Ecology of the Australian Elapid Snake Tropidechis carinatus1

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1 Journal of Herpelalogy, Vol. 6, No. 4, pp , 98 Copyright 98 Society for the Study of Amphibians and Reptiles Ecology of the Australian Elapid Snake Tropidechis carinatus RICHARD SHINE AND NEIL CHARLES3 ABSTRACT.- Tropidechis carinatus is a medium-sized, highly venomous snake found along the 'eastern coast of Australia. Dissections of 7 museum specimens were combined with field observations to document the basic natural history of T. carinatus. Adult males and females attain similar body lengths. The diet is diverse, with mammals and frogs being the major prey items. Female reproduction is seasonal, with ovulation in spring and parturition in late summer. Adult females may reproduce only in alternate years, or less often. Fecundity is low, with litters ranging from 5 to 8 offspring, each about 5 to 0 cm SVL. Both in the field and in captivity, T. carinatus is more arboreal than any other Australian elapid except for the genus Hoplocephalus. Many similarities between Tropidechis and Notechis (tigersnakes) suggest a close phylogenetic relationship between these two genera. The sole member of the genus Tropidechis is the rough-scaled snake, T. cl!!.~-:-- (Sydney). We recorded the following data bane) and the Australian Museum natus, a medium-sized ( meter) elapid from each specimen: (i) snout-vent length snake of eastern Australia. Coastal in distribution, the rough-scaled snake primar- sexual maturity or immaturity (criteria (SVL); (H) sex; (Hi) prey items in gut; (iv) ily is found in cool moist habitats (Trinca were: males-large testes or opaque efferent ducts; females-ovarian follicles> 5 et at., 97), particularly near streams in forested areas. The body is slender and mm, or enlarged oviducts); and in mature the dorsal scales are strongly keeled (Fig. females, (v) number of developing ova or ). The venom is highly toxic, with one embryos, and (vi) diameter of largest human fatality being reported (Trinca et developing ovarian follicle. al., 97). Very little is known about the RESULTS natural history of this dangerous snake. The present paper is largely based on dissection of museum specimens of T. cari- carinatuscomprised 56 juveniles, 39 mature Adult Body Sizes.- The sample of 7 T. natus; we provide data on body sizes, sexual size dimorphism, food habits and males averaged 67.6 cm SVL (SEM =.0, males, and 3 mature females. The mature reproductive cycles. Observations of T. range 48.6 to 87. cm), almost the same as carinatus behavior, both in the field and females (mean = 67. cm SVL, SEM =.3, the laboratory, are reported also. range cm). FoodHabits.-Of 7 prey items found in MATERIALS AND METHODS We examined all specimens of Tropidechis carinatus (N = 7) in the collections of the Queensland Museum (Bris- This paper is dedicated to David Fleay, in recognition of his early work on Tropidechis and his continuing contributions to Australian herpetology. Zoology A08, University of Sydney, N.S,W. 006, Australia. 3 8 Mahonia Street, Bellbowrie, Queensland 4070, Australia. Tropidechis guts, 3 (48%) were mammals (mainly house-mice) and (4%) were frogs (Table ). Anuran prey were taken by smaller snakes (i SVL = 5. cm), on average, than were mammalian prey (i snake SVL = 59.0 cm), but this difference in snake body lengths is not statistically significant (Wilcoxon rank-sum test, N = 0,7, Wn = 5.5, P > 0.0). Reproductive Cycle.-A clear seasonal pattern of ovarian activity is evident from Figure. Follicles are small (< 0 mm) for most of the year. Vitellogenesis occurs in

2 384 R. SHINE AND N. CHARLES ~ -> -... FIG.. Rough-scaled snake, Tropidechis carinatus. Photograph by A. Easton, Queensland Museum. spring (Sept.-Dec.), with ovulation in December. Rough-scaled snakes are viviparous; we examined several females with oviducal young in the course of this study. Gestation continues through summer, with parturition around March. Many adult-size females appear to be non-reproductive. For example, only 5 of 5 females collected during the period October to March were in reproductive condition; the other 0 females had inactive ovaries with follicles less than 5 mm diameter (Fig. ). Fecundity.-Litter size in Tropidechis ranges from 5 to 8, with a mean of 0. offspring (SEM =.4, N = 0). No correlation between fecundity and maternal body length is evident (Fig. 3; r =.00, N=9). Size at Birth.- The smallest field-collected T. carinatus measured 9.0 cm. Offspring from three litters born in captivity measured as follows: (i) 5.3 to 6. cm SVL, i = 5.7, N = 4; (ii) 8.7 to 9.5 cm SVL, i = 9.0, N = 9; and (iii) 5 to 7 cm total length, i = 6 cm, N = 6, with weights from 3.6gm to 4.4gm, i = 4.gm (data for last litter from G. Mengden, pers. comm.). Another female rough-scaled snake contained pigmented oviducal embryos, almost full-term: these mea- TABLE. Prey items found in guts of roughscaled snakes. Prey type Mammals-sp. unknown -rodents -Mus musculus Birds-sp. unknown Lizard - Physignathus lesueuri Frog-sp. unknown -myobatrachid sp. -Adelotus brevis -Litoria chloris -. gracilenta Number of 4 8 5

3 AUSTRALIAN ELAPID ECOLOGY " I" ;; 0 ~ 8. ~ 6 w" g 0 h M J MONTH FIG.. Seasonal variation in diameters of ovarian follicles and oviducal "eggs" in rough-scaled snakes. 0 5 V) ~.0: ~ 0 Cs '" ~ 5 ::> Z A SON D FiG. 4. Monthly variation in numbers of roughscaled snakes collected, based on museum. sured 3.6 to 4.4 cm SVL. We conclude that size at birth averages 5 to 0 cm SVL in this species. Seasonality.-An analysis of the dates on which museum specimens of Tropidechis were collected (Fig. 4) shows marked differences in abundance in different seasons. Most snakes are collected in summer (Dec.-Feb.), fewer in spring and autumn, and almost none in winter (June-Aug.). These seasonal differences in numbers are highly' significant (X with 3 df, N = 85, X=., P <.00). FieldObservations.-We have seen many rough-scaled snakes in the field, particularly in south-eastern Queensland. This species is crepuscular and nocturnal, with most specimens being found on roads at night (especially on rainy nights in summer). Occasionally, rough-scaled snakes may be found basking during the day, 8 6 " 3 w ~ 0 ~ ""pid"h', FE(UNOITY - m~ = - - = m MATERNAL'NOUT-VENT LENGTH (mm) FIG. 3. The relationship between maternal body length and litter size in rough-scaled snakes. usually curled up on tracks or in rocky areas close to creeks. Tropidechis are most common in wet areas with heavy vegetation cover (rainforest, wet sclerophyll) but are abundant also in thickets of lantana. One rough-scaled snake was seen at 030 hours on a bitumen road, attempting to consume a badly-crushed DOR frog. Tropidechis often climbs into trees, bushes and vines, and is a more consistent and capable climber than any other Australian elapid except the members of the genus Hoplocephalus. Table summarizes 9 field observations of arboreality in Tropidechis. Arboreal proclivities are obvious in captive specimens also: adult roughscaled snakes in a large outdoor enclosure at Beerwah, Qld., spend most of their time 3 to 5 ID above the ground in Melaleuca trees. These snakes leave the trees only briefly (usually in late afternoon or early morning), most often after heavy rain (pers. obs.). Three juveniles born in captivity were adept climbers (M. Fitzgerald, pers. comm.). DISCUSSION The food habits we have recorded for Tropidechis (Table ) are consistent with previous statements: frogs and mice are the main prey items (Fleay, 96; Millar, 963; Cow, 976; Beard, 979), although lizards and birds are eaten also. Previous specific include Sminthopsis (Fleay, 96), Rattus rattus (Millar, 963) and Cercartetus (Trinca et ai., 97). The presence of treefrogs and birds in the diet is con-

4 386 R. SHINE AND N. CHARLES TABLE. Field observations of arboreality in Trophidechis carinatus. Month January January June July August October November December December Height above Time of Type of vegetation ground day (h) Source of data Eucalyptus sp. 4.0m 000 pets. obs. "choko" vine.0m - Queensland museum Lantana.8 m 500 M. Fitzgerald, Crown of banana plant. m 000 M. Fitzgerald, Crown of banana plant.0m morning M. Fitzgerald, Lantana. m 400 pets. obs. Lantana.8 m 030 M. Fitzgerald, Crofton weed 0.6 m 630 M. Fitzgerald, "bushes" - night Australian Museum sistent with our observations on arboreality in Tropidechis. However, a recent review on diets of arboreal snakes (Shine, 98) reveals few consistent dietary differend~s between terrestrial and arboreal snake species. It is entirely possible that Tropidechis forages more often on the ground than in trees. The seasonal reproductive cycle of female rough-scaled snakes is similar to that described for other temperate-zone elapids (e.g. Shine, 977). Vitellogenesis is concentrated in spring, with ovulation in late spring and gestation over summer. Parturition occurs in late summer or autumn (Fig. ). Mating seasons for this species have not been determined, but a male collected in February made vigorous attempts to mate when he was placed with a female soon after capture (P. Webber, pers. comm.). One unusual feature of reproduction in this species is the high proportion of apparently non-reproductive adult females (Fig. ). The non-reproductive animals certainly were large enough to breed; indeed, they averaged slightly longer (i SVL 70. cm, SEM =.4) than did the reproducing females (i SVL 64.9 cm, SEM =.3).The data suggest that adult female Tropidechis may breed less often than annually, as is the case with many other snakes (reviewed by Bull and Shine, 979).However, sample sizes in the present study are too low to permit any firm conclusions. In conjunction with this apparently low frequency of reproduction, the small litter size of Tropidechis(i = 0. offspring) must result in a low overall reproductive rate. However, offspring tend to be larger at birth (5 to 0 cm SVL) than are offspring of other elapid species with comparable adult body sizes (e.g. Shine, 978). The collection data for museum specimens show that rough-scaled snakes are collected in greatest numbers in the warmer months of the year (Fig. 4). However, the climate is mild in the areas occupied by this species, and the snakes do not become completely inactive during winter Oune-August). Instead, specimens may be found basking on warm sunny days throughout this season (Table, and M. Fitzgerald, pers. comm.). The seasonal bias in museum specimens (Fig. 4) probably reflects the more extensive (nocturnal) movements of these snakes during summer months.

5 AUSTRALIAN ELAPID ECOLOGY 387 The arboreal behavior of rough-scaled snakes (Table ) stands in sharp contrast to other Australian elapids, which are predominantly terrestrial in habit. Only one genus, Hoplocephalus, is regularly reported to be arboreal (e.g. Cogger, 967; Heatwole et al., 973; Shine, 98). Occasional arboreality seems to be characteristic of the tigersnake, Notechis scutatus (Sharland, 96; Heatwole et al., 97; G. Webb, pers. comm.; and several observations by Shine). This is one of many characteristics in which Notechis resembles Tropidechis, and we suspect a close phylogenetic relationship between these two elapid genera. Specific points of resemblance include: (i) morphology: body coloration; scalation; dentition; venom gland musculature (McDowell, 967);similarity of body sizes between adult males and females (this paper; Shine 978); (ii) karyotype: distinctive, and similar in both species (G. Mengden and J. Bull, pers. comm.); (iii) venom: high toxicity, similar clinical effects, and neutralization of Tropidechis venom by Notechis anti venom (Covacevich, 98); (iv) b~.havior: pugnacious, crepuscular, often arboreal; (v) reproduction: viviparous; (vi) habitats:preference for relatively cool and moist areas (e.g. Cogger, 967; Trinca et al., 97). Notechis and Tropidechisdiffer from each other in many respects also, notably in the more elongated bodily form and carinate scalation of Tropidechis. Nonetheless, Fleay's (96, p. 85) description of T. carinatusas "just what one would expect of a pocket-edition Tiger Snake" is truly appropriate. It seems likely that these profound similarities between Notechis and Tropidechisreflect common ancestry rather than evolutionary convergence. Acknowledgments.-We thank J. Covacevich (Queensland Museum) and A. Greer (Australian Museum) for permis- sion to examine specimens in their care. Jeanette Covacevich and Margaret Charles deserve special thanks for their helpfulness and encouragement. M. Fitzgerald provided valuable field observations of T. carinatus, as well as insights into the ecology of this species. G. Ross identified prey items. The study was supported financially by the Australian Committee. LITERATURE Research Grants CiTED BEARD,D. J Rough-scaled snake, Tropidechis carinatus. Herpetofauna 0:6-9. BULL,J. J., ANDR. SHINE Iteroparous animals that skip opportunities Amer. Natural. 4: for reproduction. COGGER,H. G Australian reptiles in colour. A. H. & A. W. Reed, Sydney. pp. COVACEVICH, J. 98. Medically significant terrestrial snakes of northern Australia. In Pearn, J. (ed.) "Animal toxins and man." Pp Queensland Dept. of Health, Brisbane. FLEAY,D. 96. Beware-this small snake is dangerous. Viet. Natural. 77: Gow, G. F Snakes of Australia. Angus & Robertson, Sydney. 88 pp. HEATWOLE,H., S. A. MINTONJR., G. WITTEN,M. DICK, J. PARMENTER,R. SHINE, AND C PAR- MENTER.973. Arboreal habits in Australian elapid snakes. HISS-News Journal :3. McDowELL, S. B Aspidomorphus, a genus of New Guinea snakes of the family Elapidae, with notes on related genera. J. Zool. (Lond.) 5: MILLAR,D. B A preliminary study of the habits and venom of Tropidechis carinatus (Serpentes: Elapidae). Herpetofauna 963:3-7. SHARLAND,M. 96. Tasmanian wildlife. Melbourne Univ. Press, Melbourne. 86 pp. SHINE,R Reproduction in Australian elapid snakes..female reproductive cycles. Aust. J. Zool. 5: Growth rates and sexual maturation in six species of Australian elapid snakes. Herpetologica 34: Arboreality in snakes: ecology of the Australian elapid genus Hoplocephalus. Copeia, in press. TRINCA,J. C, J. J. GRAYDON,J. COVACEVICH,AND C LIMPUS. 97. The rough-scaled snake (Tropidechis carinatus) a dangerously venomous Australian snake. Med. J. Aust. : Accepted: January 98.

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