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Variation in Gametophyte Dominance in Populations of Chondrus Verrucosus (Gigartinaceae, Rhodophyta)

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Variation in Gametophyte Dominance in Populations of Chondrus Verrucosus (Gigartinaceae, Rhodophyta) Phycological Research 2008; 56: 246–254 Variation in gametophyte dominance in populations of Chondrus verrucosus (Gigartinaceae, Rhodophyta) Alecia Bellgrove,1,2* and Masakazu N. Aoki1 1Shimoda Marine Research Center, University of Tsukuba, Shimoda, Shizuoka 415-0025, Japan, and 2School of Life & Environmental Sciences, Deakin University, Warrnambool, Victoria 3280, Australia 1996) and Sweden (Lindgren & Åberg 1996). More- SUMMARY over, studies have found that the pattern of gameto- phyte dominance for Chondrus crispus Stackhouse on We describe the abundance, including spatial and tem- rocky substrata is generally temporally stable over short poral variability, of phases of the isomorphic Chondrus (monthly) and long (annual to decadal) time-scales verrucosus Mikami from Japan. Chondrus verrucosus (May 1986; Scrosati et al. 1994; Scrosati & Mudge occurred in a dense (~90% cover) and temporally stable 2004a,b). In Japan, seasonal variation in the number of bed on a small, isolated rocky outcrop (Oyakoiwa) in fertile gametophytic and tetrasporophytic thalli has Shizuoka Prefecture. Small vegetative fronds were been examined for Chondrus yendoi Yamada et Mikami always much more abundant than large vegetative and (as Iridophycus cornucopia (Postels et Ruprecht) Set- fertile fronds over the spring to late summer periods in chell et Gardner – Hasegawa and Fukuhara 1952; 1999 and 2000. Over the same period, fertile car- Hasegawa and Fukuhara 1955), but no estimates of the posporophytic fronds were generally more abundant total proportions (including fertile and non-fertile thalli) than fertile tetrasporophytic fronds, and fertile male of gametophytes and tetrasporophytes in a population fronds appeared infrequently at low densities. Using have been made, despite the relatively high species the resorcinol-acetal test, we determined the proportion diversity within the Gigartinaceae in Japan. of gametophytes and tetrasporophytes in three popula- Chondrus verrucosus Mikami often occurs in isolated tions of C. verrucosus: Oyakoiwa and Noroshi (Shi- areas along the central Pacific coast of Japan, but zuoka) in the summers of 1999 and 2000 and usually in quite dense populations (>50% cover; A. Kamehana Point (Miyagi) in autumn 2000. All popula- Bellgrove, pers. obs. 1999–2008). This suggests that tions had a significantly higher proportion of gameto- this species is capable of both long-distance dispersal phytes than tetrasporophytes in both years, although as well as short-distance dispersal within a population gametophytic proportions were lower at Noroshi (~70%) and/or vegetative regeneration. Fertile thalli can be than at Oyakoiwa (~80%) and Kamehana Point observed all year round, but there have been no studies (~97%). However, examination of all isolated individu- of the seasonality of reproduction or relative differences als sampled on Noroshi showed equal proportions of between phases for this species. each phase in 1999, but gametophyte dominance Several models have been proposed in published (74%) in 2000. Differences in dispersal and reports to explain gametophyte dominance in the Gigar- spore production between phases are discussed as tinaceae (Bhattacharya 1985; Hannach & Santelices mechanisms potentially contributing to variation in 1985; May 1986; Luxoro & Santelices 1989; Gonzalez gametophyte dominance. & Meneses 1996; Lindgren & Åberg 1996; Fierst et al. 2005). However, for Chondrus verrucosus and other Key words: dispersal, gametophyte, isomorphic, Japanese Gigartinaceae, it is premature to test models macroalgae, phase dominance, resorcinol-acetal test, explaining mechanisms controlling population dynam- tetrasporophyte. ics, without first describing the patterns of distribution and any variability in these patterns (Underwood et al. 2000). Therefore, to assess the generality of patterns found for members of the Gigartinaceae in America and INTRODUCTION Gametophyte dominance has been described for several members of the Gigartinaceae in North America *To whom correspondence should be addressed. (Mathieson & Burns 1975; Craigie & Pringle 1978; Email: [email protected] Bhattacharya 1985; May 1986; Scrosati et al. 1994; Communicating editor: G. Zuccarello. Dyck & De Wreede 1995; Scrosati 1998), Chile Received 12 September 2007; accepted 17 May 2008. (Hannach & Santelices 1985; Gonzalez & Meneses doi: 10.1111/j.1440-1835.2008.00506.x Variation in phase dominance 247 platform by approximately 150 m. The second site, (a) (b) Shizugawa Noroshi, is a sharply sloping andesite (Machida 1972) rock wall on Cape Noroshi, demarcating the south-west Shizugawa Bay Japan boundary of the bay, and approximately 90 m from Kamehana Pt Oyakoiwa at the closest point. The third site, Kamehana S’gawa Point, is a gently sloping boulder shore composed of pretertiary sedimentary rock (Anon 1983). Chondrus Izu 01 km verrucosus occurs in a dense bed dominating the lower to mid-intertidal area of Oyakoiwa (40–80 cm above (c) (d) Oyakoiwa chart datum (nearly lowest low water), MN Aoki, Izu SMRC unpubl. data, 1998–2000) and in both dense and Peninsula sparse patches along Noroshi, within a 2 m band on the 0 near vertical wall. Similarly, it occurs in dense and Oura 200 Noroshi m Bay sparse patches in the lower to mid-intertidal area of Cape Noroshi Kamehana Point, but thalli are generally smaller than in Oura Bay 0200 m Oura Bay (A. Bellgrove, pers. obs. 2000). The tidal range for Oura Bay is 2 m (from 20 cm below to Fig. 1. Study area. (a) Japan, showing the locations of Izu Pen- 180 cm above chart datum); sea temperatures typically insula and Shizugawa Bay (S’gawa); (b) Shizugawa Bay, showing range from 13 to 27°C (14–26°C monthly means) and the location of Kamehana Point and the township of Shizugawa; air temperatures from 5 to 31°C (8–29°C monthly (c) Izu Peninsula; (d) Oura Bay, showing the location of Oyakoiwa means) (Shimoda Marine Research Center, unpubl. and the 200 m transect on Noroshi. SMRC, Shimoda Marine data, 1950–2008). The tidal range of Kamehana Point Research Center. is 170 cm (from 10 cm below to 160 cm above chart datum); sea temperatures typically range from 5 to 24°C (6–23°C monthly means) (Shizugawa Nature Europe, this study aimed to determine the proportion of Center, unpubl. data, 1999–2008) and air tempera- gametophytes and tetrasporophytes in three spatially tures for nearby Ishimaki city (38°25′N, 141°18′-E) isolated populations of C. verrucosus in Japan, and to range from -2.8 to 26.9°C (0.5–23.5°C monthly see whether these proportions varied annually. Addi- means) (SDMO 2005). Tides for both Oura and Shi- tionally, in one very dense population (Oyakoiwa) we zugawa Bays follow a mixed tidal pattern with typically examined the temporal stability of the population and two unequal ebb and two flood tides per lunar day; in the monthly variation in the production of fertile fronds Oura Bay, Oyakoiwa is usually only immersed on one relative to vegetative fronds over two successive spring low tide per day during spring tides, but high tides are to late summer periods. We hypothesized that the of relatively equal magnitude throughout both the lunar perennial habit of C. verrucosus would lead to popula- cycle and year. tions that are temporally and spatially stable with Although there have been no studies of wave expo- respect to abundance and proportions of gametophytes sure or water flow within Oura Bay, Machida (1972) and tetrasporophytes. Moreover, we expected these observed differences in wave cut benches suggesting populations to be gametophyte-dominated. In contrast, within-bay differences in wave action and abrasion we hypothesized that the periodicity of fertility amongst forces. Oyakoiwa and Noroshi are typically both moder- gametophytes and tetrasporophytes may be temporally ately exposed to wave action in an otherwise relatively variable. sheltered embayment (A. Bellgrove, pers. obs. 1999– 2008). However, Oura Bay is exposed to seasonal MATERIALS AND METHODS storms and typhoons (particularly in summer) where waves up to 1 m may enter the bay and wave forces Study sites increase, particularly over Oyakoiwa and Noroshi (A. Bellgrove, pers. obs. 1999–2006). Similarly, wave Sampling was conducted at two sites within Oura exposure has not been quantified at Kamehana Point, Bay, Izu Peninsula, Shizuoka Prefecture (34°40′N, but generally the reef is moderately exposed, with high 138°57′E) and one site close to the northern extent of wave exposure during seasonal storms and typhoons (K. the distribution of Chondrus verrucosus (Yoshida 1998; Tanaka, pers. comm. 2000). Tanaka 2004) at Kamehana Point, Shizugawa Bay, ′ ′ Miyagi Prefecture (38°38 N, 141°28 E), Japan Study species (Fig. 1). The first site, Oyakoiwa, is a small (7 m ¥ 5m) isolated rocky outcrop composed of tuff breccia Chondrus verrucosus is a dioecious, perennial, benthic (Machida 1972), separated from the nearest rock red alga that occurs in the eulittoral zone on rocky 248 A. Bellgrove and M. N. Aoki substrata, primarily in the central region of the Pacific als in 1999 and 2000, respectively). The potential for coast of Japan (Mikami 1965; Yoshida 1998). Although spore coalescence in the Gigartinaceae is recognized the life cycle of C. verrucosus has not specifically been (Tveter & Mathieson 1976; Santelices et al. 1999) but studied, it is assumed to follow the triphasic life cycle for the purposes of this study, an individual was defined of other members of the genus (Taylor & Chen 1994). as one clump of upright fronds, which may have formed Gametophytes and tetrasporophytes are morphologi- either from a single spore (genet) or from coalescence cally similar. Tetraspores give rise to male and female of two or more spores (consistent with Scrosati & gametophytes and carposporophytes then develop in Mudge 2004b). Where the boundary between adjacent the female gametangia after in situ fertilization. Car- clumps was unclear due to the diffuse holdfast, we pospores then give rise to tetrasporophytes. As fertili- conservatively grouped potentially two clumps as one. zation occurs in situ, the main dispersive propagules The population on Noroshi stretches for over 200 m, are assumed to be the carpospores and tetraspores. but within a narrow vertical belt.
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