Advertisement

Marine Biology

, 166:111 | Cite as

Reproduction of the anthozoan Anemonia sulcata (Pennant, 1777) in southern Spain: from asexual reproduction to putative maternal care

  • Olga Utrilla
  • Juan Diego Castro-Claros
  • Javier Urra
  • Francisco David Navas
  • Carmen SalasEmail author
Original Paper

Abstract

Anemonia sulcata (Pennant, 1777) is a common shallow water cnidarian from rocky platform and boulder beaches in southern Spain, where it is a popular seafood item with an increasing fishery. To aid in the management of a sustainable fishery, a study on the reproduction of A. sulcata in the littoral of Malaga (southern Spain) was performed from November 2014 to September 2015, using histological methods. A total of 123 specimens were examined, with a size range (as diameter of the pedal disc) from 1.1 to 48.2 mm. The sex ratio was significantly biased to females, with 1.7 females: 1 male (χ2 = 4.45, p < 0.01). The spermatozoids and oocytes arise from the endodermal cells. The mature oocytes receive nutritive filaments (trophonema) from the endoderm cells. There were zooxanthellae in the mesenteries, tentacles and also inside the oocytes. A gastrula was observed in one individual, as well as several planula larvae in different degree of development in others. Asexual reproduction by internal budding was observed in some individuals. The studied population showed an extended reproductive cycle with a peak of spawning in April. The size and weight of sexual maturity of the studied population were 21.5 mm and 16.5 g, respectively. A positive significant correlation was observed between size and weight of individuals. We suggest that the diameter of the pedal disc should be used as the legal parameter for the management of this fishery, as this measurement is easier to take by fishermen at sea than the weight, the current legal parameter.

Notes

Acknowledgements

We thank Cristina Lucena Serrano and Gregorio Martin Caballero, technicians of the SCAI (Servicios Centrales de Apoyo a la Investigación, Universidad de Málaga) for helping in sample processing for Transmission and Scanning Electron Microscopy respectively. Special thanks are given to Serge Gofas (Dept. Biología Animal, Universidad de Malaga) for helping with the illustrations.

Funding

Field work and laboratory procedures have been supported by the Department of Animal Biology of the University of Malaga (Spain).

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of the animals were followed.

References

  1. Bingham BL, Dimond JL, Muller-Parker G (2014) Symbiotic state influences life-history strategy of a clonal cnidarian. Proc R Soc B 281:20140548.  https://doi.org/10.1098/rspb.2014.0548 CrossRefPubMedGoogle Scholar
  2. Bocharova ES (2016) Reproduction of Sea Anemones and other Hexacorals. In: Goffredo S, Dubinsky Z (eds) The Cnidaria, past, present and future. Springer, Basel, pp 239–248.  https://doi.org/10.1007/978-3-319-31305-4_15 CrossRefGoogle Scholar
  3. Bocharova ES, Kozevich IA (2011) Modes of reproduction in Sea Anemones (Cnidaria, Anthozoa). Biol Bull 38:849–860.  https://doi.org/10.1134/S1062359011090020 CrossRefGoogle Scholar
  4. Brandt K (1883a) Über die morphologische und physiologische Bedeutung des Chlorophylls bei Thieren. 2. Artikel. Mittheilungen aus der Zoologischen Station zu Neapel 2:191–302 (pl. 19–20; Anemonia pp. 257–265) Google Scholar
  5. Brandt K (1883b) Ueber Symbiose von Algen und Thieren. Arch fur Physiol 1883:445–454Google Scholar
  6. Carter MA, Thorp CH (1979) The reproduction of Actinia equina L. var. mesembryanthemum. J Mar Biol Assoc UK 59:989–1001.  https://doi.org/10.1017/S0025315400036985 CrossRefGoogle Scholar
  7. Cazurro M (1892–1893) Anemonia sulcata Pennant. Estudio anatómico-histológico de una actinia. An Soc Esp Hist Nat 4:307–379 (1–28 figs) Google Scholar
  8. Chen C, Soong K, Chen CA (2008) The smallest oocytes among broadcast-spawning actiniarians and a unique lunar reproductive cycle in a unisexual population of the sea anemone, Aiptasia pulchella (Anthozoa: Actiniaria). Zool Stud 47:37–45Google Scholar
  9. Chia FS (1976) Sea anemone reproduction: patterns and adaptive radiations. In: Mackie GO (ed) Coelenterate ecology and behavior. Springer, Boston, pp 261–270CrossRefGoogle Scholar
  10. Chia FS, Rostron MA (1970) Some aspects of the reproductive biology of Actinia equina L. (Cnidaria: Anthozoa). J Mar Biol Assoc UK 50:253–264CrossRefGoogle Scholar
  11. Clark WH, Dewel WC (1974) The structure of the gonads, gametogenesis, and sperm-egg interactions in the Anthozoa. Am Zool 14:495–510.  https://doi.org/10.1093/icb/14.2.495 CrossRefGoogle Scholar
  12. Daza JL, del Castillo F, Marquez I (2002) La pesquería del erizo y la anémona de mar en el litoral de Cádiz y Málaga. Junta de Andalucía, Consejeria de Agricultura y Pesca, Sevilla, 105p. ISBN 84-8474-041-2Google Scholar
  13. Dewel WC, Clark WH (1972) An ultrastructural investigation of spermiogenesis and the mature sperm in the anthozoan Bunodosoma cavernata (Cnidaria). J Ultrastruct Res 40:417–431CrossRefGoogle Scholar
  14. Driscoll PC, Clore GM, Beress L, Gronenborn AM (1989) A proton nuclear magnetic resonance study of the antihypertensive and antiviral protein BDS-I from the Sea Anemone Anemonia sulcata: sequential and stereospecific resonance assignment and secondary structure. Biochem 28:2178–2187CrossRefGoogle Scholar
  15. Dunn DF (1975) Reproduction of the externally brooding sea anemone Epiactis prolifera Verrill, 1869. Biol Bull 148:199–218CrossRefGoogle Scholar
  16. Eckelbarger KJ, Hand C, Uhlinger KR (2008) Ultrastructural features of the trophonema and oogenesis in the starlet sea anemone, Nematostella vectensis (Edwardsiidae). Invert Biol 127:381–395.  https://doi.org/10.1111/j.1744-7410.2008.00146 CrossRefGoogle Scholar
  17. Fautin DG (2002) Reproduction of Cnidaria. Can J Zool 80:1735–1754.  https://doi.org/10.1139/Z02-133 CrossRefGoogle Scholar
  18. Fautin DG, Mariscal RN (1991) Cnidaria: Anthozoa. In: Harrison FW, Westfall JA (eds) Microscopic anatomy of invertebrates. 2: Placozoa, Porifera, Cnidaria, and Ctenophora. Wiley, New York, pp 267–358Google Scholar
  19. Gashout SE, Ormond RF (1979) Evidence for parthenogenetic reproduction in the sea anemone Actinia equina L. J Mar Biol Ass UK 59:975–987CrossRefGoogle Scholar
  20. Goffredo S, Telò T, Scanabissi F (2000) Ultrastructural observations of the spermatogenesis of the hermaphroditic solitary coral Balanophyllia europea (Anthozoa, Scleractinia). Zoomorphology 119:231–240CrossRefGoogle Scholar
  21. Grajales A, Rodríguez E, Thornhill DJ (2016) Patterns of Symbiodinium spp. associations within the family Aiptasiidae, a monophyletic lineage of symbiotic of sea anemones (Cnidaria, Actiniaria). Coral Reefs 35:345–355.  https://doi.org/10.1007/s00338-015-1352-5 CrossRefGoogle Scholar
  22. Gutiérrez M (1967) Coloración histológica para el ovario de peces, crustáceos y moluscos. Inv Pesq 31:265–271Google Scholar
  23. Hertwig R (1882) Report on the Actiniaria dredged by H. M. S. Challenger, during the years 1873–1876. Zoology, WashingtonCrossRefGoogle Scholar
  24. Hiscock K, Southward A, Tittley I, Hawkins S (2004) Effects of changing temperature on benthic marine life in Britain and Ireland. Aquat Conserv Mar Freshw Ecosyst 14:333–362.  https://doi.org/10.1002/aqc.628 CrossRefGoogle Scholar
  25. Hofrichter R (2005) El Mar Mediterráneo: Fauna, Flora, Ecología. II/1 Guía sistemática y de identificación. Omega, Barcelona, 849p. ISBN 84-282-1355-0Google Scholar
  26. Hyman LH (1940) The Invertebrates: protozoa through ctenophora. McGraw-Hill, New York, pp 566–599Google Scholar
  27. Kahng SE, Benayahu Y, Lasker HR (2011) Sexual reproduction in octocorals. Mar Ecol Prog Ser 443:265–283.  https://doi.org/10.3354/meps09414 CrossRefGoogle Scholar
  28. Larkman AU (1984) An ultrastructural study of the establishment of the testicular cysts during spermatogenesis in the Sea Anemone Actinia fragacea (Cnidaria: Anthozoa). Gamete Res 9:303–327CrossRefGoogle Scholar
  29. Larkman AU, Carter MA (1982) Preliminary ultrastructural and autoradiographic evidence that the trophonema of the sea anemone Actinia fragacea has a nutritive function. Int J Invertebr Reprod 4:375–379CrossRefGoogle Scholar
  30. Larson P (2017) Brooding sea anemones (Cnidaria: Anthozoa: Actiniaria): paragon of diversity in mode, morphology, and maternity. Invert Biol 136:92–112.  https://doi.org/10.1111/ivb.12159 CrossRefGoogle Scholar
  31. Loseva LM (1971) Observations on Oogenesis of actinians. II. Oogenesis in Tealia crassicornis (Muell), Metridium senile (L.) and Protanthea simplex (Carlg.). Vestn Leningr Univ Biol 9:22–29Google Scholar
  32. Lyke EB, Robson EA (1975) Spermatogenesis in Anthozoa: differentiation of the Spermatid. Cell Tissue Res 157:185–205.  https://doi.org/10.1007/BF00222065 CrossRefPubMedGoogle Scholar
  33. Mercier A, Sun Z, Hamel JF (2011) Internal brooding favours pre-metamorphic chimerism in a non-colonial cnidarian, the sea anemone Urticina feline. Proc R Soc B Biol Sci 278:3517–3522.  https://doi.org/10.1098/rspb.2011.0605 CrossRefGoogle Scholar
  34. Moiseeva E, Rabinowitz C, Paz G, Rinkevich B (2017) Histological study on maturation, fertilization and the state of gonadal region following spawning in the model sea anemone, Nematostella vectensis. PLoS One 12(8):e0182677.  https://doi.org/10.1371/journal.pone.0182677 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Nyholm KG (1943) Zur Entwicklung und Entwicklungsbiologie der Ceriantharien und Anktinien. Zool Bidr Uppsala 22:87–248Google Scholar
  36. Ocaña O, den Hartog JC (2002) A catalogue of actiniaria and corallimorpharia from the Canary Islands and from Madeira. Arquipelago. Life Mar Sci 19:33–54Google Scholar
  37. Ocaña O, den Hartog JC, Brito A, Moro L, Herrera R, Martín J, Ramos A, Ballesteros E, Bacallado JJ (2015) A survey on Anthozoa and its habitats along the Northwest African coast and some islands: new records, descriptions of new taxa and biogeographical, ecological and taxonomical comments. Part I. Rev Acad Canar Cienc 27:9–66Google Scholar
  38. Orr J, Thorpe JP, Carter MA (1982) Biochemical genetic confirmation of the asexual reproduction of brooded offspring in the Sea Anemone Actinia equina. Mar Ecol Prog Ser 7:227–229CrossRefGoogle Scholar
  39. Orton JH (1920) Sea-temperature, breeding and distribution in marine animals. J Mar Biol Assoc UK 12:339–366CrossRefGoogle Scholar
  40. Schäfer W (1981) Reproduction and sexuality of Cereus pedunculatus and Actinia equina (Anthozoa, Actiniaria). Helgoländer Meeresunters 34:451–461CrossRefGoogle Scholar
  41. Schäfer W (1984) Reproduction and development of Anemonia sulcata (Anthozoa, Actiniaria). I. Reproductive cycle and oocyte structure before and after insemination. Helgoländer Meeresunters 38:135–148Google Scholar
  42. Schäfer W (1985) Reproduction and development of Anemonia sulcata (Anthozoa, Actiniaria). II. Early development, blastula and gastrula. Helgoländer Meeresunters 39:341–356CrossRefGoogle Scholar
  43. Schick JM (1991) Energy metabolism and respiratory gas exchange. In: Callow P (ed) A functional biology of sea anemones. Springer, Dordrecht, pp 119–173CrossRefGoogle Scholar
  44. Schmidt H (1970) Anthopleura stellula (Actiniaria, Actiniidae) and its reproduction by transverse fission. Mar Biol 5:245–255CrossRefGoogle Scholar
  45. Scott A, Harrison PL (2009) Gametogenic and reproductive cycles of the sea anemone, Entacmaea quadricolor. Mar Biol 156:1659–1671.  https://doi.org/10.1007/s00227-009-1201-6 CrossRefGoogle Scholar
  46. Sebens KP (1982) Asexual reproduction in Anthopleura elegantissima (Anthozoa: Actiniaria): seasonality and spatial extent of clones. Ecology 63:434–444CrossRefGoogle Scholar
  47. Shick JM, Lamb AN (1977) Asexual reproduction and genetic population structure in the colonizing sea anemone Haliplanella luciae. Biol Bull 153:604–617CrossRefGoogle Scholar
  48. Siebert AE, Spaulding JG (1976) The taxonomy, development and brooding behavior of the anemone, Cribrinopsis fernaldi sp. nov. Biol Bull 150:128–138CrossRefGoogle Scholar
  49. Smith HG (1939) The significance of the relationship between actinians and zooxanthellae. J Exp Biol 16:334–345Google Scholar
  50. Stephenson TA (1929) On methods on reproduction as specific characters. J Mar Biol Ass UK 16:131–172CrossRefGoogle Scholar
  51. Tirado C, Salas C (1998) Reproduction and fecundity of Donax trunculus L., 1758 (Bivalvia: Donacidae) in the littoral of Malaga (southern Spain). J Shellfish Res 17:169–176Google Scholar
  52. Tirado C, Rueda JL, Salas C (2011) Reproductive cycles in Atlantic and Mediterranean populations of Venus nux Gmelin, 1791 (Bivalvia: Veneridae), from southern Spain. J Shellfish Res 30:813–820CrossRefGoogle Scholar
  53. Trapani MR, Parisi MG, Toubiana M, Coquet L, Jouenne T, Roch P, Cammarata M (2014) First evidence of antimicrobial activity of neurotoxin 2 from Anemonia sulcata (Cnidaria). Invert Surv J 11:182–191Google Scholar
  54. Trippel EA, Harvey HH (1991) Comparison of methods used to estimate age and length of fishes at sexual maturity using populations of white sucker (Catostomus commersoni). Can J Fish Aquat Sci 48:1446–1495.  https://doi.org/10.1139/f91-172 CrossRefGoogle Scholar
  55. Vargas-Yáñez M, García MJ, Salat J, García-Martínez MC, Pascual J, Moya F (2008) Warming trends and decadal variability in the Western Mediterranean shelf. Glob Planet Change 63:177–184.  https://doi.org/10.1016/j.gloplacha.2007.09.001 CrossRefGoogle Scholar
  56. Vargas-Yáñez M, Moya F, García-Martínez MC, Tel E, Zunino P, Plaza F, Salat J, Pascual J, López-Jurado JL, Serra M (2010) Climate change in the Western Mediterranean Sea 1900–2008. J Mar Syst 82:171–176.  https://doi.org/10.1016/j.jmarsys.2010.04.013 CrossRefGoogle Scholar
  57. Vargas-Yáñez M, García-Martínez MC, Moya F, Balbín R, López-Jurado JL, Serra M, Zunino P, Pascual J, Salat J (2017) Updating temperature and salinity mean values and trends in the Western Mediterranean: The RADMED project. Prog Oceanogr 157:27–46CrossRefGoogle Scholar
  58. Visram S, Wiedenmann J, Douglas AE (2006) Molecular diversity of symbiotic algae of the genus Symbiodinium (Zooxanthellae) in cnidarians of the Mediterranean Sea. J Mar Biol Assoc UK 86:1281–1283.  https://doi.org/10.1017/S0025315406014299 CrossRefGoogle Scholar
  59. Wedi SE, Dunn DF (1983) Gametogenesis and reproductive periodicity of the subtidal sea anemone Urticina lofotensis (Coelenterata: Actinaria) in California. Biol Bull 165:458–472CrossRefGoogle Scholar
  60. Wiedenmann J, Elke C, Spindler KD, Funke W (2000) Cracks in the β-can: fluorescent proteins from Anemonia sulcata (Anthozoa, Actinaria). Proc Natl Acad Sci USA 97:14091–14096.  https://doi.org/10.1073/pnas.97.26.14091 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departamento de Biología Animal, Facultad de CienciasUniversidad de MálagaMálagaSpain
  2. 2.Centro Oceanográfico de Fuengirola, Instituto Español de OceanografíaFuengirolaSpain
  3. 3.Servicios Centrales de InvestigaciónUniversidad de MálagaMálagaSpain

Personalised recommendations