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Reproduction in the externally brooding sea anemone Epiactis georgiana in the Antarctic Peninsula and the Weddell Sea

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Abstract

External parental care is uncommon among actiniarians but common in Epiactis species. Here, several aspects of reproduction are analyzed for of one of them, Epiactis georgiana. Samples were collected in December, January, February, March, and April in the Antarctic Peninsula and the eastern Weddell Sea, during 1998, 2000, 2002, and 2003. Most sexually mature individuals of E. georgiana are male or female, but some are hermaphrodites. This is the first report of hermaphroditism in E. georgiana, which is the third species of the genus with this sexual pattern. The results suggest that oogenesis starts in December and that at least two generations of oocytes overlap; a third generation is often brooded externally. Putative fertilization is likely internal, and larvae and/or embryos are externally brooded on the distal part of the adult column until an advanced developmental stage. Apparently E. georgiana reproduces seasonally, probably releasing the embryos/larvae in the last months of the austral spring (December). Inter-individual variability was observed in gametogenesis. In addition, specimens from the Antarctic Peninsula were larger than those from the Weddell Sea. This study represents the first step in understanding the reproductive mode of E. georgiana.

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Acknowledgments

Special thanks are addressed to Prof. Dr. Wolf Arntz (Alfred-Wegener-Institute, Bremerhaven, Germany) who made possible our participation in several Antarctic projects and cruises. We extend our acknowledgements to the officers and crew of the R/V Polarstern and many colleagues on board during the EASIZ, ANDEEP, and BENDEX cruises for their valuable assistance. Thanks to M. Conradi (Universidad de Sevilla) who collected a considerable amount of the material analyzed in this manuscript. Comments from M. Daly, D. Fautin, and an anonymous reviewer substantially improved this manuscript. Support was provided by a MCT-CSIC grant (I3P-BPD2001-1) to E. Rodríguez and Spanish CICYT projects: ANT97-1533-E, ANT98-1739-E, ANT99-1608-E, REN2001-4269-E/ANT, REN2003-04236, and CGL2004-20141-E. This is a contribution to the SCAR program, Ecology of the Antarctic Sea Ice Zone (EASIZ) and ANDEEP contribution 159.

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Authors and Affiliations

  1. Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York, NY, 10024, USA

    E. Rodríguez

  2. Instituto Español de Oceanografía, Centro Oceanográfico de Baleares, Muelle de Poniente, s/n, 07015, Palma de Mallorca, Spain

    C. Orejas

  3. Biodiversidad y Ecología de Invertebrados Marinos, Departmento de Fisiología y Zoología, Facultad de Biología, Universidad de Sevilla, Reina Mercedes 6, 41012, Sevilla, Spain

    P. J. López-González

  4. Department of Biología Marina y Oceanografía, Institut de Ciències del Mar (CSIC), Passeig Marítim de la Barceloneta, 37–49, 08003, Barcelona, Spain

    J. M. Gili

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  1. E. Rodríguez
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Correspondence to E. Rodríguez.

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Communicated by J. P. Grassle.

E. Rodríguez and C. Orejas have equally contributed to this work.

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227_2012_2063_MOESM1_ESM.pdf

EMS 1 Data of specimens used in histological study. N is number of individuals studied. AP, Antarctic Peninsula; F, females; HP, Hermaphrodites; M, males; WS, Weddell Sea (PDF 84 kb)

227_2012_2063_MOESM2_ESM.tif

EMS 2 Epiactis georgiana, histological sections of spermatogenesis; a male gametes recognizable once grouped in cysts with 24–28 spermatogonia (E1), each covered by mesoglea, b spermatocytes visible after reaching a diameter of 5 µm in center of spermatogonia (E2), c spermatid (to 2 µm of diameter) in center of spermatic cyst, d at the end of spermatogenesis, spermatozoids (1 µm in diameter) visible in mature follicles (E3) filling center of cysts with tails converging to mesentery edge. Abbreviations: ga, gastrodermis; ms, mesoglea; sc, spermatocytes; sg, spermatogonia; sp, spermatic cyst; st, spermatid; sz, spermatozoids; t: spermatozoid tail. Scale bars: A, B, 50 µm; C, D, 0.1 mm (TIFF 58479 kb)

227_2012_2063_MOESM3_ESM.tif

EMS 3 Average measurements (± SD) of pedal disk size (mm), column height (mm) (right axis), and number of mesenteries (left axis) of female (F) and male (M) specimens in each pooled area (AP, Antarctic Peninsula; WS, Weddell Sea). N, number of individuals measured (TIFF 5983 kb)

227_2012_2063_MOESM4_ESM.pdf

EMS 4 Minimum and maximum values of range of diameter (µm) for oocytes and spermatic cysts for each month in each pooled area. Average diameter is expressed as mean (\( \bar{\rm X} \)) ± standard deviation (SD) for each oocyte category (previtellogenic, early vitellogenic, late vitellogenic, and early embryos/larvae) and spermatic cyst state defined (E1, E2, E3) in each studied month. N = number of female individuals; AP, Antarctic Peninsula; WS, Weddell Sea (PDF 96 kb)

227_2012_2063_MOESM5_ESM.tiff

EMS 5 Proportion (%) of different oocyte maturity stages, embryos/larvae, and juveniles in studied months and pooled areas. AP, Antarctic Peninsula; WS, Weddell Sea (TIFF 2022 kb)

227_2012_2063_MOESM6_ESM.tif

EMS 6 Example of observed variability in oocyte and spermatic cyst size frequency distribution among individuals in December and February between areas of study. AP, Antarctic Peninsula; WS, Weddell Sea (TIFF 15338 kb)

227_2012_2063_MOESM7_ESM.tif

EMS 7 Epiactis georgiana brooding specimens and juveniles; a, oral view of preserved female with embryos and/or larvae free in gastrovascular cavity (arrows), b preserved brooding female, c, detail of brooded juveniles. Scale bars: A, 10 mm; B, 50 mm; C, 20 mm (TIFF 28804 kb)

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Rodríguez, E., Orejas, C., López-González, P.J. et al. Reproduction in the externally brooding sea anemone Epiactis georgiana in the Antarctic Peninsula and the Weddell Sea. Mar Biol 160, 67–80 (2013). https://doi.org/10.1007/s00227-012-2063-x

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