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Population Dynamics of Edible Sea Urchins Associated with Variability of Seaweed Beds in Northern Japan

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Population Dynamics of Edible Sea Urchins Associated with Variability of Seaweed Beds in Northern Japan Aqua-BioScience Monographs, Vol. 7, No. 2, pp. 47–78 (2014) www.terrapub.co.jp/onlinemonographs/absm/ Population Dynamics of Edible Sea Urchins Associated with Variability of Seaweed Beds in Northern Japan Yukio Agatsuma Laboratory of Marine Plant Ecology Graduate School of Agricultural Science Tohoku University Tsutsumidori-Amamiya 1-1, Aoba, Sendai, Miyagi 981-8555, Japan e-mail: [email protected] Abstract Received on October 1, 2013 Effects of variability of seaweed beds on population dynamics of sea urchins have not Accepted on December 24, 2013 been studied in detail. The present study documents that population dynamics of edible Online published on June 30, 2014 sea urchins is closely associated with variability of seaweed beds in subtidal rocky re- gions in northern Japan, from larval settlement, gonad production, somatic growth, re- Keyword cruitment and seasonal migration of the sea urchins Mesocentrotus nudus, • barren Strongylocentrotus intermedius and Hemicentrotus pulcherrimus. Dibromomethane • fucoid (DBM), which is produced abundantly by crustose coralline algae, induced larval meta- • kelp morphosis of more than 80% of individuals of M. nudus and S. intermedius in the pres- • settlement ence of 34–61 ppm within 24 h, indicating its instantaneous effect on a high success of • gonad production • somatic growth metamorphosis. Conversely, 2,4-dibromophenol (DBP) and 2,4,6-tribromophenol (TBP), • recruitment which are released from kelps Eisenia bicyclis and Ecklonia kurome, killed all eight- • range extension armed larvae of M. nudus and S. intermedius in the presence of 20–50 ppm. The larval • seasonal migration metamorphosis were significantly reduced in the presence of 1–10 ppm. These suggest • reseeding that the population size of these sea urchins is enhanced on coralline barrens and reduced • sea urchin in kelp forests. Population size of M. nudus was enhanced by episodic recruitment of • seaweed bed juveniles on crustose coralline barrens affected by large-scale oceanographic processes. Growth and gonad production of M. nudus and H. pulcherrimus is greatly affected by the amount and the kind of seaweed beds, which alter the states of crustose coralline flats and large perennial kelp or fucoid forests in the course of algal succession through ocea- nographic condition. The sea urchins migrate to seaweed beds to increase in gonad size toward maturation and spawning in the species-specific reproductive cycles to succeed in reproduction. Release of hatchery-raised seeds of S. intermedius into the wild and aquaculture of wild or hatchery-raised sea urchins fed on surplus or low-priced sea foods for humans enabled the sea urchins to increase the population size and improve the gonad production and somatic growth. 1. Introduction Clements et al. 1991; Tsukidate 1992). Sargassum beds trap nutrients and contribute to high rates of primary Kelp beds are the most productive ecosystem in the production (e.g. Wanders 1976). The highest annual world (Mann 1973; Fredriksen 2003; Rysgaard and production of 8.25 kg dry/m2 was recorded in Nielsen 2006). These provide habitat and shelter for Sargassum macrocarpum in Iida Bay, Ishikawa in the rich epibionts, invertebrates and fishes (Ghelardi 1971; Sea of Japan (Taniguchi and Yamada 1978). Duggins 1980; Schultze et al. 1990). They are a key Edible sea urchins are primary consumers in coastal source of carbon in the coastal food web (Dunton and rocky-bottom ecosystems and their main diet is ma- Schell 1987; Duggins et al. 1989). Fucoid beds also rine algae (De Ridder and Lawrence 1982). About 20 play an important role as habitat of diverse epibionts species of sea urchins are consumed in the world. Most (e.g. Edgar 1983, 1991; Coston-Clements et al. 1991; sea urchins belong to the order Echinoida. All the spe- Tsukidate 1992) and spawning of fish (Coston- cies inhabit shallow waters (Lawrence 2001). Since © 2014 TERRAPUB, Tokyo. All rights reserved. doi:10.5047/absm.2014.00702.0047 48 Y. Agatsuma / Aqua-BioSci. Monogr. 7: 47–78, 2014 Fig. 1. Landing (whole weight in tons) of sea urchins by year in Japan. Data are from Ministry of Agriculture, For- estry and Fisheries. early times, high grazing intensities of several species causing destruction of seaweed communities (termed “Isoyake” in Japan) have been reported (Lawrence 1975). Population size of the sea urchins is regulated by the apex predators sea otter and killer whale in Aleu- tian Islands, Alaska (Simenstad et al. 1978; Estes et al. 1998), recruitment and disease in Nova Scotia, Canada (Miller 1985; Hart and Scheibling 1988) and an apex predator Atlantic cod and sea urchin fishery in Fig. 2. Mesocentrotus nudus (A), Strongylocentrotus inter- medius (B) and Hemicentrotus pulcherrimus (C). Reprinted the Gulf of Maine (Steneck et al. 2002). This variabil- from Lawrence JM (ed), Edible Sea Urchins; Biology and ity of sea urchin population size forces to alter the states Ecology, Color plates, 186, 2007, with permission from of crustose collaine flats and kelp forests. By contrast, Elsevier. the effect of variability of seaweed beds on the popu- lation dynamics of sea urchins has not been studied in detail. In Japan, the six species of sea urchins 2. Settlement Mesocentrotus nudus (nee Strongylocentrotus nudus) (Tatarenko and Poltaraus 1993), Strongylocentrotus in- Edible sea urchins have a larval phase of 14–40 days termedius, Hemicentrotus pulcherrimus, and then settle (Lawrence 2001). Many metamorphosed Pseudocentrotus depressus, Heliocidaris crassispina juveniles are found on crustose coralline flats, which and Tripneustes gratilla are commercially harvested. are called “barren” (Cameron and Schroeter 1980; Heliocidaris crassispina has been studied as Rowley 1989; Sano et al. 1998; Balch and Scheibling Anthocidaris crassispina, but Anthocidaris is consid- 2000). Naidenko (1996) reported that glutamine or ered a junior synonym of Heliocidaris (Hart et al. glutamine mimetics may be active components of natu- 2011). The total catches (whole weight) decreased from ral inducers from calcareous algae. Kitamura et al. 23 000 metric tons in 1987 to 7 881 metric tons in 2011 (1993) reported that larval metamorphosis of P. (Fig. 1). The catches of M. nudus and S. intermedius, depressus and H. crassispina following larval contact which are caught in Tohoku and Hokkaido, account with the articulated coralline alga Corallina pilulifera for more than 70% of the total (Agatsuma et al. 2004). is due to eicosapentaenoic acid (EPA) produced in the The present study illustrates larval settlement, go- algal thalli. A chemical cue inducing a high metamor- nad production, somatic growth, recruitment and in- phic rate of the sea urchin Strongylocentrotus teractions with seaweed beds of the edible sea urchins droebachiensis larvae after their contact with the M. nudus, S. intermedius and H. pulcherrimus (Fig. 2), coralline algae Lithothamnion glaciale, Phymatolithon which are closely associated with variability of sea- laevigatum, Phymatolithon rugulosum and Corallina weed beds in subtidal rocky regions in northern Japan. officinalis is thought to be γ-aminobutyric acid (GABA) In addition, enhancement of population size, gonad (Pearce and Scheibling 1990). Glycoglycerolipids production and somatic growth of sea urchins are docu- (sulfoquinovosyl monoacylglycerols, sulfoquinovosyl mented. diacylglycerols, monogalactosyl monoacylglycerols, doi:10.5047/absm.2014.00702.0047 © 2014 TERRAPUB, Tokyo. All rights reserved. Y. Agatsuma / Aqua-BioSci. Monogr. 7: 47–78, 2014 49 monogalactosyl diacylglycerols, digalactosyl monoacylglycerols, and digalactosyl diacylglycerols) isolated from the green alga Ulvella lens have been identified as the chemical inducers of larval settlement and metamorphosis of S. intermedius (Takahashi et al. 2002). This alga has been used as a collector for set- tlement in artificial production because it induces meta- morphosis and settlement more strongly than attached diatoms (Kawamura et al. 1983; Hokkaido Institute of Mariculture 1992). Taniguchi et al. (1994) found that two articulated coralline algae Serraticardia mazima and Calliarthron yessoense, the crustose coralline alga (dominant species in coralline communities), and Ulvella lens all induce larval metamorphosis of M. nudus. They ascertained that dibromomethane (DBM), a volatile chemical produced by all these algae (Itoh and Shinya 1994; Ohshiro et al. 1999), induced 100% Fig. 3. Glass vessel used in this study for inducing larval of larvae to metamorphose within 2 h. In that experi- metamorphosis of M. nudus and S. intermedius by ment, larval metamorphic rate was examined in petri dibromomethane (DBM). (a) Upper vessel, (b) hydrophobic membrane, (c) filter, (d) lower vessel, (e) silicon rubber plug, dishes with seawater in which DBM was dissolved to (f) acrylic stand, (g) clamp. Reprinted from Aquaculture, 251, a relatively high concentration of approximately 700 Agatsuma et al., Instantaneous effect of dibromomethane on ppm. Moreover, the effect of exposure time of the lar- metamorphosis of larvae of the sea urchins vae to DBM was not examined. The fully developed Strongylocentrotus nudus and Strongylocentrotus interme- 8-armed larvae contact the surface of the corallines just dius, 549–557, 2006, with permission from Elsevier. before metamorphosis (Taniguchi et al. 1994). Hence, metamorphosis appears to be induced by immediate reception of DBM, constantly released from the corallines (Itoh and Shinya 1994). a new system that diffuses DBM through a
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