Reproductive cycle and trophic ecology in deep versus shallow populations of the Mediterranean gorgonian Eunicella singularis (Cap de Creus, northwestern Mediterranean Sea)

Coral Reefs

Volumn 31, Issue 3, 2012, Pages 823-837

  Gori, A ^a   Viladrich, N ^b   Gili, J ^a   Kotta, M ^a   Cucio, C ^a   Magni, L ^a   Bramanti, L ^a   Rossi, S ^b  

^a INSTITUT DE CIÈNCIES DEL MAR   (Spain)

^b INSTITUT DE CIÈNCIA I TECNOLOGIA AMBIENTALS   (Spain)

Author keywords

15N 13C; Energy storage; Fatty acids; Gorgonian; Mediterranean Sea; Reproduction

Indexed keywords

ALGA; CARBON ISOTOPE; ENERGY BUDGET; FATTY ACID; INVERTEBRATE; ISOTOPIC COMPOSITION; NITROGEN ISOTOPE; PARTICULATE ORGANIC MATTER; REPRODUCTIVE CYCLE; SEASONALITY; SESSILE SPECIES; SOFT CORAL; SYMBIONT; TROPHIC ENVIRONMENT; ZOOPLANKTON;

CAP DE CREUS; CATALONIA; GERONA [CATALONIA]; MEDITERRANEAN SEA; MEDITERRANEAN SEA (NORTHWEST); SPAIN;

ALGAE; EUNICELLA SINGULARIS; GORGONIA;

EID: 84865661692     PISSN: 07224028     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00338-012-0904-1     Document Type: Article

References (81)

1. Alino PM, Coll JC (1989) Observations of the synchronized mass spawning and postsettlement activity of octocorals in the Great Barrier Reef, Australia: biological aspects. Bull Mar Sci 45: 697-707.
2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.
3. Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, Auckland. http://www. stat. auckland. ac. nz/~mja/Programs. htm.
4. Anderson MJ, ter Braak CJF (2003) Permutation tests for multi-factorial analysis of variance. J Stat Comp Sim 73: 85-113.
5. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44: 123-195.
6. Barnes H, Blackstock J (1973) Estimation of lipids in marine animal tissues: detailed investigation of the sulphophosphovanillin method for "total" lipids. J Exp Mar Biol Ecol 12: 103-118.
7. Benayahu Y, Loya Y (1983) Surface brooding in the Red Sea soft coral Parerythropodium fulvumfulvum (Forskål 1775). Biol Bull 165: 353-369.
8. Benayahu Y, Loya Y (1986) Sexual reproduction of a soft coral: synchronous and brief annual spawning of Sarcophyton glaucum (Quoy & Gaimard, 1833). Biol Bull 170: 32-42.
9. Ben-David-Zaslow R, Benayahu Y (1999) Temporal variation in lipid, protein and carbohydrate content in the Red Sea soft coral Heteroxenia fucsescens. J Mar Biol Assoc UK 79: 1001-1006.
10. Bo M, Bavestrello G, Canese S, Giusti M, Salvati E, Angiolillo M, Greco S (2009) Characteristics of a black coral meadow in the twilight zone of the central Mediterranean Sea. Mar Ecol Prog Ser 397: 53-61.
11. Bo M, Bertolino M, Borghini M, Castellano M, Covazzi Harriague A, Di Camillo CG, Gasparini G, Misic C, Povero P, Pusceddu A, Schroeder K, Bavestrello G (2011) Characteristics of the mesophotic megabenthic assemblages of the Vercelli seamount (North Tyrrhenian Sea). PLoS ONE 6: e16357.
12. Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the 'deep reef refugia' hypothesis: focus on Caribbean reefs. Coral Reefs 29: 309-327.
13. Brazeau DA, Lasker H (1989) The reproductive cycle and spawning in a Caribbean gorgonian. Biol Bull 176: 1-7.
14. Broglio E, Jónasdóttir SH, Calbet A, Jakobsen HH, Saiz E (2003) Effect of heterotrophic versus autotrophic food on feeding and reproduction of the calanoid copepod Acartia tonsa: relationship with prey fatty acid composition. Aquat Microb Ecol 31: 267-278.
15. Buesseler KO, Lamborg CH, Boyd PW, Lam PJ, Trull TW, Bidigare RR, Bishop JKB, Casciotti KL, Dehairs F, Elskens M, Honda M, Karl DM, Siegel DA, Silver MW, Steinberg DK, Valdes J, van Mooy B, Wilson S (2007) Revisiting carbon flux through the ocean's twilight zone. Science 316: 567-570.
16. Carlier A, Riera P, Amouroux JM, Bodiou JY, Grémare A (2007) Benthic trophic network in the Bay of Banyuls-sur-Mer (northwest Mediterranean, France): An assessment based on stable carbon and nitrogen isotopes analysis. Estuar Coast Shelf Sci 72: 1-15.
17. Carpine C, Grasshoff M (1975) Les gorgonaires de la Méditerranée. Bull Inst Océanogr Monaco 71: 1-140.
18. Coma R, Ribes M, Gili JM, Zabala M (2000) Seasonality in coastal benthic ecosystems. Tree 15: 448-453.
19. Dahan M, Benayahu Y (1997) Reproduction of Dendronephthya hemprichi (Cnidaria: Octocorallia): year-round spawning in an azooxanthellate soft coral. Mar Biol 129: 573-579.
20. Dalsgaard J, St John M, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46: 225-340.
21. Drew EA (1983) Light. In: Earll E, Erwin DG (eds) Sublittoral ecology. Oxford University Press, Oxford, The ecology of the shallow sublittoral benthos, pp 10-57.
22. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for the determination of sugars and related substances. Anal Chem 28: 350-356.
23. Fan TY, Dai CF (1995) Reproductive ecology of scleractinian coral Echinopora lamellosa in northern and southern Taiwan. Mar Biol 123: 565-572.
24. Ferrier-Pagès C, Peirano A, Abbate M, Cocito S, Negri A, Rottier C, Riera P, Rodolfo- Metalpa R, Reynaud S (2011) Summer autotrophy and winter heterotrophy in the temperate symbiotic coral Cladocora caespitosa. Limnol Oceanogr 56: 1429-1438.
25. Fitt WK, Pardy RL (1981) Effects of starvation, and light and dark on the energy metabolism of symbiotic and aposymbiotic sea anemones, Anthopleura elegantissima. Mar Biol 61: 199-205.
26. Gardner JPA (2000) Where are the mussels on Cook Strait (New Zeland) shores? Low seston quality as a possible factor limiting multi-species distributions. Mar Ecol Prog Ser 194: 123-132.
27. Gili JM, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Tree 13: 316-321.
28. Gili JM, Ros J (1985) Study and cartography of the benthic communities of Medes Islands (NE Spain). PSZNI Mar Ecol 6: 219-238.
29. Ginsburg R (2007) Mesophotic coral reefs are the frontier of reef exploration and research. Proceedings of the 33rd scientific meeting of the Association of Marine Laboratories of the Caribbean (AMLC) 56 (Suppl. 1): xii.
30. 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: 1571-1584.
31. Gori A, Rossi S, Berganzo-González E, Pretus JL, Dale MRT, Gili JM (2011a) Spatial distribution, abundance and relationship with environmental variables of the gorgonians Eunicella singularis, Paramuricea clavata and Leptogorgia sarmentosa (Cape of Creus, Northwestern Mediterranean Sea). Mar Biol 158: 143-158.
32. Gori A, Rossi S, Linares C, Berganzo E, Orejas C, Dale MRT, Gili JM (2011b) Size and spatial structure in deep vs shallow populations of the Mediterranean gorgonian Eunicella singularis (Cap de Creus, Northwestern Mediterranean Sea). Mar Biol 158: 1721-1732.
33. Gori A, Bramanti L, López-González P, Thoma JN, Gili JM, Grinyó J, Uceira V, Rossi S (2012) Characterization of the zooxanthellate and azooxanthellate morphotypes of the Mediterranean gorgonian Eunicella singularis. Mar Biol. doi: 10. 1007/s00227-012-1928-3.
34. Grigg RW (1977) Population dynamics of two gorgonian corals. Ecology 58: 278-290.
35. Guillén J, Palanques A, Puig P, de Durriel Madron X, Nyffeler F (2000) Field calibration of optical sensors for measuring suspended sediment concentration in the Western Mediterranean. Sci Mar 64: 427-435.
36. Harland AD, Davies PS, Fixter LM (1992) Lipid content of some Caribean corals in relation to depth and light. Mar Biol 113: 357-361.
37. Harmelin JG, Garrabou J (2005) Suivi d'une population de Paramuricea clavata (Risso, 1826) (Cnidaria, Octocorallia, Gorgonacea) dans le parc national de Port-Cros (Méditerranée, France): comparaison des états 1992 et 2004 sur le site de la Galère. S. Sci Rep Port-Cros Natl Park 21: 175-191.
38. Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Stambler N (ed) Dubinsky Z. Coral reefs, An ecosystem in transition. Springer Science + Business Media.
39. Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA, Pyle RL, Zawada DG, Appeldoorn R (2010) Theme section on "Mesophotic coral ecosystems: Characterization, ecology, and management". Coral Reefs 29: 247-251.
40. Hiscock K (1983) Water movement. In: Earll E, Erwin DG (eds) Sublittoral ecology. Oxford University Press, Oxford, The ecology of the shallow sublittoral benthos, pp 58-96.
41. Jacob U, Brey T, Fetzer I, Kaehler S, Mintenbeck K, Dunton K, Beyer K, Struck U, Pakhomov EA, Arntz WE (2006) Towards the trophic structure of the Bouvet Island marine ecosystem. Polar Biol 29: 106-113.
42. Jokiel PL, Ito RY, Liu PM (1995) Night irradiance and synchronization of lunar release of planula larvae in the reef coral Pocillopora damicornis. Mar Biol 88: 167-174.
43. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69: 373-386.
44. Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, Hinderstein L, Toonen RJ (2010) Community ecology of mesophotic coral reef ecosystems. Coral Reefs 29: 255-275.
45. Kojis BL, Quinn NJ (1984) Seasonal and depth variation in fecundity of Acropora palifera at two reefs in Papua New Guinea. Coral Reefs 3: 165-172.
46. Kruger A, Schleyer MH, Banayahu Y (1998) Reproduction in Anthelia glauca (Octocorallia: Xeniidae). I. Gametogenesis and larval brooding. Mar Biol 131: 423-432.
47. Linares C, Coma R, Garrabou J, Díaz D, Zabala M (2008) Size distribution, density and disturbance in two Mediterranean gorgonians: Paramuricea clavata and Eunicella singularis. J Appl Ecol 45: 688-699.
48. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
49. Menza C, Kendall M, Hile S (2008) The deeper we go the less we know. Int J Trop Biol 56: 11-24.
50. Oksanen J, Kindt R, Legendre P, O'Hara RB (2005) Vegan: community ecology package. Version 1. 7-81. http://cran. r-project. org.
51. Patton JS, Battey JF, Rigler MW, Porter JW, Black CC, Burris JE (1983) A comparison of the metabolism of bicarbonate 14C and acetate 1-14C and the variability of species lipid composition in reef corals. Mar Biol 75: 121-130.
52. R Development Core Team (2007) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051- 07-0, URL. http://www. R-project. org.
53. Ribes M, Coma R, Gili JM (1999) Heterogeneous feeding in benthic suspension feeders: the natural diet and grazing rate of the temperate gorgonian Paramuricea clavata (Cnidaria: Octocorallia) over a year cycle. Mar Ecol Prog Ser 183: 125-137.
54. Ribes M, Coma R, Rossi S (2003) Natural feeding of the temperate asymbiotic octocoral gorgonian Leptogorgia sarmentosa (Cnidaria: Octocorallia). Mar Ecol Prog Ser 254: 141-150.
55. Ribes M, Coma R, Rossi S, Micheli M (2007) Cycle of gonadal development in Eunicella singularis (Cnidaria: Octocorallia): trends in sexual reproduction in gorgonians. Invertebr Biol 126: 307-317.
56. Rinkevich B, Loya Y (1987) Variability in the pattern of sexual reproduction of the coral Stylophora pistillata at Eilat, Red Sea: a long-term study. Biol Bull 173: 335-344.
57. Rooney J, Donham E, Montgomery A, Spalding H, Parrish F, Boland R, Fenner D, Gove J, Vetter O (2010) Mesophotic coral ecosystems in the Hawaiian Archipelago. Coral Reefs 29: 361-367.
58. Ros J, Romero J, Ballesteros E, Gili JM (1985) Diving in blue water. The benthos. In: Margalef R (ed) Western Mediterranean. Pergamon Press, pp 233-295.
59. Rossi S, Gili JM (2009) The cycle of gonadal development of the soft bottom-gravel gorgonian Leptogorgia sarmentosa in the NW Mediterranean sea. Invertebr Reprod Dev 53: 175-190.
60. Rossi S, Tsounis G (2007) Temporal and spatial variation in protein, carbohydrate, and lipid levels in Corallium rubrum (Anthozoa, Octocorallia). Mar Biol 152: 429-439.
61. Rossi S, Grémare A, Gili JM, Amouroux JM, Jordana E, Vétion G (2003) Biochemical characteristic of settling particulate organic matter at two north-western Mediterranean sites: a seasonal comparison. Estuar Coast Shelf Sci 58: 423-434.
62. Rossi S, Gili JM, Coma R, Linares C, Gori A, Vert N (2006) Seasonal cycles of protein, carbohydrate and lipid concentrations in Paramuricea clavata: (Anthozoa, Octocorallia): evidences for summer-autumn feeding constraints. Mar Biol 149: 643-665.
63. Rossi S, Tsounis G, Orejas C, Padrón T, Gili JM, Bramanti L, Teixidó N, Gutt J (2008) Survey of deep-dwelling red coral (Corallium rubrum) populations at Cap de Creus (NW Mediterranean). Mar Biol 154: 533-545.
64. Sebens KP (1987) The ecology of indeterminate growth in animals. Annu Rev Ecol Syst 18: 371-407.
65. Sier CJS, Olive PJW (1994) Reproduction and reproductive variability in the coral Pocillopora verrucosa from the Republic of Maldives. Mar Biol 118: 713-722.
66. Sink KJ, Boshoff W, Samaai T, Timm PG, Kerwath SE (2006) Observations of the habitats and biodiversity of the submarine canyons at Sodwana Bay. S Afr J Sci 102: 466-474.
67. Slattery M, McClintock JB (1995) Population structure and feeding deterrence in three shallow-water Antarctic soft corals. Mar Biol 122: 461-470.
68. Soler-Membrives A, Rossi S, Munilla T (2011) Feeding ecology of NW Mediterranean sea spiders (Pycnogonida): temporal variation in fatty acid composition. Estuar Coast Shelf Sci 92: 588-597.
69. Stimson JS (1987) Location, quantity and rate of change in quantity of lipids in tissue of hawaiian hermatypic corals. Bull Mar Sci 41: 889-904.
70. Théodor J (1967) Contribution a l'étude des gorgones (VII): écologie et comportement de la planula. Vie Milieu 18: 291-301.
71. Théodor J (1969) Contribution a l'étude des gorgones (VIII): Eunicella stricta aphyta sous-espèce nouvelle sans zooxanthelles proche d'une espèce normalement infestée par ces algues. Vie Milieu 20: 635-638.
72. Tolosa I, Treignier C, Grover R, Ferrier-Pagès C (2011) Impact of feeding and short-term temperature stress on the content and isotopic signature of fatty acids, sterols, and alcohols in the scleractinian coral Turbinaria reniformis. Coral Reefs 30: 763-774.
73. Treignier C, Grover R, Ferrier-Pagès C, Tolosa I (2008) Effect of light and feeding on the fatty acid and sterol composition of zooxanthellae and host tissue isolated from the scleractinian coral Turbinaria reniformis. Limnol Oceanogr 53: 2702-2710.
74. True MA (1970) Étude quantitative de quatre peuplements sciaphiles sur substrat rocheux dans la région marseillaise. Bull Inst Océanogr Monaco 69: 1-48.
75. Tsounis G, Rossi S, Araguren M, Gili JM, Arntz WE (2006a) Effects of spatial variability and colony size on the reproductive output and gonadal development cycle of the Mediterranean red coral (Corallium rubrum L.). Mar Biol 143: 513-527.
76. Tsounis G, Rossi S, Laudien J, Bramanti L, Fernández N, Gili JM, Arntz W (2006b) Diet and seasonal prey capture rate in the Mediterranean red coral (Corallium rubrum L.). Mar Biol 149: 313-325.
77. Virgilio M, Airoldi L, Abbiati M (2006) Spatial and temporal variations of assemblages in a Mediterranean coralligenous reef and relationships with surface orientation. Coral Reefs 25: 265-272.
78. Vize PD (2006) Deepwater broadcast spawning by Montastraea cavernosa, Montastraea franksi, and Diploria strigosa at the Flower Garden Banks, Gulf of Mexico. Coral Reefs 25: 169-171.
79. Weinberg S, Weinberg F (1979) The life cycle of a gorgonian: Eunicella singularis (Esper, 1794). Bijdr Dierk 48: 127-140.
80. West JM, Harvell CD, Walls AM (1993) Morphological plasticity in a gorgonian coral (Briareum asbestinum) over a depth cline. Mar Ecol Prog Ser 94: 61-69.
81. Zhukova NV, Kharlamenko VI (1999) Sources of essential fatty acids in the marine microbial loop. Aquat Microb Ecol 17: 153-157.