Home Range and Movements of Rhabdophis Tigrinus in a Title Mountain Habitat of Kyoto, Japan

Home Range and Movements of Rhabdophis tigrinus in a Title Mountain Habitat of Kyoto, Japan

Author(s) Kojima, Yosuke; Mori, Akira

Citation Current Herpetology (2014), 33(1): 8-20

Issue Date 2014-02

URL http://hdl.handle.net/2433/199666

Type Journal Article

Textversion publisher

Kyoto University Home Range and Movements of Rhabdophis tigrinus in a Mountain Habitat of Kyoto, Japan Author(s): Yosuke Kojima and Akira Mori Source: Current Herpetology, 33(1):8-20. Published By: The Herpetological Society of Japan DOI: http://dx.doi.org/10.5358/hsj.33.8 URL: http://www.bioone.org/doi/full/10.5358/hsj.33.8

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Current Herpetology 33(1): 8–20, February 2014 doi 10.5358/hsj.33.8 © 2014 by The Herpetological Society of Japan

Home Range and Movements of Rhabdophis tigrinus in a Mountain Habitat of Kyoto, Japan

YǄǈǊǁƻ KOJIMA* Ƶǃƺ AǁƿǇƵ MORI

Department of Zoology, Graduate School of Science, Kyoto University, Sakyo, Kyoto 606–8502, JAPAN

Abstract: We conducted a radio-tracking study on Rhabdophis tigrinus to assess its spatial ecology in the Ashiu Forest Research Station, Kyoto, Japan from 2009 to 2010. The study site is located in a temperate mountain area and includes forests, grasslands, a river, open riverbanks, and small brooks. We estimated the width and area of home ranges for 11 and 10 individuals, respectively. Home range size showed a large individual variation, with home range width ranging from 97 to 997 m and area ranging from 1.3 to 11.0 ha. 4BAFAKLQÖKAL?SFLRPPBUR>IAF÷BOBK@BPLOB÷B@QPLC?LAVPFWBLKELJB range size. Tracked snakes tended to aggregate in riverside areas in spring, although females were sometimes found away from the river. Compared to spring, snakes in summer and fall were relatively dispersed and more likely to be located in brookside areas or places apart from water bodies. Eight individuals moved from riverside areas to brookside areas in summer. We located hibernation sites of nine individuals. Before hibernation, four individuals moved to a mountain ridge or a steep rocky slope where snakes were KBSBOCLRKAFKT>OJBOPB>PLKP TEBOB>PQEBLQEBOÖSBFKAFSFAR>IPEF?BOK>QBA TFQEFKQEBFOT>OJ PB>PLKELJBO>KDB +BFQEBOPBUKLO?LAVPFWBPBBJBAQL be related to the occurrence of migratory movements in summer and before hibernation. Previous studies based on visual surveys have suggested bimodal seasonal activity of R. tigrinus, with peaks in spring and fall. However, activity of the tracked snakes in our study did not decrease in summer compared to that in spring, suggesting underestimation of summer activity in the visual survey method. Our results suggest that R. tigrinus migrates to use AF÷BOBKQE>?FQ>QP>JLKDPB>PLKP >IQELRDEQEBOBFPFKAFSFAR>IS>OF>QFLKFK migratory behavior.

Key words: Space use; Seasonal migration; Hibernation site; Radiotelemetry; Snakes; Colubridae

IǃǉǇǄƺǊƹǉƿǄǃ @MHL@KRQDìDBSRL@MX@RODBSRNESGDHQDBNKNFX @MC G@R HLONQS@MS BNMRDPTDMBDR ENQ ëSMDRR Spatial pattern and movements of mobile 'NKS (M RM@JDR E@BSNQR @ðDBSHMF movement include physiological requirements * Corresponding author. Tel: +81–75–753–4076; SNëMCKNB@SHNMRENQSGDQLNQDFTK@SHNM'TDX Fax: +81–75–753–4075; et al., 1989; Whitaker and Shine, 2002, 2003). E-mail address: [email protected] Many snake species move long distances KOJIMA & MORI—HOME RANGE AND MOVEMENTS OF SNAKE 9 between hibernacula and warm-season home nuchal glands, under the skin surface of its ranges before and after hibernation (Gregory, neck region (Nakamura, 1935). Recent studies 1982). Food acquisition is another important using chemical analyses have demonstrated its factor. Short-term aggregation and seasonal highly unusual chemical defensive system migration to areas with high prey density is related to these glands (Hutchinson et al., known in snakes, and thus spatiotemporal 2007, 2008, 2012; Mori et al., 2012). CHRSQHATSHNMNEOQDXG@R@RSQNMFHMìTDMBDNM #DROHSDSGDBNMRHCDQ@AKDRBHDMSHëB@SSDMSHNM snake movement pattern (Arnold and Wassersug, that has been paid to R. tigrinus, information 1978; Gregory et al., 1987; Madsen and Shine, on its spatial ecology is relatively scarce. 1996). Reproductive activities are also known Fukada (1992) showed its monthly abundance SN@ðDBSLNUDLDMS %NQDW@LOKD L@KDRNE and spatial distribution in an agricultural many snake species increase movements dur- habitat, and Moriguchi and Naito (1983) ing the mating season, presumably to search reported movement distances obtained by a for mates (Reinert and Zappalorti, 1988; mark-recapture method in a similar habitat. Secor, 1994; Duvall and Schuett, 1997). However, individual movement patterns and Female snakes often travel long distance to space usage have remained unexplored because reach oviposition sites (Parker and Brown, snakes in those studies were not individually 1972; Madsen, 1984). followed. Furthermore, no studies have been Rhabdophis tigrinus (Colubridae: Natricinae) conducted in relatively undisturbed natural is one of the most common snakes in Japan, habitats. In the present study, we used radio- being found in a variety of habitats from for- telemetry to investigate the spatial pattern ests to agricultural lands (Mishima et al., and movements of free-ranging R. tigrinus 1978; Moriguchi, 1982; Fukada, 1992). Thus, throughout the year in a mountain habitat of R. tigrinus is one of the most well-known *XNSN 2ODBHëB@KKX VD@SSDLOSDCSNDRSHL@SD snake species in Japan. Fukada (1992) sum- home range size, describe seasonal movement marized data on many aspects of its natural patterns of individual snakes in a natural history, such as abundance, food habits, hiber- G@AHS@S @MC DWOKNQD ONRRHAKD RDWT@K CHðDQ- nation, and growth. His study also described ences in space usage and movement. the seasonality of reproductive activities: Mating occurs mainly in fall (from October to MƵǉƻǇƿƵǂǈ Ƶǃƺ MƻǉƾǄƺǈ November) and also in spring (from April to June); Oviposition takes place from late June Study site to mid-August. Several studies have reported This study was conducted in the Ashiu Forest a bimodal peak in encounter rate of R. tigrinus, Research Station of the Field Science Education with one peak in spring and the other in fall, and Research Center, Kyoto University (35°18'N, suggesting bimodal seasonal activity (Fukada, 135°43'E), Japan. The altitude of the study 1958; Moriguchi, 1982; Moriguchi and Naito, area ranges from 355 to 725 m. Air tempera- 1982; Kadowaki, 1996). Diets of R. tigrinus ture of the study site is lowest in January (the in nature have been reported in many articles, average air temperature is 0C), and highest and they have shown that R. tigrinus mainly in August (the average air temperature is feeds on anurans (e.g., Uchida and Imaizumi, 25C). The ground is usually covered with 1939; Moriguchi and Naito, 1982). Extensive snow from early December until late April. behavioral studies have also been conducted, Maximum snow depth exceeds 2 m. The Yura especially regarding prey-handling behavior River runs across the study site, and many (e.g., Mori, 1997, 2006) and anti-predator RL@KKAQNNJRìNVHMSNSGDQHUDQ%HF 3GD behavior (e.g., Mutoh, 1983; Mori et al., 1996). study site is hilly terrain, and most areas are An early anatomical study showed that R. covered with dense forest consisting mainly of tigrinus possesses unusual structures, called Aesculus turbinata, Pterocarya rhoifolia, 10 Current Herpetol. 33(1) 2014

mistakenly released at a point 530 m away from their original capture points. Nonetheless, they voluntarily returned to a site near their respective original capture points in 32 days. After releasing snakes, we tried to locate each individual during the daytime approxi- mately once a week until October. Whenever possible, the exact positions of the snakes were BNMëQLDCUHRT@KKX 6GDMQ@CHNRHFM@KRVDQD coming out of a clump of vegetation, we recorded the approximate position of the snake within the vegetation. We always attempted to Fƿƽ. 1. Map of the study site. Black line and bold KNB@SDRM@JDR@S@RTîBHDMSCHRS@MBDSN@UNHC gray lines represent the Yura River (note that the disturbance. Coordinates of the locations were QHUDQHRRGNVMHMFQ@XHMSGDRTARDPTDMSëFTQDR@MC taken with a GPS (model 60CSx Garmin Int.). brooks, respectively. Dotted black line: trail. Narrow When we found a snake hiding deep under the gray lines: contour lines at intervals of 10 m. Black ground in November, we terminated tracking bar: scale of 100 m. of that individual for the year, recording that it had started to hibernate. We resumed Quercus cripula, Q. salicina and coniferous tracking the snakes in mid-April of the follow- plantations (mostly Cryptomeria japonica). ing year. Grasslands dominated by Miscanthus and PhragmitesFQ@RRDR@QDRB@SSDQDCHMNODMì@S Data analysis areas along the bank of the river. There is a The home range of each snake was estimated RL@KKO@CCXëDKCB@ G@@CI@BDMSSNSGD by the minimum convex polygon method. We river and a small trail along the river. determined width and area of home ranges for individuals that were relocated more than ten Radiotelemetry @MCëUDSHLDR QDRODBSHUDKX 6DCHCMNSDRSH- We walked through the study site mainly mate home range size for ID Nos. 1 and 5 (see along the trail, the river, and the brooks in above). Home range widths were measured on June 2009 and from May to June 2010 to col- ArcMap 9 (ESRI, Redlands, CA). Home range lect R. tigrinus for radiotelemetry. We areas were calculated using the Animal searched for snakes visually and collected Movement extension (Hooge and Eichenlaub, them by hand. Additionally, a female (ID No. 2000) for ArcGIS. 10) and three males (ID Nos. 16, 18, and 21) 2D@RNMRVDQDCDëMDC@RVHMSDQ-NUDLADQ were collected in April 2010 near the hiberna- to April), spring (May and June), summer tion sites of tracked snakes (see Results). We (July and August), and fall (September and surgically implanted radio-transmitters (Holohil, October). We estimated 50 and 95 percent SB-2, 5 g) in 11 females and 13 males, all of utilization distributions of tracked snakes in which had body masses greater than 50 g (for each season using the Kernel method. The surgical methods, see Reinert and Cundall, Home Range Tools extension for ArcGIS 1982 and Nishimura et al., 1995). All females (Rodgers et al., 2007) was used for Kernel used for radiotelemetry were gravid in the density estimation. The smoothing parameter gestation season (from May to mid-July). h was calculated with the reference bandwidth After a three- to ten-day recovery period from method (href) in Home Range Tools. surgery (average 6.8 days), the snakes were 6DCDëMDCLNUDLDMSCHRS@MBD@RSGDCHRS@MBD released at their initial site of capture, except between two consecutive locations. Movement for ID Nos. 1 and 5. These individuals were distances were measured on ArcMap 9 (ESRI, KOJIMA & MORI—HOME RANGE AND MOVEMENTS OF SNAKE 11

Redlands, CA). We excluded data from the locations of males in spring were less than analysis when the interval between two con- 50 m from the river. Females also mainly used secutive locations was less than 5 days or more riverside areas, but in six of 43 (14%) locations than 15 days. We also excluded movement females were located at places more than 50 m C@S@ NE (# -NR @MC CTQHMF SGD ëQRS (up to 290 m) from the river. Four tracked days following their release (see above). There females were found in such habitat in spring. V@RMNRHFMHëB@MSBNQQDK@SHNMADSVDDMHMSDQU@K For example, female ID No. 3 moved from a of locations and movement distance in the riverside area to a brookside area in early June data used for this analysis (Spearman’s corre- and moved back to the riverside area by late lation test, r=0.13, P=0.22). June (see Fig. 6A below). In summer and fall,

RƻǈǊǂǉǈ We recorded a total of 198 locations for 24 snakes. Tracking duration ranged from 2 to 396 days (average 147 days), and the number of relocations for individual snakes ranged from 1 to 24 times (average 9.0 times). Thirteen HMCHUHCT@KRVDQDQDKNB@SDCKDRRSG@MëUDSHLDR because of the death of the snake (n=2) or loss of radio signals. Accordingly, we estimated the width and area of home ranges for 11 and 10 individuals, respectively. The width and area of home ranges ranged from 97 to 997 m and from 1.3 to 11.0 ha, respectively. We did Fƿƽ. 2. Home ranges (minimum convex polygon) MNSëMCNAUHNTRDðDBSRNERDWNQANCXRHYDNM of 10 tracked snakes (ID Nos. 3, 4, 6, 10, 12, 13 14, home range size (Table 1). Home ranges were 17, 18, 20). Solid and dotted polygons are home largely overlapping both within and between ranges of females and males, respectively. Narrow sexes (Fig. 2). In spring, snakes predomi- gray lines: contour lines at intervals of 10 m. Black nantly used riverside areas (Fig. 3A). All 34 bar: scale of 100 m.

TƵƸǂƻ 1. Summary data and home range of 13 Rhabdophis tigrinus tracked by radiotelemetry. ID: iden- SHëB@SHNMMTLADQ 25+RMNTS UDMSKDMFSG

25+ Tracking Number of Home range Home range ID Sex (mm) Tracking period days relocations width (m) area (ha) 3 F 702 19 Jun 2009 – 20 Jul 2010 396 18 394 6.3 4 F 745 9 Oct 2009 – 17 Jun 2010 251 13 505 2.1 5 F 750 17 Jun 2010 – 4 Nov 2010 140 12 — — 6 F 754 19 Jun 2009 – 5 Jul 2010 381 28 923 11.0 10 F 834 29 Apr 2010 – 5 Aug 2010 98 10 637 6.0 12 M 540 24 Jun 2009 – 17 Jun 2010 358 11 607 11.0 13 M 560 23 Jun 2009 – 5 May 2010 316 13 97 2.2 14 M 591 7 Jul 2009 – 16 Sep 2009 71 10 481 2.3 16 M 622 29 Apr 2010 – 5 Aug 2010 98 7 319 — 17 M 625 5 Jun 2010 – 4 Nov 2010 152 14 532 7.7 18 M 676 29 Apr 2010 – 4 Nov 2010 189 9 290 1.3 20 M 681 5 Jun 2010 – 4 Nov 2010 152 12 997 5.9 22 M 709 29 Jul 2009 – 16 Sep 2009 49 6 372 — 12 Current Herpetol. 33(1) 2014

Fƿƽ. 3. Seasonal changes in distribution of tracked snakes. A) spring, B) summer, C) fall, D) winter. White and black dots represent location points of females and males, respectively. Kernel density isopleths of 95% and 50% are outlined in black, and the 95% Kernel density area is colored with gray. Narrow gray lines: contour lines at intervals of 10 m. Black bar: scale of 100 m. both females and males still predominantly and then moved 285 m to a brookside area by used riverside areas, but they were relatively early August (Fig. 4D). The snakes moved dispersed and were more likely to be located vertically at most 130 m during these move- near the brooks or in the middle of the forest ments. The snakes performed these movements away from water bodies (Fig. 3B, C). This irrespective of sex and body size (Fig. 4). resulted in relatively large Kernel density areas We located the hibernation sites of nine in summer and fall compared to those in individuals. Five (three females and two males) spring. hibernated within the area where the snakes Several individuals showed similar patterns spent warmer seasons (Fig. 5). The remaining of seasonal movements. Four females and four individuals (one female and three males) four males showed long distance movements moved before hibernation to an area where from riverside areas to brookside areas at they were never found in warmer seasons some time between late July and August (Fig. (Fig. 6A, C). The maximum distance of these 4). The maximum distance of these move- movements was 380 m. The snakes moved ments was 580 m. For example, ID No. 20 was vertically at most 130 m during these move- located near the river from June to mid-July ments. Neither sex nor body size seemed to be KOJIMA & MORI—HOME RANGE AND MOVEMENTS OF SNAKE 13

Fƿƽ. 4. Movements from riverside to brookside in summer. A) No. 5 (female), B) No. 10 (female), C) No. 18 (male), D) No. 20 (male). Dots represent location points, and large dots are location points near brooks. Consecutive location points are connected with a solid line and an arrow, and large arrows represent movement to brookside areas. Narrow gray lines: contour lines at intervals of 10 m. Black bar: scale of L (#-N V@RQDKD@RDC@S@CHðDQDMSONHMSEQNLHSRNQHFHM@KB@OSTQDONHMSATSLNUDCA@BJSNSGD@QD@ near the capture point in 32 days (19 Jul), after which movement pattern is shown here. related to the occurrence of these movements The distributions of movement distance were (Figs. 5, 6). After emerging from hibernation, right skewed in all seasons (Fig. 7). Snakes three of the four snakes moved back to the exhibited relatively short movements in spring area where they had spent warmer seasons in and winter: distances moved were more than the previous year (we did not continue radio- 50 m in 48% and 21% of observations in tracking for the fourth individual). For exam- ROQHMF@MCVHMSDQ QDRODBSHUDKX +NMFLNUD- ple, ID No. 3 moved 340 m from a riverside ments were relatively common in summer and area to a mountain ridge in mid-October and fall: distance moved was more than 50 m in moved back to the riverside area at the begin- 69% and 76% of observations in summer ning of the next May (Fig. 6A). The hiberna- and fall, respectively. Movement distance did tion sites of the four individuals that migrated not decrease in summer, although previous before or after hibernation were situated on a studies on R. tigrinus have suggested bimodal mountain ridge or a steep rocky slope rising seasonal activity, with summer reduction of from the river, all of which faced south. In activity compared to that of spring and fall. April, we found four additional R. tigrinus in these hibernation sites and started radio- DƿǈƹǊǈǈƿǄǃ tracking them. They moved to riverside areas after release, showing a movement pattern .TQRSTCXOQDRDMSRSGDëQRSQ@CHNSDKDLDSQHB similar to that of their neighbors (Fig. 6B, D). data on Rhabdophis tigrinus. These data 14 Current Herpetol. 33(1) 2014

Fƿƽ. 5. Movement patterns of the tracked snakes that did not migrate before hibernation. A) No. 5 ( female), B) No. 6 (female), C) No. 17 (male), D) No. 20 (male). Dots represent location points, and large dots are hibernation sites. Consecutive location points are connected with a solid line and an arrow. Narrow gray lines: contour lines with at intervals of 10 m. Black bar: scale of 100 m. ID No. 5 was released at a CHðDQDMSONHMSEQNLHSRNQHFHM@KB@OSTQDONHMSATSLNUDCA@BJSNSGD@QD@MD@QSGDB@OSTQDONHMSHMC@XR (19 Jul), after which movement pattern is shown here. showed seasonal migration of R. tigrinus. A our study was not very large, so the home common pattern exists regarding migratory range sizes shown here are likely to have been movements among tracked snakes although underestimated. However, neither home range there was individual variation in occurrence @QD@MNQVHCSGRGNVDC@RHFMHëB@MSBNQQDK@- or absence of migration. Contrary to the sug- tion with the number of relocations (Spearman’s gestion from previous studies, our results correlation test, the former, r=0.43, P=0.28; showed unimodal seasonal activity of R. tigri- the latter, r=0.40, P=0.19). The estimated nus Q@SGDQ SG@M AHLNC@K MNSGDQ ëMCHMF home range size of R. tigrinus was moderate V@R SGD CHðDQDMBDR HM LNUDLDMS O@SSDQM compared to that of other species of snakes between gravid females and males. The (Macartney et al., 1988), although there was following discussion refers to possible causes large variation in both the width and area of of observed pattern in home range, migratory the home range in our study. The relatively movements, seasonal activity, and sexual large home ranges of some R. tigrinus were CHðDQDMBDRHMLNUDLDMS due to their long-range seasonal migrations in In general, home range size estimated by the summer and/or for hibernation. We did not minimum convex polygon method is highly ëMCNAUHNTRDðDBSRNERDWNQANCXRHYDNMSGD dependent on the number of relocations and is pattern of migratory behavior. largely underestimated when sample size is Several snakes in our study moved up to small (Girard et al., 2002). The sample size of 380 m to and from hibernation sites. Migration KOJIMA & MORI—HOME RANGE AND MOVEMENTS OF SNAKE 15

Fƿƽ. 6. Movements before and/or after hibernation. A) No. 3 (female), B) No. 10 (female), C) No. 12 (male), D) No. 16 (male). Dots represent location points, and large dots are hibernation sites. Consecutive location points are connected with a solid line and an arrow, and large arrows represent movement to hibernacula. Narrow gray lines: contour lines at intervals of 10 m. Black bar: scale of 100 m. to and from the hibernation site is a common Kanagawa Prefecture moves greater distances phenomenon among snakes in temperate before and after hibernation compared to regions (Gregory, 1982). The movements per- during warmer seasons. Migration related to formed by R. tigrinus before and after hiber- hibernation might be a common phenomenon nation are likely to be associated with migra- among populations of R. tigrinus. tion between the feeding areas and appropri- The hibernation sites of the individuals that ate hibernation sites. Fukada (1958) investi- migrated before or after hibernation were situ- gated the spatial distribution of R. tigrinus in ated on a mountain ridge or a steep rocky ì@S NODM@FQHBTKSTQ@KK@MCRB@OD@KNMF@QHUDQ slope facing south. Southern exposure is a in Kyoto. He showed that most snakes found common feature of north-temperate hiberna- by visual searching were distributed near the SHNMRHSDRHMRM@JDR@MCOQDRTL@AKXNðDQRSGDQ- hibernacula in April and October but that mal advantages during hibernation or spring snakes were scattered throughout the whole of emergence (Harvey and Weatherhead, 2006). the study area from July to September, sug- On the mountain ridge and the steep rocky gesting aggregation to hibernacula and post- slope, we found several individuals of R. hibernation dispersal. Similarly, based on tigrinus other than the tracked ones in early data obtained from mark-recapture methods, spring. In contrast, we found no other R. Moriguchi and Naito (1983) suggested that R. tigrinus near the hibernation sites of the indi- tigrinus in a riverside agricultural area in viduals that hibernated within their warm- 16 Current Herpetol. 33(1) 2014

Fƿƽ. 7. Histograms of distance moved between two successive locations. A) spring, B) summer, C) fall, D) winter. Black and white parts of columns represent frequency of males and females, respectively. The interval between two successive locations was from 5 to 15 days. season home range. Aggregation at a hiber- in migratory behavior. We do not believe that naculum has been reported in other popula- SGD @ARDMBD NE LHFQ@SHNM V@R SGD DðDBS NE tion of R. tigrinus (Fukada, 1958). These implantation of the transmitter. If implanta- observations may suggest that R. tigrinus SHNM NE SGD SQ@MRLHSSDQ @ðDBSDC SGD RM@JD¥R hibernates in aggregation at favorable hiber- movement, smaller snakes would be expected nacula, like many other snakes in the northern to be more vulnerable to it because their ratio temperate zone (Gregory, 1984; Sexton et of transmitter to body mass is larger, and they al., 1992). would show less tendency to migrate, which Nonetheless, some individuals hibernated was not the case in our study. within the area they used in warmer seasons. In spring, tracked Rhabdophis tigrinus +NMFLNUDLDMSROQDRTL@AKXHMBTQSGDQHRJNE tended to aggregate in the riverside areas. mortality as well as energetic costs (Huey and Possible causes of this aggregation are ther- Pianka, 1981; Gibbons and Semlitsch, 1987). moregulation and/or search for food. Open 3GDQDENQD SGDSQ@CDNðADSVDDMSGDADMDëSRNE G@AHS@S NðDQR HMBQD@RDC RNK@Q Q@CH@SHNM SG@S using a favorable hibernation site and the cost facilitates thermoregulation, and thus snakes of migration might have resulted in variation often prefer such habitat (Reinert, 1993; KOJIMA & MORI—HOME RANGE AND MOVEMENTS OF SNAKE 17

Blouin-Demers and Weatherhead, 2001). Weatherhead and Charland, 1985). In our Open habitat is limited in our study site, where study, the snakes in spring preferentially used terrain is hilly and most of the area is covered open riverside areas where presumably snakes with dense forest. Riverside areas are open are more easily found by visual search, and in and seem to provide favorable basking sites summer they used other habitats, such as for snakes, which might attract snakes emerg- dense forest, more frequently. Thus, a reduc- ing from hibernation. The main food of R. tion in encounter likelihood in summer could tigrinus at the study site is Rhacophorus AD DWOK@HMDC AX CHðDQDMBDR HM CDSDBS@AHKHSX frogs (Mori and Vincent, 2008). These frogs between spring and summer habitats. These @FFQDF@SDHMSGDO@CCXëDKCENQQDOQNCTBSHNM results imply that encounter rate by visual (Kojima, personal observation), and their search is not necessarily a direct indicator of CDMRHSX@QNTMCSGDO@CCXëDKC@MCRTQQNTMC- the activity level of snakes and is likely to be ing riverside areas remarkably increases in HMìTDMBDCAXR@LOKHMFLDSGNCR2DHFDK spring. Quantitative analyses of thermal 6DCHCMNSëMCNAUHNTRRDWT@KCHðDQDMBDR quality and food availability are needed to in either home range size or movement dis- verify the cause of spring aggregation to river- tance. Males of many snake species move side areas. more than females and have larger home In summer, tracked R. tigrinus moved from ranges, presumably due to mate-searching riverside areas to brookside areas. Fukada behavior (Reinert and Zappalorti, 1988; Secor, (1958) suggested that the spatial distribution 1994; Duvall and Schuett, 1997), whereas such of R. tigrinusHR@ðDBSDCAXENNC@U@HK@AHKHSX RDWT@K CHðDQDMBDR @QD MNS ENTMC HM NSGDQ Migration in response to food availability has snakes (Plummer, 1981; Reinert and Kodrich, been suggested in other snakes (e.g., Madsen 1982; Wasko and Sasa, 2009). Rhabdophis and Shine, 1996). Given that food availability tigrinus may be an example of the latter type, for R. tigrinus is highly seasonal (Hirai, 2004; although the number of relocations in our Mori and Vincent, 2008), utilization of habi- RSTCXL@XMNSG@UDADDMRTîBHDMSSNBNMBKTCD tat with high food availability is one possible SG@SSGDQDHRMNRDWT@KCHðDQDMBD explanation for the summer migration. In several species of snakes, females have Further investigation of the relationship been reported to travel rapidly over long dis- between food availability and snake move- tances shortly before egg-laying to reach ovi- ment pattern will be required to test this pos- position sites (Parker and Brown, 1972; sibility. Madsen, 1984). It has also been shown that Bimodal peaks of seasonal activity have gravid female snakes often reduce their move- been suggested in several studies on temperate ments during gestation and remain in a snakes (e.g., Jackson and Franz, 1981; Gibbons restricted area (Shine, 1979; Brown et al., and Semlitsch, 1981, 1987; Dalrymple et al., 1982; Reinert and Kodrich, 1982; Gregory et +DXM@TCDS@K 6HSGQDRODBSSN al. 1987; Charland and Gregory, 1995). Our R. tigrinus, previous studies based on visual study on R. tigrinus RGNVDC CHðDQDMBDR HM surveys have reported bimodal seasonal activ- movement pattern between gravid females ity, with one peak in spring and the other in and males. Gravid females used both riverside fall (Fukada, 1958; Moriguchi, 1982; areas and habitat apart from the river, in con- Moriguchi and Naito, 1982; Kadowaki, 1996). trast to males in the same season, which However, our radio-telemetric data showed remained in the riverside areas. The move- that the movement distance of R. tigrinus ments away from the river are puzzling does not decrease in summer, compared to because females appear to lay eggs in the ROQHMF $MBNTMSDQQ@SDL@XAD@ðDBSDCAXE@B- grassland along the river (Kojima, unpub- SNQR NSGDQ SG@M @BSHUHSX KDUDK RTBG @R CHðDQ- lished data), and thus such movements are ence of observability among habitats (e.g., unlikely to be related to searching for an ovi- 18 Current Herpetol. 33(1) 2014 position site. A detailed investigation of habi- Animal Behaviour 54: 329–334. tat use is required to elucidate why female R. FǊǁƵƺƵ, H. 1958. Biological studies on the tigrinus show such an unusual movement pat- RM@JDR (5 2D@RNM@K OQDU@KDMBD HM SGD ëDKCR tern during gestation. Bulletin of the Kyoto Gakugei University Ser B (15): 25–41, 2 pls. AƹǁǃǄǌǂƻƺƽƻǑƻǃǉǈ FǊǁƵƺƵ, H. 1992. Snake Life History in Kyoto. Impact Shuppankai, Tokyo. 3GHR OQNIDBS V@R ëM@MBH@KKX RTOONQSDC HM GƿƸƸǄǃǈ, J. W. Ƶǃƺ SƻǑǂƿǉǈƹƾ, R. D. 1981. O@QSAX@&Q@MS HM HCENQ2BHDMSHëB1DRD@QBG Terrestrial drift fences with pitfall traps: An ef- C (23570115) and the Global COE Program fective technique for quantitative sampling of (A06) to Kyoto University. We thank H. Ikuri animal populations. Brimleyana 7: 1–16. and other local people at Ashiu for permitting GƿƸƸǄǃǈ, J. W. Ƶǃƺ SƻǑǂƿǉǈƹƾ, R. D. 1987. us to conduct research on their properties. We Activity patterns. p. 396–421. In: R. A. Seigel, J. @QD @KRN HMCDASDC SN SGD RS@ð NE SGD RGHT T. Collins, and S. S. Novak (eds.), Snakes: Forest Research Station for enabling us to Ecology and Evolutionary Biology. Macmillan, conduct this research, and members of our New York. laboratory for assisting this research. Thanks GƿǇƵǇƺ, I., OǊƻǂǂƻǉ, J-P., CǄǊǇǉǄƿǈ, R., to A. Durso and E. Nakajima for proofread- DǊǈǈƵǊǂǉ, C., Ƶǃƺ BǇƻǉǄǃ + $ðDBSRNE HMFNESGHRL@MTRBQHOSENQìTDMBXHM$MFKHRG R@LOKHMF DðNQS A@RDC NM &/2 SDKDLDSQX NM home-range size estimations. The Journal of +ƿǉƻǇƵǉǊǇƻ Cƿǉƻƺ Wildlife Management 66: 1290–1300. GǇƻƽǄǇǎ, P. T. 1982. Reptilian hibernation. p. AǇǃǄǂƺ, S. J. Ƶǃƺ WƵǈǈƻǇǈǊƽ, R. J. 1978. 53–154. In: C. Gans and F. H. Pough (eds.), #HðDQDMSH@KOQDC@SHNMNMLDS@LNQOGHB@MTQ@MR Biology of the Reptilia, Vol. 13: Physiology D. by garter snakes (Thamnophis): Social behavior B@CDLHB/QDRR +NMCNM as a possible defense. Ecology 59: 1014–1022. GǇƻƽǄǇǎ, P. T. 1984. Communal denning in BǂǄǊƿǃ-DƻǑƻǇǈ, G. Ƶǃƺ WƻƵǉƾƻǇƾƻƵƺ, P. J. snakes. p. 57–75. In1 2DHFDK + $ 'TMS ) 2001. Habitat use by black rat snakes (Elaphe + *MHFGS + ,@KDQDS @MC- + 9TRBGK@FDCR obsoleta obsoleta) in fragmented forests. Vertebrate Ecology and Systematics: a Tribute Ecology 82: 2882–2896. to Henry S. Fitch (10). University of Kansas BǇǄǌǃ, W. S., Pǎǂƻ, D. W., GǇƻƻǃƻ, K. R., Ƶǃƺ Museum of Natural History Miscellaneous FǇƿƻƺǂƵƻǃƺƻǇ, J. B. 1982. Movements and /TAKHB@SHNMR +@VQDMBD temperature relationships of timber rattlesnakes GǇƻƽǄǇǎ, P. T., MƵƹƵǇǉǃƻǎ, J. M., Ƶǃƺ+ƵǇǈƻǃ, (Crotalus horridus) in northeastern New York. K. W. 1987. Spatial patterns and movements. p. Journal of Herpetology 16: 151–161. 366–395. In: R. A. Seigel, J. T. Collins, and S. S. CƾƵǇǂƵǃƺ, M. B. Ƶǃƺ GǇƻƽǄǇǎ, P. T. 1995. Novak (eds.), Snakes: Ecology and Evolutionary Movements and habitat use in gravid and non- Biology. Macmillan, New York. gravid female garter snakes (Colubridae: HƵǇǋƻǎ, D. S. Ƶǃƺ WƻƵǉƾƻǇƾƻƵƺ, P. J. 2006. Thamnophis). Journal of Zoology (London) Hibernation site selection by eastern massasau- 236: 543–561. ga rattlesnakes (Sistrurus catenatus catenatus) DƵǂǇǎǑǅǂƻ, G. H., SǉƻƿǃƻǇ, T. M., NǄƺƻǂǂ, R. J., near their northern range limit. Journal of Ƶǃƺ BƻǇǃƵǇƺƿǃǄ, JǇ., F. S. 1991. Seasonal Herpetology 40: 66–73. @BSHUHSX NE SGD RM@JDR NE +NMF /HMD *DX HƿǇƵƿ, T. 2004. Dietary shifts of frog eating Everglades National Park. Copeia 1991: 294– snakes in response to seasonal changes in prey 302. availability. Journal of Herpetology 38: 455– DǊǋƵǂǂ, D. Ƶǃƺ SƹƾǊƻǉǉ, G. W. 1997. Straight- 460. line movement and competitive mate searching HǄǂǉ, R. D. 2003. On the evolutionary ecology of in prairie rattlesnakes, Crotalus virdis viridis. species’ range. Evolutionary Ecology Research KOJIMA & MORI—HOME RANGE AND MOVEMENTS OF SNAKE 19

5: 159–178. Herpetology 22: 61–73. HǄǄƽƻ, P. N. Ƶǃƺ EƿƹƾƻǃǂƵǊƸ, W. M. 2000. MƵƺǈƻǃ, T. 1984. Movements, home range size Animal Movement Extension for ArcGIS. and habitat use of radio-tracked grass snakes Alaska Science Center, Biological Science (Natrix natrix) in southern Sweden. Copeia .îBD 42&DNKNFHB@K2TQUDX MBGNQ@FD 1984: 707–713. HǊƻǎ, R. B., PƻǉƻǇǈǄǃ, C. R., AǇǃǄǂƺ, S. J., Ƶǃƺ MƵƺǈƻǃ, T. Ƶǃƺ Sƾƿǃƻ, R. 1996. Seasonal migra- PǄǇǉƻǇ, W. P. 1989. Hot rocks and not-so-hot tion of predators and prey—a study of pythons rocks: retreat-site selection by garter snakes and and rats in tropical Australia. Ecology 77: 149– its thermal consequences. Ecology 70: 931–944. 156. HǊƻǎ, R. B. Ƶǃƺ PƿƵǃǁƵ, E. R. 1981. Ecological MƿǈƾƿǑƵ, J., TƵǁƻǃƵǁƵ, S., SƻǃƽǄǁǊ, S., Ƶǃƺ consequences of foraging mode. Ecology 62: OǁǄƹƾƿ, I. 1978. Faunal survey of amphibians 991–999. and reptiles. p. 77–98. In: Reports of Environmental HǊǉƹƾƿǃǈǄǃ, D. A., MǄǇƿ, A., SƵǋƿǉǏǁǎ, A. H., Researches of the Tamagawa River Basin 3, BǊǇƽƾƵǇƺǉ, G. M., WǊ, X., MƻƿǃǌƵǂƺ, J., Foundation of Environmental Protection of Ƶǃƺ SƹƾǇǄƻƺƻǇ, F. C. 2007. Dietary seques- Tokyo, Tokyo. tration of defensive steroids in nuchal glands of MǄǇƿ, A. 1997. A comparison of predatory the Asian snake Rhabdophis tigrinus. behavior of newly hatched Rhabdophis tigrinus Proceedings of the National Academy of 2DQODMSDR "NKTAQHC@D NM EQNFR @MC ëRG Science 104: 2265–2270. Japanese Journal of Herpetology 17: 39–45. HǊǉƹƾƿǃǈǄǃ, D. A., SƵǋƿǉǏǁǎ, A. H., MǄǇƿ, A., MǄǇƿ (RGD@CëQRSHMFDRSHNMDRRDMSH@KHM MƻƿǃǌƵǂƺ, J., Ƶǃƺ SƹƾǇǄƻƺƻǇ, F. C. 2008. gape-limited predators? Prey-handling behavior Maternal provisioning of sequestered defensive of the anurophagous snake Rhabdophis tigri- steroids by the Asian snake Rhabdophis tigrinus (Colubridae). Canadian Journal of Zoology nus. Chemoecology 18: 181–190. 84: 954–963. HǊǉƹƾƿǃǈǄǃ, D. A., SƵǋƿǉǏǁǎ, A. H., MǄǇƿ, A., MǄǇƿ, A., BǊǇƽƾƵǇƺǉ, G. M., SƵǋƿǉǏǁǎ, A. H., BǊǇƽƾƵǇƺǉ, G. M., MƻƿǃǌƵǂƺ, J., Ƶǃƺ RǄƸƻǇǉǈ, K. A., HǊǉƹƾƿǃǈǄǃ, D. A., Ƶǃƺ SƹƾǇǄƻƺƻǇ, F. C. 2012. Chemical investiga- GǄǇƿǈ, R. C. 2012. Nuchal glands: A novel de- tions of defensive steroid sequestration by the fensive system in snakes. Chemoecology 22: Asian snake Rhabdophis tigrinus. Chemoecology 187–198. 22: 199–206. MǄǇƿ +Ƶǎǃƻ, D., Ƶǃƺ BǊǇƽƾƵǇƺǉ, G. M. JƵƹǁǈǄǃ, D. R. Ƶǃƺ FǇƵǃǏ, R. 1981. Ecology of 1996. Description and preliminary analysis of the eastern coral snake (Micrurus fulvius) in antipredator behavior of Rhabdophis tigrinus northern peninsula Florida. Herpetologica 37: tigrinus, a colubrid snake with nuchal glands. 213–228. Japanese Journal of Herpetology 16: 94–107. KƵƺǄǌƵǁƿ, S. 1996. Ecology of a Japanese snake MǄǇƿ, A. Ƶǃƺ Vƿǃƹƻǃǉ, S. E. 2008. An integra- community: Resource use patterns of the three tive approach to specialization: Relationships sympatric snakes, Rhabdophis tigrinus, Elaphe among feeding morphology, mechanics, behav- quadrivirgata, and EIGQRPMBML@ @JMKFMøG. iour, performance and diet in two syntopic Bulletin of Tsukuba University Forests (12): snakes. Journal of Zoology (London) 275: 47– 77–148. 56. +ƻǎǃƵǊƺ, G. C., RƻƵǉƿ, G. J., Ƶǃƺ BǊƹƾƻǇ, E. H. MǄǇƿƽǊƹƾƿ, H. 1982. Appearance, movements, and 2008. Annual activity patterns of snakes from food habits of snakes at Minasegawa, Kanagawa, central Argentina (Córdoba province). Studies Japan. The Snake 14: 44–49. on Neotropical Fauna and Environment 43: MǄǇƿƽǊƹƾƿ, H. Ƶǃƺ NƵƿǉǄ, S. 1982. Activities 19–24. and food habits of Amphiesma vibakari (Boie) MƵƹƵǇǉǃƻǎ, J. M., GǇƻƽǄǇǎ, P. T., Ƶǃƺ+ƵǇǈƻǃ, and Rhabdophis tigrinus (Boie). The Snake 14: K. W. 1988. A tabular survey of data on move- 136–142. ments and home ranges of snakes. Journal of MǄǇƿƽǊƹƾƿ, H. Ƶǃƺ NƵƿǉǄ, S. 1983. Tracing of 20 Current Herpetol. 33(1) 2014

distance of movement of Rhabdophis tigrinus Natural Resources, Centre for Northern Forest !NHDHM@O@CCXëDKCAXL@QJ QDB@OSTQDLDSG- Ecosystem Research, Thunder Bay, Ontario. od. The Snake 15: 14–15. SƻƹǄǇ 2 , $BNKNFHB@K RHFMHëB@MBD NE MǊǉǄƾ, A. 1983. Death-feigning behavior of the movements and activity range for the sidewind- Japanese colubrid snake Rhabdophis tigrinus. er, Crotalus cerastes. Copeia 1994: 631–645. Herpetologica 39: 78–80. Sƻƿƽƻǂ, R. A. 1986. Ecology and conservation of NƵǁƵǑǊǇƵ, K. 1935. On a new integumental poi- an endangered rattlesnake, Sistrurus catenatus, son gland found in the nuchal region of a snake, in Missouri, USA. Biological Conservation 35: Natrix tigrina. Memoirs of the College of 333–346. Science, Kyoto Imperial University Ser. B 10: SƻǍǉǄǃ, O. J., JƵƹǄƸǈǄǃ, P., Ƶǃƺ BǇƵǑƸǂƻ, J. E. 229–240, 1 pl. 1992. Geographic variation in some activities NƿǈƾƿǑǊǇƵ, M., AǁƵǑƿǃƻ, H., OǎƵƺǄǑƵǇƿ, Y., associated with hibernation in nearctic pitvi- TƵǑƵǁƿ, H., Ƶǃƺ KƵǑǊǇƵ, T. 1995. Tracking pers. p. 337–345. In: J. A. Campbell and E. D. of Habu by radio telemetry 3. Annual Report of Brodie Jr. (eds.), Biology of the Pitvipers, Selva, Habu Study Section, Okinawa Prefectural Tyler. Institute of Health and Environment (18): 111– Sƾƿǃƻ, R. 1979. Activity patterns in Australian 124. elapid snakes (Squamata: Serpentes: Elapidae). PƵǇǁƻǇ, W. S. Ƶǃƺ BǇǄǌǃ, W. S. 1972. Telemetric Herpetologica 35: 1–11. study of movements and oviposition of two fe- UƹƾƿƺƵ, K. Ƶǃƺ IǑƵƿǏǊǑƿ, Y. 1939. On the food male Masticophis t. taeniatus. Copeia 1972: habits of snakes. Animal Survey Report 9: 892–895. 143–208. PǂǊǑǑƻǇ, M. V. 1981. Habitat utilization, diet WƵǈǁǄ, D. K. Ƶǃƺ SƵǈƵ, M. 2009. Activity pat- and movements of a temperate arboreal snake terns of a neotropical ambush predator: spatial (Opheodrys aestivus). Journal of Herpetology ecology of the fer-de-lance (Bothrops asper, 15: 425–432. Serpentes: Viperidae) in Costa Rica. Biotropica RƻƿǃƻǇǉ, H. K. 1993. Habitat selection in snakes. 41: 241–249. p. 201–240. In: R. A. Seigel and J. T. Collins WƻƵǉƾƻǇƾƻƵƺ, P. J. Ƶǃƺ CƾƵǇǂƵǃƺ, M. B. 1985. (eds.), Snakes: ecology and behavior. McGraw- Habitat selection in an Ontario population of Hill, New York. the snake, Elaphe obsoleta. Journal of RƻƿǃƻǇǉ, H. K. Ƶǃƺ CǊǃƺƵǂǂ, D. 1982. An im- Herpetology 19: 12–19. proved surgical implantation method for radio- WƾƿǉƵǁƻǇ, P. B. Ƶǃƺ Sƾƿǃƻ, R. 2002. Thermal tracking snakes. Copeia 1982: 702–705. biology and activity patterns of the eastern RƻƿǃƻǇǉ, H. K. Ƶǃƺ KǄƺǇƿƹƾ, W. R. 1982. brownsnake (Pseudonaja textilis): a radiotele- Movements and habitat utilization by the metric study. Herpetologica 58: 436–452. Massasauga, Sistrurus catenatus catenatus. WƾƿǉƵǁƻǇ, P. B. Ƶǃƺ Sƾƿǃƻ, R. 2003. A radio- Journal of Herpetology 16: 162–171. telemetric study of movements and shelter- RƻƿǃƻǇǉ, H. K. Ƶǃƺ ZƵǅǅƵǂǄǇǉƿ, R. T. 1988. site selection by free-ranging brownsnakes Timber rattlesnakes (Crotalus horridus) of the (Pseudonaja textilis, Elapidae). Herpetological Pine Barrens: Their movement patterns and Monographs 17: 130–144. habitat preference. Copeia 1988: 964–978. RǄƺƽƻǇǈ, A. R., CƵǇǇ, A. P., BƻǎƻǇ ' + SǑƿǉƾ + Ƶǃƺ Kƿƻ, J. G. 2007. HRT: Home Accepted: 14 August 2013 Range Tools for ArcGIS. Ontario Ministry of