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Aspects of the Larval Biology of the Sea Anemones Anthopleura Elegantissima and A

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Aspects of the Larval Biology of the Sea Anemones Anthopleura Elegantissima and A Invertebrate Biology 121(3): 190-201. 0 2002 American Microscopical Society, Inc. Aspects of the larval biology of the sea anemones Anthopleura elegantissima and A. artemisia Virginia M. Weis,a E. Alan Verde, Alena Pribyl,” and Jodi A. Schwarz Department of Zoology, Oregon State University, Corvallis, OR 9733 1, USA Abstract. We investigated several aspects of the larval biology of the anemone Anthopleura elegantissima, which harbors algal symbionts from two different taxa, and the non-symbiotic A. artemisiu. From a 7-year study, we report variable spawning and fertilization success of A. elegantissima in the laboratory. We examined the dynamics of symbiosis onset in larvae of A. elegantissima. Zoochlorellae, freshly isolated from an adult host, were taken up and retained during the larval feeding process, as has been described previously for zooxanthellae. In ad- dition, larvae infected with zooxanthellae remained more highly infected in high-light condi- tions, compared to larvae with zoochlorellae, which remained more highly infected in low-light conditions. These results parallel the differential distribution of the algal types observed in adult anemones in the field and their differential tolerances to light and temperature. We report on numerous failed attempts to induce settlement and metamorphosis of larvae of A. elegun- tissima, using a variety of substrates and chemical inducers. We also describe a novel change in morphology of some older planulae, in which large bulges, resembling tentacles, develop around the mouth. Finally, we provide the first description of planulae of A. artemisia and report on attempts to infect this non-symbiotic species with xooxanthellae and zoochlorellae. Additional key words: Cnidaria, Anthozoa, Actiniaria, larval settlement, melainorphic induccr, symbiosis, zoochlorellae, zooxanthellae The 4 species of the sea anemone genus Anthopleu- the late summer. Siebert (1 974) and Smith (I 986) ex- ra found along the western coast of North America- amined laboratory-induced spawning, embryological A. ekgantissima (BRANDT 18%), A. soh (PEARSE& development, and morphology and behavior of plank- FRANCIS2000), A. xanthogrammica (BIIANDTI835), totrophic planula larvae of A. elegantissima and A. and A. avtemisia (DANA1846)-are conspicuous mem- xanthogrammica. Finally, Sebens ( 198 1 a, 1982) de- bers of rocky intertidal communities. A. elegantissima scribed recruitment of larvae from both species into in particular, which is common along the coast from mussel beds adjacent to sites with adult anemones. No Alaska to Baja California, can form clonal aggrega- life history studies have focused on either A. sola or tions that occupy large areas within the mid-intertidal A. artemisia. zone, to the exclusion of other competitors (Dayton A. elegantissima and A. xunthogmmmica form sym- 1971; Sebens 1981a; Fitt et al. 1982). Despite their bioses with two different types of unicellular algae importance in these communities, examination of the (Muscatine 197 1 ; Muller-Parker & Davy 200 1 ), di- sexual reproductive cycle and life histories of these noflagellates from the genus Symhiodinium (zooxan- anemones has been restricted to a handful of studies. thellae, LaJeunesse & Trench 2000) and one or more Ford (1 964), Jennison (1 979), and Sebens (1 98 1 b) de- taxonomically undescribed chlorophytes (zoochlorel- scribed gametogenesis and an annual reproductive cy- he). As in other cnidarian-algal symbioses, the algae cle in A. elegantissima and A. xanthogrammica that provide the anemones with photosynthetically fixed or- started with gonad development (both species are di- ganic carbon and the host anemone in turn supplies oecious) in the late fall and ended with spawning in the algae with inorganic nutrients, a stable environ- ment, and a refuge from herbivory (reviewed in Mus- ’’ Author for correspondence. Ph: 541-737-4359. Fax: 541- catine 1990; Muscatine & Weis 1992; Muller-Parker 737-050 1. E-mail: [email protected] & D’Elia 1997). Anemones of both species containing ‘’ Present address: Center for Liinnology, University of Col- these different algal types are differentially distributed orado, Boulder, CO 80309, USA along a latitudinal and tidal-height gradient, with Larval biology of Anthopleura eleguntissimu 191 anemones in more northerly and lower intertidal lo- 1988) and the scleractinian coral Fungia scuturia cations containing predominantly zoochlorellae and (Krupp 1983; Schwarz et al. 1999). anemones in more southerly and higher intertidal lo- What started as the search for an ideal model for cations containing predominantly zooxanthellae (Bates the study of cnidarian larval biology and symbiosis 2000; Secord & Augustine 2000). onset has instead developed into a 7-year love/hate re- This distribution of algal types has been attributed lationship with larvae of A. elegantissima. Despite our to differential physiological tolerance of the algae to best efforts, answers to key questions surrounding de- temperature and light, with zooxanthellae well adapted velopmental processes, such as spawning and fertiliza- to relatively high-light and warm conditions compared tion patterns and settlement and metamorphosis, re- to zoochlorellae, which are better adapted to cooler, main elusive. Here we report results from studies on lower-light environments (Verde & McCloskey symbiosis onset, specifically in the examination of in- 1996a,b, 2001, in press; Saunders & Muller-Parker fection dynamics of the larvae by both zooxanthellae 1997). A. soh, a newly described, solitary sister spe- and zoochlorellae and in the differential infection by cies to A. eleguntissima (Francis 1979; McFadden et zooxanthellae and zoochlorellae as a function of light al. 1997; PEARSE& FRANCIS2000), is restricted to lat- regime. We describe a morphological change in some itudes below the likely southern limit of zoochlorellae mature larvae that may represent the development of (Secord & Augustine 2000) and is symbiotic only with tentacles before settlement. Further, we provide the zooxanthellae. A. artemisia is a non-symbiotic species first description of larvae of A. artemisia and the re- (Hand 1955; PEARSE& FRANCIS2000). Recent molec- sponse of this non-symbiotic species to exposure to ular phylogenetic studies have grouped A. elegantis- zooxanthellae and zoochlorellae. We also report on sima,A. sola, and A. xunthogrummica into an eastern some key failures in our examinations of larval A. ele- Pacific clade, whereas A. artemisia groups with other guntissima. We describe variability in spawning and conspecifics in a distinct western Pacific clade, despite fertilization success through the study period, that has its occurrence in the eastern Pacific (Geller & Walton hampered our ability to continue studies of larvae. In 2001). addition, we describe our numerous failed attempts to Larvae of A. ekgnntissima and A. xanthogrummica induce settlement and metamorphosis of thcsc larvae, are oval planulae, - 150 pm long and 100 p,m wide with the aim of preventing repetition of thesc ap- with a conspicuous apical tuft of numerous elongate proaches by other researchers in future studies. cilia present at the aboral pole (Siebert 1974). They swim actively in the water column (Siebert 1974), feed Methods by extrusion of a mucous thread that traps food (Sie- Animal maintenance, gamete collection, and larval bert 1974; Schwarz et al. 2002), and persist in culture cultures for as long as 3 months (Smith 1986). Despite attempts by many workers to induce settlement by the addition Adults of Anthopleura elegantissima, to be used as of various natural substrates, such as mussel shells, broodstock and as sources of freshly isolated algae, rocks, and macrophytes, to larval cultures (Siebert were collected at various times from 1990 to 2001, 1974; Smith I986), no larvae have ever been observed from the following locations along the Pacific coast of to undergo settlement and metamorphosis. the U.S.: Santa Cruz, California; Strawberry Hill, Nep- Gametes and larvae of A. elegantissima and A. xun- tune Beach, Seal Rock, and Boiler Bay, Oregon; and thogrammica lack symbiotic algae (Siebert 1974). Swirl Rocks, Washington. Zooxanthellat-e animals These anemones must therefore acquire symbionts were collected from all locations, but all zoochlorellate from the environment during their development. We animals were collected at Swirl Rocks. Experimcnts in were initially interested in larvae of A. elegantissima 1995 and 1996 were performed at Long Marinc Lab- as a model for the study of the onset of symbiosis oratory (University of California Santa Cruz) in Santa between sexually produced cnidarian offspring and Crux, California; those in 1997-200 1 were performed their symbiotic zooxanthellae. Symbiosis onset in A. at Hatfield Marine Science Center (Oregon State Uni- elegantissima can begin in the larval phase during the versity) in Newport, Oregon; and those in the summer feeding process, whereby zooxanthellae, freshly iso- of 2000 were performed at Walla Walla College Ma- lated from adults, are taken in along with food rine Station, Anacortes, Washington. All foreign ma- (Schwarz et al. 2002). Algae are phagocytized by host terial adhering to the anemones (e.g., fragments of gastrodermal cells and ultimately persist in the gas- shell and macroalgae) was removed after collection trodermal tissue. A similar process of algal acquisition and individual anemones were allowed to attach to (infection) by feeding during the larval stage has been bricks (3-10 anemones
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