HeadL 18, 19%.
Burmese adult males average smaller (322.0 mm) than females (325.7 mm) in SVL but not greatly (p = 0.85). Females range from 253–436 mm SVL, males 222–471 mm SVL (Table 2). As noted above, Thai adult males are significantly smaller (p = 0.02) than adult females (Table 2). The large difference of nearly 50 mm in mean length likely results from the small sample sizes of both males and females. In spite of the difference in sample sizes, the pattern of dimorphism between the Burmese and Thai samples display is similar although not identical (Table 2). The Burmese sample displays sexual dimorphism in TailL (68.3 & 80.8 mm, Student's t p ≤ 0.05), and three proportions, TailL/TotL, TailL/SVL and Interorb/HeadL (see preceding paragraph for values). The Thai sample is dimorphic in two measurements (SVL, Tail) and two proportion (TailL/SVL, TailL/TotL). Comparison of the two samples (Table 2) shows females to be larger in SVL, HeadL, HeadW, and with shorter tails in both Burmese and Thai samples. The females larger than males occurs also for NarEye and OrbD in Thai specimens and the converse for those and other measurement in the Burmese samples. The non-dimorphic proportions have similar values (Table 2) for Myanmar and Thailand. Overall, the measurements and proportions are similar for the two regional samples. Where the two differ, it is likely the difference in sample size and the presence of larger individuals in the Burmese sample. Larger sample size typically yields a larger range of values and a larger standard deviation.
Scalation (Table 3) with the exception of ventrals and subcaudals shows low variation. Ventral counts are not sexual dimorphic. The difference in the number of subcaudals in the Burmese sample is significant (p = 0.040) but not in the Thai sample. Further there is only slight differences in the median values and ranges of all scalation features (Table 3) between individuals from Myanmar and Thailand.
To examine regional differentiation, we partitioned our Burmese sample into four, non-overlapping regional samples (Kachin-Sagaing n = 13, Rakhine 15, Ayeyarwady-Yangon 10, and Tanintharyi 12) and performed Student's t test on the total character set for every paired combination of these samples. An examination of the data in a tabular format suggested no difference in any of the character metrics within any regional pair; however, comparison of the mensural and scalation characters by the t test indicated otherwise. Significant differences (p ≤ 0.05) were evident in Ventral for the K-S to R pair; Interorb, Subcaud for K-S to A-Y pair; none for K-S to T pair; Postorb for the R to A-Y pair; TailL, HeadL, HeadW, NarEye, Tempor1, Ventral for R to T pair; and TailL, HeadL, NarEye, Interorb, Ventral, Subcaud for A-Y to T pair.
Our ten coloration characters focus on patterns or coloration of a specific area of the body. This narrow focus is intentional for a tabulation of variation and to permit analysis of possible differences between sexes, adults and juveniles, and geographic regions. Owing to the discovery of significant sexual dimorphism in five coloration traits in adults and four in juveniles, the sample sizes for the latter two comparisons (maturity and geography) are inadequate for statistical testing.
General coloration (GenColor) addresses the overall impression of a snake's color from light to dark. GenColor is not sexually dimorphic in adults, although it is in juveniles. The majority (51%) of the adults are medium brown, similarly for juveniles (47% medium brown) Ventral trunk color (VntTrnk) also reports the total ventral color of a snake. Unlike dorsal color (GenColor), females and males (both adults and juveniles) differ (Table 4) with females usually two-toned, lighter anteriorly than posteriorly, whereas males are as likely to be uniformly light as two-toned ventrally.
We identified two features of ventral coloration in the head and neck area: color of chin and throat (VntChinTh) and presence or absence of chin stripe (VntChinSt). Both characters are sexually dimorphic in adults but only VntChinTh in juveniles. Juveniles are not dimorphic with most (85-90%) with a partial or complete chin stripe. Females have darker throats than males (Table 4) in both juveniles and adult males. In adults, females usually (82%) have a partial or complete light chin stripe and males (76%) a uniformly light chin with no stripe.
We recognized five features on the upper surface of the head that we could unambiguously characterize: middorsal color pattern (HedDors); nape stripe (NapeStrp); postorbital stripe (Postorb); supralabial color (SuplabC); and temporal color (TempC). Two of these (SuplabC, Postorb) are sexually dimorphic in adults (Table 4) and one (SuplabC) in immatures. Interestingly, both of the dimorphic features involve the side of the head with males having lighter faces than females, that is, females have darker lips (SublabC) (94%) and poorly defined postorbital stripes (Postorb) (61%) in contrast to males' lighter lips and sharply defined postorbital stripes; note however, that the temporal area (TempC) is usually light in both sexes.
Occurrence and abundance
The notes associated with our MHS data indicate that the recently captured mockvipers were all found in forested situation, either secondary or primary. Further, most individuals were discovered on the ground. One individual, however, was captured on a bush about 1.3 above the ground. These observations agree with most published habitat notes, although some populations appear to have a higher “tolerance” for more human-disturbed and/or open habitats (e.g., Dieckmann et al. 2013 and Kuntz 1963 – Taiwan).
Our data for the annual activity is weak although indicative of lower abundance/activity during the Burmese cool and dry seasons (December to April) with increasing abundance (i.e., frequency of observance/capture) through the monsoon (May–June to September–October). That general conclusion is commonly reported in the general literature on this species and frequently with less evidence than we present. The strongest evidence for increased activity during the monsoon and shortly thereafter is presented by Rahman and colleagues (2013) from the Lawachara National Park, Bangladesh (24.3414N 91.7977E). They observed frequency of DOR (dead-on-road) snakes through a full monsoon-dry cycle (14 continuous months). No individuals were seen during the cool dry period of December through February, an occasional individual in March through May, then increasing numbers June to November, peaking in September (n = 57). Their data also suggest that P. pulverulentus was the most abundant snake species at Lawachara, with Dendrelaphis pictus (n = 38), Xenochrophis piscator (36), Rhabdophis himalayanus (34), and Trimeresurus albolabris (25) next in relative abundance. This narrower geographic and habitat focus show a relative abundance similar pattern as our abundance estimate (Fig. 4). Saint Girons & Pfeffer (1971) evaluated the abundance of Cambodian snakes (n = 576 individuals of 37 species) captured in three surveys in 1968 and 1969. They divided their species among five behavioral-habitat categories. Semiaquatic snake were the most abundant snakes (40% of total snake sample and 14% of the species). Terrestrial snakes were the third most abundant group (27% of species) with a total of ten species; P. pulverulentus and Ptyas korros occurred in equal numbers and were the two most abundant species, placing the mockviper in approximately the same abundance category as in our Myanmar sample.
Sex, maturity and reproduction
Unfortunately, our reproductive data provides minimal information on reproductive seasonality, none on fetal development time and similar details on reproduction in P. pulverulentus. For the Burmese population, our data indicate that maturity most frequently occurs between 250–300 mm SVL in both female and males. That size range for maturity is also the likely one for the Thai sample. With a single Burmese female with oviducal eggs (December), two females with large vitellogenic follicles (July, October), and none with fetuses, we are unable to predict accurately birth and mating dates; however, the extended period (January, May, July, August, September, October, and December) of males with large testes and epididymides suggest non-seasonal reproduction. This conflict between male and female data results more from our limited data set and will remain uncertain until a year-long reproductive study is performed. Further in spite of this species widespread occurrence and moderate abundance, reproductive data is sparse and fragmentary. Pope (1935) provided an early summary of reproductive data. He noted that Wall had reported a neonate from Yangon in June and the discovery of a gravid female from northern Myanmar in October. Unfortunately, these data do not resolve a reproductive cycle for Burmese populations. Similarly our data on number of enlarged vitellogenic follicles (4–7) is not a reliable estimate of actual litter size at birth. Smith (1943) reported 3–10 neonates in July to September. That litter size is widely reported in the general literature although Smith's source(s) was not reported. The number ten likely derived from Pope's (1935: 326) report of “10 well-developed eggs” in a Yenping specimen (USNM 65394). We have re-examined that specimen (403 mm SVL, tail 85 mm), and it contains only seven large (11 to 13.6 mm long) vitellogenic follicles in the ovary; the oviducts are large and lightly folded. In Taiwan, four short-term captive females captured in April and May gave birth to six, seven and ten (2) neonates (Dieckmann et al. 2013) in June. Presumably another female laid four shelled, infertile eggs; authors were unclear whether these eggs were part of a litter count in their four birthing females. Dieckmann et al. (2013) provided mass but no length measurements for the females or their offspring. Whitaker & Captain (2004) give 150–180 mm total length for Indian P. pulverulentus neonates and litter size as 3–10 neonates (presumably from Smith, 1943) and births in July to September. We suspect a median clutch size of six young for Burmese females; even though, the number of observed enlarged vitellogenic follicles (4–7 in our sample) is likely an unreliable indicator of the final clutch size.
The most reliable data on reproduction in P. pulverulentus derives from Saint Girons (1972), who performed histology on its gonads in his Cambodian sample. Males were in peak spermatogenesis in August to November. The females had sperm in their reproductive tract in January and two to 10 greatly enlarge follicles in January. Other were reproductively quiet in June, August, and November. Contrasting these data with Dieckmann's Taiwan birthdates indicate variable reproductive seasonality across the wide distribution of the mockviper. Auffenberg (1980) suggested a seasonal cycle in the Komodo population with birthing in December and January at the beginning of the wet season. He also proposed 3–8 offspring based on enlarged follicles.
The diet of P. pulverulentus is strongly associated with its dentitional morphology. The mockviper has distinct enlarged anterior maxillary teeth that enable this species to specialize on skinks (Greene 1989). Venom subdues the prey for subsequent constriction and positioning the prey for swallowing. The mockviper is likely in a slow, evolutionary race with skinks. Anatomical evidence (Jackson & Fritts 1996) suggests that the large anterior teeth penetrate the armored (osteoderms) skin and allow the racheting jaw movement to position the posterior fangs for penetration and venom delivery. Earlier studies have shown that P. pulverulentus is a predominantly skink predator eating a variety of genera and species, particularly terrestrial/semifossorial species. Greene (1989) demonstrated that skinks represented 58% of his sample of 113 mock vipers. His data match our results; he similarly noted that frogs are also a major component of mockviper diets. Other genera within Lamprophiidae subfamily Pseudaspidinae have similar maxillary dentition and a specialized diet of skinks. For example, Pythonodipsas carinata, a little known Southwest African pseudaspidine, has a diet principally composed of geckos and skinks (Branch et al. 2010). Our Burmese sample included no snakes although mockvipers occasionally consume non-venomous colubrid snakes (Greene 1989).
In addition to the dentition morphology adapted for holding hard and smooth scaled skink, the venom rapidly subdues prey. Shaw (in Smith 1943) reported an Amphiesma stolatum dying in 16 minutes after being bitten by a mockviper.
Rasmussen (1975) limited his morphological analysis to scalation and maxillary teeth thereby limiting the comparison of our body measurements (Fig. 5) to his larger and broader geographic sample. Surprisingly at least to us, is the limited amount of size data in the herpetological literature and commonly when presented, the data derive from another source (often a secondary one) and is a maximum total length. We have searched the literature and offer a brief summary of measurements that derive from measured specimens. Most data were presented as total lengths [TotL]; where possible, we converted to SVL: Nepal ♀ 770 mm, ♂ 650 mm TotL (Gruber 2002); Myanmar ♀ 326 mm 253–436 mm SVL, ♂ 322 mm 222–471 mm SVL (mean and range, our Table 2); Thailand ♀ 319 mm 282–350 mm, ♂ 272 mm 217–312 mm SVL (mean and range, our Table 2); Cambodia ♀ 305 mm 278–340 mm, ♂ 230–250 mm SVL (Saint Girons 1972); Vietnam ♀ & ♂ 410–542 mm TotL (Ziegler 2002); China (three largest) ♀ 382–421 mm & ♂ 349–381 mm SVL; Taiwan ♀ & ♂ 444–635 mm TotL (Kuntz 1963); Philippines ♀ 342–590 mm, ♂ 355–385 mm TotL (Taylor 1922). There is a general uniformity of size across the broad geographic distribution with most adults being 280–450 mm SVL (∼340–540 mm TotL).
The maximum size (TotL) is reported as 770 mm (Whitaker & Captain 2004) and 635 mm (Kuntz 1963). No matter which length is correct, these lengths are exceptional and do not represent the body sizes of most individuals in any population (see for example the body lengths listed above and Table 2 and Fig. 5).
Our Burmese sample shows no statistically significant sexual dimorphism (Table 2) in any adult measurement even though the tail of males averages 11 mm longer than females. In contrast, the proportion TailL/SVL is significant shorter in females than in males. The Thai sample is dimorphic in tail length in both measurement and proportion (Table 2). Saint Girons (1972) similarly reported dimorphism in his Cambodian sample with tails 16–17% of TotL for females and 19–20% for males; note that these percentages are less than ours because we compare tail to SVL not total length.
Head measurements show a single dimorphism in the Burmese sample; relative head width (Intorb/HeadL) is broader in females than in males. The Thai sample displays no dimorphism and otherwise match the measurements of the Burmese sample (Table 2).
Rasmussen (1975) summarized variation in head scalation with emphasis on loreals and preoculars. The variation observed in our Burmese and Thai samples (Table 3) presumably would be encompassed in his larger sample, yet we found more variation than he reported. For example, he noted no variation in the number of supralabials (8) and infralabials (7); our modal and median values match his counts, although we observed a range of six to nine supralabials and the same for infralabials in Burmese individuals. Pope (1935) also observed variation in supralabials. For the number of loreals, Rasmussen reported none to four with one to two loreals as the most frequent number. One to two loreals occurred in Burmese specimens with one being the most frequent condition in the Burmese and Thai samples. Postocular, primary and secondary temporal scale counts of our samples (Table 3) match the Rasmussen data.
Dorsal scale row counts were the most consistent meristic character, 17 scales anteriorly and middorsally, and 17, rarely 15 posteriorly. Rasmussen (1975) and other authors (e.g., Smith 1945) report 15 as invariant for the posterior dorsal scale count. In contrast, we found 17 as the most frequent (96% Myanmar, 100% Thai samples) with 15 as a rare variant (4%) for posterior scale rows. This difference may reflect that our counts were taken commonly more anterior than the standard one head length from the vent.
The number of ventral and subcaudal scales is commonly dimorphic in snakes, i.e., females with more ventrals and fewer subcaudals and the converse in males. That trend is evident in P. pulverulentus, although the difference between adult females and males is not statistically significant because of the broad ranges of ventrals and subcaudals in both sexes. For ventrals, Burmese females have medians of 158.5 (131–180), males 159 (127–180), very similar in both median and ranges. The situation in our Thai sample is similar (Table 3), although there is a broader difference between the median of females 159.5 (149–172) and males 149 (141–162). Rasmussen (1975) observed a clinal variation in Myanmar with ventral number increasing from south to north. As noted in our regional comparison of Burmese samples, we found no significant difference between north and south Myanmar. We attribute his results to small sample size (Fig. 5).
Rasmussen summarized his data on ventrals and subcaudals in four figures (1975: figs. 5–8). He was unable to discern any geographic pattern in the variation observed. We thought that this lack of resolution might be the result of his inclusion of numerous small samples in his graphs. Selecting his localities with female and male samples of ≥10 individuals each (Table 5) does not resolve the complexity of the variation or yield any clear pattern of regional variation. His results conform with his large sample that Taiwan mockvipers have the highest means in both ventrals and subcaudals of any population; however, the ranges of Taiwan snakes overlaps strongly with his samples from Mindanao, NE Sumatra, and total Thailand (Table 5). Although the means for our Burmese sample are lower than those of Taiwan, the ranges of the Burmese females and males encompass the ranges of both sexes from Taiwan.
The lack of a geographic pattern also exists for the subcaudal scales (Table 5). Taiwan again has the highest means for females and males, and again the ranges of the Taiwan females and males strongly overlaps the other localities (Table 5). Our Burmese sample again encompasses the ranges of the Rasmussen's large Taiwan sample. This sample is larger than our Burmese sample and, in our opinion, accurately reflects the total variation expected for a regional sample.
We agree with Rasmussen's assessment that there is no discernable geographic pattern. We suspect variation observed results from local selection/adaptation to microhabitat conditions including different predators and differential prey.
We found the precloacal to be entire in all but seven specimens. All other researchers have reported the precloacal (anal) scale to be entire in all specimens. This condition is likely also for Burmese mockvipers; however, some specimens had this scales cut during preparation, and we decided to record the precloacal as divided when the cut was difficult to discern between natural division and dissection.
Numerous authors mentioned a variable color pattern for the population of P. pulverulentus which they have studied. Rasmussen (1975) summarized some of the earlier observations and noted a consensus that females were generally darker than males. He also noted a different dorsal pattern in the Sundas and Philippine, especially prominent in males, where the dorsal spots are joined in a zig-zag pattern. Leviton (1983) also noted that females tend to be darker than males and further that different patterns occurred on different islands of the Philippines. Auffenberg (1980) reported females darker than males in Komodo and his illustration of snakes' venters highlighted a strikingly different coloration between males and females.
No previous researchers attempted to quantify coloration differences, hence only trends and general impressions have been reported; the purported difference lack statistical support. Our coding of coloration quantifies coloration differences and permits a statistical assessment of differences between age classes and sexes. For the Burmese sample (Table 4), females are not significantly darker dorsally (GenColor) than males, and both share the same intensity (level of visibility) of the dorsal pattern (DorsTrnk). Females are darker ventrally; most are two-toned (VntTrnk), have dusky chins and throat (VntChinTh) and lack a median mental stripe (VntChinSt). Females also possess significantly darker faces than males, i.e., darker supralabials (SuplabC) and obscure postorbital stripe (Postorb). Comparison of juveniles to adults of the same sex (Table 4) reveals that juveniles and adults of the same sex are more similar in coloration to one another than to members of the opposite sex.
Having identified consistent difference in coloration in females and males (Fig. 6), and in both juveniles and adults, several questions arise, for example: Does the coloration difference lead to behavioral differences? Do females and males use coloration traits for reproductive recognition? Can we as herpetologists use the coloration difference to identify females and males? We can only answer this latter question with a “maybe.” Because no coloration trait occurred exclusively in one sex, there is no absolute difference between females and males; however, if a Burmese mockviper has a dark chin, dark or dusky supralabials, and a two-toned venter, it is most likely a female.
Comments on distribution and taxonomy.—Psammodynastes pulverulentus has broad distribution across tropical Asia (Fig. 1) from central Nepal (∼85°E) and eastern India (Orissa) to Taiwan (∼121°E) and latitudinally from ∼17° N in NE Indian and Myanmar south to ∼-9° S in the Lesser Sunda Islands (Flores). Such a distribution for a single species is immediately suspect. As herpetologists have examined pan-Asian species of frogs and reptiles, it has become evident that most represent species complexes, e.g., Xenochrophis piscator (Vogel & David 2012); however for P. pulverulentus, data supporting regional diversification remain elusive.
Within Myanmar, we noted variable levels of character differentiation among four regional pairs. Does this differentiation reflect actual or incipient speciation? We suggest that it does not represent either and feel that the differences observed result from small sample sizes and unequal distribution of sexes (Kachin-S 5♀♀, 7♂♂; Rakhine 8, 6; Ayeyarwady-Y 7, 3; Tanintharyi 5, 6) and these factors cause some of the regional differences. Also the unequal distribution of body sizes within the samples would also affect the absolute differences in mensural traits between sample pairs. As systematists, we thought as we began the study that there was a possibility of two species in Myanmar, northern vs. southern as occurs in other reptiles; however, our data does not offer support for regional differentiation.
Pope (1935) reported that the Taiwanese population possess the highest number of ventral scales then reported for any population of P. pulverulentus and suggested the possibility of recognizing this population as distinct at a subspecific level. Rasmussen (1975) confirmed the high number of ventrals with large samples of females and males, but as we noted earlier, he was reluctant to take any taxonomic action owing to high variation of ventrals in other samples/populations and the overlap of the ranges of some populations with the Taiwan population. Zhao (1995) followed Pope's suggestion and formally named the Taiwan population as Psammodynastes pulverulentus pappenfussi. The problem with this action is that only some members of P. p. pappenfussi are distinguishable from members of other Asian population, and more importantly, Zhao failed to examine variation on the adjacent mainland. We do not, however, recommend synonymizing this name. Our reason, also lacking adequate substantiation, is that we believe it likely that P. pulverulentus will prove to be a species complex when it is subjected to a broad genetic analysis. Once genetic units are recognized, some of the morphological variation will similarly sort into discrete morphological units.
Just as our inability to recognize regional differentiation within in P. pulverulentus, the taxonomic placement of Psammodynastes at the subfamilial and familial level has been in question since Boie first placed it in the family Dendrelaphidae. Herpetologist alike had Psammodynastes scattered into multiple subfamilies. Boulenger in 1896 conjoined the opisthoglyphous snakes into a large subfamily called Dipsadomorphinae. This subfamily was considered to contain many independent lineages therefore was subsequently disassembled. Smith (1943) placed the mockviper in Colubrinae, owing to the anterior maxillary teeth. Various subfamilial suggestions arose based on strictly morphological traits. Natricinae (Mcdowell, 1987) was proposed for the semicentrifugal sulcus on hemipenis and presence of a posterior hypapophysis. Pyron et al. (2013) in a broad genomic analysis placed P. pulverulentus into the subfamily Pseudaspidinae (BSV = 100). This placement was done without considering any morphological traits, a quite different approach compared to past suggestions and analyses based on many optical and dentitional characters when placing the mockviper on a subfamilial level.
Foremost, we wish to thank the Burmese members our Myanmar Herpetology Survey (MHS) teams, all of which were staff of Myanmar's Nature and Wildlife Conservation Division (NWCD), Forestry Department, for the procurement of the Burmese sample of mockvipers. The success of the MHS program resulted from the dedication and hard work of team members. Surveys began in August 1997, although formally and most actively from November 1999 through March 2010 with a hiatus in 2005 and 2006. Jens V. Vindum, California Academy of Sciences, trained the team members in herpetological field techniques and coordinated their field work (eight to ten months each year) with the various directors of the NWCD. The surveys were supported by the Biodiversity program of the National Sciences Foundation (DEB-9971861, DEB-0451832), and assorted research funds of the California Academy of Science (CAS) and the National Museum of Natural History – Smithsonian Institution (USNM). We thank the preceding organizations and their administrative staffs for their support and advocacy of this project. The authors acknowledge and thank the collections management staffs of CAS and USNM for their ready assistance in specimen and data access. JHM thanks the Chevy Chase-Bethesda High School intern program and Ms. Stacy Farrar for providing time during the regular school days and term to pursue this research project. We also thank J. Block and J. Murphy for their careful reviews of an early draft of the manuscript and three anonymous reviewers for a final prepublication review.
Specimens are arranged north to south by division and state (Myanmar) or province (Thailand).
Myanmar. Kachin: CAS 221250, 233001, 233023, 240982, 245215, 245505, USNM 587183, 587230, 587360-362. Sagaing: 232204, 239189. Shan: none. Mandalay: CAS 231361, 232163. Chin: CAS 233209, 233230, 233294, 233297, 233331, 235367, 235370-372, 235374. Magway: none. Rakhine: CAS 216604, 216499, 220382, 220429, 220461, 221998, 222001, 232786, 239868, 239894, 239935, 240101, 241271, 241522, USNM 587234. Bago: none. Kayin,: none. Kayah: none. Ayeyarwady: CAS 213503, 213575, 239335, 239383, 239472, 239533, USNM 587232-233. Yangon: CAS 213329, 213366. Mon: none. Tanintharyi: CAS 222277, 243907, 245992, 246314, 246748, 246772, 246797, 247491, 247974, USNM 34502, 587235-236.
Thailand: Chiang Mai: USNM 84752, 101649. Tak: USNM 101036-038. Lamphun: USNM 76845, 81859, 84831. Kanchanaburi: USNM 70336, 72140, 94739-741, 94794. Nakhon Panthom: USNM 72715. Nakhon Ratchasima: USNM 79616, 100992. Chantiburi: USNM 76835, 79484-485. Prachuap Kiri Khan: USNM 94933-935. Trang: USNM 19839, 19866, 23753 26220.
Literature sources of distributional data, west to east: Nepal, Schleich and Kästle (2002); India, Mohapatra et al. (2010), Dutta et al. (2009); Bangladesh, Khan (1982); Thailand, Chan-ard, Parr and Nabhitabhata (2015), Taylor (1965); Laos, Stuart (1999); Cambodia, Saint Girons (1972), St. Girons and Pfeffer (1971); Vietnam, Campden-Main (1970), Nguyen et al. (2009); China, Pope (1935), Zhao and Adler (1993); Taiwan, Dieckmann et al. (2013), Kuntz (1973); Malaysia – peninsular, Grismer (2011); Singapore, not present Lim and Lim (1992); Sumatra, David and Vogel, 1996; Bali, McKay (2006); Borneo, Inger and Lian (1996), Malkmus et al. (2002), Murphy et al. (1994), Stuebing (1991); Flores and Komodo, Auffenberg (1980), Zug and Kaiser (2014); Sulawesi, in den Bosch (1958). Koch (2012); Philippines, Leviton (1983), Taylor (1922).
Locality data from some of the preceding references are plotted in Fig. 1; most are not.
Definitions of Characters
Head length (HeadL): Distance from tip of snout to posterior edge of jaw.
Head width (HeadW): Transverse distance from left to right posterior edges of jaw.
Internarial width or snout width (SnW): Transverse distance from left to right nares.
Interorbital width (Interorb): Transverse distance from anterodorsal edges of left and right orbits.
Naris to eye distance (NarEye): Distance from center of nares to anterior edge of orbit.
Orbital diameter (OrbD): Distance from anterior edge to posterior edge of orbit.
Snout to eye distance (SnEye): Distance from tip of snout to anterior edge of orbit.
Snout-vent length (SVL): Distance from tip of snout to center of vent.
Tail length (TailL): Distance from center of vent to tip of tail.
Total length (TotL): Total length of specimen; SVL + TailL.
Dorsal scale rows, anterior (DorsAnt): Number of dorsal scale rows at one head-length behind head.
Dorsal rows midbody (DorsMidb): Number of dorsal scale rows at midbody.
Dorsal rows posterior (DorsPost): Number of dorsal scale rows at one head-length anterior of vent.
Infralabials (Inflab) Number of enlarged scales bordering the mouth from the mental to below the posterior border of eye.
Loreals (Loreal): Number of loreal scales.
Precloacal (= anal) scale (Precl): Two states, entire (undivided) and split (divided, two scales).
Preoculars (Preoc): Number of preocular scales.
Postoculars (Postoc): Number of postocular scales.
Subcaudals (Subcaud): Number of subcaudal scales, excluding tip scale.
Supralabials (Suplab): Number of enlarged scales bordering the mouth from the rostral to below the posterior border of eye.
Temporals, anterior (TempAnt): Number of anterior temporal scales.
Temporals, posterior (TempPost): Number of posterior temporal scales.
Ventrals (Vntl): Number of ventral scales; used Dowling's (1951) standard method.
We recognized and coded 10 features of coloration for which we believed that we could consistently record the various states for each feature.
Dorsal trunk markings, DorsTrnk: 0, dark-edged white blotches middorsally on at least the anterior third of the trunk; 1, blotches present by indistinct; 2, no well-defined blotches dorsally on trunk.
General dorsal color, GenColor: 0, light brown; 1, medium brown; 2, dark brown; 3, rufous.
Head, middorsal color pattern, HedDors: 0, light cone-shaped area from snout to between eyes; 1, dark cone from snout to between eyes.
Nape stripe, NapeStrp: 0, middorsal light stripe on nape; 1, middorsal dark stripe on nape; 2, no stripe present.
Postorbital stripe, Postorb: 0, distinct and well-define stripe from posterior edge of eye to near corner of jaw; 1, stripe present, indistinct and nearly matching surrounding color.
Supralabial color, SuplabC: 0, light to slightly dusky; 1, medium to dark dusky.
Temporal color, TempC: 0, light and contrasting colored; 1, dull or dark, not contrasting to surrounding scales.
Ventral chin stripe, VntChinSt: 0, chin uniformly dusky, no stripe; 1, chin with a partial median light stripe; 2, complete light stripe from tip of chin to anterior throat; 3, chin uniformly light, no stripe.
Ventral color, chin and throat, VntChinTh. Background color of chin and throat: 0, light; 1, dusky.
Ventral color, background, VntTrnk. Background color of venter from rear of throat to the vent: 0, uniformly light; 1, two toned, light anteriorly, dusky posteriorly; 2, uniformly dark.
Editor: Rick Hochberg