Advertisement

Coral Reefs

, Volume 34, Issue 4, pp 1207–1216 | Cite as

Demographic responses to warming: reproductive maturity and sex influence vulnerability in an octocoral

  • Rosana Arizmendi-Mejía
  • Jean-Baptiste Ledoux
  • Sergi Civit
  • Agostinho Antunes
  • Zoi Thanopoulou
  • Joaquim Garrabou
  • Cristina Linares
Report

Abstract

Ocean warming, caused by climate change, is critically impacting marine coastal ecosystems. Benthic organisms, such as anthozoans, are increasingly submitted to high temperatures that cause massive mortalities in tropical and temperate seas. To broaden our understanding of their response to thermal stress, we tested the putative role of reproductive maturity and sex in the susceptibility of the Mediterranean red gorgonian, Paramuricea clavata, to high temperatures. We experimentally compared the response to thermal stress of sexually immature (i.e., juveniles) versus mature individuals (i.e., adults), and of males versus females. Colonies’ response was firstly assessed by measuring the percentage of tissue area exhibiting necrosis. Then, the reproductive output (i.e., fertility, size, and number of gonads) of both sexes was characterized. When compared to juveniles, adults showed a significantly higher percentage of necrosis, suggesting that during the reproductive period they are more vulnerable to high temperatures. Males and females showed a similar percentage of tissue damage and a significant decrease in their reproductive output. However, females’ reproduction was more impacted, suggesting that females are more susceptible to thermal stress than males. A differential energy investment in reproduction may be the underlying cause of the observed responses. Adults invest a large proportion of their energy budget in reproduction; hence, they have fewer resources available to cope with stress, compared to juveniles. A similar situation seems to apply to females, with respect to males. Considering the current ocean-warming trend, our results imply that the long-term viability of shallow populations of long-lived anthozoans may be jeopardized in the future. This study reveals potential demographic consequences of warming that go beyond its associated increment of mortality rates. Given the important ecological role of many anthozoan species, these results can help better predict the future effects of climate change on coastal ecosystems.

Keywords

Reproduction Thermal stress Climate change Anthozoans Paramuricea clavata 

Notes

Acknowledgments

We kindly thank Dr. Núria Teixidó and Clara Casado for their invaluable help during sampling and the onset of the experiment, and Elvira Martínez for her support during the experimental setting. We are also greatly thankful to Dr. Stuart A. Sandin (Topic Editor) and two anonymous reviewers for their constructive suggestions, which greatly improved the quality of this article. This study was partially funded by the Spanish Ministry of Economy and Competitivity through the Smart Project (CGL2012-32194) and by the “Organismo Autonomo de Parques Nacionales” through the Corclim Project (579S/2012). Additional funding was provided by a Ramon y Cajal research contract (RyC-2011-08134) to CL, a PhD grant (FI-DGR 2011) from the CUR-DIUE-Generalitat de Catalunya and the European Social Fund to RAM, a research grant (2014 SGR 464) from the Departament d’Economia i Coneixement de la Generalitat de Catalunya to SC, and a postdoctoral grant (SFRH/BPD/74400/2010) from Fundação para a Ciência e a Tecnologia (FCT) to JBL.

Supplementary material

338_2015_1332_MOESM1_ESM.docx (1.7 mb)
Supplementary material 1 (DOCX 1713 kb)

References

  1. Airi V, Gizzi F, Falini G, Levy O, Dubinsky Z, Goffredo S (2014) Reproductive efficiency of a mediterranean endemic zooxanthellate coral decreases with increasing temperature along a wide latitudinal gradient. PLoS One 9:e91792PubMedCentralCrossRefPubMedGoogle Scholar
  2. Arizmendi-Mejía R, Linares C, Garrabou J, Antunes A, Ballesteros E, Cebrian E, Díaz D, Ledoux J-B (2015) Combining genetic and demographic data for the conservation of a Mediterranean marine habitat-forming species. PLoS One 10:e0119585PubMedCentralCrossRefPubMedGoogle Scholar
  3. Baird AH, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 237:133–141CrossRefGoogle Scholar
  4. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195Google Scholar
  5. Bally M, Garrabou J (2007) Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change. Glob Chang Biol 13:2078–2088CrossRefGoogle Scholar
  6. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7, http://CRAN.R-project.org/package=lme4
  7. Bensoussan N, Romano J-C, Harmelin J-G, Garrabou J (2010) High resolution characterization of northwest Mediterranean coastal waters thermal regimes: To better understand responses of benthic communities to climate change. Estuar Coast Shelf Sci 87:431–441CrossRefGoogle Scholar
  8. Bensoussan N, Romano JC, Harmelin JG, Crisci C, Pascual J, Garrabou J (2009) Warming trends, regional fingerprints and future trajectories of NW Mediterranean coastal waters. In: Pergent-Martini C, Brichet M (eds) Proc 1st Mediterr Symp Conserv Coralligenous and other Calcareous Bio-concretions. RAC/SPA, Tunis, p 167–168Google Scholar
  9. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2008) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135CrossRefGoogle Scholar
  10. Calow P (1979) The cost of reproduction - a physiological approach. Biol Rev 54:23–40CrossRefPubMedGoogle Scholar
  11. Calow P (1985) Adaptive aspects of energy allocation. In: Tytler P, Calow P (eds) Fish energetics - new perspectives. Croom Helm, Sydney, pp 13–31CrossRefGoogle Scholar
  12. Cerrano C, Bavestrello G (2008) Medium-term effects of die-off of rocky benthos in the Ligurian Sea. What can we learn from gorgonians? Chem Ecol 24:73–82CrossRefGoogle Scholar
  13. Cerrano C, Arillo A, Azzini F, Calcinai B, Castellano L, Muti C, Valisano L, Zega G, Bavestrello G (2005) Gorgonian population recovery after a mass mortality event. Aquat Conserv 15:147–157CrossRefGoogle Scholar
  14. Cerrano C, Bianchi CN, Cattaneo-Vietti R, Bava S, Morganti C, Morri C, Pico 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 3:284–293CrossRefGoogle Scholar
  15. Coma R, Lasker HR (1997) Small-scale heterogeneity of fertilization success in a broadcast spawning octocoral. J Exp Mar Bio Ecol 214:107–120CrossRefGoogle Scholar
  16. Coma R, Zabala M, Gili J-M (1995a) Sexual reproductive effort in the Mediterranean gorgonian Paramuricea clavata. Mar Ecol Prog Ser 117:185–192CrossRefGoogle Scholar
  17. Coma R, Ribes M, Zabala M, Gili J-M (1995b) Reproduction and cycle of gonadal development in the Mediterranean gorgonian Paramuricea clavata. Mar Ecol Prog Ser 117:173–183CrossRefGoogle Scholar
  18. Coma R, Ribes M, Zabala M, Gili J (1998a) Growth in a modular colonial marine invertebrate. Estuar Coast Shelf Sci 47:459–470CrossRefGoogle Scholar
  19. Coma R, Ribes M, Gili J-M, Zabala M (1998b) An energetic approach to the study of life-history traits of two modular colonial benthic invertebrates. Mar Ecol Prog Ser 162:89–103CrossRefGoogle Scholar
  20. Coma R, Ribes M, Serrano E, Jiménez E, Salat J, Pascual J (2009) Global warming-enhanced stratification and mass mortality events in the Mediterranean. Proc Natl Acad Sci USA 106:6176–6181PubMedCentralCrossRefPubMedGoogle Scholar
  21. Crisci C (2011) Effets du changement climatique sur les écosystèmes littoraux de la Mer Méditerranée Nord-Occidentale: étude de la relation entre les conditions de température et la réponse biologique pendant les événements de mortalité massive. Ph.D. thesis, Université de la Méditerranée, p 193Google Scholar
  22. Crisci C, Bensoussan N, Romano J-C, Garrabou J (2011) Temperature anomalies and mortality events in marine communities: insights on factors behind differential mortality impacts in the NW Mediterranean. PLoS One 6:e23814PubMedCentralCrossRefPubMedGoogle Scholar
  23. Cupido R, Cocito S, Sgorbini S, Bordone A, Santangelo G (2008) Response of a gorgonian (Paramuricea clavata) population to mortality event: recovery or loss? Aquat Conserv 18:984–992CrossRefGoogle Scholar
  24. Cupido R, Cocito S, Barsanti M, Sgorbini S, Peirano A, Santangelo G (2009) Unexpected long-term population dynamics in a canopy-forming gorgonian coral following mass mortality. Mar Ecol Prog Ser 394:195–200CrossRefGoogle Scholar
  25. Cupido R, Cocito S, Manno V, Ferrando S, Peirano A, Iannelli M, Bramanti L, Santangelo G (2012) Sexual structure of a highly reproductive, recovering gorgonian population: quantifying reproductive output. Mar Ecol Prog Ser 469:25–36CrossRefGoogle Scholar
  26. Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G, Alvarez-Filip L, Baca B, Bartels E, Bastidas C, Bouchon C, Brandt M, Bruckner AW, Bunkley-Williams L, Cameron A, Causey BD, Chiappone M, Christensen TRL, Crabbe MJC, Day O, de la Guardia E, Díaz-Pulido G, DiResta D, Gil-Agudelo DL, Gilliam DS, Ginsburg RN, Gore S, Guzmán HM, Hendee JC, Hernández-Delgado E, Husain E, Jeffrey CFG, Jones RJ, Jordán-Dahlgren E, Kaufman LS, Kline DI, Kramer P, Lang JC, Lirman D, Mallela J, Manfrino C, Maréchal J-P, Marks K, Mihaly J, Miller WJ, Mueller EM, Muller EM, Orozco Toro C, Oxenford H, Ponce-Taylor D, Quinn N, Ritchie KB, Rodríguez S, Ramírez AR, Romano S, Samhouri JF, Sánchez J, Schmahl GP, Shank BV, Skirving WJ, Steiner SCC, Villamizar E, Walsh SM, Walter C, Weil E, Williams EH, Roberson KW, Yusuf Y (2010) Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005. PLoS One 5:e13969Google Scholar
  27. 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 15:1090–1103CrossRefGoogle Scholar
  28. Gori A, Linares C, Rossi S, Coma R, Gili JM (2007) Spatial variability in reproductive cycle of the gorgonians Paramuricea clavata and Eunicella singularis (Anthozoa, Octocorallia) in the Western Mediterranean Sea. Mar Biol 151:1571–1584CrossRefGoogle Scholar
  29. Gori A, Linares C, Viladrich N, Clavero A, Orejas C, Fiorillo I, Ambroso S, Gili J-M, Rossi S (2013) Effects of food availability on the sexual reproduction and biochemical composition of the Mediterranean gorgonian Paramuricea clavata. J Exp Mar Bio Ecol 444:38–45CrossRefGoogle Scholar
  30. Grigg RW (1977) Population dynamics of two gorgonian corals. Ecology 58:278–290CrossRefGoogle Scholar
  31. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162CrossRefPubMedGoogle Scholar
  32. Harvell C, Kim K, Burkholder J, Colwell R, Epstein P, Grimes D, Hofmann E, Lipp E, Osterhaus A, Overstreet R, Porter J, Smith G, Vasta G (1999) Emerging Marine Diseases - Climate Links and Anthropogenic Factors. Science 285:1505–1510CrossRefPubMedGoogle Scholar
  33. Hayward A, Gillooly JF (2011) The Cost of Sex: Quantifying Energetic Investment in Gamete Production by Males and Females. PLoS One 6:e16557PubMedCentralCrossRefPubMedGoogle Scholar
  34. Henry LA, Hart M (2005) Regeneration from injury and resource allocation in sponges and corals – a review. Int Rev Hydrobiol 90:125–158CrossRefGoogle Scholar
  35. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  36. Hudson LN, Isaac NJB, Reuman DC (2013) The relationship between body mass and field metabolic rate among individual birds and mammals. J Anim Ecol 82:1009–1020PubMedCentralCrossRefPubMedGoogle Scholar
  37. Huete-Stauffer C, Vielmini I, Palma M, Navone A, Panzalis P, Vezzulli L, Misic C, Cerrano C (2011) Paramuricea clavata (Anthozoa, Octocorallia) loss in the Marine Protected Area of Tavolara (Sardinia, Italy) due to a mass mortality event. Mar Ecol 32:107–116CrossRefGoogle Scholar
  38. Hughes TP (1984) Population dynamics based on individual size rather than age: a general model with a reef coral example. Am Nat 123:778–795CrossRefGoogle Scholar
  39. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933CrossRefPubMedGoogle Scholar
  40. Jonsson N, Jonsson B, Hansen LP (1991) Energetic cost of spawning in male and female Atlantic salmon (Salmo salar L.). J Fish Biol 39:739–744CrossRefGoogle Scholar
  41. Kipson S, Linares C, Teixidó N, Bakran-Petricioli T, Garrabou J (2012) Effects of thermal stress on early developmental stages of a gorgonian coral. Mar Ecol Prog Ser 470:69–78CrossRefGoogle Scholar
  42. Kozłowski J, Wiegert RG (1986) Optimal allocation of energy to growth and reproduction. Theor Popul Biol 29:16–37CrossRefPubMedGoogle Scholar
  43. Kramarsky-Winter E, Loya Y (2000) Tissue regeneration in the coral Fungia granulosa: the effect of extrinsic and intrinsic factors. Mar Biol 137:867–873CrossRefGoogle Scholar
  44. Kunz TH, Orrell KS (2004) Energy costs of reproduction. In: Cleveland C.J. (eds) Encyclopedia of energy. Elsevier, pp 423–442Google Scholar
  45. Kuznetsova A, Brockhoffn PB, Christensen RHB (2013) lmerTest: Tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). R-Version:1.1-0. http://cran.rproject.org/web/packages/lmerTest/index.html
  46. Lasker HR (2005) Gorgonian mortality during a thermal event in the Bahamas. Bull Mar Sci 76:155–162Google Scholar
  47. Lesser MP (2007) Coral reef bleaching and global climate change: Can corals survive the next century? Proc Natl Acad Sci USA 104:5259–5260PubMedCentralCrossRefPubMedGoogle Scholar
  48. Lesser MP (2013) Using energetic budgets to assess the effects of environmental stress on corals: are we measuring the right things? Coral Reefs 32:25–33CrossRefGoogle Scholar
  49. Leuzinger S, Anthony KRN, Willis BL (2003) Reproductive energy investment in corals: scaling with module size. Oecologia 136:524–531CrossRefPubMedGoogle Scholar
  50. Linares C, Doak D (2010) Forecasting the combined effects of disparate disturbances on the persistence of long-lived gorgonians: a case study of Paramuricea clavata. Mar Ecol Prog Ser 402:59–68CrossRefGoogle Scholar
  51. Linares C, Coma R, Zabala M (2008a) Effects of a mass mortality event on gorgonian reproduction. Coral Reefs 27:27–34CrossRefGoogle Scholar
  52. Linares C, Coma R, Diaz D, Zabala M, Hereu B, Dantart L (2005) Immediate and delayed effects of a mass mortality event on gorgonian population dynamics and benthic community structure in the NW Mediterranean Sea. Mar Ecol Prog Ser 305:127–137CrossRefGoogle Scholar
  53. Linares C, Coma R, Mariani S, Díaz D, Hereu B, Zabala M (2008b) Early life history of the Mediterranean gorgonian Paramuricea clavata: implications for population dynamics. Invertebr Biol 127:1–11CrossRefGoogle Scholar
  54. Marshall P, Schuttenberg H (2006) Adapting coral reef management in the face of climate change. Coast Estuar Stud 61:223–241CrossRefGoogle Scholar
  55. McWilliams JP, Coté IM, Gill JA, Sutherland WJ, Watkinson AR (2005) Accelerating impacts of temperature-induced coral bleaching in the Caribbean. Ecology 86:2055–2060CrossRefGoogle Scholar
  56. Mendes JM, Woodley JD (2002) Effect of the 1995–1996 bleaching event on polyp tissue depth, growth, reproduction and skeletal band formation in Montastraea annularis. Mar Ecol Prog Ser 235:93–102CrossRefGoogle Scholar
  57. Michalek-Wagner K, Willis BL (2001) Impacts of bleaching on the soft coral Lobophytum compactum I. Fecundity, fertilization and offspring viability. Coral Reefs 19:231–239CrossRefGoogle Scholar
  58. Mokhtar-Jamaï K, Pascual M, Ledoux JB, Coma R, Féral JP, Garrabou J, Aurelle D (2011) From global to local genetic structuring in the red gorgonian Paramuricea clavata: The interplay between oceanographic conditions and limited larval dispersal. Mol Ecol 20:3291–3305CrossRefPubMedGoogle Scholar
  59. Negri AP, Marshall PA, Heyward AJ (2007) Differing effects of thermal stress on coral fertilization and early embryogenesis in four Indo Pacific species. Coral Reefs 26:759–763CrossRefGoogle Scholar
  60. Oceana (2009) Especies amenazadas. Propuesta para su protección en Europa y España. URL: http://www.fundaciocatalunya-lapedrera.com/sites/default/files/Oceana_ESPECIES_AMENAZADAS.pdf
  61. Oliver J, Babcock R (1992) Aspects of the fertilization ecology of broadcast spawning corals: sperm dilution effects and in situ measurements of fertilization. Biol Bull 409–417Google Scholar
  62. Oren U, Benayahu Y, Lubinevsky H, Loya Y (2001) Colony integration during regeneration in the stony coral Favia favus. Ecology 82:802–813CrossRefGoogle Scholar
  63. Parker GA (1982) Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J Theor Biol 96:281–294CrossRefPubMedGoogle Scholar
  64. Parker GA, Baker RR, Smith VGF (1972) The origin and evolution of gamete dimorphism and the male-female phenomenon. J Theor Biol 36:529–553CrossRefPubMedGoogle Scholar
  65. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New YorkCrossRefGoogle Scholar
  66. Pinheiro J, Bates D, DebRoy S, Sarkar D and R Core Team (2015) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-120, http://CRAN.R-project.org/package=nlme
  67. Ponti M, Perlini RA, Ventra V, Grech D, Abbiati M, Cerrano C (2014) Ecological shifts in Mediterranean coralligenous assemblages related to gorgonian forest loss. PLoS One e 9:102782CrossRefGoogle Scholar
  68. Previati M, Scinto A, Cerrano C, Osinga R (2010) Oxygen consumption in Mediterranean octocorals under different temperatures. J Exp Mar Bio Ecol 390:39–48CrossRefGoogle Scholar
  69. Ramírez-Llodra E (2002) Fecundity and life-history strategies in marine invertebrates. Adv Mar Biol 43:87–170CrossRefPubMedGoogle Scholar
  70. Randall CJ, Szmant AM (2009) Elevated temperature reduces survivorship and settlement of the larvae of the Caribbean scleractinian coral, Favia fragum (Esper). Coral Reefs 28:537–545CrossRefGoogle Scholar
  71. Richmond R, Hunter C (1990) Reproduction and recruitment of corals: comparisons among the Caribbean, the Tropical Pacific, and the Red Sea. Mar Ecol Prog Ser 60:185–203CrossRefGoogle Scholar
  72. Salat J, Pascual J (2002) The oceanographic and meteorological station at l’Estartit (NW Mediterranean). In: Briand F (ed) Tracking long-term hydrological change in the Mediterranean Sea. CIESM Workshop Series, CIESM, Monaco, p 29–32Google Scholar
  73. Sier CJS, Olive PJW (1994) Reproduction and reproductive variability in the coral. Mar Biol 118:713–722CrossRefGoogle Scholar
  74. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averit KB, Tignor M, Miller HL (2007) Climate Change 2007: The physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge and New York p 996Google Scholar
  75. Somot S, Sevault F, Déqué M, Crépon M (2008) 21st century climate change scenario for the Mediterranean using a coupled atmosphere–ocean regional climate model. Glob Planet Change 63:112–126CrossRefGoogle Scholar
  76. Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268CrossRefGoogle Scholar
  77. Szmant AM, Gassman NJ (1990) The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8:217–224CrossRefGoogle Scholar
  78. Tardent P (1985) The differentiation of germ cells in Cnidaria. In: Halvorson HO, Monroy A (Eds) The origin and evolution of sex. Alan R. Liss Incorporated, New York, pp. 163–197Google Scholar
  79. Torres JL, Armstrong R, Weil E (2008) Enhanced ultraviolet radiation can terminate sexual reproduction in the broadcasting coral species Acropora cervicornis, Lamarck. J Exp Mar Bio Ecol 358:39–45CrossRefGoogle Scholar
  80. Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871-1971. Aldine Publishing Company, Chicago, pp 139–179Google Scholar
  81. True M (1970) Etude quantitative de quatre peuplements sciaphiles sur substrats rocheux dans la région marseillaise. Bulletin de l’Institut Océanographique de Monaco 1410:1–48Google Scholar
  82. Tsounis G, Martinez L, Bramanti L, Viladrich N, Gili J, Martinez A, Rossi S (2012) Anthropogenic effects on reproductive effort and allocation of energy reserves in the Mediterranean octocoral Paramuricea clavata. Mar Ecol Prog Ser 449:161–172CrossRefGoogle Scholar
  83. Van Veghel MLJ, Bak RPM (1994) Reproductive characteristics of the polymorphic Caribbean reef building coral Montastrea annularis. III. Reproduction in damaged and regenerating colonies. Mar Ecol Prog Ser 109:229–233CrossRefGoogle Scholar
  84. Ward S (1995) Two patterns of energy allocation for growth, reproduction and lipid storage in the scleractinian coral Pocillopora damicornis. Coral Reefs 14:87–90CrossRefGoogle Scholar
  85. Yong L, Grober MS (2013) Sex differences in the energetic content of reproductive tissues in the Blackeye Goby, Rhinogobiops nicholsii. Environ Biol Fishes 97:321–328CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Rosana Arizmendi-Mejía
    • 1
    • 2
  • Jean-Baptiste Ledoux
    • 2
    • 3
  • Sergi Civit
    • 4
  • Agostinho Antunes
    • 3
    • 5
  • Zoi Thanopoulou
    • 1
    • 6
  • Joaquim Garrabou
    • 2
    • 7
  • Cristina Linares
    • 1
  1. 1.Departament ďEcologia, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  2. 2.Institut de Ciències del Mar (ICM-CSIC)BarcelonaSpain
  3. 3.CIMAR/CIIMAR, Centro Interdisciplinar de Investigação Marinha e AmbientalUniversidade do PortoPortoPortugal
  4. 4.Departament ďEstadística, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  5. 5.Departamento de Biologia, Faculdade de CiênciasUniversidade do PortoPortoPortugal
  6. 6.Department of Environmental SciencesUniversity of the AegeanMytileneGreece
  7. 7.Institut Méditerranéen d’Océanologie (MIO)Marseille Cedex 9France

Personalised recommendations