Breeding Activity of a Stream-Breeding Toad, Bufo Torrenticola

Breeding Activity of a Stream-Breeding Toad, Bufo torrenticola

HIROSHI TSUJI AND TAKEO KAWAMICHI

Abstract: The breeding activity of the stream-breeding toad (Bufo torrenticola) was studied in Mie Prefecture for three years from 1990 to 1992. Aggregation in the main pool, which was intensively investigated, occurred explosively in early April for 12- 14 days. The oviposition period was 5-11 days in the main pool, and 14-17 days in the entire length of stream. First, many toads appeared on a particular section of the migration path, on their way to the stream. In about 300 individuals captured in the main pool, the males: female ratio was 2.0-2.4:1. The daily number of toads found in the main pool showed the normal distribution pattern with a sharp peak in the middle of the breeding period. Toads appeared to be most active during the nighttime. The onset of migration to the stream was affected by soil temperature rather than by air temperature; during the three years, maximum soil temperatures were 10.0-11.0℃, and minimum soil temperatures ranged 8.5-9.0℃ . Oviposition activity in the main pool in 1991 and 1992 occurred in the later half of the breeding period, when the minimum water temperature was above 10.0℃. Breeding activity, however, was not strongly associated with weather conditions, probably because breeding is performed underwater. Key words: Bufo torrenticola; Stream-breeding toad; Migration; Breeding Activity; Oviposition

The genus Bufo has a wide distribution cover- (Maeda and Matsui, 1989). Its tadpoles have ing temperate and tropical regions and is com- poorly developed external gills, a well-developed prised of more than 200 species (Duellman and oral disk, a short tail, and a poorly developed Trueb, 1986). Most Bufo species breed in lentic tail fin, all of which are probably adaptive to waters, such as ponds, marshes, and temporary torrential environments (Matsui, 1975; Iwasawa pools (e. g., Blair, 1972; Beebee, 1983), whereas and Saito, 1989). Information on the breeding species breeding in lotic waters, such as streams, ecology of this species, however, is largely lack- are extremely rare. Only a few species are so far ing (Matsui, 1976; Tsuji and Kawamichi, 1996). known as stream breeders (Tevis, 1966; Blair, In this paper, therefore, we examine the 1972; Zhao et al., 1989; Yang, 1991; Lips & breeding activity of B. torrenticola in natural Krempels, 1995). Although many researchers conditions, focusing on the following three have reported the reproductive ecology and aspects: (1) migration to a breeding stream, (2) mating behavior of still-water breeders (reviewed temporal patterns in the breeding activity, and by Wells, 1977; Arak, 1983), there are few cor- (3) influence of weather conditions on the responding data for stream breeders in Anura, breeding activity. except for a few species (Metter, 1964; Dole and Durant, 1974; Kusano and Fukuyama, 1987, MATERIALS AND METHODS 1989; Fukuyama et al., 1988; Fukuyama and Study site.-This study was conducted along Kusano, 1989, 1991). a 1500m stretch of the Higashimata-dani, a Bufo torrenticola is a large mountain toad branch of the Hirakura River (34°27'N, whose breeding and larval development occur in 136°15'E; 440-600m elevation), in the Misugi rocky torrents in central Japan (Matsui, 1988; Forest of Mie University and is located 60km Maeda and Matsui, 1989). This species has southwest of Tsu City, Mie Prefecture, central several morphological differences in both adults Japan. In this typical rocky stream, riffles are and tadpoles from B. japonicus, the Japanese 2-5m wide and 15-30cm deep, and the pools are still-water breeding common toad. Bufo torren- 5-10m wide and 0.5-2m deep. The stream ticola has an indistinct tympanum, longer limbs, banks are rocky, shaded by tree foliage, and the and elongated skin on the back in breeding males stream runs through conifer plantations and natural deciduous broad-leaved forests. A Accepted 1 Oct. 1996 forest trail runs along the stream. 118 Jpn. J. Herpetol. 16(4). 1996

The "main pool", at an altitude of 500m, was period. All toads detected were marked, their the breeding pool with the greatest number of locations were noted on maps with the time of egg-strings in the study site every year (Tsuji and capture, and they were released outside the Kawamichi, 1996). This pool was elliptic in fence. The census on the trail was conducted shape, and was 12m×7m in size in 1990. It also in 1992 when the cloth fence was not set up. was deformed by a typhoon in the autumn of The temporal change in the number of toads 1990 to 16m×7m thereafter. The maximum was intensively monitored in the main pool; water depth ranged from 60cm to 90cm during a census was taken 1-3 times every day and the three breeding seasons. Its rock base is par- 3-7 times every night throughout the three tially covered with rocks of various sizes, gravel, breeding periods. During each census, the and sand. A sloping waterfall with a height of number of single males, single gravid females, 10m flows into this pool. The current is relative- and amplexed pairs were counted, individual ly fast in the central part of the pool, but the marks were identified, and unmarked individuals shores are quiet. The right bank of this pool is a were marked. In 1991 and 1992, toads appear- rocky cliff, and the left bank is a bushy slope ing in the main pool were captured as much as towards the trail, which is about 20m above the possible; the percentage of the marked toads in main pool. the last census on each day was about 80%. In Observations. -This study was carried out in 1990, however, the capture rate of toads was three consecutive breeding seasons between 1990 much lower. To examine the movements of and 1992. The study period in the main pool marked toads from the trail to the stream and was between 1 and 21 April 1990, between 23 between the main pool and downstream to it, March and 20 April 1991, and between 25 March censuses were conducted from the main pool to and 20 April 1992. In 1991 and 1992, the study 200m downstream (the lowest major breeding included the entire breeding period in the main site), once in the daytime and once at nighttime pool, but in 1990 the survey in the main pool was every day throughout the breeding period in conducted only in the oviposition period. On 1991. almost every day and night during the study The days from the first to final emergence of periods, the main pool and the trail were regular- toads in the main pool were regarded as the ly investigated in order to detect toads. The breeding period, or the time of breeding activi- daytime and nighttime censuses were conducted ty. The days from the first to final oviposition in between 0700 and 1700 h, and between 1800 and the main pool and throughout the whole stream 0400 h, respectively. Observations at night were regarded as the oviposition period. The were made using a 4.5-volt headlamp and/or a cessation of oviposition in the whole stream 6-volt flashlight, neither of which appeared to was confirmed by counting egg-strings newly disturb the toads' behaviour. deposited every 1-2 days, after the breeding Toads were captured by hand or with the aid activity in the main pool ceased. The date of of a net. Captured individuals were marked by egg-laying was determined, based on the develo- uniquely toe-clipping them for permanent iden- pmental stages of the eggs and embryos (Iwasawa, tification and by attaching a waist band with a 1987). numbered tag for behavioural observations. Daily air temperatures, soil temperatures Both individuals of amplexed pairs were marked (20cm underground), and the amount of without separating the pairs; a numbered plastic precipitation during the study were obtained tag (5mm × 5mm) was stuck to their heads with from the Meteorological Station (513m eleva- cyanoacrylic glue (see Howard, 1988). All mark- tion) in this forest. The annual mean ed toads were released within 15 min at their temperature was 12.4℃, and the annual points of capture. precipitation was 2500mm. Water temperature In 1990 it was found that many toads at the in the main pool (30cm below the surface) was beginning of the breeding period appeared at a measured during every population census in particular part of the trail on the way to their 1991 and 1992. breeding sites in the stream. In order to capture the toads passing through the trail, a cloth drift RESULTS fence 60cm high was set up in 1991 on the Migration from trail to stream. -Bufo torren- stream side along 250m of the trail. A census ticola first emerged on a particular part (about on the trail along the drift fence was conducted 200m long) of the trail along the stream every 2-4 times every day and 2-5 times every night, year (Fig. 1). A few breeding toads were found more frequently at the beginning of the breeding higher than the extent of the drift fence, but no TSUJI AND KAWAMICHI-TOAD BREEDING ACTIVITY 119

FIG. 1. Left: the main study site (dotted) in Higashimata-dani. Current direction is from top to bottom . Right: movements of Bufo torrenticola between the trail and stream in 1991. Circles on the trail indicate marking points of single males: open circles were those males recaptured later in the main pool and solid circles are those recaptured at smaller points downstream. Open and solid stars indicate single gravid females and paired females, respectively. Arrows near the the trail indicate the extent of the drift fence. toads were found below it. The earliest date of 2). There was a difference between sexes in their appearance on the trail or the nearby forest floor way of emergence on the trail in 1991; 66.3% was fairly consistent for three years: 2 April (61) of the 92 single males appeared at night, 1990, 6 April 1991, and 4 April 1992 (Fig. 2). In whereas 89.3% (25) of the 28 females (single or 1990 and 1992, the emergence of toads on the paired) were found in the daytime (Fisher's exact trail lasted only for three days, while in 1991, the probability test; p<0.0001). Females also tend- year when the drift fence was set up on the trail, ed to appear slightly later in the month than their emergence lasted for eight days, and the males (Fig. 2). numbers of both sexes were much greater (Fig. In 1991, a total of 113 males (single= 92; 120 Jpn. J. Herpetol. 16(4). 1996

FIG. 2. Seasonal changes in the total number of Bufo torrenticola appearing on one day (from 9 hr to 8 hr on next morning) in the main pol and on the trail in 1990-1992. Closed and open columns represent males and females, respectively. Asterisks and open triangles indicate, respectively, days on which no investigation took place and days on which investigation was conducted only on the trail. The solid line below the dates indicates the oviposition period in the main pool (the broken line shows day on which oviposition was not observed). paired = 21) and 28 females (single = 7; was significantly biased towards males (Binomial paired = 21) were captured along the drift fence; test; p<0.01). The numbers of toads captured the sex ratio was 4.0: 1 (males: female), which on the trail without the drift fence or on the TSUJI AND KAWAMICHI-TOAD BREEDING ACTIVITY 121 nearby forest floor in 1990 and 1992 were Emergence in the main pool. -Toads began to considerably fewer than in 1991: 41 males appear in the main pool on the same day as their (single=40; paired=1) and 2 females (single=1; earliest appearance on the trail in 1991, and one paired=1) in 1990, and 25 males (single=24; day before in 1992 (Fig. 2). Toads were present paired=1) and 1 paired female in 1992. Hence, in the main pool between 6 and 17 April the sex ratio in both years was strongly male (12 days) in 1991, and between 3 and 16 April biased (p<0.001 in both). (14 days) in 1992. In 1990, the period between Of the 92 single males captured along the drift the earliest emergence on the trail (2 April) and fence in 1991, 47 (51.1%) were recaptured in the the latest day in the main pool (16 April) was stream, still single. Similarly, 12 (42.9%) of the 15 days (Fig. 2). 28 females were recaptured in the stream. The A total of 205 males and 95 gravid females spatial relationship between the marked points were individually counted in the main pool in on the trail and the first recapture in the stream 1991, and 208 males and 106 gravid females in suggests that males and females appearing on 1992; in 1990 the number of captured toads was the trail moved straight to the nearby stream only 120 males and 49 gravid females due to (Fig. 1). insufficient efforts at capture. The overall sex Of the 47 single males which moved from the ratios in the main pool were much less male trail to the stream, 10 (21.3%) moved between biased than those on the trail: 2.4 in 1990, pools during the breeding period in 1991. Three 2.2 in 1991, and 2.0 in 1992 (Binomial test; (25.0%, all paired) of the 12 females also moved p < 0.01 for 1990, p<0.001 for 1991 and 1992). between breeding sites in the stream. These The daily number of toads found in the main individuals of both sexes usually moved pool during the breeding period varied widely: downstream (nine males downstream, one 2-95 for males and 0-34 for females in 1991, and upstream; two females downstream, one 1-109 for males and 0-65 for females in 1992 upstream). (Fig. 2). In 1990, the daily toad number was 1- During the routine census between the main 34 for males and 0-14 for females, due to fewer pool and a 200m downstream stretch in 1991, 13 captures. The change of daily numbers in each single males (6.3%) of the 205 males marked in sex was similar between 1991 and 1992; both the main pool were recaptured downstream, and sexes showed a normal distribution pattern with 15 (15.8%, all paired) of 95 gravid females mark- a sharp peak in the middle of the breeding period ed in the main pool went downstream (see Tsuji (not significant for skewness, but significant at and Kawamichi, 1996); this difference between α=0.05 level for kurtosis in all cases; Fig.2). In sexes was significant (x2=24.47 , dF=1, 1990, however, there was no large peak in the dai- p=0.0162). Single males moved downstream ly number (Fig. 2). The daily numbers of both for 54.6m on average (range=10-110m), and sexes were highly correlated in all three years paired females moved downstream for 76.7m on (Spearman's rank correlation coefficient; 1990: average (10-210m); this difference between sexes rs=0.917, N=12; 1991: rs=0.938, N=12; 1992: was not significant (Mann-Whitney U-test, rs = 0.924, N =14; p <0.003 in all), indicating z=-1.281, p>0.05). On the other hand, few that emergence was synchronized between sexes. individuals of either sexes moved from Male tended to arrive in the main pool slightly downstream to the main pool. Only four earlier than females. Over half the males mark- (6.3%) of 64 males marked downstream from ed as single entered the main pool before the the main pool were recaptured in the main pool; onset of oviposition activity: 55.6% (74/133) in none of 15 females were recaptured in the main 1991 and 63.6% (89/140) in 1992. Females pool. (single or paired) tended to enter the main pool Many individuals probably drifted into the after the onset of activity: 61.1% (58/95) in 1991 main pool. In 1992, of 12 single males and two and 64.2% (68/106) in 1992. This difference pairs marked at a breeding site above the main between sexes was significant in both years (1991: pool, six (50.0%) and two (100%), respectively, x2 = 5.53, dF =1, p=0.0187; 1992: x2=17.41 were then recaptured in the main pool. On dF=1, p<0.0001). the other hand, few individual toads moved Unmarked males appeared in the main pool upstream from the main pool, presumably during most days of the breeding period. On prevented from doing so by the large waterfall. those particular days, however, the number of One exception was a female in amplexus that was recaptured males, after the first day, exceeded once observed climbing the steep rocky cliff that of new ones (8 of 11 days in 1990, 7 of beside the waterfall. 11 days in 1991, and 11 of 13 days in 1992; Fig. 122 Jpn. J. Herpetol. 16(4). 1996

2). Females showed a reversed pattern; the oviposition were between 1800 and 0600 h(x2= number of new females exceeded that of recap- 12.52, dF=1, p <0.001). In all three years, tured ones on many days (7 of 9 days in 1990, 7 the earliest oviposition was observed on the day of 10 days in 1991, and 8 of 9 days in 1992; when the numbers of both males and females Fig. 2). reached a peak in the main pool: 6 April 1990 Toads were found in the main pool not only at (the first peak), 11 April 1991, and 9 April 1992 night but also in the daytime. Throughout the (Fig. 2). The oviposition period lasted for breeding period in 1991, however, the maximum 11 days in 1990, 6 days in 1991, and 5 days in number of toads in the main pool was always 1992, usually occurring in the latter part of the greater at night than in the daytime (Fig. 3); the breeding period (Fig. 2). The days of oviposi- proportion of daytime to night each day was tion were 10 in 1990, five in 1991 and 1992. 39.5% on average (SD=28.6, range=0-79.5%, About 80% of ovipositions occurred during the N=12). The proportion was high in the middle first half of the oviposition period in all three of the breeding period, especially between 11 years. and 13 April, corresponding to the most active The earliest oviposition in the whole stream days for oviposition; the proportion of the occurred in the main pool in 1990 and 1991. In daytime to night for these three days was 70.9% 1992, however, earlier oviposition occurred in on average (Fig. 3). another pool, 90m downstream from the main In each census, single males usually out- pool, one day prior to the earliest oviposition in numbered pairs and single gravid females, at any the main pool. The final oviposition was observ- time of day (Fig. 3). The proportion of single ed in a pool in the uppermost-stream (660m males to the total number of toads (single away from the main pool, altitudinally 80m males+pairs or single females) in each census higher than the main pool; Fig. 1, left) on 24 tended to be higher at night (79.2±17.4%, April in 1991 and 22 April in 1992. These dates N=12) than in the daytime (65.4±16.7%, were respectively eight and nine days after the N=10), although the difference was not signifi- final oviposition day in the main pool. cant (U-test; z=-1.620, p>0.05). In 1990, the delayed oviposition was observed Oviposition activity. -Oviposition usually also in the lower stream on 22 April, six days occurred at night; 35 (76.1%) of 46 sightings of after the final oviposition in the main pool.

FIG. 3. Changes in the maximum number of Bufo torrenticola found in the main pool in daytime and nighttime censuses in 1991. Underlined dates indicate the oviposition period in the main pool. TSUJI AND KAWAMICHI-TOAD BREEDING ACTIVITY 123

TABLE 1. Soil, air, water temperatures (C), and rainfall (mm) and the dates of the emergence of the toads on the trail and the main pool for the years 1990-1992. Data, except for water temperature, were derived from un- published records from the Misugi forest of Mie University. Water temperature in 1990 is the mean value at 1800-2400 h. Closed and open triangles show the date of the earliest emergence on the trail and earliest oviposition in the main pool, respectively. Solid lines indicate the emergence period of the toads in the main pool. 124 Jpn. J. Herpetol. 16(4). 1996

Therefore, the oviposition period in the whole stream was 14 days in 1991, and 15 days in 1992, DISCUSSION but 17 days in 1990 (although in this year the Migration.-This study revealed for the first stream was not completely investigated). time the breeding season and partial routes of Influence of weather on breeding activity. - migration to breeding sites in stream-breeding The emergence of toads on the trail was pro- Bufo torrenticola. Individuals of both sexes bably affected more by soil temperature than air migrated to breeding sites explosively and just temperature. Soil temperatures on the earliest before oviposition. As a consequence, there dates of emergence on the trail showed extremely were less than seven days between the earliest narrow ranges for the three years: 10.0-11.0℃ arrival in the main pool and the onset of oviposi- at the maximum and 8.5-9.0℃ at the minimum tion activity. In still-water breeding Bufo, this "p (Table 1). On the other hand, air temperatures re-oviposition period" is generally longer on those days ranged more widely: 16.0-18.5℃ because some individuals arrive at breeding sites at the maximum and 7.0-9.5℃ at the minimum very early (see Matsui, 1987). For example, the (Table 1). Rainfall over 20mm was also record- pre-oviposition period is about 2-3 weeks for ed on the earliest dates of emergence in 1991 and B. bufo (Davies and Halliday, 1979; Loman 1992 (Table 1). The weather was clear on the and Madsen, 1986), and about 10 days for B. first day in 1990 when only one individual emerg- japonicus (Okuno, 1986). Variation in the time ed, but 17 toads appeared on the second day in of migration may be due to the difference in rainy weather. hibernating sites; in B. japonicus, individuals Oviposition activity in 1991 and 1992 began hibernating in sunny areas wake earlier than when the minimum water temperature was above those at others (Okuno, 1986). The short pre- 10℃ (Table 1). In 1990, however, the oviposi- oviposition period in the B. torrenticola in this tion activity was initiated at a water temperature study might have been caused by simultaneous of 7.3℃ . Precipitation did not appear to have awakening of individual toads at uniform hiber- any effect on the onset of oviposition activity nation sites, because most of the forest floor in (Table 1). the study site received little sunlight. The patterns of fluctuation in mean air The hibernation sites of B. torrenticola have temperature during the breeding period differed not been detected. In the non-breeding season, between 1990 and the following two years. In individuals disperse throughout the stream and the latter two years, mean air temperature was adjacent forest floor. Indeed, some individuals relatively stable from the beginning to the mid- marked in the main pool during the breeding dle of the breeding period, but it dropped at the season were later found about 600m end (Table 1). In contrast, in 1990, a steep drop downstream in the non-breeding season (Tsuji, in air temperature occurred from the beginning unpubl. data). Two possible patterns appear to the middle breeding period; the minimum air to exist in the migration of B. torrenticola to temperature on 5 and 6 April dropped to 1.0℃ breeding sites; they hibernate at activity sites in and 1.5℃, respectively(Table 1). the non-breeding season and move to breeding To clarify meteorological factors affecting the sites in the spring, a characteristic of B. emergence of toads in the main pool in 1991 and japonicus (Okuno, 1984b), or they move near 1992, the relationships between the daily toad to breeding sites before hibernation, as has number and meteorological variables were been noted of B. bufo in Switzerland (Heusser, examined: air temperature, water temperature, 1968). The fact that B. torrenticola appeared at and rainfall. Evidence indicated that no single a narrow stretch of the trail for a short period at meteorological factor clearly affected the the beginning of the breeding period suggests emergence of toads. Mean and minimum air the second possibility. temperatures were positively correlated with the After arriving in the stream, some males and daily toad number only in males in 1992 (mean: females moved between breeding pools, mostly rs=0.564, minimum: rs=0.576; p<0.05 in downstream. Females appearing in the main both). Mean water temperature was positively pool moved downstream more than males. This correlated with the daily toad number in both datum suggests that males tend to stay at one sexes only in 1992 (male: rs=0.548; female: breeding site during the breeding period and that rs = 0.627; p<0.05 in both). Rainfall was not some females move between breeding sites, correlated with the daily toad number in either perhaps in search of a better oviposition site. year. Movements between breeding sites may be a characteristic of stream-breeders, because both TSUJI AND KAWAMICHI-TOAD BREEDING ACTIVITY 125 sexes of B. japonicus move very little between tropical Miyako Island is a prolonged breeder breeding sites during the same breeding period (Maeda and Matsui, 1989). In subtropical or (Okuno, 1984a). Rana sakuraii, a Japanese tropical Taiwan, still-water breeding B. stream-breeding frog, usually drifts downstream melanosticus and stream-breeding B. bankoren- during the breeding period (Kusano and sis are both prolonged breeders (Yang, 1991). Fukuyama, 1987, 1989). Thus, water currents Therefore, the duration of the breeding period in could very likely cause the downstream Bufo in East Asia may be associated with local movements between breeding sites with these temperatures. stream-breeders. Breeding activity in the main pool.-Ex- Breeding season and period. -Bufo japonicus plosive breeders often form dense aggregations exhibits a greater geographical variation in of hundreds or thousands of individuals, usually the time of reproduction, ranging from mid- at temporary and semi-permanent waters (e.g., November to early July (Matsui, 1989). Its Gittins et al., 1980; Howard and Kluge, 1985; breeding period occurs earlier in warmer Jacobson & Vandenberg, 1991). This cir- regions; the relationship between the date of cumstance was also the case for B, torrenticola breeding and annual mean air temperature is in this study; about 200 males and 100 females ag- negatively linear, but in the localities with gregated in the main pool. Although breeding annual mean temperature between 5 and 12℃ the sites were randomly distributed along nearly date of breeding is almost constant (Matsui, 1000m of the 1500m stream, the main pool was 1989). Similarly, for B. torrenticola, the annual the largest breeding site every year (Tsuji and mean temperatures at the study site and at other Kawamichi, 1996). It seems to be easy for males sites for the breeding dates fit with this relation- and females of explosive breeders in still water to ship (see Fig. 2 in Matsui, 1987), suggesting that gather at a given "traditional" site because males the reproductive timing of B. torrenticola basical- generally vocalize in choruses that probably ly corresponds to that of B. japonicus. At sites advertise the locations of breeding sites to where both species live sympatrically, however, females (Wells, 1977). On the other hand, it is B. torrenticola appears to breed later, though it strange that both sexes of B. torrenticola gather is not clear just how much later (Maeda and explosively at particular sites, since males lack Matsui, 1989). advertisement calls, at least on land (Matsui, The breeding of B. japonicus begins earlier in 1988; Tsuji, unpubl. obs.), and pools suitable as localities that are at lower latitudes, or at lower breeding sites are dispersed all along the stream altitudes at the same latitude (Matsui, 1989). (Tsuji and Kawamichi, 1996). Bufo japonicus This altitudinal trend was also found for B. also lacks advertisement calls, but enters and torrenticola. At Ohdaighara, which is about leaves breeding ponds by the same route using 1000m higher than the study site but at a similar geotactic memory based on olfactory cues (Ishii latitude, B. torrenticola begins breeding in late et al., 1995). The main pool contained the April, 2-3 weeks later than at the study site largest aggregation of toads, in all likelihood (Matsui, 1976). Because B. torrenticola is because it was the most suitable site for breeding distributed in much smaller areas than B. migration since its relatively gently sloped banks japonicus, the range of its breeding season also provided an easy access route to and from the could be narrower, lasting for two months at stream. In addition, the depths and shallows of the longest. the main pool were probably appropriate for Temporal patterns of reproduction in Anura the toad mating and spawning. are generally divided into two categories, ex- Unlike many frogs and toads in the temperate plosive breeding and prolonged breeding (Wells, zone, breeding adults of B. torrenticola were 1977). The present study shows that B. torren- active at night and in the daytime both during ticola is a typical explosive breeder; two weeks migration and in the main pool. However, they for the breeding period and only one week for appeared to prefer night to daytime, because the oviposition period in the main pool, and two their oviposition was done mostly at night, and weeks for the oviposition period in the whole because the number of toads in the main pool at stream. In the breeding period in various Bufo night always exceeded the daytime number. species (Wells, 1977), there appears no clear rela- Rana sakuraii, the earliest anuran to breed in tionship between the duration of the breeding spring, also shows diurnal activity (Kusano and period and the climate zone. In Japan, B. Fukuyama, 1989). The diurnal breeding activi- japonicus in temperate Honshu Island is an ty of these species may be associated with early explosive breeder, whereas B. miyakonis in sub- breeding in spring, when important potential 126 Jpn. J. Herpetol. 16(4). 1996 predators such as snakes are inactive (Kusano higher soil temperature in B. torrenticola may and Fukuyama, 1989). In fact, we observed a result in its breeding later than B. japonicus at snake preying on a breeding toad only once the same localities. during the three breeding periods. In addition, Precipitation is another potentially important there is another possible explanation for the factor affecting the onset of breeding activity in diurnal activity of B. torrenticola. Jacobson and explosive breeders (Blair, 1960; Jacobson and Vandenberg (1991) pointed out that the diurnal Vandenberg, 1991; Krupa, 1994). The onset of activity pattern in the golden toad B. periglenes breeding activity in B. japonicus is also affected is coupled with its striking colour dimorphism in by precipitation (Okuno, 1985). In R, sakuraii, visual mate recognition. Because B. torren- the movement to the stream in autumn occurs ticola also has relatively remarkable colour during rainy nights (Kusano and Fukuyama, dimorphism (Maeda and Matsui, 1989), greenish 1987). This observation is true for B. torren- brown for males, and reddish brown for females ticola as well; the days when more than four in- in our population, this sexual dimorphism may dividuals first appeared on the trail were rainy have a role in males finding females, and may for the three years. For anurans with a low be related to the considerable diurnal activity. tolerance for desiccation, therefore, high humidi- Meteorological factor affecting breeding activity could be the requirement for movement on ty. -Since anurans are poikilotherms and have a the ground. low tolerance for desiccation, their breeding In two of three years oviposition began when activity is affected by weather conditions, such the minimum water temperature was above as temperature and precipitation (see Duellman 10℃. However, in 1990, the oviposition activi- and Trueb, 1986). In explosive breeders, the ty was initiated at much less than 10℃; this relationship between the onset of breeding and observation suggests that the onset of oviposi- weather conditions has been well investigated tion activity may be determined not only by ex- (e. g., Savage, 1961; Hisai and Sugawara, 1978; ogenous factors, but also by endogenous ones. Okuno, 1985). Because explosive breeders in Actually, the period from the earliest emergence the temperate zone begin migration at the onset of toads on the trail to the earliest oviposition of breeding activity, soil temperature could be was fairly stable for the three years, being 4- one of the most important factors affecting their 6 days (Fig. 2). emergence (Aoyagi et al., 1977; Hisai and The emergence of B. torrenticola in the main Sugawara, 1978; Gittins et al., 1980). In our pool throughout the breeding period was not study, soil temperature, especially the minimum strongly associated with weather conditions; temperature, during the earliest emergence on there was no clear relationship between the daily the trail showed an extremely narrow range for toad number in the main pool and three years (1.0℃ for the maximum, 0.5℃ for meteorological variables such as air or water the minimum), compared to air temperature temperatures and rainfall. This may be because (2.5℃ for both). its breeding is performed on the pool bottom In B. japonicus, soil temperature at the onset (Matsui, 1976; Tsuji, unpubl. obs), a place of breeding activity is relatively constant among which is apparently less affected by weather con- difrerent localities: 6.0℃ (minimum at a depth ditions; the difference between the maximum of 5cm)in Tokyo(20-50 m elevation; Hisai and and minimum water temperatures during the Sugawara, 1978), 6.6℃ (at a depth of 20cm breeding period in 1991 and 1992 was only 3.0- at 1600 h) in Matsumoto (1000m elevation; 4.2℃ in the main pool, compared to an air Aoyagi et al., 1977), and 8.0℃ (at a depth of temperature of 17.5-19.0℃. Rana sakuraii 10cm at 1900 h) in Hachioji (180m elevation; also breeds underwater in streams, but its Serizawa and Kanai, 1970). Uwa et al. (1981) breeding activity was affected by water also reported similar soil temperatures at a depth temperature; its activity is lowered when water of 20cm at night during the spring emergence of temperature was below 4℃ (Kusano and B. japonicus at four breeding sites in Nagano Fukuyama, 1989). On the other hand, the Prefecture: 6.6℃ at 1000m elevation,6.6℃ at breeding activity of B. torrenticola was slightly 1100m, 8.3℃ at 640m, and 9.4℃ at 360m. In interrupted by cold weather, because of the the present study, the maximum and minimum warmer breeding season. Nevertheless, the soil temperature at the onset of breeding activity absence of large peaks of activity during the was 10.5℃ and 8.8℃ on average for the three breeding period and the extended oviposition years, indicating higher levels for B. torrenticola period in 1990 might have been due to severe than for B. japonicus. The response to the cold weather at the beginning of the breeding TSUJI AND KAWAMICHI-TOAD BREEDING ACTIVITY 127 period. Precipitation did not affect the breeding GITTINS, S. P., A. G. PARKER AND F. M. SLATER. activity of these two stream breeders. As 1980. Population characteristics of the common pointed out by Kusano and Fukuyama (1989), toad (Bufo bufo) visiting a breeding site in mid- breeding underwater may protect them from the Wales. J. Anim. Ecol. 49: 161-173. HEUSSER,H. 1968. Die Lebensweise der Erdkrote, danger of desiccation. Bufo bufo (L.); Wanderungen und Sommerquar- ACKNOWLEDGMENTS.-Wewould like to thank the tiere. Rev. Suisse Zool. 75: 927-982. following people for helping with our field work: H. HISAI, N. AND T. SUGAWARA.1978. Ecological Ebisudani, H. Fujita, M. Kishimoto (Miyazaki), T. studies of Bufo bufo japonicus Schlegel. V. The relation between appearances and the climatic condi- Mizuta, M. Nishigaki, T. Ohno, Y. Segawa, and T. tions at breeding season. Misc. Rep. Natl. Park for Teraoka. Thanks are also due to M. Matsui, Y. Nat. Stud. (8): 135-149. (in Japanese with Tomida, S. Yamagishi, and M. Kohda for their useful English summary) advice on this study, and to S. Ishii and T. Kusano for HOWARD,R. D. 1988. Sexual selection on male body providing literature. The staff of the Misugi Forest of size and mating behaviour in American toads, Mie University kindly allowed us to study in this forest Bufo americanus. Anim. Behav. 36(6): 1796-1808. and to use the meteorological data. We specially HOWARD,R. D. ANDA. G. KLUGE.1985. Proximate thank the Sakamoto family for their willing help mechanisms of sexual selection in wood frogs. during the time spent living at the study site. Evolution 39(2): 260-277. ISHII, S., K. KUBOKAWA,M. KIKUCHIAND M. NISHIO. LITERATURE CITED 1995. Orientation of the toad, Bufo japonicus, AOYAGI,M., BUFO RESEARCHGROUP AND H. UWA. toward the breeding pond. Zool. Sci. 12: 475-484. 1977. Studies on the breeding behavior of the toad, IWASAWA,H. 1987. Normal table of development. Bufo bufo formosus, at lake Misuzu. I. Effect of In: A. Urano and K. Ishihara (eds.), Biology of underground temperature on the spring emergence. Toad. p. 256-265. Shokabo, Tokyo. (in Japanese) J. Fac. Sci. Shinshu Univ. 12(1): 65-77. (in Japanese IWASAWA, H. AND K. SAITO. 1989. Adaptive with English abstract) characteristics related to a torrential habitat in ARAK, A. 1983. Male-male competition and mate Bufo torrenticola larvae: comparison with those of choice in anuran amphibians. In: P. Bateson (ed.), the still water-breeding species Bufo japonicus Mate Choice. p. 181-210. Cambridge Univ. Press, formosus. Sci. Rep. Niigata Univ., Ser. D (Biol.) Cambridge. (26): 13-25. BEEBEE,T. J. C. 1983. The Natterjack Toad. Oxford JACOBSON, S. K. AND J. J. VANDENBERG.1991. Univ. Press, Oxford. 159 p. Reproductive ecology of the endangered golden toad BLAIR, W. F. 1960. A breeding population of the (Bufo periglenes). J. Herpetol. 25(3): 321-327. Mexican toad (Bufo valliceps) in relation to its KRUPA, J. J. 1994. Breeding biology of the Great environment. Ecology 41(1): 165-174. Plains toad in Oklahoma. J. Herpetol. 28(2): 217- BLAIR, W. F. (ed.) 1972. Evolution in the Genus 224. Bufo. Univ. Texas Press, Austin and London. KUSANO,T. ANDK. FUKUYAMA.1987. Body size and 459 p. breeding activity of a stream-breeding ranid frog DAVIES, N. B. AND T. R. HALLIDAY.1979. Com- (Rana sp.) in the Bonboni River, Itsukaichi-machi, Tokyo. Jpn. J. Herpetol. 12(2): 65-71. (in Japanese petitive mate searching in male common toads, Bufo bufo. Anim. Behav. 27(4): 1253-1267. with English abstract) DOLE,J. W. ANDP. DURANT.1974. Movements and KUSANO,T. ANDK. FUKUYAMA.1989. Breeding activi- seasonal activity of Atelopus oxyrhynchus (Anura: ty of a stream-breeding frog (Rana sp.). In: M. Atelopodidae) in a Venezuelan cloud forest. Copeia Matsui, T. Hikida, and R. C. Goris (eds.), Current 1974(1): 230-235. Herpetology in East Asia. p. 314-322. Herpetol. DUELLMAN,W. E. AND L. TRUEB. 1986. Biology of Soc. Japan, Kyoto. Amphibians. McGraw-Hill, New York, 670 p. LIPS, K. R. ANDD. M. KREMPELS.1995. Eggs and tad- FUKUYAMA,K., T. KUSANOAND M. NAKANE.1988. A pole of Bufo fastidiosus Cope, with comments on radio-tracking study of the behaviour of females of reproductive behavior. Copeia 1995(3): 741-746. the frog Buergeria buergeri (Rhacophoridae, LOMAN, J. AND T. MADSEN. 1986. Reproductive Amphibia) in a breeding stream in Japan. Jpn. J. tactics of large and small male toads Bufo bufo. Herpetol. 12(3): 102-107. Oikos 46(1): 57-61. FUKUYAMA,K. AND T. KUSANO.1989. Sexual size MAEDA,N. ANDM. MATSUI.1989. Frogs and Toads dimorphism in a Japanese stream-breeding frog, of Japan. Bun-ichi Sogo Shuppan, Tokyo. 206 p. (in Buergeria buergeri (Rhacophoridae, Amphibia). In: Japanese with English abstract) M. Matsui, T. Hikida, and R. C. Goris (eds.), Cur- MATSUI,M. 1975. A new type of Japanese toad larvae rent Herpetology in East Asia. p.306-313. Herpetol. living in mountain torrents. Zool. Mag. 84(3): 196- Soc. Japan, Kyoto. 204. FUKUYAMA,K. ANDT. KUSANO.1991. Factors affec- MATSUI,M. 1976. A new Japanese toad, Bufo torren- ting breeding activity in a stream-breeding frog, ticola. I, II. Nature Study. 22(9): 105-110, 22(12): Buergeria buergeri. J. Herpetol. 26(1): 88-91. 145-148. (in Japanese) 128 Jpn. J. Herpetol. 16(4). 1996

MATSUI,M. 1987. Geographic variation in breeding 35(5): 621-630. (in Japanese with English synopsis) and its factor. In: A. Urano and K. Ishihara (eds.), SAVAGE,R. M. 1961. The Ecology and Life History Biology of Toad. p. 19-31. Shokabo, Tokyo. (in of the Common Frog (Rana temporaria tem- Japanese) poraria). Sir Issac Pitman & Sons, Ltd., London. MATSUI,M. 1988. A review for the Japanese stream 221 p. toad. The Natural History of Japan. 2(8): 48-55. (in SERIZAWA,S. AND I. KANAI. 1970. Morphological Japanese) and ecological notes on Bufo bufo formosus. Rep. MATSUI,M. 1989. Breeding strategy in the Japanese Nat. Sci. Mus. Takao. (Tokyo) (2): 25-45. (in common toad, Bufo japonicus. In: M. Matsui, T. Japanese with English summary) Hikida, and R. C. Goris. (eds.), Current TEVIS, L. JR. 1966. Unsuccessful breeding by desert Herpetology in East Asia. p. 332-341. Herpetol. toads (Bufo punctatus) at the limit of their Soc. Japan, Kyoto. ecological tolerance. Ecology 47(5): 766-775. METTER,D. E. 1964. A morphological and ecological TSUJI, H. AND T. KAWAMICHI. 1996. Breeding comparison of two populations of the tailed frog, habitats of a stream-breeding toad, Bufo torren- Ascaphus truei Stejneger. Copeia 1964(1): 181-195. ticola, in an Asian mountain torrent. J. Herpetol. OKUNO, R. 1984a. Studies on the natural history of 30(3): 451-454. the Japanese toad, Bufo japonicus japonicus. I. UWA, H . , Y. WATANABE,Y. SAKAKURA,S. ASAI AND Habitat groups and the interactions among them. H. SHIONO. 1981. Estimation of the spring Jpn. J. Ecol. 34(1): 113-121. (in Japanese with emergence of the toad, Bufo bufo formosus, using English synopsis) underground temperature. Zool. Mag. 90: 157-163. OKUNO, R. 1984b. Studies on the natural history of (in Japanese with English summary) the Japanese toad, Bufo japonicus japonicus. III. WELLS,K. D. 1977. The social behavior of anuran Seasonal and nocturnal fluctuations of toad activity. amphibians. Anim. Behav. 25(3): 666-693. Jpn. J. Ecol. 34(3): 331-339. (in Japanese with YANG, Y.-J. 1991. Frogs and Toads in Yang-ming- English synopsis) shan National Park. Yang-ming-shan National OKUNO,R. 1985. Studies on the natural history of the Park's Publicatiion, Taiwan. 95 p. (in Chinese) Japanese toad, Bufo japonicus japonicus. VIII. ZHAO,E., G. WU ANDR. F. INGER. 1989. Ecological Climatic factors influencing the breeding activity. and geographic distribution of the amphibians of Jpn. J. Ecol. 35(4): 527-535. (in Japanese with Sichuan, China. Copeia 1989(3): 549-557. English synopsis) OKUNO,R. 1986. Studies on the natural history of the Laboratory of Animal Sociology, Faculty of Japanese toad, Bufo japonicus japonicus. IX. Male Science, Osaka City University, Sugimoto, behaviors during breeding season. Jpn. J. Ecol. Sumiyoshi-ku, Osaka, 558 JAPAN

要旨渓流繁殖性ナガレヒキガエルの繁殖活動辻広志・川道武男渓流繁殖性ナガレヒキガエルの繁殖活動を3 川への移動開始は気温よりも地温の影響を受けシーズンにわたって調査した.繁殖活動は4月ると思われ,最高地温と最低地温の3年間の範前半の短期間(12-14日)であった.産卵は淵囲はそれぞれ,10.0-11.0℃ と8.5-9.0℃ であで行われ,産卵期間は5-11日で,川全域ではった.淵での産卵活動はふつう,繁殖期間の後 14-17日だった.繁殖期の初めに川沿いの林道半に最低水温が10.0℃ を超えた時に行われの特定の区間で,川への移動途中の個体が多数た.繁殖活動は繁殖期間中の気象の影響を強く捕獲された.淵では約300個体が捕獲され,性受けるとは思えなかった.これは本種の繁殖行比は2.0-2.4:1で雄に偏っていた.淵での出現動が安定した水温の水中で行われるためと考え個体数の日変動のパターンは繁殖期間の中頃にられる. ピークをもつ正規分布型を示した.日中でも繁 (558大阪市住吉区杉本大阪市立大学理学殖活動は見られたが,夜の方が活発であった. 部動物社会学研究室)