Japanese Journal of Herpetology 14(4): 191-197., Dec. 1992 (C)1992 by The HerpetologicalSociety of Japan

Sexual Difference in Annual Activity and Home Range of the Japanese Pond , japonica, Assessed by Mark-recapture and Radio-tracking Methods

TAKASHI YABE

Abstract: The annual activity and home range of the Japanese pond turtle, Mauremys japonica, were investigated from 1985 to 1990 in the northern part of Mie Prefecture by means of mark-recapture and radio-telemetry. The lived mainly in paddies from May to August when paddies were irrigated. When the irrigation period was over, however, the main habitat of the turtles changed from paddies to brooks and ponds from September to April of the following year. Females were captured more fre- quently than males in the irrigation period, whereas males were found more frequently in the non-irrigation period. In the mating season, mainly from September to April, males walked around more frequently and were active at lower water temperature than females. The mean home range size in the brook was estimated to be 99m in males and 40m in females by means of radio-tracking, and 71m in males and 47m in females by mark recapture. The higher activity and larger home range of males during the period from fall to spring of the following year are attributed to active searching for sta- tionary females by males. Key words: Mauremys japonica; Mating behavior; Annual activity; Home range; Radio-telemetry

Morreale et al. (1984) pointed out that the time. Especially there has been no report on the relative activity levels of males and females mating behavior of M. japonica, because it is through the year changed according to differen- very difficult to observe it in the field. tial reproductive activities of the sexes, and they In the present work, the mating season of showed such a change in scripta. M. japonica was confirmed, and the sexual But only a few papers have been published about differences of the annual activity pattern and of the annual change of activity in relation to the home range use during the mating season mating. Some investigators reported the diffe- were examined by means of intensive mark-recap- rences of home range sizes between sexes in ture survey and radio-tracking in the field. I some turtles or (Mahmoud, 1969; Bury, discuss the ecological significance of such 1972; Rose and Judd, 1975; Judd and Rose, differences in relation to sexual activity. 1983; Chase et al., 1989; Schubauer et al., 1990). But the relation between the sexual diffe- MATERIALS AND METHODS rence of the home range sizes and reproduc- Study area.-The study area is located in the tive activity of both sexes is not well known. northern part of Mie Prefecture (Fig. 1). The The Japanese pond turtle, Mauremys japonica area included several brooks, two ponds (A and Temminck et Schlegel ( , sub- B in Fig. 1), and paddy fields. The brooks had family Batagurinae), is distributed in the Hon- many underwater holes made by erosion. The shu, Shikoku, and Kyushu Islands of Japan (Ern- depth of the brook water was less than 40cm st and Barbour, 1989) and lives in streams or and the width less than 3m, except for point C ponds at the foot of mountains. In a previous in Fig. 1, where the water depth was 1m or paper (Yabe, 1989), I reported the population deeper. Running water was clear. The water structure and the sexual dimorphism in body size surface of the brook was shaded by the leaves of of M. japonica in an area of the northern part of plants growing on the banks during summer. Mie Prefecture where the present study was also Pond A was 60m in diameter and surrounded by conducted, but the life history of this in woods. Pond B was an artificial dam with a the field was not thoroughly ascertained at that length of 70m and a maximum width of 20m. Paddy fields were generally irrigated only during Accepted 12 Oct. 1992 the period from May to August each year. The 192 Jpn. J. Herpetol. 14 (4). 1992

ed: time, location, microhabitat, behavior, weather conditions, individual code, sex, and age. Carapace length (CL) and plastron length, body weight, and water temperature were also measured. Body size at sexual maturity was estimated at 80mm in CL for males and 150mm in CL for females, because the minimum size of the male which performed courtship in the field was 81.3mm in CL, and because that of the female containing eggs in the examination by X- ray photographs (Yabe, unpubl. data) was 151.8mm in CL. The location of the capture point was recorded on a 1:2500 map. When a turtle was found during patrol, its behavior was carefully observed and recorded before capture, especially mating, walking, and hiding in the water. Radio-telemetry.-Radio-trackings were con- ducted from October 1989 to January 1990 in to examine the home ranges of the FIG. 1. A map showing the study area encircled by turtles. Eight mature males and eight mature a dashed line. Shaded areas are paddies, black females were fitted with a small radio tag triangle a mountain top, "C" the place in the brook weighing 7 to 8g (equivalent to 3 to 5% of male deeper than 1m, and the large arrow the direction of body weight and about 1% of female weight) on water current. the anterior marginal scutes. The location of the radio-tagged turtles was detected with a turtle population of the study area was isolated hand-held, two-element unidirectional Yagi from the others (Yabe, 1989). antenna or a bidirectional loop antenna. The Mark-recapture survey. -Mark-recaptures were located about 14 times a month. were conducted 220 times from May 1985 to Home range.-In this paper the home range December 1990. Following a previously arrang- in the brooks during the non-irrigation period is ed plan, I systematically walked through the analyzed, but not that in the ponds during the study area and captured turtles by hand or with a non-irrigation period or in the paddy area during dipnet. After measuring and recording the the irrigation period. The home range size was items listed below, the captured turtle was releas- defined as the curvilinear distance between the ed at the point of capture as soon as possible. uppermost and lowest capture points along a The searches in the brooks were conducted brook, as the turtles living in the brooks moved mainly during the non-irrigation period of 7- along the brooks during the non-irrigation 14 times a month. Each search started at 0900 period. In this analysis, the data on those in- or 1000h, and three to six hours were required to dividuals which were captured more than twice patrol all brooks. A fiberscope (OLYMPUS IF per season in the brooks were used. 8D3-20) was sometimes used to examine the in- side of the underwater holes. All brooks were RESULTS divided into many sections by ribbon marks at in- Seasonal change of habitat.-A total of 384 in- tervals of 20m in order to distinguish each sec- dividuals (including 166 males, 184 females, and tion. 34 juveniles were captured and marked during During the irrigation period, all paddy areas the whole study period. The total number of were patrolled 3-5 times a week. A capturing captures during the period of six years was 1585, patrol started at morning (0800-0900h) and ter- except in the radio-tracking experiment. minated at sunset. A round of all paddies re- Turtles were usually found in the paddies in quired 2 days. the period from May to August during which the In order to catch the turtles in ponds, four paddies were irrigated. However, they were baited funnel traps were set in pond A in fall and found only in the brooks and ponds in the spring, and two in pond B. period from September to April of the following Measurements and records.-At each capture, year. The number of individuals which over- the following items were examined and record- wintered in pond A and pond B was 87 (in- YABE-SEXUAL DIFFERENCE IN TURTLE ECOLOGY 193 cluding 30 males, 52 females, and 5 juveniles) and 33 (19 males, 13 females, and 1 juveniles), respectively. These figures were mainly ascer- tained by trap catches. The number of turtles which overwintered in brooks was 186 (including 101 males, 70 females, and 15 juveniles) . The other 78 turtles were captured neither in brooks nor in ponds during the non-irrigation periods . Mating behavior.-In the field, mating took place as follows: 1) a male first tried to take a position in front of a female; 2) facing her, he waved his forelimb several times with his sole FIG. 3. Monthly change of sex ratio of captured turtles. "Males+Females" represents the total outward; 3) his forelimb was waved by turns; 4) number of captures in each month, and "Days" the he went backward when she sometimes stretched total number of days on which mark-recaptures were her neck forward or went ahead and continued conducted in the study period of six years. An waving; 5) he went behind her when she stopped asterisk indicates the months in which captured moving, and mounted her, clasping the edge of number was significantly different between sexes (chi- her carapace with the claws of his hindlimb, and square test, p<0.05). Shaded area is the same as in 6) finally he copulated with her. The entire pro- Fig. 2. cess took place underwater. Sometimes two or three males simultaneously attempted to court a ed when the water temperature was in the range

single female. from 5.5C to 28.7C (Mean±SD=14.2C±5 .3, Courtship behavior was mainly observed from N of observations=33). September to April of the following year, except Activity pattern.-Males were captured more January and February during which the water frequently than females during the period from temperature in the daytime was lower than 9.0C September to April of the following year (Fig . (the measured minimum value was 2.3C), the 3). This indicates that males were quite active as coldest period in the year (Fig. 2). The mating compared with females in this period. During behaviors were classified into two categories , the period from May to August, however , the courtships 1 and 2. Courtship 1 indicates the situation was reversed. category where a male chased a female or waved The instances of walking in the water each his forelimb against her. Courtship 2 represents month were more frequent in males than in the category where a male closely faced a females from September to April of the follow- female. This action was one of the phases of ing year (Fig. 4). Since the total number of mating behavior, though chasing or courtship observed individuals was greatly different in each behavior was not observed, because turtles in the month, the vertical axis was expressed by the pro- study area usually lived alone and such an action portion of walking individuals to the total was regarded as a result of male's searching for a numbers of observed individuals. The frequen- female to mate. Courtship behavior was observ-

FIG. 4. A seasonal change in proportion of in- FIG. 2. The monthly change in number of in- dividuals walking in the water to total number of dividuals (male+female) which exhibited mating observed individuals. Solid circles represent males , behavior. Shaded area represents the months in which and hollow ones females. Numbers shown above the turtles lived only in brooks and ponds . For the ex- graph indicate total numbers observed. Shaded area planation of courtship categories 1 and 2, see the text. is the same as in Fig. 2. 194 Jpn. J. Herpetol. 14 (4). 1992

FIG. 5. Relationship between the water tem- perature in the brooks and ponds and the propor- FIG. 6. The home ranges ascertained by radio- tion in number of individuals hiding in the water to tracking of 16 individuals during the period from Oc- total observed individuals. Symbols are same as in tober 1990 to January 1991. Males and females were Fig. 4. shown by solid and hollow circles, respectively. Numbers indicate individual identity codes. cy of walking was significantly different from September to April of the following year bet- the total number of observed individuals. It is ween sexes (x2=19.98, dF=1, p<0.001), but the certain that, when water temperature fell below frequency was not significantly different from 5C, all females hid at the bottom of brooks. May to August (x2=0.04, dF=1, 0.8

TABLE 1. A list of home range sizes in males and females. YABE-SEXUAL DIFFERENCE IN TURTLE ECOLOGY 195 understanding the sexual difference of activity the sexual activity. 2) Differential activity of the pattern in the field. sexes is primarily caused by the different In this study, aggressive or fighting behavior, reproductive processes of the sexes. 3) During which meant the defense or the acquisition of a the mating season, males become more active mate, territory, or food, was not observed. than females because males move frequently in Home range size.-The tracing of radio-tagg- order to increase their opportunities of mating. ed individuals revealed that each individual 4) During the nesting season, activity levels of possessed a distinct home range in the mating females equal or exceed those of males because season. In this study, a home range means the females move frequently in order to find suitable fixed part of a brook used for the habitat of a nesting sites. The pattern of the sex ratio in the given turtle. A Male's home range was general- captures in two populations of T. scripta in- ly larger than the female's when both overlapped vestigated by Morreale et al. (1984) and a popula- on the same part of a brook (Fig. 6). For exam- tion of C. insculpta studied by Carroll and ple, home ranges of males No. 1459 and No. Ehrenfeld (1978) also fitted the model. 0357 were larger than those of females No. 1469 Higher frequency of underwater walking of and No. 49. Home range size varied from 14m males during the period from September to April to 219m in males (Mean±SD=99.3±65.6m, of the following year, higher activity of males at N=8), and from 0m to 91m in females low temperatures, and larger home range of (Mean±SD=39.8±27.8m, N=8: Table 1). males along the brooks were revealed in this The difference in home range size between sexes study. These three tendencies, as well as the was statistically significant (Mann-Whitney U- male-biased sex ratio in captured individuals dur- test; U=13, p=0.05). ing the period from September to April of the The home ranges were also examined by the following year, are also attributed to the fact mark-recapture method. In this case, the mean that males move more frequently than females in size was estimated to be 70.9m in mature males order to increase their chance of encountering (SD=82.4, range=0-625m, N=99) and 46.5m the females. in mature females (SD=59.4, range=0-180m, The frequency of walking behavior in Novem- N=13). The difference between both means ber was larger than was expected. This may be was slightly significant (Mann-Whitney U-test; because walking was frequently observed instead z=1.60, p=0.055). of mating behavior, which was observed less fre- quently than was expected in November. The DISCUSSION proportion of walking in March was smaller It is said that, in mature males of most emydid than was expected. This may be because mating turtles in the temperate zone, courtship behavior was frequently observed instead of behaviors are observable in spring and fall, and walking behavior, most of which was to search possibly even in warm periods during winter for mates. (Gibbons and Greene, 1990). Gasith and Sidis The cloacal temperature, which is equal to the (1985) reported that the mating behavior of body temperature, was the same as the water Mauremys caspica rivulata was observed from temperature in this study when the turtle had September to May of the following year, with a been staying in the water (Yabe, unpubl. data). peak from January to February, the coldest Mauremys japonica was still active even at low period having monthly mean air temperature of water temperatures (3.0C in male and 5.0C in 13C-14C. Similar sexual activity in spring and female) in spite of the fact that the fall was also reported in Clemmys insculpta (Far- generally have a tendency to become inactive at rell and Graham, 1991), Chrysemys picta (Gib- low temperatures due to poikilothermy (Hut- bons, 1968), and T. scripta (Gibbons and chison, 1979 for review). The lowest water Greene, 1990). temperature for male M. japonica, 3.0C, is The pattern of the annual change of the sex lower than that of any other turtle so for examin- ratio in the captures of M. japonica fitted the ed, and that of females, 5.0C, is equal to that of model proposed by Morreale et al. (1984), which serpentina, which has the lowest predicts the relative activity levels of males and temperature among the turtles so far examined females if different reproductive processes of (Hutchison, 1979). According to Gasith and sexes are the primary determinants of differential Sidis (1985), M. caspica rivulata was sexually ac- activity. This model is based on the following tive when the cloacal temperature was 12.0C in assumptions: 1) The annual change of the sex the field and 8.0C in the experimental outdoor ratio in the captures is caused by the difference in tank. In the present study, M. japonica was 196 Jpn. J. Herpetol. 14 (4). 1992 observed to be sexually active even at 5.5C, CHASE,J. D., K. R. DIXON, J. E. GATES,D. JACOBS, which is a lower water temperature than was AND G. J. TAYLOR.1989. Habitat characteristics, described for M. caspica rivulata. population size, and home range of the bog turtle, Clemmys Muhlenbergii, in Maryland. J. Herpetol. Both the mark-recapture method and the 23 (4): 356-362. radio-telemetry were used in the present study to ERNST, C. H. AND R. W. BARBOUR. 1989. Turtles of examine the home range of M. japonica. The the World. Smithson. Inst. Press, Washington, mark-recapture method made it possible to D. C., and London. 313 p. assess the home range in the whole non-irriga- FARRELL,R. F. ANDT. E. GRAHAM.1991. Ecological notes on the turtle Clemmys insculpta in north- tion period and to collect data on the home western New Jersey. J. Herpetol. 25 (1): 1-9. ranges of many individuals, whereas home range GASITH,A. AND I. SIDIS. 1985. Sexual activity in the use of the individuals was observed more exactly terrapin, Mauremys caspica rivulata, in Israel, in by the radio-telemetry than by the mark-recap- relation to the testicular cycle and climatic factors. ture method. As to the home range size, the J. Herpetol. 19 (2): 254-260. assessments by both of the methods showed the GIBBONS,J. W. 1968. Reproductive potential, acti- same result: the males had larger home ranges vity, and cycles in the , Chrysemys than the females. picta. Ecology 49 (3): 399-409. There are many works on the home range of GIBBONS,J. W. AND J. L. GREENE. 1990. Reproduc- tion in the slider and other species of turtles. In: turtles and tortoises, and they showed the home J. W. Gibbons (ed.), Life History and Ecology of range of the male was larger than that of the the Slider Turtle. p. 124-134. Smithson. Inst. female in Clemmys marmorata (Bury, 1972), Press, Washington, D. C., and London. berlandieri (Rose and Judd, 1975; GIBBONS,J. W., J. L. GREENE,AND J. D. CONGDON. Judd and Rose, 1983), Clemmys muhlenbergii 1990. Temporal and spatial movement patterns of (Chase et al., 1989), and T. scripta (Schubauer et sliders and other species. In: J. W. Gibbons (ed.), al., 1990). Although most of the investigators Life History and Ecology of the Slider Turtle. did not consider the relation between reproduc- p. 201-215. Smithson. Inst. Press, Washington, tive activity of sexes and sexual difference in the D. C., and London. home range size, such a tendency as larger home HUTCHISON, V. H. 1979. Thermoregulation. In: Harless, M. and H. Morlock (eds.), Turtles: perspec- range in males should be attributed to males' tives and research. p. 207-228. John Wiley & higher activity of searching for females as is the Sons, Inc., New York. case of M. japonica. Males' higher mobility JUDD, F. W. ANDF. L. ROSE. 1983. Population struc- due to mate searching in M. japonica was ex- ture, density and movements of the Texas pressed as the possession of larger home range in Gopherus berlandieri. Southwestern Naturalist. males than in females, whereas such mobility in 28 (4): 387-398. T. scripta was expressed as the higher frequency MAHMOUD,I. T. 1969. Comparative ecology of the of the extrapopulational movement by males kinosternid turtles of Oklahoma. Southwestern Naturalist. 14: 31-66. (not examined; from (Morreale et al., 1984; Gibbons et al., 1990). Schubauer et al.. 1990) MORREALE,S. J., J. W. GIBBONS,AND J. D. CONGDON. ACKNOWLEDGMENTS.-I would like to express my 1984. Significance of activity and movement in the cordial gratitude to Prof. K. Miyashita and Dr. T. yellow-bellied slider turtle ( scripta). Kusano of Tokyo Metropolitan University for reading Can. J. Zool. 62 (6): 1038-1042. and criticizing this manuscript. I am very grateful to ROSE, F. L. AND F. W. JUDD. 1975. Activity and the other members of the Laboratory of the home range size of the Texas tortoise, Gopherus Ecology of Tokyo Metropolitan University for critical berlandieri, in south Texas. Herpetologica appraisal of this study. I am very thankful to Mr. M. 31 (4): 448-456. Nakane in Kamakura City for supplying the radio- SCHUBAUER,J. P., J. W. GIBBONS,AND J. R. SPOTILA. tags. I am also very thankful to Dr. M. Matsui of 1990. Home range and movement patterns of slider Kyoto University for his advice on this manuscript. turtles inhabiting Par Pond. In: J. W. Gibbons (ed.), Life History and Ecology of the Slider Turtle. LITERATURE CITED p. 223-232. Smithson. Inst. Press, Washington, D. C., and London. BURY, R. B. 1972. Habitat and home range of the YABE, T. 1989. Population structure and growth of Pacific pond turtle, Clemmys marmorata, in a the Japanese pond turtle, Mauremys japonica. stream community. Ph. D. dissertation. University Jpn. J. Herpetol. 13(1): 7-9 of California, Berkeley. (not examined; from Schubauer et al., 1990) CARROLL, T. E. AND D. W. EHRENFELD. 1978. In- Department of Biology, Faculty of Science, termediate-range homing in the wood turtle, Clem- Tokyo Metropolitan University, Minami-Osawa mys insculpta. Copeia 1978 (1): 117-126. 1-1, Hachioji-Shi, Tokyo, 192-03 JAPAN YABE-SEXUAL DIFFERENCE IN TURTLE ECOLOGY 197

要 旨 標識再捕法 および ラジオテ レメ トリー に よ って調 べたニホンイシガメMauremys japonicaの 活動性 の季節変化 と行動圏 の 性差 について 矢部 隆 1985年 か ら1990年 にかけ て,三 重県桑名郡多 回以上捕獲 できた成熟個体 につ いては雄71m, 度 町 の 一 画 に お い て,ニ ホ ン イ シ ガ メ 雌47mで あ り,電 波発 信器装着個体 では雄 Mauremys japonicaの 行動を調べた.捕 獲率は, 99m,雌40mで あ った.求 愛 ・交尾行動が1 夏には雌 の方が高 いが,秋 か ら翌年 の春 にかけ 月 と2月 を除 いた秋か ら翌年 の春に高い頻度で ては雄 の方が高 く,水 中において歩行行動が観 観察 され たので,雄 の方が秋か ら翌年 の春にか 察 され る割合 も秋か ら翌年 の春にかけ ては雄 の け て活動的 な理 由は,交 尾相手を探策す ること 方 が高か った.ま た低水温下 におけ る活動性 も である と考 えられ る. 雄 の方が高か った.調 査地のイ シガメは,秋 か ら春 までを谷川,あ るいは池 で過 ご していた. (192-03東 京 都八 王子市 南大 沢1-1東 京 都 谷 川 の 平 均 利 用 長 は,標 識 再 捕 調 査 で2 立大学理学部生物学科)