O . kikuzatoi through a series of field surveys as below.

Current Herpetology 23(2): 73-80, December 2004 (c)2004 by The Herpetological Society of Japan

Field Observations on a Highly Endangered , Opisthotropis kikuzatoi (: ), Endemic to Kumejima Island, Japan

HIDETOSHI OTA*

Tropical Biosphere Research Center, University of the Ryukyus, Nishihara, Okinawa 903-0213, JAPAN

Abstract: The Kikuzato's brook snake, Opisthotropis kikuzatoi, is a highly endangered aquatic or semiaquatic endemic to Kumejima Island of the Okinawa Group, Ryukyu Archipelago. Field studies were carried out for some ecological aspects of this species by visiting its almost every month from April 1996 to March 1997. The results demonstrate that the snake is active almost throughout the year. It is also suggested that the snake tends to be diurnal in the warmer season, and nocturnal in the cooler season. Observations on a case of autonomous emergence onto the land, very slow growth, and predation on small crabs, are also provided.

Key words: Opisthotropis kikuzatoi, Field census; Activity pattern; Body temper- ature; Kumejima Island

INTRODUCTION broadleaf evergreen forest: see below), led Environment Agency of Japan assign O. The Kikuzato's brook snake Opisthotropis kikuzatoi to the highest Red List Category kikuzatoi, is a small colubrid species endemic (IA) as one of the two most critically endan- to Kumejima Island of the Okinawa Group, gered of Japan (Matsui, 1991; Ota, Ryukyu Archipelago. Since its original 2000). This snake is also protected by laws of description by Okada and Takara (1958: as a both the National Government of Japan and member of the Liopeltis), no more than the Prefectural Government of Okinawa (Ota, ten individuals have been known to science 2000). (five preserved specimens and other five indi- To the present, very few ecological data, viduals examined and released: Toyama,1983; largely obtained through captive observations, Ota and Mori, 1985; OPBE, 1993). Such an are available for O. kikuzatoi (Ota and Mori, extremely limited distribution and rarity of 1985; Mori and Nakachi,1994: but see OPBE observations, along with apparent progression [1993] for a few field observations). Such a in the reduction and fragmentation of its puta- scarcity of field data obviously makes it diffi- tive habitat (i.e., running waters surrounded by cult to develop effective conservation mea- sures for this critically endangered species. Recently I obtained some ecological data for * Tel: +81-98-895-8937; Fax: +81-98-895-8966; E-mail address: [email protected] 74 Current Herpetol. 23(2) 2004

MATERIALS AND METHODS D611) equipped with glass sensor probe. Each snake captured was sexed by everting Of the ten individuals of Opisthotropis the hemipenes or by examining the external kikuzatoi hitherto reported, all but one were shape of the tail base, and then was subjected found under the water in streams and brooks to examination for snout-vent length (SVL), running on the floor of the evergreen broad- tail length (TL), body weight (BW), and ven- leaf forest (Toyama, 1983; Ota and Mori, tral (VT, sensu Dowling,1951) and subcaudal 1985; OPBE,1993). The other individual was counts (SC). Of these, SVL and TL were also found in a stream in the forest, but with measured to the nearest mm with a tape almost no surface water because of the measure, and BW to the nearest 0.1g with a summer drought (OPBE,1993). I thus fixed a portable electronic balance (Shimazu AXEWB- census course along a middle 350m portion of 35). Stomach contents were examined by pal- one brook, which was located on the border pation and forced regurgitation. For females, between the evergreen broadleaf forest on the oviductal eggs were also examined by palpa- mountain side and open grassy vegetation on tion. Finally the snake was individually marked the lowland side. by ventral clipping and released at the point During the period from April 1996 to March where it was captured. The whole process was 1997, I, together with one or two field assis- completed within 15 min so as not to exhaust tants, visited the site every month but October, the snake through handling. staying there for 24 hours (see Appendix 1 for Even while a captured snake was examined, further details). In each visit, census was the census was also continued as scheduled by carried out every hour from 0600 to 2000 and a field assistant. other than O. every second hour from 2000 to 0600 by slowly kikuzatoi encountered during the census were (ca 10m/min) walking on the lowland side also recorded. along the stream, searching for the both in the water and on the banks. For the RESULTS census at night, a flashlight was used as an aid. At the beginning of each census, water temper- Opisthotropis kikuzatoi was found 11 times ature (measured 10mm below the surface), air during the study period. Snakes were invari- temperature (measured in shade at 1m above ably active, moving on the bottom of the the ground), and water depth were measured stream, when they were first located. In a at a fixed standard point (henceforth referred finding in June, the snake successfully escaped to as SWT, SAT, and SWD, respectively). by suddenly emerging onto the forest side bank When a snake was found, its behavior was and quickly entering dense shrubbery. Of the continuously observed as long as possible. remaining ten findings in which snakes were However, when its escape into vegetation or captured for further examination (see above), other obstacles was likely, the snake was one in the early afternoon of 26 August and captured immediately. After capture, its body another after midnight of March 23 involved temperature (BT) was measured within 30 sec the same individual (Fig. 1). Snakes involved by inserting the sensor probe of an electronic in the remaining eight captures included no thermometer (thermistor) into the cloaca. Water recaptures. temperature (WT: 10mm below the surface) Of the nine individuals examined, four and air temperature (AT: in shade, 1m above (captured in July, August and March, Septem- the ground) were also measured at the point ber, and December) were males, and the where the snake was located at capture. All remaining five (April, July, September, Novem- temperature measurements (including SWT, ber, and December) were females. Data for SAT and SWD) were taken to the nearest quantitative external characters of these speci- 0.1 C using thermistor (Takara Digimulti mens were combined with data from previous OTA-FIELD OBSERVATIONS OF ENDANGERED SNAKE 75

FIG. 1. Times of day at which Opisthotropis kikuzatoi were found. Stippled area represents the extent of night (i. e., from sunset to the next sunrise) in each survey period (24h). The horizontal bar denotes dura- tion of observation of a given individual after its initial detection. Arrows indicate data from the same recap- tured individual.

TABLE 1. Morphological characters (x±SD, followed by ranges in parentheses) of male and female Opisthotropis kikuzatoi. Data from the present and previous studies (i. e., Toyama, 1983; Ota and Mori, 1985; OPBE,1993) are incorporated.

studies (Toyama, 1983; Ota and Mori, 1985; 31-75mm (Appendix 1), whereas WT, AT, OPBE, 1993) and were compared between and WD at capture (x±SD, followed by sexes (Table 1). In all these characters (SVL, ranges in parentheses) were 22.7±4.05 (16.4- TL, VT, and SC), no statistically significant 28.5)C,23.7±6.43(14.5-31.1)C, and 34.0± differences were recognized between males 29.73(11-105)mm, respectively. BT of the and females (ANOVA, P>0.05). SVL and BW snake at capture,24.7±5.21(16.4-29.2)C, of the recaptured male were, respectively, was significantly correlated with both WT 354mm and 9.2g at initial capture, and (r2=0.895, t=10.32, P<0.001) and AT (r2= 357mm and 9.1g at recapture, showing no 0.857, t=9.93, P<0.001). BT was almost discernible growth during the period of nearly consistently higher than WT, and also substan- seven months. tially exceeded AT when AT was equivalent to The time of day at which the snakes were or lower than 26.2 C. In contrast, BT was dis- found varied from 0200 to 1405. From April tinctly lower than AT when AT was 30.0 C or to August all snakes were found from late higher (Fig. 2). Regression lines for WT and morning to early afternoon, whereas all BT during the warmer (i.e., April-September) findings but one (for a female found at 0905 and cooler seasons (November-March: see of 24 November) were made between midnight Appendix 1), BT= 0.215*WT+22.98 (n=6, and sunrise during the period from September r2=0.60, t=2.44, P<0.05) and BT=1.397* to March (Fig. 1). WT-6.73 (n=4, r2= 0.98, t=9.48, P<0.05), SWT, SAT, and SWD in the present study respectively, significantly differed from each varied from 16.3-27.2 C, 12.7-32.0 C, and other in slope (ANCOVA: F=55.6, P<0.001), 76 Current Herpetol. 23(2) 2004

ing some more or less aquatic species (e.g., Mushinsky et al [1980], Shine and Lambeck [1985], and other papers cited in Gibbons and Semlitsch [1987]). Most such studies are about species in almost aseasonal tropics, or at much higher latitudes where low temperatures have crucial effects upon the winter activity of ecto- therms by forcing them into hibernation. In contrast, very little information is available regarding snakes in the subtropical regions (including the Ryukyu Archipelago), where seasonal climatic changes are prominent on the one hand, but winter temperature is not neces- sarily so low as to force ectotherms into hiber- nation on the other hand (e.g., Koba, 1962; Ota, 1994; Mori et al., 2002). The present results suggest that Opisthotropis kikuzatoi FIG. 2. Body temperatures of O. kikuzatoi (BT) remains active almost throughout the year in relation to water temperatures (WT) at capture. Open circles represent data obtained in the daytime, (Fig. 1), although the failure in finding even a and closed circles at night. Arrows indicate data single snake in the January and February from the same recaptured individual. Vertical bars surveys may reflect a drop in its activity during denote the differences of BT from air temperatures the middle-late winter when ambient tempera- (AT) at capture. The solid line shows the location tures are lowest (Appendix 1). of BT=WT. The dotted line and dashed line repre- With respect to the daily activity pattern, sent regression lines for data obtained in the several studies have also been conducted for warmer (i. e., April-September, n=6) and the cooler aquatic snakes, leading to recognition of a few seasons (November-March, n=4), respectively. See distinct patterns. Shine and Lambeck (1985), text for their equations. for example, clarified that the tropical acro- chordid species, Acrochordus arafurae, is but not in position (F=3.56, P>0.05). primarily nocturnal, whereas Voris and Karns Of the total of ten snakes examined (count- (1996) and Karns et al. (2001) demonstrated ing the recaptured male in duplicate), only one that two tropical homalopsines, Enhydris male, captured at 04:00 of 22 December plumbea and E. enhydris, are active both day (BT=17.2 C, WT=17.6 C, AT= 14.6 C, and and night. For the genus Opisthotropis, sev- WD = 38mm), had stomach contents, which eral Chinese and Southeast Asian species, consisted of three half-digested juveniles of the such as O. andersoni, O. kuatunensis, O. freshwater crab, Candidiopotamon kumeji- lateralis, O. latouchii, and O. typica, are mense. In the study area, freshwater crabs of implicitly or explicitly referred to as nocturnal, comparable sizes were seen in relatively high whereas O. baleatus as diurnal (Pope, 1935; density from May to September, and in Zhong,1984; Karsen et al., 1986; Mori,1993; distinctly lower density from November to Zhao et al., 1998). It is, however, almost April (Appendix 2). For the five females, no certain that all these statements were made on oviductal eggs were detected by palpation. the basis of limited observations and thus are rather anecdotal. Only Mori and Nakachi DISCUSSION (1994) attempted a quantitative approach to the daily activity pattern of the genus by video- A number of studies has been carried out on recording and analyzing activities for two the seasonal activity patterns in snakes includ- female O. kikuzatoi in captivity. The results OTA-FIELD OBSERVATIONS OF ENDANGERED SNAKE 77 indicated that both females were most active in BT of O. kikuzatoi in the warmer season, the morning and least so at night, and these mostly distinctly higher than WT irrespective authors thus suspected this species to be pri- of time of day at capture but with a less steep marily diurnal unlike many other congeneric slope of the regression line, suggest the snake's species (see above). motive thermoregulation, presumably by use In the present study, however, five out of 11 of both sunlight (day) and heated ground observations of active snakes were made at surface (night). Also, the position of the night, although the remainder were in the regression line suggests that the snake prefers daytime. Furthermore, one male, found active 29-30 C as an active body temperature (Fig. in the daytime at first capture, was recaptured 2). Further studies are needed to verify each after midnight (Fig. 1). These suggest that the of the issues assumed above. daily activity pattern of O. kikuzatoi is more variable than was assumed by Mori and ACKNOWLEDGMENTS Nakachi (1994). Considering that captive observation by Mori and Nakachi (1994) was I thank Masaru Horigami and Noriaki conducted from July to August, such an incon- Sakaguchi of the Environment Agency of sistency between their result and the present Japan (EM,=Japan Ministry of Environment observation may actually reflect seasonal vari- at present) for the budget arrangement for this ation in daily activity in this species. study as a part of EAJ's Research Project on Mori and Nakachi (1994) also reported that the Current Status of Endengered Wildlife of in the morning the two captive O. kikuzatoi Japan. Special thanks are due Masaru were frequently active on the land portion in Horigami, Akiko Ito, Setsuko Iwanaga, Mika an otherwise water-filled cage. Observation of Ota, Noriaki Sakaguchi, Ayako Shima, and a snake escaping into the land vegetation in Ken Takahashi for helping with the field June (see above) confirms that O. kikuzatoi work on Kumejima Island. Constructive criti- occasionally autonomously emerges from cisms from two anonymous reviewers greatly water and utilizes the land habitat. improved the manuscript. Data analyses and Mushinsky et al. (1980) reported that some manuscript preparation were supported by a semiaquatic natricine snakes in a warm tem- Grant-in-Aid to the 21st Century COE Project perate area of the southern US tend to be at the University of the Ryukyus from the nocturnal in summer and diurnal in winter. Japan Ministry of Education, Sports, Culture, Such a pattern of seasonal variation in daily and Science (Monbusho). activity is also reported for a number of other As is mentioned in the text, handling of temperate snakes, and is usually explained on Opisthotropis kikuzatoi is strictly regulated by the ground of behavioral adaptation to the the laws of the Japanase National Govern- seasonally varying thermal environment ment and of the Okinawa Prefectural Govern- (Mushinsky et al., 1980; Gibbons and Seml- ment. This research was carried out under itsch, 1987; Peterson et al., 1993). In this official permissions from these governments. regard, the daily activity pattern of O. kikuza- toi, tending to be nocturnal in the cooler LITERATURE CITED season and diurnal in the warmer season, looks puzzling (Figs. 1 and 2). Other factors, DOWLING, H. G. 1951. A proposed standard such as seasonally varying patterns of food system of counting ventrals in snakes. Brit. J. availability, mating intensity, and predation Herpetol. 1: 97-99. pressure, may be responsible for such an GIBBONS, J. W. AND R. D. SEMLITSCH. 1987. apparently paradoxical pattern (see Gibbons Activity patterns. p. 396-421. In: R. A. Seigel, J. and Semlitch [1987] for review of factors T. Collins, and S. S. Novak (eds.), Snakes: affecting activity patterns in snakes). Ecology and Evolutionary Biology. MacMillan 78 Current Herpetol. 23(2) 2004

Publ. Co., New York. servation. Survey Reports on Natural Monu- KARNS,D. R., H. K. VORIS,T. CHAN-ARD,J. C. ments of Okinawa Prefecture. No. 33. Okinawa GOODWIN,AND J. C. MURPHY. 2001. The Predectural Board of Education, Naha. (in spatial ecology of the rainbow water snake, Japanese) Enhydris enhydris (Homalopsinae) in southern OTA, H. 1994. Female reproductive cycles in the Thailand. Herpetol. Nat. Hist. 7: 97-115. northernmost populations of the two gekkonid KARSEN,S. J., M. W. LAU,AND A. BOGADEK.1986. lizards, Hemidactylus frenatus and Lepidodac- Hong Kong Amphibians and Reptiles. Urban tylus lugubris. Ecol. Res. 9:121-130. Council, Hong Kong. OTA, H. 2000. Kikuzato's brook snake, Opistho- KOBA,K. 1962. Studies on the Snakes of the Genus tropis kikuzatoi. p. 24-25. In: Japan Wildlife Trimeresurus of the Amami and Tokara Islands, Research Center (ed.), Revised Red Data Book Japan. Japan Society for the Promotion of of Japan. Amphibians and Reptiles. Environ- Science, Tokyo. (in Japanese with English ment Agency of Japan, Tokyo. (in Japanese with summary) English summary) MATSUI, M. 1991. Kikuzato's brook snake, OTA, H. AND A. MORI. 1985. On the fourth Opisthotropis kikuzatoi. p. 224-225. In: Nature specimen of Opisthotropis kikuzatoi. Snake 17: Conservation Bureau, Japan Agency of Envi- 160-162. ronment (ed.), the Threatened Wild Animals of PETERSON, C. R., A. R. GIBSON, AND M. E. Japan (), the Red Data Book. Japan DORCAS. 1993. Snake thermal ecology: the Wildlife Research Center, Tokyo. (in Japanese) causes and consequences of body-temperature MORI, A. 1993. A note on the sidewinding locomo- variation. p. 241-314. In: R. A. Seigel and J. T. tion in two colubrid snakes, Opisthotropis Collins (eds.), Snakes: Ecology and Behavior. typical and Pseudoxenodon macrops. Snake 25: McGraw-Hill, New York. 67-70. POPE, C. H. 1935. The Reptiles of China. Natural MORI, A. AND A. NAKACHI. 1994. Laboratory History of Central Asia, X. American Museum observations on the daily activity of the endan- of Natural History, New York. gered stream snake, Opisthotropis kikuzatoi SHINE,R. ANDR. LAMBECK.1985.A radiotelemetric (Reptilia, Squamata, Colubridae) from Kume- study of movements, thermoregulation and habitat jima Island, Japan. Isl. Stud. Okinawa 12: 25-35. utilization of Arafura filesnakes (Serpentes: Acro- MORI, A., M. TODA, AND H. OTA. 2002. Winter chordidae). Herpetologica 41: 351-361. activity of the hime-habu ( okinavensis) TOYAMA,M. 1983. Taxonomic reassignment of the in the humid subtropics: foraging on breeding colubrid snakes, Opheodrys kikuzatoi, from anurans at low temperatures. p. 329-344. In: G. Kume-jima Island, Ryukyu Archipelago. Jpn. J. W. Schuett, M. Hoggren, M. E. Douglass, and Herpetol.10: 33-38. H. W. Greene (eds.), Biology of Vipers. Eagle VORIS,H. K. AND D. R. KARNS. 1996. Habitat Mountain Publ. Co., Utah. utilization, movements, and activity patterns of MUSHINSKY,H. R., J. J. HEBRARD,AND M. G. Enhydris plumbea (Serpentes: Homalopsinae) WALLEY.1980. The role of temperature on the in a rice paddy wetland in Borneo. Herpetol. behavioral and ecological associations of sympa- Nat. Hist. 4:111-126. tric water snakes. Copeia 1980: 744-754. ZHAO,E., M. HUANG,AND Y. ZONG.1998. Fauna OKADA,Y. ANDT. TAKARA.1958. A new species of Sinica. Reptilia, Vol. 3. Squamata. Serpentes. Liopeltis (Ophidia, Colubridae) from Ryukyu Science Press, Beijing. (in Chinese) Islands. Bull. Biogeogr. Soc. Japan 20(3): 1-3. ZHONG, C. 1984. A new record of the snakes of (in Japanese with English resume) Jiangxi province-Opisthotropis kuatunensis OKINAWAPREFECTURAL BOARD OF EDUCATION Pope. Acta Herpetol. Sinica 3: 20. (in Chinese) (OPBE) (ed.) 1993. Kikuzato's Stream Snake (Opisthotropis kikuzatoi): Its Status and Con- OTA-FIELD OBSERVATIONS OF ENDANGERED SNAKE 79 80 Current Herpetol. 23(2) 2004

APPENDIX 2 Other animals observed in the stream during each of the monthly survey. Abbreviations are as follows. D, daytime. N, night. FCL, large freshwater crab. FCS, small freshwater crab. SS, small shrimp. MS, Macro- brachium sp. DL, dragonfly larva. FL, firefly larva. AM, Anguilla marmorata. BJ, Buergeria japonica. MO, Microhyla ornata. RC, Rana catesbeiana. AP, Amphiesma pryeri. +, ten or fewer individuals in maximum per census. + +, more than ten individuals in maximum per census.

Accepted: 15 October 2004