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The reproductive cycle of the sea urchin Arbacia lixula in northwest Mediterranean: potential influence of temperature and photoperiod

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Abstract

We studied the reproductive cycle of the sea urchin Arbacia lixula in a subtidal population from northeast Spain over four years using a gonadosomatic index (GSI) and gonad histology. Our results show that the GSI of A. lixula follows a seasonal cycle which peaks in May–July and attains its lowest values in October–November every year. The time course of the GSI matched closely the photoperiod cycle. We also found a remarkable inter-annual variability in the maximum value of GSI, which correlated with mean water temperature during the gonad growth period (winter and spring). Gonad histology was also in agreement with a single gametogenic cycle per year in this species. We explored the application of circular statistics to present and analyse gonadal development data, which allowed us to adequately handle the high intra-individual variability detected, with several developmental stages commonly found within the same gonad. The picture that emerged is one of a gametogenic timing driven by photoperiod, while the amount of reproductive output is determined by temperature. This is coherent with the tropical origin of the species and lends support to recent warnings about an increase in the abundance of this species in the Mediterranean as a result of global warming, with associated increased impact potential in sublittoral communities.

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References

  • Ballesteros E (1988) Composición y estructura de la comunidad infralitoral de Corallina elongata Ellis & Solander 1786, de la Costa Brava (Mediterráneo Occidental). Inv Pesq 52:135–151

    Google Scholar 

  • Ballesteros E (1993) Species composition and structure of a photophilic algal community dominated by Halopteris scoparia (L.) Sauvageau from the North-Western Mediterranean. Collect Bot (Barcelona) 22:5–24

    Google Scholar 

  • Barbaglio A, Sugni M, Di Benedetto C, Bonasoro F, Schnell S, Lavado R, Porte C, Candia-Carnevali DM (2007) Gametogenesis correlated with steroid levels during the gonadal cycle of the sea urchin Paracentrotus lividus (Echinodermata: Echinoidea). Comp Biochem Physiol A Mol Integr Physiol 147:466–474

    Article  Google Scholar 

  • Bay-Schmith E, Pearse JS (1987) Effect of fixed daylengths on the photoperiod regulation of gametogenesis in the sea urchin Strongylocentrotus purpuratus. Invertebr Reprod Dev 11:287–294

    Article  Google Scholar 

  • Benedetti-Cecchi L, Bulleri F, Cinelli F (1998) Density dependent foraging of sea urchins in shallow subtidal reefs on the west coast of Italy (Western Mediterranean). Mar Ecol Prog Ser 163:203–211

    Article  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188. doi:10.1214/aos/1013699998

    Article  Google Scholar 

  • Bonaviri C, Vega Fernández T, Fanelli G, Badalamenti F, Gianguzza P (2011) Leading role of the sea urchin Arbacia lixula in maintaining the barren state in southwestern Mediterranean. Mar Biol 158:2505–2513

    Article  Google Scholar 

  • Booth JG, Hall P, Wood ATA (1993) Balanced importance resampling for the bootstrap. Ann Stat 21:286–298

    Article  Google Scholar 

  • Brewin PE, Lamare MD, Keogh JA, Mladenov PV (2000) Reproductive variability over a four-year period in the sea urchin Evechinus chloroticus (Echinoidea: Echinodermata) from differing habitats in New Zealand. Mar Biol 137:543–557. doi:10.1007/s002270000366

    Article  Google Scholar 

  • Brogger MI, Martinez MI, Penchaszadeh PE (2010) Reproduction of the sea urchin Arbacia dufresnii (Echinoidea: Arbaciidae) from Golfo Nuevo, Argentina. J Mar Biol Assoc UK 90:1405–1409

    Article  Google Scholar 

  • Bulleri F, Benedetti-Cecchi L, Cinelli F (1999) Grazing by the sea urchins Arbacia lixula L. and Paracentrotus lividus Lam. in the Northwest Mediterranean. J Exp Mar Biol Ecol 241:81–95. doi:10.1016/S0022-0981(99)00073-8

    Article  Google Scholar 

  • Byrne M (1990) Annual reproductive cycles of the commercial sea urchin Paracentrotus lividus from an exposed intertidal and a sheltered subtidal habitat on the west coast of Ireland. Mar Biol 104:275–289

    Article  Google Scholar 

  • Canty A, Ripley B (2009) Boot: Bootstrap R (S-Plus) functions. R package version 1.2-41. http://cran.r-project.org/web/packages/boot/index.html. Accessed 27 Oct 2012

  • Cerrano C, Bavestrello G, Bianchi CN, Cattaneo-Vietti R, Bava S, Morganti C, Morri C, Picco P, Sara G, Schiaparelli S, Siccardi A, Sponga F (2000) A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (North-western Mediterranean), summer 1999. Ecol Lett 3:284–293

    Article  Google Scholar 

  • Cohen J, Foster J, Barlow M, Saito K, Jones J (2010) Winter 2009–2010: a case study of an extreme Arctic oscillation event. Geophys Res Lett 37:L17707. doi:10.1029/2010GL044256

    Google Scholar 

  • Dumont C, Pearce CM, Stazicker C, An YX, Keddy L (2006) Can photoperiod manipulation affect gonad development of a boreo-arctic echinoid (Strongylocentrotus droebachiensis) following exposure in the wild after the autumnal equinox? Mar Biol 149:365–378

    Article  Google Scholar 

  • Ebert TA (1968) Growth rates of the sea urchin Strongylocentrotus purpuratus related to food availability and spine abrasion. Ecology 49:1075–1091

    Article  Google Scholar 

  • Efron B (1987) Better bootstrap confidence intervals. J Am Stat Assoc 82:171–185

    Article  Google Scholar 

  • Fenaux L (1968) Maturation des gonades et cycle saisonnier des larves chez A. lixula, P. lividus et P. microtuberculatus à Villefranche-Sur-Mer. Vie Milieu Ser A Biol Mar 19:1–52

    Google Scholar 

  • Fernandez C, Boudouresque CF (1997) Phenotypic plasticity of Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment. Mar Ecol Prog Ser 152:145–154

    Article  Google Scholar 

  • Fisher NI (1993) Statistical analysis of circular data. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Francour P, Boudouresque CF, Harmelin JG, Harmelin-Vivien ML, Quignard JP (1994) Are the Mediterranean waters becoming warmer? Information from biological indicators. Mar Pollut Bull 28:523–526

    Article  Google Scholar 

  • Fuji A (1960) Studies on the biology of the sea urchin III. Reproductive cycles of two sea urchins, Strongylocentrotus nudus and Strongylocentrotus intermedius. Bull Fac Fish Hokkaido Univ 11:49–57

    Google Scholar 

  • Garrabou J, Perez T, Sartoretto S, Harmelin JG (2001) Mass mortality event in red coral Corallium rubrum populations in the Provence region (France, NW Mediterranean). Mar Ecol Prog Ser 217:263–272

    Article  Google Scholar 

  • Garrabou J, Coma R, Bensoussan N, Bally M, Chevaldonné P, Cigliano M, Diaz D, Harmelin JG, Gambi MC, Kersting DK, Ledoux JB, Lejeusne C, Linares C, Marschal C, Pérez T, Ribes M, Romano JC, Serrano E, Teixido N, Torrents O, Zabala M, Zuberer F, Cerrano C (2009) Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Chang Biol 15:1090–1103

    Article  Google Scholar 

  • Gianguzza P, Bonaviri C (2013) Chapter 19: Arbacia in JM Lawrence (ed) Sea urchins: biology and ecology, 3rd edn. Developments in aquaculture and fisheries science 38. Elsevier, pp 275–283. doi:10.1016/B978-0-12-396491-5.00019-8

  • Gianguzza P, Agnetta D, Bonaviri C, Di Trapani F, Visconti G, Gianguzza F, Riggio S (2011) The rise of thermophilic sea urchins and the expansion of barren grounds in the Mediterranean Sea. Chem Ecol 27:129–134

    Article  Google Scholar 

  • Gianguzza P, Bonaviri C, Prato E, Fanelli G, Chiantore M, Privitera D, Agnetta D (2013) Hydrodynamism and its influence on the reproductive condition of the edible sea urchin Paracentrotus lividus. Mar Environ Res 85:29–33. doi:10.1016/j.marenvres.2012.12.007

    Article  CAS  Google Scholar 

  • Guidetti P, Dulcic J (2007) Relationships among predatory fish, sea urchins and barrens in Mediterranean rocky reefs across a latitudinal gradient. Mar Environ Res 63:168–184

    Article  CAS  Google Scholar 

  • Guidetti P, Fraschetti S, Terlizzi A, Boero F (2003) Distribution patterns of sea urchins and barrens in shallow Mediterranean rocky reefs impacted by the illegal fishery of the rock-boring mollusc Lithophaga lithophaga. Mar Biol 143:1135–1142. doi:10.1007/s00227-003-1163-z

    Article  Google Scholar 

  • Guillou M, Lumingas LJL (1998) The reproductive cycle of the “blunt” sea urchin. Aquac Int 6:147–160

    Article  Google Scholar 

  • Harmelin JG, Hereu B, de Maisonnave LM, Teixidor N, Domínguez L et al. (1995) Indicateurs de biodiversité en milieu marin: les échinodermes. Fluctuations temporelles des peuplements d’échinodermes à Port-Cros. Comparaison entre les années 1982–84 et 1993–95. Technical report for the Port-Cros National Park, France

  • Hernández JC, Brito A, García N, Gil-Rodríguez MC, Herrera G, Cruz-Reyes A, Falcón JM (2006) Spatial and seasonal variation of the gonad index of Diadema antillarum (Echinodermata: Echinoidea) in the Canary Islands. Sci Mar 70:689–698

    Article  Google Scholar 

  • Kelly M (2001) Environmental parameters controlling gametogenesis in the echinoid Psammechinus miliaris. J Exp Mar Biol Ecol 266:67–80

    Article  Google Scholar 

  • King CK, Hoegh-Guldberg O, Byrne M (1994) Reproductive cycle of Centrostephanus rodgersii (Echinoidea), with recommendations for the establishment of a sea urchin fishery in New South Wales. Mar Biol 120:95–106

    Google Scholar 

  • Lejeusne C, Chevaldonné P, Pergent-Martini C, Boudouresque CF, Pérez T (2010) Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends Ecol Evol 25:250–260

    Article  Google Scholar 

  • Lemon J (2006) Plotrix: a package in the red light district of R. R News 6:8–12

    Google Scholar 

  • Lessios HA (1991) Presence and absence of monthly reproductive rhythms among eight Caribbean echinoids off the coast of Panama. J Exp Mar Biol Ecol 153:27–47

    Article  Google Scholar 

  • Ling SD, Johnson CR, Frusher S, King CK (2008) Reproductive potential of a marine ecosystem engineer at the edge of a newly expanded range. Glob Chang Biol 14:907–915

    Article  Google Scholar 

  • Ling SD, Johnson CR, Frusher S, Ridgway K (2009) Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proc Natl Acad Sci USA 106:22341–22345

    Article  CAS  Google Scholar 

  • López S, Turon X, Montero E, Palacín C, Duarte CM, Tarjuelo I (1998) Larval abundance, recruitment and early mortality in Paracentrotus lividus (Echinoidea). Interannual variability and plankton-benthos coupling. Mar Ecol Prog Ser 172:239–251

    Article  Google Scholar 

  • Lozano J, Galera J, Lopezl S, Turon X, Morera G (1995) Biological cycles and recruitment of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats. Mar Ecol Prog Ser 122:179–191

    Article  Google Scholar 

  • Lund U, Agostinelli C (2010) Circular: circular statistics. R package version 0.4. http://cran.r-project.org/package=circular. Accessed 28 Dec 2012

  • Mardia KV (1976) Linear-circular correlation coefficients and rhythmometry. Biometrika 63:403–405

    Article  Google Scholar 

  • Martin Y, Bonnefont JL, Chancerelle L (2002) Gorgonians mass mortality during the 1999 late summer in French Mediterranean coastal waters: the bacterial hypothesis. Water Res 36:779–782

    Article  CAS  Google Scholar 

  • Martínez-Pita I, Sánchez-España AI, García FJ (2008) Gonadal growth and reproduction in the sea urchin Sphaerechinus granularis (Lamarck 1816) (Echinodermata: Echinoidea) in southern Spain. Sci Mar 72:603–611

    Google Scholar 

  • McClintock J, Watts S (1990) The effects of photoperiod on gametogenesis in the tropical sea urchin Eucidaris tribuloides. J Exp Mar Biol Ecol 139:175–184

    Article  Google Scholar 

  • Meidel SK, Scheibling RE (1998) Annual reproductive cycle of the green sea urchin, Strongylocentrotus droebachiensis, in differing habitats in Nova Scotia, Canada. Mar Biol 131:461–478

    Article  Google Scholar 

  • Mortensen T (1935) A monograph of the Echinoidea. II. Bothriocidaroida, Melonechinoida, lepidocentroida, and Stirodonta. Reitzel & Oxford Univ. Press, Copenhagen & London

    Google Scholar 

  • Nédélec H (1983) Sur un nouvel indice de réplétion pour les oursins réguliers. Rapp P-v Reun Cons Int Explor Sci Mer Medit Monaco 28:149–151

    Google Scholar 

  • Palacín C, Turon X, Ballesteros M, Giribet G, López S (1998) Stock evaluation of three littoral echinoid species on the Catalan coast (North-Western Mediterranean). Mar Ecol 19:163–177. doi:10.1111/j.1439-0485.1998.tb00460.x

    Article  Google Scholar 

  • Pearse JS (1981) Synchronization of gametogenesis in the sea urchins Strongylocentrotus purpuratus and S. franciscanus. In: Clark WH Jr, Adams TS (eds) Advances in invertebrate reproduction. Elsevier North Holland, Amsterdam

    Google Scholar 

  • Pearse JS, Cameron RA (1991) Echinodermata: Echinoidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates. Echinoderms and lophophorates, vol 6. Boxwood Press, Pacific Grove, CA, pp 513–662

  • Pearse JS, Pearse VB, Davis KK (1986) Photoperiodic regulation of gametogenesis and growth in the sea urchin Strongylocentrotus purpuratus. J Exp Zool 237:107–118

    Article  Google Scholar 

  • Pecorino D, Lamare MD, Barker MF (2013) Reproduction of the Diadematidae sea urchin Centrostephanus rodgersii in a recently colonized area of northern New Zealand. Mar Biol Res 9:157–168

    Article  Google Scholar 

  • Pedrotti ML (1993) Spatial and temporal distribution and recruitment of echinoderm larvae in the Ligurian Sea. J Mar Biol Assoc UK 73:513–530

    Article  Google Scholar 

  • Petit G, Delamare-Deboutteville C, Bougis P (1950) Le fichier faunistique du laboratoire Arago. Vie Milieu Ser A Biol Mar 1:356–360

    Google Scholar 

  • Privitera D, Noli M, Falugi C, Chiantore M (2011) Benthic assemblages and temperature effects on Paracentrotus lividus and Arbacia lixula larvae and settlement. J Exp Mar Biol Ecol 407:6–11

    Article  Google Scholar 

  • Régis MB (1979) Analyse des fluctuations des índices physiologiques chez deux échinoides (Paracentrotus lividus) (Lmk) et Arbacia lixula (L.) du Golfe de Marseille. Tethys 9:167–181

    Google Scholar 

  • Sala E, Ribes M, Hereu B, Zabala M, Alvà V, Coma R, Garrabou J (1998) Temporal variability in abundance of the sea urchins Paracentrotus lividus and Arbacia lixula in the Northwestern Mediterranean: comparison between a marine reserve and an unprotected area. Mar Ecol Prog Ser 168:135–145

    Article  Google Scholar 

  • Sánchez-España AI, Martínez-Pita I, García FJ (2004) Gonadal growth and reproduction in the commercial sea urchin Paracentrotus lividus (Lamarck, 1816) (Echinodermata: Echinoidea) from southern Spain. Hydrobiol 519:61–72

    Article  Google Scholar 

  • Shpigel M, McBride SC, Marciano S, Lupatsch I (2004) The effect of photoperiod and temperature on the reproduction of European sea urchin Paracentrotus lividus. Aquaculture 232:343–355

    Article  Google Scholar 

  • Spirlet C, Grosjean P, Jangoux M (1998) Reproductive cycle of the echinoid Paracentrotus lividus: analysis by means of the maturity index. Invertebr Reprod Dev 34:69–81

    Article  Google Scholar 

  • Spirlet C, Grosjean P, Jangoux M (2000) Optimization of gonad growth by manipulation of temperature and photoperiod in cultivated sea urchins, Paracentrotus lividus (Lamarck) (Echinodermata). Aquaculture 185:85–99

    Article  Google Scholar 

  • Stefanini G (1911) Di alcune Arbacia fossili. Riv Ital Paleontol 17:51–52

    Google Scholar 

  • Tavares YAG (2004) Biologia reprodutiva dos equinóides Echinometra lucunter (Linnaeus,1758) e Arbacia lixula (Linnaeus, 1758) na Ilha da Galheta, litoral paranaense, Brasil. Doctoral thesis, Universidade Federal do Paraná

  • Tortonese E (1965) Echinodermata. Fauna d’Italia vol. VI. Calderini, Bologna

    Google Scholar 

  • Turon X, Palacín C, Ballesteros M, Dantart L (1995) A case study of stock evaluation on littoral hard substrata: echinoid populations on the north-east coast of Spain. In: Eleftheriou et al (ed) Biology and ecology of shallow coastal waters. 28 EMBS Symposium. Olsen & Olsen, pp 333–340

  • Uthicke S, Schaffelke B, Byrne M (2009) A boom-bust phylum? Ecological and evolutionary consequences of density variations in echinoderms. Ecol Monogr 79:3–24

    Article  Google Scholar 

  • Walker CW, Lesser MP (1998) Manipulation of food and photoperiod promotes out-of-season gametogenesis in the green sea urchin, Strongylocentrotus droebachiensis: implications for aquaculture. Mar Biol 132:663–676

    Article  Google Scholar 

  • Walker CW, Unuma T, Lesser MP (2007) Gametogenesis and reproduction of sea urchins. In: Lawrence JM (ed) Edible sea urchins: biology and ecology, 2nd edn. Developments in aquaculture and fisheries science, vol 37. Elsevier, Amsterdam, pp 11–33

  • Wangensteen OS, Turon X, García-Cisneros A, Recasens M, Romero J, Palacín C (2011) A wolf in sheep’s clothing: carnivory in dominant sea urchins in the Mediterranean. Mar Ecol Prog Ser 441:117–128

    Article  Google Scholar 

  • Wangensteen OS, Turon X, Pérez-Portela R, Palacín C (2012) Natural or naturalized? Phylogeography suggests that the abundant sea urchin Arbacia lixula is a recent colonizer of the Mediterranean. PLoS One 7:e45067

    Article  CAS  Google Scholar 

  • Yoshida M (1952) Some observations on the maturation of the sea urchin Diadema setosum. Annot Zool Jpn 25:265–271

    Google Scholar 

  • Zamora S, Stotz W (1992) Ciclo reproductivo de Loxechinus albus (Molina 1782) (Echinodermata: Echinoidea) en dos localidades de la IV Región, Coquimbo, Chile. Rev Chil Hist Nat 65:121–133

    Google Scholar 

  • Zar JH (1996) Biostatistical analysis. Prentice-Hall International, Englewood Cliffs

    Google Scholar 

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Acknowledgments

We thank Sandra Garcés, Alex García-Cisneros, Patrick Erwin, Núria Massana, Mari Carmen Pineda and Guillem Santamaria for help with sampling and Sandra Ortiz and Marta Jové for laboratory assistance. We are indebted to Ramón Roqueta and the staff of Andrea’s Diving (Tossa de Mar) for assistance in the field. This work was funded by projects CTM2010-22218 from the Spanish Government, 2009SGR-484 from the Catalan Government, BIOCON 08-187/09 from BBVA Foundation and 287844 (COCONET) of the European Community’s Seventh Framework Programme (FP7/2007–2013).

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  1. Department of Animal Biology and Institut de Recerca de la Biodiversitat (IRBio), University of Barcelona, Av. Diagonal 643, 08028, Barcelona, Spain

    Owen S. Wangensteen, Maria Casso & Creu Palacín

  2. Center for Advanced Studies of Blanes (CEAB-CSIC), C. Accés a la Cala St. Francesc, 14, 17300, Blanes, Girona, Spain

    Xavier Turon

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  1. Owen S. Wangensteen
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Correspondence to Owen S. Wangensteen.

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Communicated by M. Byrne.

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227_2013_2303_MOESM1_ESM.tif

Fig. S1 Comparison between monthly values (mean ± SE) of the gonadosomic index chosen in this work (GSI, % wet weight) and two other gonadosomatic indices, GSI-DW (% dry weight) and Nédélec GSI. (dry weight of the gonads divided by test diameter cubed) (TIFF 3937 kb)

227_2013_2303_MOESM2_ESM.tif

Fig. S2 Monthly mean sea surface temperature measured at L’Estartit Meteorological Station (red dashed line) and daily mean sea surface temperature measured in situ at Tossa de Mar during part of the present study (blue continuous line) showing the good correlation between both measurements. (TIFF 4001 kb)

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Wangensteen, O.S., Turon, X., Casso, M. et al. The reproductive cycle of the sea urchin Arbacia lixula in northwest Mediterranean: potential influence of temperature and photoperiod. Mar Biol 160, 3157–3168 (2013). https://doi.org/10.1007/s00227-013-2303-8

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