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Behavior of Juveniles of the Japanese Endemic Species

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Behavior of Juveniles of the Japanese Endemic Species JOURNAL OF CRUSTACEAN BIOLOGY, 22(3): 532–537, 2002 BEHAVIOR OF JUVENILES OF THE JAPANESE ENDEMIC SPECIES CAMBAROIDES JAPONICUS (DECAPODA: ASTACIDEA: CAMBARIDAE), WITH OBSERVATIONS ON THE POSITION OF THE SPERMATOPHORE ATTACHMENT ON ADULT FEMALES Tadashi Kawai and Gerhard Scholtz (TK, corresponding) Hokkaido Nuclear-Energy Environmental Research Center, Miyaoka, 261-1, Kyowa, Hokkaido 045-0123, Japan (kawaita@fishexp.pref.hokkaido.jp); (GS) Humboldt-Universita¨tzuBerlin, Institut fu¨r Biologie/Vergleichende Zoologie, Philippstraße 13, Downloaded from https://academic.oup.com/jcb/article/22/3/532/2679704 by guest on 02 October 2021 D-10115 Berlin, Germany ([email protected]) ABSTRACT The behavior of juveniles of the Japanese endemic crayfish Cambaroides japonicus (Decapoda: Cambaridae) was observed in the field and in the laboratory. In addition, the occurrence and placement of spermatophores on adult females is described from specimens inhabiting small brooks at Otaru and Hamamasu, Hokkaido, Japan, sampled from 1998 to 1999. The second stage juveniles left their mother permanently after some exploration behavior. In adult females, spermatophores were attached to the surface of the seminal receptacle (annulus ventralis), which is situated at the posterior margin of the seventh thoracic sternite. In C. japonicus the invagination of the annulus ventralis is not deep enough to hide the male spermatophores. Previous studies of the Astacidae reported that juveniles left their mother at the second stage, that spermatophores were attached to the surfaces of sternal plates of the last three pereopods, and that an annulus ventralis did not exist. In contrast, Cambaridae juveniles normally detach from the mother at the third stage, but they may detach and stay longer with the parent until the fourth stage. There is variability in this trait. The spermatophores are completely hidden in the annulus ventralis of adult females. Therefore, although C. japonicus belongs to the family Cambaridae, the juvenile stage that detaches from the mother is the same as that reported in Astacidae. The position of the spermatophore attached to the adult female exhibits an intermediate state between that of the Astacidae and that of the Cambaridae. The crayfishes in the Northern Hemisphere In most species of the American Cambaridae, (Astacoidea) are assigned to the Cambaridae the spermatophores are completely buried in the and the probably paraphyletic Astacidae annulus ventralis (seminal receptacle) of adult (Scholtz, 1998, 1999, 2001). The species as- females and not visible from the outside (Hagen, signed to the Astacidae occur in Europe and east 1870; Snodgrass, 1952; Fitzpatrick, 1995). In of the North American Cordillera. The Cambari- Astacidae, spermatophores are attached to the dae occur in East Asia (Asian Cambaridae) and surface of sternal plates of the posterior on the Atlantic side of North and Central pereopods in the female (Mason, 1970a, b; America (American Cambaridae) (Hobbs, Kossmann, 1972; Ingle and Thomas, 1974). 1942; Scholtz, 1995). The Asian Cambaridae In Asian Cambaridae (Cambaroides), the comprise only the genus Cambaroides (Hobbs, behavior of the juveniles and the attachment 1974). of spermatophores have not yet been studied. In the American Cambaridae, first and second The present paper describes these features in the stage juveniles remain attached to the mother’s Japanese endemic species C. japonicus (De pleopods, not becoming independent until the Haan, 1841). third juvenile stage in some species, perhaps even later (Price and Payne, 1984). In Astaci- MATERIALS AND METHODS dae, juveniles detach from the mother at the Field Survey second stage. Albrecht (1982) and Scholtz Field surveys were conducted at Otaru (43°1400500N, (1995) suggested that this earlier independence 141°0005000E) and Hamamasu (43°2900000N, 141°2301500E), of the juveniles in Astacidae might be an apo- Hokkaido, Japan. At each site, there is a small brook, and morphy of this group. the brooks are of similar size (approximately 150-m length, 532 KAWAI AND SCHOLTZ: REPRODUCTION OF JAPANESE CRAYFISH 533 Downloaded from https://academic.oup.com/jcb/article/22/3/532/2679704 by guest on 02 October 2021 Fig. 1. Change of water temperature, juvenile behavior, and occurrence frequency of spermatophore at the survey sites, Otaru and Hamamasu. The occurrence frequency was calculated as 100 Â numbers of females with eggs, juveniles, or spermatophores ⁄ total number of adult females of each sampling. The adult female is defined as carapace length of more than 20 mm. a maximum of 5-cm depth, and a maximum of 1-m width). its margin, the second stage juveniles have a telson bearing Most crayfish were collected by hand from underneath numerous plumose setae on the margin, and in the third stage boulders or fallen leaves. No burrows were found. Fifteen uropods are present. Terminology follows Holdich (1992), sampling stations were established in each brook, and Hopkins (1967), Payne (1972), and Van Deventer (1937). specimens at each station were sampled in a 1m2 quadrat. A total of 15 collections were made at Otaru (July through Aquarium Observations December, 1999) and 14 at Hamamasu (July to December, 1998). At both sampling stations, the populations were Aquarium observations were conducted in July and dense (over 6.0 individuals/m2). August, 1998. Ten ovigerous females (mean POCL, 23.1 ± The postorbital carapace length (from the posterior 0.6 SE mm; range, 20.4–25.5) from Hamamasu were portion of the eye socket to the posterior margin of the maintained individually in an aquarium (length 20 cm, carapace, abbreviated as POCL; Fitzpatrick, 1978) of each width 15 cm, height 15 cm) with recirculating filter system specimen was measured to the nearest 0.1 mm using dial and aeration. Water in the aquaria was changed every week. calipers. Because females reach maturity at approximately Gravel and shelter (plastic pipe of 10-cm length and 20-mm 20-mm POCL (Kawai et al., 1994, 1997), breeding status inner diameter) were provided to each aquarium. Water (with eggs, juveniles, or spermatophores) of females more temperature was controlled using a cooler with a thermostat than 20-mm POCL were recorded. Stages of juveniles were to give a mean 18.1 ± 0.3 SE, range 15.1–20.7°C, which is determined based on the morphology of the telson, after similar to the water temperature in the brook in Hamamasu. Scholtz and Kawai (2002); the first stage juveniles have a Flake type fish food (Tetra Werke Co., Ltd.) was added round-shaped telson with hook-like setae precursors along every day. Natural day length, using natural light, was 534 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 3, 2002 Downloaded from https://academic.oup.com/jcb/article/22/3/532/2679704 by guest on 02 October 2021 Fig. 2. Spermatophores attached to the ventral surface of a female (23.4-mm postorbital carapace length collected at Otaru, Hokkaido, Japan, 3 October 1999). Scale bar is 3 mm. maintained. After the juveniles had hatched, the behavior of first stage juveniles attached to females were 10 juveniles at each aquarium (total 100 individuals) was collected during the period from 19 July monitored daily for a 10-min period during 0900–1100 hours. The ethogram of juveniles was determined according (17.0°C) to 26 July (18.0°C). The second stage to Andrews (1916), Levi et al. (1999), Price and Payne juveniles, both attached to the mother and free- (1984), and Tack (1941). Dependent is defined as juveniles living at the bottom of the brook, were found clinging to the mother’s pleopods; exploration is when from 2 August (18.7°C) to 17 August (16.9°C). juveniles go on excursions but rapidly returned to their Females with spermatophores were collected mother when alarmed; and independent is permanent sepa- ration from mother. The stage of juveniles was observed every from 3 October (13.5°C) to 10 December three days. (4.0°C) in Otaru, and from 22 September (13.9°C) to 10 December (6.2°C) in Hamamasu RESULTS (Fig. 1). The spermatophores occurred only in Field Survey and around the annulus ventralis of females and In total 1,162 individuals were collected from were not spread over the sternum (Fig. 2). the two brooks (490 in Otaru, 672 in Hamama- su). In Otaru, the first stage juveniles were only Aquarium Observations found with females collected on 15 July (water In all ten aquaria, the first stage juveniles temperature, 15.1°C), and no free-living juve- cling to the pleopods of their mothers through niles of the first stages were collected at any date the second stage (Fig. 3). The duration of the (Fig. 1). Females with second stage juveniles first stage was 4.6 ± 0.2 SE (range, 4–6 days). occurred from 24 July (15.3°C) to 1 August That of the second stage was 27.1 ± 1.7 (24–38 (19.7°C). Free-living second stage juveniles d). The second stage juveniles initiated explora- were observed under the gravel from 28 July tion around their mother and eventually became (15.1°C) to 8 August (20.6°C). In Hamamasu, independent. However, in exception to this, a few KAWAI AND SCHOLTZ: REPRODUCTION OF JAPANESE CRAYFISH 535 Downloaded from https://academic.oup.com/jcb/article/22/3/532/2679704 by guest on 02 October 2021 Fig. 3. Behavior of juvenile under laboratory rearing conditions. Ten ovigerous females were kept in each aquarium, and behavior of 10 different juveniles at each aquarium (total 100 individuals) were monitored daily. Dependent is defined as juveniles clinging to the mother’s pleopods; exploration is when juveniles go on excursions but rapidly returned to their mother when alarmed; and independent is permanent separation from mother. juveniles from two females left their mothers in and sometimes even at the fourth stage (Price the third stage.
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