Historical record of Corallium rubrum and its changing carbon sequestration capacity: A meta-analysis from the North Western Mediterranean

English version

Autoři: Miguel Mallo ^aff001; Patrizia Ziveri ^aff001; Victoria Reyes-García ^aff001; Sergio Rossi ^aff001
Působiště autorů: Institut de Ciència i Tecnologia (ICTA), Universitat Autònoma de Barcelona (UAB), Bellaterra, Barcelona, Spain ^aff001; Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain ^aff002; Dipartimento di Scienze e Tecnologie Biologiche e Ambientali (DiSTeBA), Università del Salento, Lecce, Italy ^aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223802

Souhrn

Background

There is a scarcity of long time-span and geographically wide research on the health status of Corallium rubrum, including limited research on its historical ecology and carbon sequestration capacity.

Objectives

To reconstruct the temporal trends of the most reported C. rubrum population parameters in the Northwestern Mediterranean Sea and to determine the changes in total carbon sequestration by this species.

Data sources

Quantitative and qualitative, academic and grey documents were collected from scientific web browsers, scientific libraries, and requests to scientists.

Study eligibility criteria

Documents with original information of basal diameter, height and/or weight per colony, with a depth limit of 60 m in the Catalan and Ligurian Seas were analyzed.

Synthesis methods

We calculated yearly average values of C. rubrum biometric parameters, as well as estimated total weight, carbon flux, and carbon fixation in the structures of C. rubrum’s colonies.

Results

In both study areas, the values of the selected morphometric parameters for C. rubrum decreased until the 1990s, then increased from the 2000s, with average values surpassing the levels of the 1960s (Ligurian Sea) or reaching levels slightly lower than those of the 1980s (Catalan Sea). The difference in carbon sequestered between the oldest (1960s: Ligurian Sea; 1970s: Catalan Sea) and the lowest (1990s) biomass value of colonies is nearly double.

Limitations

Quantitative data previous to the 1990s are very limited. Information on recent recovery trends in C. rubrum parameters is concentrated in a few areas and biased towards colonies in marine protected areas, with scarce quantitative information from colonies in other areas.

Conclusions

The halt in the C. rubrum decreasing trend coincided with the exhaustion of tree-like colonies and the first recovery response due to effective protection measures in some areas. Nevertheless, C. rubrum climate change mitigation capacity through carbon sequestration can be drastically reduced from its potential in only a few decades.

Klíčová slova:

Corals – Habitats – Biodiversity – Conservation science – Biometrics – Carbon sink – Carbon sequestration

Zdroje

1. Boudouresque C-F, Blanfluné A, Harmelin-Vivien M, Personnic S, Ruitton S, Thibault T, Verlaque M. Where seaweed forests meet animal forests: the examples of macroalgae in coral reefs and the Mediterranean coralligenous ecosystem. In: Rossi S, Bramanti L, Gori A, Orejas C, editors. Marine animal forests. Springer International Publishing; 2017:369–398.

2. Boudouresque C-F. Marine biodiversity in the mediterranean: status of species, populations and communities. Sci Rep Port-Cros natl Park Fr. 2004;20:97–146.

3. Ballesteros E. Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol An Annu Rev. 2006;44:123–195.

4. Rossi S, Bramanti L, Broglio E, Gili JM. Trophic impact of long-lived species indicated by population dynamics in a short-lived hydrozoan, Eudendrium racemosum. Mar Ecol Prog Ser. 2012;97–111.

5. Montefalcone M, Morri C, Bianchi CN, Bavestrello G, Piazzi L. The two facets of species sensitivity: stress and disturbance on coralligenous assemblages in space and time. Mar Pollut Bull. 2017;117:229–238. doi: 10.1016/j.marpolbul.2017.01.072 28185652

6. Roghi F, Parravicini V, Montefalcone M, Rovere A, Morri C, Peirano A, et al. Decadal evolution of a coralligenous ecosystem under the influence of human impacts and climate change. Biol Mar Medit. 2010;17(1):59–62.

7. Coma R, Pola E, Ribes M, Zabala M. Long-term assessment of temperate octocoral mortality patterns, protected vs. unprotected areas. Ecol Appl. 2004;14(5):1466–478.

8. Linares C, Coma R, Diaz D, Zabala M, Hereu B, Dantart L. 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. 2005;305:127–137.

9. Rossi S. The destruction of the ‘animal forests’ in the oceans: towards an over-simplification of the benthic ecosystems. Ocean Coast Manag. 2013;84:77–85.

10. Betti F, Bavestrello G, Bo M, Asnaghi V, Chiantore M, Bava S, et al. Over 10 years of variation in Mediterranean reef benthic communities. Mar Ecol. 2017;38. p. 14.

11. Bianchi CN, Morri C. Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Mar Pollut Bull. 2000;40(5):367–376.

12. Sala E, Knowlton N. Global marine biodiversity trends. Annu Rev Environ Resourc. 2006;31:93–122.

13. Tsounis G, Rossi S, Grigg R, Santangelo G, Bramanti L, Gili J-M. The exploitation and conservation of precious corals. Oceanogr Mar Biol An Annu Rev. 2010;48:161–212.

14. Rossi S, Tsounis G, Orejas C, Padrón T, Gili JM, Bramanti L, et al. Survey of deep-dwelling red coral (Corallium rubrum) populations at Cap de Creus (NW Mediterranean). Mar Biol. 2008;154:533–545.

15. Tsounis G, Rossi S, Gili J-M, Arntz W. Population structure of an exploited benthic cnidarian: the case study of red coral (Corallium rubrum L.). Mar Biol. 2006;149:1059–1070.

16. Knittweis L, Aguilar R, Alvarez H, Borg JA, Evans J, Garcia S, et al. New depth record of the precious red coral Corallium rubrum for the Mediterranean. In: Rapp Comm int Mer Médit. 2016. p. 467.

17. Marschal C, Garrabou J, Harmelin JG, Pichon M. A new method for measuring growth and age in the precious red coral Corallium rubrum (L.). Coral Reefs. 2004;23:423–432.

18. Vielzeuf D, Garrabou J, Baronnet A, Grauby O, Marschal C. Nano to macroscale biomineral architecture of red coral (Corallium rubrum). Am Mineral. 2008;93:1799–1815.

19. Picciano M, Ferrier-Pagès C. Ingestion of pico- and nanoplankton by the Mediterranean red coral Corallium rubrum. Mar Biol. 2007;150:773–782.

20. Cattaneo-Vietti R, Bo M, Cannas R, Cau A, Follesa C, Meliadò E, et al. An overexploited Italian treasure: past and present distribution and exploitation of the precious red coral Corallium rubrum (L., 1758) (Cnidaria: Anthozoa). Ital J Zool. 2016;83(4):443–455.

21. Tescione G. The Italians and their coral fishing. Fausto Fiorentino (Ed.) Napoli, Italia. 1968. p. 490.

22. Santangelo G, Carletti E, Maggi E, Bramanti L. Reproduction and population sexual structure of the overexploited Mediterranean red coral Corallium rubrum. Mar Ecol Prog Ser. 2003;248:99–108.

23. Costantini F, Fauvelot C, Abbiati M. Fine-scale genetic structuring in Corallium rubrum: evidence of inbreeding and limited effective larval dispersal. Mar Ecol Prog Ser. 2007;340:109–119.

24. Costantini F, Rossi S, Pintus E, Cerrano C, Gili JM, Abbiati M. Low connectivity and declining genetic variability along a depth gradient in Corallium rubrum populations. Coral Reefs. 2011;30:991–1003.

25. Garrabou J, Harmelin JG. A 20-year study on life-history traits of a harvested long-lived temperate coral in the NW Mediterranean: insights into conservation and management needs. J Anim Ecol. 2002;71:966–978.

26. Bramanti L, Iannelli M, Santangelo G. Mathematical modelling for conservation and management of gorgonians corals: youngs and olds, could they coexist? Ecol Modell. 2009;220(21):2851–2856.

27. Garrabou J, Linares C, Montero-Serra I, Ledoux B, Lopez-Sanz À, Olvera À, et al. Informe sobre l’estat de les poblacions de coral vermell (Corallium rubrum) a les aigües de Catalunya. 2017. p. 38.

28. Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, et al. Global trajectories of the long-term decline of coral reef ecosystems. Science. 2003;301(5635):955–958. doi: 10.1126/science.1085706 12920296

29. Garrabou J, Sala E, Linares C, Ledoux JB, Montero-Serra I, Dominici JM, et al. Re-shifting the ecological baseline for the overexploited Mediterranean red coral. Sci Rep. 2017;7:1–6. doi: 10.1038/s41598-016-0028-x

30. Cau A, Bramanti L, Cannas R, Follesa MC, Angiolillo M, Canese S, et al. Habitat constraints and self-thinning shape Mediterranean red coral deep population structure: implications for conservation practice. Sci Rep. 2016;6:1–10. doi: 10.1038/s41598-016-0001-8

31. Rossi S, Coppari M, Viladrich N. Benthic-pelagic coupling: new perspectives in the animal forests. In: Rossi S, Bramanti L, Gori A, Orejas C, editors. Marine animal forests. Springer International Publishing; 2017:855–886.

32. Linares C, Garrabou J, Hereu B, Diaz D, Marschal C, Sala E, et al. Assessing the effectiveness of marine reserves on unsustainably harvested long-lived sessile invertebrates. Conserv Biol. 2011;26(1):88–96. doi: 10.1111/j.1523-1739.2011.01795.x 22098377

33. Bavestrello G, Bo M, Bertolino M, Betti F, Cattaneo-Vietti R. Long-term comparison of structure and dynamics of the red coral metapopulation of the Portofino Promontory (Ligurian Sea): a case-study for a Marine Protected Area in the Mediterranean Sea. Mar Ecol. 2015;36:1354–1363.

34. Boavida J, Paulo D, Aurelle D, Arnaud-Haond S, Marschal C, Reed J, et al. A well-kept treasure at depth: Precious red coral rediscovered in Atlantic deep coral gardens (SW Portugal) after 300 years. PLoS One. 2016;11(1):1–26.

35. Thurstan RH, Pandolfi JM, zu Ermgassen PSE. Animal forests through time: historical data to understand present changes in marine ecosystems. In: Rossi S, Bramanti L, Gori A, Orejas C, editors. Marine animal forests. Springer International Publishing; 2017:947–964.

36. Gatti G, Bianchi CN, Parravicini V, Rovere A, Peirano A, Montefalcone M, et al. Ecological change, sliding baselines and the importance of historical data: lessons from combing observational and quantitative data on a temperate reef over 70 years. PLoS One. 2015;10(2):1–20.

37. Marbà N, Díaz-Almela E, Duarte CM. Mediterranean seagrass (Posidonia oceanica) loss between 1842 and 2009. Biol Conserv. 2014;176:183–190.

38. Lotze HK, Coll M, Dunne JA. Historical Changes in Marine Resources, Food-web structure and ecosystem functioning in the Adriatic Sea, Mediterranean. Ecosystems. 2011;14(2):198–222.

39. Holon F, Boissery P, Guilbert A, Freschet E, Deter J. The impact of 85 years of coastal development on shallow seagrass beds (Posidonia oceanica L. (Delile)) in South Eastern France: a slow but steady loss without recovery. Estuar Coast Shelf Sci. 2015;165:204–212.

40. Ferretti F, Myers RA, Serena F, Lotze HK. Loss of large predatory sharks from the Mediterranean Sea. Conserv Biol. 2008;22(4):952–964. doi: 10.1111/j.1523-1739.2008.00938.x 18544092

41. Ardizzone G, Belluscio A, Maiorano L. Long-term change in the structure of a Posidonia oceanica landscape and its reference for a monitoring plan. Mar Ecol. 2006;27:299–309.

42. Jackson JBC. Reefs since Columbus. Coral Reefs. 1997;16(January):23–32.

43. Julius Solinus G. Collectanea rerum memorabilum. Berolini, editor. 1895. p. 392.

44. García-Rodríguez M, Massò C. Estudio biométrico de poblaciones de coral rojo (Corallium rubrum) del litoral de Gerona (NE de España). Bol Inst Esp Ocean. 1986;3(4):61–64.

45. Cattaneo-Vietti R, Bavestrello G, Cerrano C. Prime osservazioni sul corallo rosso profondo lungo il Promontorio di Portofino. In: Seconda ricerca sul corallo rosso nelle acque italiane. Centro Lubrense Esplorazioni Marine: Ministero per le risorse agricole, alimentari e forestali; 1995;104–112.

46. Bavestrello G, Cerrano C, Cattaneo-Vietii R. Biological interactions affecting the growth rates of red coral (Corallium rubrum) colònies. In: Proceedings of the international workshop on red coral science, management, and trade: lessons from the Mediterranean. Bussoletti E, Cottingham D, Bruckner A, Roberts G, Sandulli R, editors. NOAA Technical Memorandum CRCP-13. Naples, Italy: Silver Spring, MD; 2010;151–158.

47. Bavestrello G, Abbiati M, Angiolillo M, Betti F, Bo M, Canese S, et al. Remotely Operated Vehicles (ROVs) as powerful tools for the evaluation of the conservation status of deep red coral banks. In: 2nd Mediterranean symposium on the conservation of coralligenous & other calcareous bio-concretions (Portoroz, Slovenia, 29–30 October 2014). 2015;31–36.

48. Gili i Sardà J. Estudio sistemático y ecológico de los cnidarios bentónicos de las Islas Medes (Girona). Universidad Autónoma de Barcelona; 1980. p. 467.

49. Bramanti L, Vielmini I, Rossi S, Tsounis G, Iannelli M, Cattaneo-Vietti R, et al. Demographic parameters of two populations of red coral (Corallium rubrum L. 1758) in the North Western Mediterranean. Mar Biol. 2014;161(5):1015–1026.

50. Montero-Serra I, Garrabou J, Doak DF, Figuerola L, Hereu B, Ledoux JB, et al. Accounting for life-history strategies and timescales in marine restoration. Conserv Lett. 2017;00(0):1–9.

51. Descamp P, Carteron S. Corail rouge de la Côte Vermeille: état des lieux 2004. 2004. p. 38.

52. Hereu B, Linares C, Zabala M. Avaluació de l’impacte de l’episodi d’espoli de corall vermell (Corallium rubrum) de la zona protegida de les illes Medes detectat druant l’hivern de 2000. In: Seguiment temporal de la reserva marina de les Illes Medes. Informe anual. Universitat de Barcelona, Departament de Medi Ambient, Generalitat de Catalunya. 2000:51–60.

53. García-Rodríguez M, Massó C. Modelo de explotación por buceo del coral rojo (Corallium rubrum L.) del Mediterráneo. Boletín del Inst Español Oceanogr. 1986;3(4):75–82.

54. Sardà R, Rossi S, Martí X, Gili JM. Marine benthic cartography of the Cap de Creus (NE Catalan Coast, Mediterranean Sea). Sci Mar. 2012;76:159–171.

55. Hereu B, Quinana X. El fons marí de les illes Medes i el Montgrí: quatre dècades de recerca per a la conservació. Hereu B, Quinana X, editors. Càtedra d’ecosistemes litorals Mediterranis; 2013. p. 195.

56. Payrot J, Hartmann V, Cadène F. Plan de gestion 2015–2019 de la Reserve Naturelle Marine de Cerbère-Banyuls, section A, diagnostic de la RNMCB: informations générales, environnement, biodiversité, cadre socio-économique et culturel, vocation à accueillir le public et intérët pédagogique. Conseil Général des Pyrénées-Orientales. 2014. p. 85.

57. Cánovas-Molina A, Montefalcone M, Vassallo P, Morri C, Bianchi CN, Bavestrello G. Combining literature review, acoustic mapping and in situ observations: an overview of coralligenous assemblages in Liguria (NW Mediterranean Sea). Sci Mar. 2016;80(1):7–16.

58. Tsounis G, Rossi S, Laudien J, Bramanti L, Fernández N, Gili JM, et al. Diet and seasonal prey capture rates in the Mediterranean red coral (Corallium rubrum L.). Mar Biol. 2006;149:313–325.

59. Previati M, Scinto A, Cerrano C, Osinga R. Oxygen consumption in Mediterranean octocorals under different temperatures. J Exp Mar Bio Ecol. 2010;390:39–48.

60. McCloskey LR, Wethey DS, Porter JW. Measurement and interpretation of photosynthesis and respiration in reef corals. In: Stoddart D, Johannes R, editors. Coral reefs: research methods. Monogr Oceanogr Methodol (UNESCO); 1978. p. 379–396.

61. Coppari M. The importance of benthic suspension feeders in the biogeochemical cycles: active and passive suspension feeders in coralligeneos community. Universitat Autònoma de Barcelona. Universitat Autònoma de Barcelona; 2015. p. 119.

62. Instrucción sobre el modo de recoger los mariscos, o sean caracoles, conchas, corales y otros productos marinos, que hayan de servir para el estudio de la historia natural. p. 11.

63. Maluquer J. Instruccions per a la recol·lecció, preparació i conservació d’animals marins. Musei Barc Sci Nat Opera. 1917;1:1–55.

64. Pons J. Coralls i corallers a la costa gironina. Revista de Girona. 1989;55–60.

65. Coll M, Piroddi C, Steenbeek J, Kaschner K, Lasram FBR, Aguzzi J, et al. The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS One. 2010;5(8):1–36.

66. Goffredo S, Dubinsky Z. The Mediterranean Sea: its history and present challenges. Fauna. Springer, Germany. 2014. p. 654.

67. Gray JS. Marine biodiversity: patterns, threats and conservation needs. Biodivers Conserv. 1997;6:153–175.

68. Ascione C. The art of coral: myth, history and manufacture from ancient times to the present. In: Cicogna F, Cattaneo-Vietti R, editors. Red coral in the Mediterranean Sea: art, history and science. Roma: Min. Ris. Agr. Al. For.; 1993. p. 11–36.

69. Rossi S. The sea that once was. In: Rossi S, editor. Oceans in decline. Copernicus Books, Springer-Nature Switzerland; 2019;13–21.

70. Giannini F, Gili J, Santangelo G. Relationships between the spatial distribution of red coral Corallium rubrum and coexisting suspension feeders at Medas Islands Marine Protected Area (Spain). Ital J Zool. 2003;70:233–239.

71. Tortonese E. The Mediterranean red coral and its associated fauna. Sea Frontiers, Miami. 1963;9(4):205–211.

72. Weinberg S. Autoecology of shallow-water octocorallia from Mediterranean rocky substrata, I. The Banyuls area. Bijdr tot Dierkd. 1979;49(1):1–15.

73. Lastras G, Canals M, Ballesteros E, Gili JM, Sanchez-Vidal A. Cold-water corals and anthropogenic impacts in La Fonera submarine canyon head, Northwestern Mediterranean Sea. PLoS One. 2016;11(5):1–36.

74. Purpura G. Osservazioni sulla pesca del corallo rosso nell’antichità. 2006. p. 14.

75. Plujà i Canals A. El corall vermell. Farella, La revista de Llançà. 1999;23–26.

76. Torntore SJ. Italian coral beads: characterizing their value and role in global trade and cross-cultural exchange. Doctoral dissertation, University of Minnesota. 2002. p. 245.

77. Lleonart J, Camarasa JM. Un document inèdit de 1722 sobre la pesca a les costes de Catalunya del naturalista català Joan Salvador i Riera. Drassana Revista del Museu Marítim de Barcelona. 1988;31–37.

78. Ortíz A, Massó C, Soriano O, Limia J. La barra italiana como arte de pesca del coral rojo (Corallium rubrum L.) en el mar de Alborán (SE de España). Boletín del Inst Español Oceanogr. 1986;3(4):83–92.

79. Audivert M. El coral i l’Estartit. In: L’Estartit i les Medes. Granollers, Barcelona: Montblanc-Martin. 1971. p. 422.

80. Roghi G. La febbre rossa. La strada del corallo: una storia italiana. Mondo sommerso. 1966;(6). p. 35.

81. Ghidiglia C. L’industria del corallo in Italia. G degli Econ. 1892;5(Anno 3):479–510.

82. Mazzarelli G. Banchi di corallo esplorati dalla R. Nave “Volta” nell’estate del 1913. Roma: Ministero di agricoltura, industria e commercio; 1915. p. 178.

83. Dantan JL. Recherches sur la croissance du corail rouge (Corallium rubrum Lamarck). Bull soc zool Fr. 1928;53(1):42–46.

84. Tsounis G, Rossi S, Bramanti L, Santangelo G. Management hurdles for sustainable harvesting of Corallium rubrum. Mar Policy. 2013;39:361–364.

85. Tsounis G. Jewel of the deep: Are the modern incarnations of age, old traditions, coral diving and craftsmanship, selling Mediterranean red coral out? Natural History Magazine. 2009;118(3):30–35.

86. Bini G, Maldura CM. La pesca delle spugne e del corallo. Firenze; 1938. p. 100.

87. Santangelo G, Abbiati M. Red coral: conservation and management of an over-exploited Mediterranean species. Aquat Conserv Mar Freshw Ecosyst. 2001;11:253–259.

88. Food and Agriculture Organization. General Fisheries Commission for the Mediterranean technical consultation on red coral of the Mediterranean. Fisheries report No. 413. Torre del Greco, Italy; 1988.

89. Fuchs A. Banyuls: une réserve grand cru. Le Monde de la mer. 1990;56–58.

90. Salmona P, Verardi D. The Marine Protected Area of Portofino, Italy: a difficult balance. Ocean Coast Manag. 2001;44:39–60.

91. Linares C, Rovira G, Cabrito A, Aspillaga E, Capdevila P, López-Sanz A, et al. Seguiment de les poblacions de corall vermell al Parc Natural de Cap de Creus i al Parc Natural del Montgrí, les Illes Medes i el Baix Ter. In: Seguiment del medi marí al Parc Natural del Cap de Creus i al Parc Natural del Montgrí, les Illes Medes i el Baix Ter. Memòria 2017. 2018;71–94.

92. Environnement Septentrion. Étude des populations de corail rouge dans la Réserve Naturelle Marine de Cerbère-Banyuls et en périphérie (Côte Vermeille). Marseille. 2015. p. 50.

93. Calcinai B, Cerrano C, Bavestrello G, Milanese M, Sarà M. Il popolamento di spugne perforatrici di Corallium rubrum e di alcuni madreporari del Promontorio di Portofino. Boll Mus Ist biol Univ Genova. 2000;64–65:53–59.

94. Senes L, Santarelli B, Barsotti G. Red coral from Portofino Promontory. Boll Mus Ist biol Univ Genova. 2000;64–65:87–94.

95. Cattaneo-Vietti R, Bavestrello G, Senes L. Red coral from the Portofino Promontory (Ligurian Sea). In: Cicogna F, Cattaneo-Vietti R, editors. Red coral in the Mediterranean Sea: art, history and science. Roma: Min. Ris. Agr. Al. For. 1993;109–130.

96. Tortonese E. Bionomia marina della regione costiera fra Punta della Chiappa e Portofino (Riviera Ligure di Levante). Arch di Oceanogr e Limnol. 1958;11(2):167–210.

97. Maluquer J. Treballs oceanogràfics en la costa del Empurdà. Barcelona, Spain: Junta de Ciències Naturals de Barcelona; 1916. p. 261.

98. Tur JM, Godall P. Consideraciones preliminares sobre la ecología de los antozoos del litoral sur de la Costa Brava. Oecologia Aquat. 1982;6:175–183.

99. Programa-Bentos. Estudio ecológico de las comunidades bentónicas de sustratos duros de la zona superior de la plataforma continental Mediterranean española. 1973. p. 265.

100. Carus JV. Prodromus faunae Mediterraneae Koch E, editor. Stuttgart. 1885;1. p. 524.

101. Arias-Ortiz A, Serrano O, Masqué P, Lavery PS, Mueller U, Kendrick GA, et al. A marine heatwave drives massive losses from the world’s largest seagrass carbon stocks. Nat Clim Chang. 2018;8:338–344.

102. Rossi S, Bramanti L, Gori A, Orejas C. An overview of the animal forests of the world. In: Rossi S, Bramanti L, Gori A, Orejas C, editors. Marine animal forests. Springer International Publishing; 2017. p. 26.

103. Duarte CM, Marbà N, Gacia E, Fourqurean JW, Beggins J, Barrón C, et al. Seagrass community metabolism: assessing the carbon sink capacity of seagrass meadows. Global Biogeochem Cycles. 2010;24(4):1–8.

104. Hughes TP, Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, et al. Climate change, human impacts, and the resilience of coral reefs. Science. 2003;301(929–933):929–934.

105. Calvo E, Simó R, Coma R, Ribes M, Pascual J, Sabatés A, et al. Effects of climate change on Mediterranean marine ecosystems: the case of the Catalan Sea. Clim Res. 2011;50:1–29.

106. Bianchi CN. Climate change and biological respones in the marine benthos. Atti del 12° Congr dell’Associazione Ital di Oceanol e Limnol. 1997;1:3–20.

107. Galli G, Solidoro C, Lovato T. Marine heat waves hazard 3D maps and the risk for low motility organisms in a warming Mediterranean Sea. Front Mar Sci. 2017;4:1–14.

108. Galli G, Bramanti L, Priori C, Rossi S, Santangelo G, Tsounis G, et al. Modelling red coral (Corallium rubrum) growth in response to temperature and nutrition. Ecol Modell. 2016;337:137–148.

109. Garrabou J, Coma R, Bensoussan N, Bally M, Chevaldonné P, Cigliano M, et al. Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Chang Biol. 2009;15:1090–1103.

110. Torrents O, Tambutté E, Caminiti N, Garrabou J. Upper thermal thresholds of shallow vs. deep populations of the precious Mediterranean red coral Corallium rubrum (L.): assessing the potential effects of warming in the NW Mediterranean. J Exp Mar Bio Ecol. 2008;357:7–19.

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

112. Perez T, Garrabou J, Sartoretto S, Harmelin J-G, Francour P, Vacelet J. Mortalité massive d’invertébrés marins: un événement sans précédent en Méditerranée nord-occidentale. Comptes Rendus l’Académie des Sci Sci la Vie. 2000;323:853–865.

113. Le Goff C, Tambutté E, Venn AA, Techer N, Allemand D, Tambutté S. In vivo pH measurement at the site of calcification in an octocoral. Sci Rep. 2017;7(1):1–14. doi: 10.1038/s41598-016-0028-x

114. Bramanti L, Movilla J, Guron M, Calvo E, Gori A, Dominguez-Carrió C, et al. Detrimental effects of ocean acidification on the economically important Mediterranean red coral (Corallium rubrum). Glob Chang Biol. 2013;19:1897–1908. doi: 10.1111/gcb.12171 23505003

115. Bramanti L, Magagnini G, De Maio L, Santangelo G. Recruitment, early survival and growth of the Mediterranean red coral Corallium rubrum (L 1758), a 4-year study. J Exp Mar Bio Ecol. 2005;314:69–78.

116. Coppari M, Zanella C, Rossi S. The importance of coastal gorgonians in the blue carbon budget. Sci Rep. 2019:9(13550):1–12.

117. Marsili CLF. Extrait d’une lettre ecrite de Cassis, prés de Marseille, le 18 de Decembre 1706 à Monsieur l’Abbé Bignon, par Monsieur le Comte Marsilli, touchant quelques branches de corail qui ont fleuri. Suppl du J des Sçavans. 1707;59–66.

118. Marsili LF. Histoire physique de la mer. Ouvrage enrichi de figures dessinées d’après le naturel. Amsterdam: La Compagnie; 1725. p. 173.

119. de Lacaze Duthiers M. On the reproduction of red coral. Ann Mag Nat Hist. 1862;9(52):335–336.

120. de Lacaze-Duthiers H. Histoire naturelle du corail, organisation, reproduction, pêche en Algérie, industrie et commerce. Baillière et Fils JB, editor. Paris: M. le Ministre de l’instruction publique et de M. le governeur général de l’Algérie; 1864. p. 443.

121. True MA. Étude quantitative de quatre peuplements sciaphiles sur substrat rocheux dans la région Marseillaise. Bull l’Institut Océanographique. 1970;69(1401):1–48.

122. Carpine C, Grasshoff M. Les gorgonaires de la Méditerranée. Bull l’Institut Océanographique. 1975;71(1430). p. 140.

123. Marin J, Reynal de Saint-Michel L. Premières données biométriques sur le corail rouge, Corallium rubrum LMCK, de Corse. Rapp Comm int Mer Médit. 1981;27(2):171–173.

124. Marion AF. Esquisse d’une topographie zoologique du Golfe de Marseille. Ann du Musée d’Histoire Nat Marseille—Zool. 1883;1(1). p. 108.

125. Gilet R. Particularites de la zonation marine sur les cotes rocheuses s’etendant entre Nice et la frontiere italienne. Recl des Trav la Stn Mar d’Endoume. 1954;12:41–49.

126. Peres JM, Picard J. Considerations sur l’etagement des formations benthiques. Recl des Trav la Stn Mar d’Endoume. 1956;18:15–30.

127. Gautier Y V. Recherches sur les biocoenoses benthiques des côtes de Camargue et du Golfe de Fos. Recl des Trav la Stn Mar d’Endoume. 1957;22(13):55–64.

128. Laborel J, Pérès JM, Picard J, Vacelet J. Étude directe des fonds des parages de Marseille de 30 à 300 m avec la soucoupe plongeante Cousteau. Bull l’Institut Océanographique. 1961;(1206):1–16.

129. Vaissière R. Contributions à l’étude bionomique de la Méditerranée occidentale (Côte du Var et des Alpes maritimes-côte occidentale de Corse). I—Généralités. Bull l’Institut Océanographique. 1964;63(1310):1–12.

130. Peres JM, Picard J. Noveau manuel de bionomie benthique de la Mer Mediterranee. 1964. p. 137.

131. Picard J. Recherches qualitatives sur les biocoenoses marines des substrats meubles dragables de la région Marseillaise. Recl des Trav la Stn Mar d’Endoume. 1965;36(52). p. 160.