Tuesday, April 7, 2015

Boie’s Mud Snake, Hypsiscopus plumbea (Boie, 1827)

Homalopsis plumbea Boie, 1827 Isis von Oken, column 560. Type locality: Java. Holotype: RNHL 1163. Collector: Unknown.

Hypsirhina hardwickii Gray, 1835 2:187, Fig. 1 Illustrations of Indian Zoology. Holotype: BMNH 1946.1.2.44, presented by Gen, Hardwicke. Type Locality: Penang. Collector: Unknown. [The holotype has 19 - 19 - 18 dorsal scale rows, 125 ventral scales and 34 subcaudal scales and is a female. The chin shields are about equal in length. These characters are consistent with other peninsular Malaysian specimens.]

Coluber plumbeus - Eydoux and Gervais, 1837: 3, pl 16, fig 1.Magasin de Zoologie,  Hypsirhina plumbea - Gray, Zoologica Miscellany, p. 66.

Hypsicopus plumbea – Fitzinger, 1843:25Systema Reptilium,

Eurostus plumbeus - Duméril, Bibron, and Duméril, 1854, 7:955, pl. 84, Figure 2  Érpétologie Générale... Reptiles.

Enhydris plumbea - Stejneger, 1898: 12(3):222 Journal of the College of Science.

Etymology. The name plumbea is probably derived from the Latin plumbeus meaning “of lead.” This is most likely in reference to the dark gray dorsal coloration found in many larger specimens of this species. Common Names: Yellow Bellied Watersnake (Campden-Main, 1970); The Lead-Coloured Hypsirhina, Harwicke's Hypsirhina, The Ular Aer (Gray, 1849); Hainanese name is “Pum-twa.” (Gressitt, 1940);  “Mei Sa” (southeastern China) (Gressitt, 1941); Mud Creeper (Hoesel, 1959); Lead Water Snake, Plumbeous Water Snake (Reitinger, 1978); Olive Water Snake (Karsen et al., 1986); Common Rice Paddy Snake, Water Snake (Kuntz, 1963);  Boie’s Water Snake (Wall, 1924); Orange-Bellied Mud Snake (Stuebing and Inger, 1999).

Distribution.  This is a widely distributed species ranging from the Andaman Islands (India) and Myanmar eastward across the Indochinese Peninsula (including Laos) and southern China southward into Indonesia. It is present on many, if not all, Indonesian islands and extends its distribution eastward to Sulawesi. However, AMNH 3840 is said to be from the Molucca Islands, if true this would extend the eastern edge of the range. Saltwater may be a barrier for this species however, it occurs on many Indonesian and Malaysian islands, and it may have reached these islands at times of lower sea levels or its association with rice paddy may have allowed it to spread with agricultural humans.  Also, elevation does not seem to be a serious barrier for this lowland snake, in that it colonizes elevations to least 1200 m. Mell (1929b) found it up to 700 m in Kwangtung, China; Smith (1943) obtained one at Bockor in the Elephant Mountains of Cambodia at 3000 feet (914 m); and Deuve (1970) reported it in Laos as reaching an altitude of 1200 m.

Diagnosis. A small snake with 19 scale rows at mid-body, 119 - 142 ventral scales, a small internasal scale that is isolated from the loreals, upper labials 2 - 3 or 2 - 4 usually contact the loreal, and lower labials 1 - 4 contact the anterior chin shields. Other homalopsids with 19 scale rows at mid-body are Miralia. alternans and Raclitia indica. Of these species both have a banded dorsal pattern, alternans has lower labials 1 - 5 in contact with the anterior chin shield, and indica has a ventral count in the range of 173 - 175.

Size. The largest individual of 91 specimens was a 713 mm female with a 63 mm tail from Kabin Buri, Thailand. The largest male had a total length of 473 mm and a 53 mm tail. Male tail/SVL ratios ranged from 0.12 - 0.19, the range for females was 0.10 - 0.17. Bergman (1960) gave maximum length for males as 420 mm with a 64 mm tail, and 426 mm for females with a 53 mm tail. Saint Girons (1972) measured a 424 mm female, and a 298 mm male from the Cambodian population. Neonates are small; Pope (1935) reports a range of 122 - 160 mm.

External Morphology. The head is distinct from the neck and slightly depressed. The body is cylindrical. The head shields of some males are tuberculate (this may be a seasonal phenomenon).  On the head the rostral scale is visible from above, pentagonal, and broader than tall. The nasals are relatively large, larger than the internasals or the prefrontals. They are usually semi-divided, rarely completely divided. The cleft usually contacts a labial, but may also contact the loreal or internasal. The internasal is single and not in contact with the loreal. It has about the same area as one of the prefrontals, and slightly penetrates the nasals. The pair of prefrontals makes contact with the loreals. The frontal length is about the same as the interorbital distance, and less than the eye-nostril distance. The parietals are about 1.5 times the length of the frontal. The loreal is single, square, and in contact with the second and third upper labials. The supraocular has a broad posterior margin and a narrower anterior margin; the single preocular (rarely divided) is higher than broad; postoculars number two; there are no subocular scales. The temporal formula is 1 + 2 + 3. The upper labials number eight; the seventh is the largest; the fourth, the fifth, or more often the fourth and fifth enter the orbit.  On the chin the lower labials number 9 - 11, usually 10 and the first 4 - 6 (usually the first five) contact the anterior chin shields. The anterior chin shields are broader than the posterior pair, but their lengths are variable from one population to another. A pair of smaller scales separates the posterior pair; these may be tuberculate in some males. The gulars number 2 - 5. On the body the dorsal scale rows number 19 - 19 - 17, but eight (8.8%) specimens showed 15 scale rows near the vent; and two males from Sulawesi have 18 and 19 rows near the vent. The first row is ovate and the scales become more elongated toward mid-body, all are smooth. However, in males the dorsal scales in the first three rows, 5 - 6 scales anterior to the vent, may have tubercles; also, the scales immediately lateral to the vent may have tubercles. The anal plate is divided and slightly longer than the preceding ventral. The ventral scales number 117 - 142 and do not show sexual dimorphism in any of the populations examined, the ventral scales are 3 - 3.5 times the length of a nearby dorsal scale. On the tail the dorsal scales on the tail are ovate, some on the midline are enlarged, and are similar to those elsewhere on the body.  The subcaudal scales are paired and number 29 - 46.. The Vietnam, Thailand, mainland China, and Taiwan populations show sexual dimorphism is the subcaudal counts, while the Sabah population does not. At the base of the tail the width is 79% of the height based upon an average of five specimens. Not included in the table are three males from Sulawesi that had the highest subcaudal counts, 43 - 47.

Color and Pattern. The crown of the head is uniform gray, with the head shields having a light colored margin. Scale rows 1 - 2 or 1 - 3 are the same yellow-cream color as the belly. Scale rows above this are a uniform gray. The ventral side of the tail has a midline, zigzag stripe. Older adults may be uniform black, younger animals may be an olive green with black pigment on some scales and pink, orange, or yellow patches on the face, particularly on the labials. Thailand specimens tend to have a uniform gray pattern above dorsal scale row three. The ventral pattern is uniform cream or yellow. All peninsular Malaysia specimens examined show vertebral spots that are darker than the surrounding pigment, their ventral scales have some pigment, and the midline of the tail has a zigzag stripe. Vietnam specimens tend to be a uniform gray or black above dorsal scale row three, and the belly tends to be uniform with the exception of the zigzag stripe under the tail. Sabah (East Malaysia, Borneo) specimens have a “net-like” pattern that results from each scale having a light central spot. Vertebral spots are also present in some specimens. They also have some scattered dark pigment toward the edge of each ventral, and a zigzag stripe on the midline of the tail. Photographs of H. plumbea with several different color patterns are in field guides and other publications. This species may have some ability to change color.

Habitat. This is an aquatic snake, but it is the most terrestrial of the homalopsids studied to date based upon field observations. In Sabah, Voris and Karns, (1996) found this snake associated with wet sites (wallows, marshes, ditches, stream, pond banks) where it was most frequently found in the tangle of roots and mud 10 - 20 cm below surface debris during the day and night. They studied this animal in an old rice paddy that was being used as a water buffalo pasture, with buffalo wallows. The snakes were concentrated around the edges of these wallows and while they occasionally moved they were mostly sedentary. Collection of this snake by hand required the destruction of its habitat by pulling the mats of grass from around the edges of the wallows, thus they used funnel traps. In southern Thailand the species was found in a wet meadow, and was collected in funnel traps submerged along the shoreline (Murphy et al., 1999). In northern Thailand it was collected in gill nets set in stagnant ponds. In central Thailand it was hand collected at night by walking rice padi dikes and examining shallow water and the mud substrate with a flashlight. It occurs from sea level to at least 1200m (Deuve, 1970; Mell, 1922; Smith, 1943); see comment in the Distribution section.
            Other comments from the literature describing this species habitat follow. Batchelor (1958) wrote, "...at Asahan, seems to favor the padi sawahs, and the more overgrown, sluggish ditches." Campden-Main (1970) said it is, "...almost entirely aquatic...The species is particularly common in the rice paddies and drainage ditches near Bien Hoa [Vietnam]. Several specimens crossing the road through rice paddies at night were collected at Phan Rang [Vietnam]. Boulenger (1903) quoted field notes from Annandale and Robinson who wrote, “Essentially aquatic but often found under dead trees some distance from water.” Flower (1899) found it, "...frequents freshwater-ponds or rivulets, but one I found under a stone some little distance from any water." Karsen et al. (1986) stated, "An almost totally aquatic lowland species found in sluggish or slow-flowing streams, ponds and cultivated fields. Is predominantly nocturnal, emerging to forage for food at night. In rainy weather may wander overland...Has been recorded from few areas owing to its secretive habits but is expected to occur in many more habits." Saint Girons (1972) found this species away from water in the dry season, but notes that it prefers rice fields and marshland. Wall (1903) commented, "All my specimens were caught in or about a sluggish stream near our camp at Kowloon." Kuntz (1963) wrote about the Taiwan population, “As the name implies, this snake is common to rice paddy and wet agricultural areas, usually at lower altitudes. E. plumbea is frequently found in the same habitat with Natrix [=Xenochrophis] piscator. It is unusually active at night. On rainy nights it may migrate into yards of homes near or adjacent to agricultural areas. E. plumbea has been found inside homes in Taipei and its suburbs.”  Pope (1935) wrote, "In Fukien and on Hainan I failed to detect and marked differences between the habitat preferences of plumbea and chinensis…” Museum material comes with the following habitat information: “Kunai grass area, some brush” (CAS-SU13688); “found in drainage ditch after heavy rain at night” (CAS144021); “found in mountain agricultural area” (USNM 142508-12).

Diet and Feeding Behavior. Hypsiscopus plumbea feeds on fish and amphibians, including amphibian larvae. Voris and Karns (1996) examined 20 snakes caught by hand that contained food from a population at Kayumadang, Sabah, Malaysia, 14 of these had identifiable remains of amphibians, including an egg mass, three unidentifiable tadpoles, and ten adult frogs. Four of the 10 frogs were the four-lined treefrog, Polypedates leucomystax (Family Rhacophoridae), and six were unidentifiable as to species. Two snakes contained the walking catfish, Claris teysmanni (Family Clariidae). Snakes caught in traps were forced to regurgitate and produced tadpoles less frequently than fish. Snakes maintained in captivity readily ate fish and tadpoles. Additionally, a Sabah specimen (SSM REP0580b) not included in Voris and Karns (1996) (325 mm SVL/47 mm tail, 37.4g female) contained an 8.0 g Rana [=Fejervarya] limnocharis (Family Ranidae).  Individuals in this population fed both day and night. During the day the snakes fed on fish and tadpoles from ambush sites in the mud-root tangle, at night they became active foragers. Snakes that were using a nearby stream were more mobile than those using the wallow microhabitats. Other literature supports its fish and frog-eating habits across its distribution. Schmidt (1927) examined five Chinese specimens that contained prey, three contained Rana and two contained Microhyla. Gressitt (1941) reported Rana [=Fejervarya] limnocharis, a fish, and a crustacean from specimens from southeastern China. In Taiwan, Kuntz (1963) reported "...its food consists of loaches and amphibians." In Hong Kong, Karsen et al. (1986) found this snake to be "…an excellent scavenger, consuming even decaying flesh. Diet includes frogs and fish."  Pauwels and Lenglet (2003) reported the eel like fish Macrognathgus siamensis (Family Mastacembelidae) to the list of fish plumbea will feed on.

Pope (1929) hypothesized food partitioning between this species and Enhydris chinensis from a relatively small sample of specimens, he wrote, "Examination of the stomachs has shown that plumbea lives on an amphibian diet, chinensis, a fish diet. Seven stomachs of the present series of plumbea contained frog remains and the rest were empty or nearly so, while fishes were found in the four chinensis stomachs. These two snakes are enabled to inhabit the same fields through avoidance of competition in feeding, one preying on fish, the other on frogs." This hypothesis is not supported by more recent studies that show plumbea to have a diet composed of fish and amphibians. Deuve’s (1970) assertion that plumbea feeds on mollusks; and Gressitt’s (1941) statement that it feeds on crustaceans, are in need of further documentation.

 Mori (1998) used captive neonate and year-old plumbea to study prey handling.  Almost all of his observations were made while the snakes were feeding underwater. He noted that neonates frequently dropped prey and had to recapture it, and he found that they were still dropping prey at the sixth feeding. Prey was always swallowed head first, and prey-handling time increased with larger prey items. H. plumbea also used bilateral movement of the jaws followed by neck-bending when swallowing prey. The larger the prey, the longer the snake held it in its mouth before swallowing, envenomation was probably occurring during this time. 

Reproduction. Litter Size. For this study 19 gravid females from Taiwan were examined.  Snout-vent lengths ranged from 282 - 480 mm, and they contained 2 -18 embryos (= 8.7).  The RCM (n = 18) ranged from 0.064 - 0.596 (= 0.29). The effort per embryo ranges from 0.307 - 1.770 (= 1.23). These litter sizes mostly fall within the range of those reported elsewhere in the literature. Schmidt (1927) reported 4 - 11 eggs in a “number of females from Hainan;" Pope (1929) found eight females from China contained 2 - 9 eggs (= 5.9); Pope (1935) reported 2 - 11 young, (= 6), and stated birthing is over in August; Maki (1931) reported 10 - 15 young from the Taiwan population; Taylor and Elbel (1958) found 14 ovarian eggs in a female from Thailand; St. Girons and Pfeffer (1971) reported 10 eggs in a female from Cambodia; Karsten et al. (1986) examined Hong Kong specimens and report a litter of five young; Cox (1991) stated females average nine per litter. 

Timing. In Cambodia, St. Girons (1972) described young being born in the spring; in Laos, Deuve (1970) found neonates throughout the rainy season and stated the young are born April through August; Saint Girons and Pfeffer (1972) suggest the young are born in spring in Cambodia. And, St. Girons (1972) suggested that in Cambodia males start spermatogenesis in August, sexual activity occurs in November, and females start vitellogenesis in November, with parturition in the spring.

Batchelor (1958) discussing  plumbea wrote,  "I once had a female taken from an estate well which produced nearly thirty youngsters during the following twelve hours, each a little under three inches in length, greenish in colour...The adult was 10" in length...was dark purplish brown in colour with a series of black vertebral spots." The large litter size, adult size, and color of the offspring make the identification of the snake this statement questionable.

Predators. Mao (1970) found the krait, Bungarus multicinctus, and the common cobra, Naja naja prey upon plumbea. Voris and Karns (1996) suggested that the mud-root tangle is a relatively predator-free microhabitat. They found it very difficult to extract the snakes from this refuge and it seems likely that the snakes are relatively safe from wading birds and large predatory fish. However, plumbea is probably not safe from snake predators, in this environment. The population studied by Voris and Karns (Sabah, East Malaysia) was relatively sedentary and spent the day in the mud-root tangle, but became more active at night. It also seems likely that plumbea is subject to predation from a variety of large fish with which it shares its aquatic habitat, particularly snakeheads (family Ophicephalidae).

Campden-Main (1970) noted that defense behavior in this species differs with its habitat when it is encountered. He wrote, "The species will not hesitate to bite if disturbed out of water, but in the water they are shy and always attempt to escape." This may account for the conflicting descriptions of its behavior. Batchelor (1963) wrote, it "...merely buried its head in the soil or under a leaf when disturbed, hoping presumably, that the action rendered it invisible." Kuntz (1963) wrote about the behavior of Taiwan specimens. "This snake will strike without provocation and in contrast to most species is capable of jumping or striking distances considerably greater than the body length. When excited or attempting to escape from an intruder, it moves rapidly by a series of erratic lateral jumps. At times the snake will land on its back or side, flip its body quickly and take off at 90 degrees from the original path of movement." And, Pope (1935) described its behavior in China,
The markedly fierce behavior of plumbea when on the defensive has been recorded by Flower (1899, l.c.) and Schmidt (1927, l.c.) While on guard, the body forms a single loop and the neck is bent sharply like a crook. The strike is little more than a frantic jab. I have seen a specimen progress on a smooth floor by throwing its body forward so the tail sometimes even fell in front of the head. This is most unusual behavior for a snake.

Venom. Karsen et al. (1986) wrote, “Although listed as venomous, it is not considered dangerous to man as its venom has low toxicity. Its bite may cause slight swelling at most." D. Karns (personal communication) found that envenomation results in a immediate burning sensation followed by local swelling, but no systemic effects; and compared the effects to a bee sting.

Folklore. On Thailand’s Khorat Plateau local people told us that they use plumbea to rid buildings of ant infestations. The snakes are cooked and then placed around the inside of a building. The ants then eat the snakes and die, or turned into a winged form and disappear.

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