sm84n3-5018

Coexistence of the reef-building coral Cladocora caespitosa and the canopy-forming alga Treptacantha ballesterosii: description of a new Mediterranean habitat

Alèssia Pons-Fita 1, Jana Verdura 2, Jorge Santamaría 2, Diego K. Kersting 3, Enric Ballesteros 1

1 Centre d’Estudis Avançats de Blanes-CSIC, Blanes, Spain.
(AP-F) (Corresponding author) E-mail: alessia.pns@gmail.com. ORCID-iD: https://orcid.org/0000-0003-1828-6003
(EB) E-mail: kike@ceab.csic.es. ORCID-iD: https://orcid.org/0000-0001-5532-5337
2 GRMAR, Institut d’Ecologia Aquàtica, Departament de Ciències Ambientals, Universitat de Girona, Girona, Spain.
(JV) E-mail: janaverdura@gmail.com. ORCID-iD: https://orcid.org/0000-0003-0662-1206
(JS) E-mail: jorgesantamariaperez@gmail.com. ORCID-iD: https://orcid.org/0000-0003-4425-6297
3 Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Institut de Recerca de la Biodiversitat (IRBIO), Universitat de Barcelona, Barcelona, Spain.
(DKK) E-mail: diegokersting@gmail.com. ORCID-iD: https://orcid.org/0000-0002-2049-7849

Summary: Shallow Mediterranean rocky environments are usually dominated by macroalgae, but the stony colonial zooxanthellate coral Cladocora caespitosa is able to build extensive banks in some particular areas. Although zooxanthellate corals and benthic macroalgae are expected to compete for light and space when overlapping in the same habitat, there is previous evidence that C. caespitosa and Mediterranean macroalgae do not suffer from competitive exclusion when living together. Here we characterize a new and unique Mediterranean habitat where the reef-building coral C. caespitosa and erect seaweeds of the order Fucales (Cystoseira s.l.) coexist. In this new habitat C. caespitosa reaches 34% cover and densities of Cystoseira s.l. (mainly Treptacantha ballesterosii) are much higher than values reported from other sites. Interestingly, abundances of T. ballesterosii and C. caespitosa show a positive relationship, suggesting that some kind of facilitation mechanism is taking place. These findings challenge the theory of competitive exclusion between corals and macroalgae and launch a wide array of possible open discussions on coral-macroalgae interactions.

Keywords: Cladocora caespitosa; Treptacantha; Cystoseira; habitat; coral-algal interactions; Mediterranean Sea.

Coexistencia del coral formador de arrecifes Cladocora caespitosa y la macroalga formadora de dosel Treptacantha ballesterosii: descripción de un nuevo hábitat mediterráneo

Resumen: Los ambientes rocosos someros del Mediterráneo están habitualmente dominados por macroalgas, no obstante, el coral colonial zooxantelado Cladocora caespitosa es capaz de formar bancos extensos en algunos lugares. Aunque es predecible que los corales con zooxantelas y las algas bentónicas compitan por la luz y el espacio cuando coinciden en el mismo hábitat, hay evidencias previas de que C. caespitosa y las algas mediterráneas no se excluyen competitivamente cuando viven juntas. En este trabajo se caracteriza un nuevo y único hábitat mediterráneo donde el coral formador de arrecifes C. caespitosa y algas erectas del orden Fucales (Cystoseira s.l.) coexisten. En este hábitat nuevo C. caespitosa alcanza coberturas del 34% y las densidades de Cystoseira s.l. (principalmente de Treptacantha ballesterosii) son mucho mayores que los valores encontrados en otros lugares. Remarcablemente, las abundancias de T. ballesterosii y C. caespitosa muestran una relación positiva, sugiriendo que existe algún tipo de mecanismo de facilitación. Este hallazgo pone en jaque la teoría de exclusión competitiva entre corales y macroalgas, a la vez que puede iniciar un amplio abanico de discusiones en las interacciones entre corales y macroalgas.

Palabras clave: Cladocora caespitosa; Treptacantha; Cystoseira; hábitat; interacciones corales-algas; mar Mediterráneo.

Citation/Como citar este artículo: Pons-Fita A., Verdura J., Santamaría J., Kersting D.K., Ballesteros E. 2020. Coexistence of the reef-building coral Cladocora caespitosa and the canopy-forming alga Treptacantha ballesterosii: description of a new Mediterranean habitat. Sci. Mar. 84(3): 263-271. https://doi.org/10.3989/scimar.05018.11B

Editor: E. Cebrián.

Received: November 22, 2019. Accepted: May 22, 2020. Published: June 17, 2020.

Copyright: © 2020 CSIC. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0) License.

Contents

Summary
Resumen
Introduction
Materials and methods
Results
Discussion
Acknowledgements
References

INTRODUCTIONTop

The most distinct trait of tropical marine ecosystems is the presence of coral reefs build by zooxanthellate scleractinian corals. Although coral reefs are scarce or absent outside tropical environments, there are a few Mediterranean scleractinian corals of the 37 existing ones that can potentially behave as reef-builders (Morri et al. 2000Morri C., Peirano A., Bianchi C.N., et al. 2000. Cladocora caespitosa: A colonial zooxanthellate Mediterranean coral showing constructional ability. Reef Encounter 27: 22-25.). Indeed, the unique zooxanthellate coral that has the capacity to build extensive beds and banks (sensu Peirano et al. 1998Peirano A., Morri C., Mastronuzzi G., et al. 1998. The coral Cladocora caespitosa (Anthozoa, Scleractinia) as a bioherm builder in the Mediterranean Sea. Mem. descritt. Carta Geol. Italia 52: 59-74.) is the Mediterranean pillow coral Cladocora caespitosa (Linné, 1767) (Zibrowius 1982Zibrowius H. 1982. Taxonomy in ahermatypic scleractinian corals. Palaeont. Amer. 54: 80-85., Morri et al. 1994Morri C., Peirano A., Bianchi C.N., et al. 1994. Present day bioconstructions of the hard coral, Cladocora caespitosa (L.) (Anthozoa, Scleractinia), in the Eastern Ligurian Sea (NW Mediterranean). Biol. Mar. Medit. 1: 371-373., Peirano et al. 2001Peirano A., Morri C., Bianchi C.N., et al. 2001. Biomass, carbonate standing stock and production of the mediterranean coral Cladocora caespitosa (L.). Facies 44: 75-80.), which can be considered a habitat former in locations where colonies concentrate in high densities and reach large sizes (Kružić and Požar-Domac 2003Kružić P., Požar-Domac A. 2003. Banks of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic Sea. Coral Reefs 22: 536., Kersting and Linares 2012Kersting D.K., Linares C. 2012. Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar. Ecol. 33: 427-436.).

Due to their reduced distribution, small size and generally low colony densities, Mediterranean coral bioconstructions have not been studied as extensively as tropical coral bioconstructions have. Nevertheless, an important effort has been made during the last few decades to study the distribution, characteristics and ecology of the main C. caespitosa bioconstructions in the Mediterranean Sea (e.g. Schiller 1993Schiller C. 1993. Ecology of the symbiotic coral Cladocora caespitosa (L.) (Faviidae, Scleractinia) in the Bay of Piran (Adriatic Sea): I. Distribution and biometry. Mar. Ecol. 14: 205-219., Kersting et al. 2014aKersting D.K., Teixidó N., Linares C. 2014a. Recruitment and mortality of the temperate coral Cladocora caespitosa: implications for the recovery of endangered populations. Coral Reefs 33: 403-407., Kersting and Linares 2019Kersting D.K., Linares C. 2019. Living evidence of a fossil survival strategy raises hope for warming-affected corals. Sci. Adv. 5: eaax2950.). C. caespitosa is characterized by slow growth, low recruitment rates and limited larval dispersal ability, which make this species very sensitive to disturbances (Kersting et al. 2014aKersting D.K., Teixidó N., Linares C. 2014a. Recruitment and mortality of the temperate coral Cladocora caespitosa: implications for the recovery of endangered populations. Coral Reefs 33: 403-407.). At present, shallow C. caespitosa bioconstructions have suffered a steep decline (Casado-Amezúa et al. 2015Casado-Amezúa P., Kersting D.K., Linares C., et al. 2015. Cladocora caespitosa. The IUCN Red List of Threatened Species 2015: e.T133142A75872554). The main anthropogenic causes, which often show synergistic effects, are pollution (Kružić and Požar-Domac 2007Kružić P., Požar-Domac A. 2007. Impact of tuna farming on the banks of the coral Cladocora caespitosa in the Adriatic Sea. Coral Reefs 26: 665., El Kateb et al. 2016El Kateb A., Stalder C., Neururer C., et al. 2016. Correlation between pollution and decline of Scleractinian Cladocora caespitosa (Linnaeus, 1758) in the Gulf of Gabes. Heliyon 2: e00195.), warming (Rodolfo-Metalpa et al. 2005Rodolfo-Metalpa R., Bianchi C.N., Peirano A., et al. 2005. Tissue necrosis and mortality of the temperate coral Cladocora caespitosa. Ital. J. Zool. 72: 271-276., Kersting et al. 2013Kersting D.K., Bensoussan N., Linares C. 2013. Long-term responses of the endemic reef-builder Cladocora caespitosa to Mediterranean warming. PLoS ONE 8: e70820., 2015Kersting D.K., Cebrian E., Casado C., et al. 2015. Experimental evidence of the synergistic effects of warming and invasive algae on a temperate reef-builder coral. Sci. Rep. 5: 18635.) and invasive species (Kersting et al. 2014bKersting D.K., Ballesteros E., De Caralt S., et al. 2014b. Invasive macrophytes in a marine reserve (Columbretes Islands, NW Mediterranean): spread dynamics and interactions with the endemic scleractinian coral Cladocora caespitosa. Biol. Inv. 16: 1599-1610., 2014cKersting D.K., Ballesteros E., Bensoussan N., et al. 2014c. Long-term monitoring of Cladocora caespitosa reefs in the Columbretes Islands: From mapping to population dynamics and threats. In Bouafif C., Langar H., et al. (eds), Proceedings of the Second Mediterranean Symposium of coralligenous and other calcareous bioconcretions (Portoroz, Slovenia, 29-30 October 2014). RAC/SPA publ., Tunis. pp. 89-94., 2015Kersting D.K., Cebrian E., Casado C., et al. 2015. Experimental evidence of the synergistic effects of warming and invasive algae on a temperate reef-builder coral. Sci. Rep. 5: 18635.). All these relevant features urged IUCN to include this species in the Red List with the status “Endangered” (Casado-Amezúa et al. 2015Casado-Amezúa P., Kersting D.K., Linares C., et al. 2015. Cladocora caespitosa. The IUCN Red List of Threatened Species 2015: e.T133142A75872554) and the species also appears in the List of Endangered and Threatened Species of the Barcelona Convention (Annex II UNEP-MAP-RAC/SPA 2013UNEP/MAP/RAC-SPA. 2013. Protocol concerning specially protected areas and biological diversity in the Mediterranean. Annex II. List of endangered or threatened species. 7 pp.).

Mediterranean shallow rocky bottoms are usually dominated by algal stands (Zabala and Ballesteros 1989Zabala M., Ballesteros E. 1989. Surface-dependent strategies and energy flux in benthic marine communities or, why corals do not exist in the Mediterranean. Sci. Mar. 53: 1-15.). However, with the exceptions of the Alboran Sea and the Messina Strait, kelps are not present in Mediterranean shallow rocky bottoms and most existing canopy-forming algae belong to the order Fucales (Ochrophyta) (Rodríguez-Prieto et al. 2013Rodríguez-Prieto C., Ballesteros E., Boisset F., et al. 2013. Guía de las macroalgas y fanerógamas marinas del Mediterráneo Occidental. Ediciones Omega, Barcelona, 656 pp.). Until recently, only two genera of Fucales—Cystoseira and Sargassum—had been reported from the Mediterranean. Molecular tools identified up to three different clades inside the Mediterranean species previously included in the genus Cystoseira (Draisma et al. 2010Draisma S.G., Ballesteros E., Rousseau F., et al. 2010. DNA sequence data demonstrate the polyphyly of the genus Cystoseira and other Sargassaceae genera (Phaeophyceae). J. Phycol. 46: 1329-1345., Bruno de Sousa et al. 2019Bruno de Sousa C., Cox C.J., Brito L., et al. 2019. Improved phylogeny of brown algae Cystoseira (Fucales) from the Atlantic-Mediterranean region based on mitochondrial sequences. PLoS ONE 14: e0210143.), which resulted in the splitting of the former Cystoseira species into three genera, namely Cystoseira, Treptacantha and Carpodesmia (Orellana et al. 2019Orellana S., Hernández M., Sansón M. 2019. Diversity of Cystoseira sensu lato (Fucales, Phaeophyceae) in the eastern Atlantic and Mediterranean based on morphological and DNA evidence, including Carpodesmia gen. emend. and Treptacantha gen. emend. Eur. J. Phycol. 54: 447-465.), a segregation that was also justified by morphological features (Orellana et al. 2019Orellana S., Hernández M., Sansón M. 2019. Diversity of Cystoseira sensu lato (Fucales, Phaeophyceae) in the eastern Atlantic and Mediterranean based on morphological and DNA evidence, including Carpodesmia gen. emend. and Treptacantha gen. emend. Eur. J. Phycol. 54: 447-465.). Nevertheless, we will commonly refer here to the species included in these three genera as Cystoseira sensu lato (or Cystoseira s.l.), since they share several ecological features. Cystoseira s.l. can make extensive canopy-forming algal beds from the upper infralittoral zone down to the upper circalittoral zone (0 to 50 m depth) (Giaccone and Bruni 1973Giaccone G., Bruni A. 1973. Le Cistoseire e la vegetazione sommersa del Mediterraneo. Atti Ist. Veneto Sci. Lett. Arti 131: 59-103., Sant 2003Sant N. 2003. Algues bentòniques mediterrànies: comparació de mètodes de mostreig, estructura de comunitats i variació en la resposta fotosintètica. Ph.D. Thesis, Universitat de Barcelona, 250 pp.). These beds are very productive (Ballesteros 1988Ballesteros E. 1988. Estructura y dinámica de la comunidad de Cystoseira mediterranea Sauvageau en el Mediterráneo Noroccidental. Inv. Pesq. 52: 313-334., 1990aBallesteros E. 1990a. Structure and dynamics of the community of Cystoseira zosteroides (Turner) C. Agardh (Fucales, Phaeophyceae) in the north-western Mediterranean. Sci. Mar. 54: 217-229., bBallesteros E. 1990b. Structure and dynamics of the Cystoseira caespitosa Sauvageau (Fucales, Phaeophyceae) community in the North-Western Mediterranean. Sci. Mar. 54: 155-168.) and highly structured in three-dimensions, making them a perfect site for nursery (Cheminée et al. 2013Cheminée A., Sala E., Pastor J., et al. 2013. Nursery value of Cystoseira forests for Mediterranean rocky reef fishes. J. Exp. Mar. Biol. Ecol. 442: 70-79., 2017Cheminée A., Pastor J., Bianchimani O., et al. 2017. Juvenile fish asemblages in temperate rocky reefs are shaped by the presence of macroalgae canopy and its three dimensional structure. Sci. Rep. 7: 14638.) and shelter and a source of food for a large number of species (Boudouresque 1971Boudouresque C.F. 1971. Recherches de bionomie analytique, structurale et expérimentale sur les peuplements benthiques sciaphiles de Méditerranée occidentale (fraction algale): la sous-strate sciaphile des peuplements des grandes Cystoseira de mode battu. Bull. Mus. Natl. Hist. Nat. Marseille 31: 79-104., 1972Boudouresque C.F. 1972. Recherches de bionomie analytique, structurale et expérimentale sur les peuplements benthiques sciaphiles de Méditerranée Occidentale (fraction algale): le sous-strate sciaphile d’un peuplement photophile de mode calme, le peuplement à Cystoseira crinita. Bull. Mus. Nat. Hist. Nat. Marseille 32: 253-263., Ballesteros et al. 1998Ballesteros E., Sala E., Garrabou J., et al. 1998. Community structure and frond size distribution of a deep water stand of Cystoseira spinosa (Phaeophyta) in the Northwestern Mediterranean. Eur. J. Phycol. 33: 121-128.). Accordingly, species of Cystoseira s.l. are the most representative macroalgae thriving in well-preserved Mediterranean environments.

Most species of Mediterranean Fucales are undergoing a severe decline (e.g. Bianchi et al. 2014Bianchi C.N., Corsini-Foka M., Morri C., et al. 2014. Thirty years after-dramatic change in the coastal marine habitats of Kos Island (Greece), 1981-2013. Medit. Mar. Sci. 15: 482-497., Thibaut et al. 2015Thibaut T., Blanfuné A., Boudouresque C.F., et al. 2015. Decline and local extinction of Fucales in French Riviera: the harbinger of future extinctions? Medit. Mar. Sci. 16: 206-224., Mariani et al. 2019Mariani S., Cefalì M.E., Chappuis E., et al. 2019. Past and present of Fucales from shallow and sheltered shores in Catalonia. Reg. Stud. Mar. Sci. 32: 100824.), although this is not always the case for all the species (Thibaut et al. 2014Thibaut T., Blanfuné A., Markovic L., et al. 2014. Unexpected abundance and long-term relative stability of the brown alga Cystoseira amentacea, hitherto regarded as a threatened species, in the north-western Mediterranean Sea. Mar. Pollut. Bull. 89: 305-323., Blanfuné et al. 2019Blanfuné A., Boudouresque C.F., Verlaque M., et al. 2019. The ups and downs of a canopy-forming seaweed over a span of more than one century. Sci. Rep. 9: 5250.) or all places (Sales and Ballesteros 2010Sales M., Ballesteros E. 2010. Long-term comparison of algal assemblages dominated by Cystoseira crinita (Fucales, Heterokontophyta) from Cap Corse (Corsica, North Western Mediterranean). Eur. J. Phycol. 45: 404-412., Thibaut et al. 2016Thibaut T., Blanfuné A., Boudouresque C.F., et al. 2016. Unexpected temporal stability of Cystoseira and Sargassum forests in Port-Cros, one of the oldest Mediterranean marine National Parks. Crypt. Algol. 37: 61-91., Blanfuné et al. 2016Blanfuné A., Boudouresque C.F., Verlaque M., et al. 2016. The fate of Cystoseira crinita, a forest-forming Fucale (Phaeophyceae, Stramenopiles), in France (North Western Mediterranean Sea). Estu. Coast. Shelf. Sci. 181: 196-208.). Pollution is the main threat affecting the survival of Cystoseira s.l. populations (Munda 1974Munda M. 1974. Changes and succession in the benthic algal associations of slightly polluted habitats. Rev. Int. Oceanogr. Med. 34: 37-52., Arévalo et al. 2007Arévalo R., Pinedo S., Ballesteros E. 2007. Changes in the composition and structure of Mediterranean rocky-shore commnities following a gradient of nutrient enrichment: descriptive study and test of proposed methods to assess water quality regarding macroalgae. Mar. Pollut. Bull. 55: 104-113., Sales et al. 2011Sales M., Cebrian E., Tomas F., et al. 2011. Pollution impacts and recovery potential in three species of the genus Cystoseira (Fucales, Heterokontophyta). Estuar. Coast. Shelf. Sci. 92: 347-357.), although other pressures such as climate change, habitat destruction, overgrazing by sea urchins, outcompetition by mussels, increased turbidity, sediment loads, net fishing, human trampling and even scientific sampling have been blamed for declines of Cystoseira s.l. (Cormaci and Furnari 1999Cormaci M., Furnari G. 1999. Changes of the benthic algal flora of the Tremiti Islands (southern Adriatic) Italy. Hydrobiologia 398-399: 75-79., Thibaut et al. 2005Thibaut T., Pinedo S., Torras X., et al. 2005. Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France, North-western Mediterranean). Mar. Pollut. Bull. 50: 1472-1489., Gianni et al. 2013Gianni F., Bartolini F., Airoldi L., et al. 2013. Conservation and restoration of marine forests in the Mediterranean Sea and the potential role of Marine Protected Areas. Adv. Oceanogr. Limnol. 4: 83-101.). As a result, in many places algal communities have shifted from complex and productive forests of Cystoseira s.l. to simpler and less-productive habitats such as barren grounds, encrusting corallines and turf algae beds or low-complexity erect algae stands (Sala et al. 1998Sala E., Boudouresque C.F., Harmelin-Vivien M. 1998. Fishing, trophic cascades, and the structure of algal assemblages: evaluation of an old but untested paradigm. Oikos 82: 425-439., Boudouresque 2004Boudouresque C.F. 2004. Marine biodiversity in the Mediterranean: status of species, populations and communities. Trav. Sci. Parc Nat. Port-Cros 20: 97-146., Thibaut et al. 2005Thibaut T., Pinedo S., Torras X., et al. 2005. Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France, North-western Mediterranean). Mar. Pollut. Bull. 50: 1472-1489.).

Due to the observed patterns of decline in several Mediterranean areas, the multiple pressures affecting populations of Cystoseira s.l. and their role as habitat formers, all the species (with the exception of Cystoseira compressa) have been included in the List of Endangered and Threatened Species of the Barcelona Convention (UNEP-MAP-RAC/SPA 2013UNEP-MAP-RAC/SPA. 2013. Protocol concerning specially protected areas and biological diversity in the Mediterranean. Annex II. List of endangered or threatened species. 7 pp.), and some of them are listed in the Bern Convention (1979: Appendix I). Understanding the ecological interactions of their populations with other key community components is therefore extremely important to guide management towards the conservation of these species and the maintenance of their ecosystem functions.

Here we report on the discovery of a new Mediterranean habitat co-dominated by C. caespitosa and several species of Cystoseira s.l., mainly Treptacantha ballesterosii. In particular, we aim at (1) describing C. caespitosa cover and colony size, (2) describing Cystoseira s.l. densities and sizes (when possible) and (3) inferring the relationship between macroalgal abundance (mainly T. ballesterosii density) and coral cover. The description of this new habitat will warn other scientists to look for this kind of formations in other Mediterranean localities and will serve as a baseline for the future monitoring of this newly discovered habitat and its highly threatened species and their relationships.

MATERIALS AND METHODSTop

Study site

Exploratory dives and sampling were performed in November 2017 and July 2019 in Es Banc (38.726564°N, 1.391309°E), located in the western part of Formentera (Balearic Islands, W Mediterranean Sea), close to Punta Gavina. The sampling site is included in the Freus d’Eivissa i Formentera marine protected area, where artisanal fishing is allowed. The area where both C. caespitosa and Cystoseira s.l. species coexist in large densities extends around 1150 m2 (Fig. 1).

figure

Full size image

Fig. 1. – A, Western Mediterranean. Scale bar: 500 km. B, arrow indicates the sampling site, Es Banc, located on the northwestern side of Formentera island. Scale bar: 3 km. C, surveyed area of 1150 m2 displayed as a white frame (source: Google Earth).

Sampling methods

Cladocora caespitosa cover in the sampling location was measured using a line-intercept method on a transect line (5 transects of 50 m length) (English et al. 1997English S., Wilkinson C., Baker V. (eds). 1997. Survey manual for tropical marine resources. Australian Institute of Marine Science, Townsville, Australia, 390 pp., Kersting et al. 2017)Kersting D.K., Cebrian E., Verdura J., et al. 2017. A new Cladocora caespitosa population with unique ecological traits. Medit. Mar. Sci. 18: 38-42.. The relationships between C. caespitosa abundance and Cystoseira s.l. densities were estimated using 625 cm2 quadrat frames divided into 25 (5×5 cm) subquadrats. The abundance of C. caespitosa was quantified as the number of subquadrats where C. caespitosa was present (Sala and Ballesteros 1997Sala E., Ballesteros E. 1997. Partitioning of space and food resources by three fishes of the genus Diplodus (Sparidae) in a Mediterranean rocky infralittoral ecosystem. Mar. Ecol. Prog. Ser. 152: 273-283., Sant et al. 2017Sant N., Chappuis E., Rodríguez-Prieto C., et al. 2017. Cost-benefit of three different methods for studying Mediterranean rocky benthic assemblages. Sci. Mar. 81: 129-138., Teixidó et al. 2018Teixidó N., Gambi M.C., Parravacini V., et al. 2018. Functional biodiversity loss along natural CO2 gradients. Nat. Comm. 9: 5149.). In the same quadrats, Cystoseira s.l. individuals were identified visually at the species level and counted. The size of each individual belonging to Treptacantha ballesterosii and Treptacantha cf. elegans was measured as the length of the primary axis using a ruler (Ballesteros et al. 1998Ballesteros E., Sala E., Garrabou J., et al. 1998. Community structure and frond size distribution of a deep water stand of Cystoseira spinosa (Phaeophyta) in the Northwestern Mediterranean. Eur. J. Phycol. 33: 121-128., 2009Ballesteros E., Garrabou J., Hereu B., et al. 2009. Deep-water stands of Cystoseira zosteroides C. Agardh (Fucales, Ochrophyta) in the Northwestern Mediterranean: Insights into assemblage structure and population dynamics. Estuar. Coast. Shelf. Sci. 82: 477-484.). Carpodesmia brachycarpa and Cystoseira compressa do not have a primary axis since they are caespitose, i.e. have several primary axes arising from a single basal disc (Giaccone and Bruni 1973Giaccone G., Bruni A. 1973. Le Cistoseire e la vegetazione sommersa del Mediterraneo. Atti Ist. Veneto Sci. Lett. Arti 131: 59-103., Cormaci et al. 2012Cormaci M., Furnari G., Catra M., et al. 2012. Flora marina bentonica del Mediterraneo: Phaeophyceae. Accad. Gioenia Boll. 45: 1-508.), and therefore size was not estimated.

Data analysis

Size of each coral colony was obtained as the length in cm of the transect line occupied by each colony (Kersting et al. 2017Kersting D.K., Cebrian E., Verdura J., et al. 2017. A new Cladocora caespitosa population with unique ecological traits. Medit. Mar. Sci. 18: 38-42.). Kolmogorov-Smirnov tests were performed to test normality of the size class frequency distributions of C. caespitosa and Cystoseira s.l. within populations. For raw data series, descriptive statistics were calculated: minimum, maximum, mean values, standard deviation and skewness according to Sokal and Rohlf (1995)Sokal R.R., Rohlf F.J. 1995. Biometry: the principles and practice of statistics in biological research. W.H. Freeman and Co., New York, USA, 887 pp.. Linear regression analyses were used to determine how Cystoseira s.l. densities varied with C. caespitosa abundance, using 0.05 as the significance level. Statistical analyses were performed using Systat 11.0 (SPSS Inc. 2004).

RESULTSTop

Cladocora caespitosa colonies thrive at the study site between 8 and 12 m depth on a continuous rocky platform, sheltered from the prevailing winds (mainly east) (Fig. 2). The coral colonies concentrate in the area, forming a wide bed. C. caespitosa covers on average 33.7±16.0 % (±SD, n=5) of the substrate and reaches values of up to 40% of cover. The size class frequency distribution of this population is unimodal but does not follow a normal distribution (K-S, d=0.77, p<0.0001) (Fig. 3). The skewness of the distribution is significantly positive (g1=1.841), which indicates the predominance of small classes in the population. The mean colony size is 15.7±15.4 cm (±SD, n=546), ranging from 2 to over 100 cm, with a maximum size of 146 cm.

figure2

Full size image

Fig. 2. – Views (November 2017, above; July 2019, below) of the habitat dominated by Cladocora caespitosa and Treptacantha ballesterosii. Note that most of the algal thalli are settled on coral colonies.

figure3

Full size image

Fig. 3. – Size class structure of Cladocora caespitosa colonies starting at the class interval of 5 cm (colonies measuring 1-5 cm) (n=546).

Treptacantha ballesterosii individuals are interspersed among and on the coral colonies, making a special seascape dominated by both coral colonies and macroalgae (Fig. 2). T. ballesterosii stands for 90% of the individuals belonging to Cystoseira s.l., while specimens identified as T. cf. elegans, C. brachycarpa and C. compressa show a much lower abundance (Fig. 4). The mean density of T. ballesterosii is 206 individuals m–2. The main axes of T. ballesterosii support a considerable epiphytic load mainly composed of turf-forming algae like Haliptilon virgatum (Fig. 2).

figure4

Full size image

Fig. 4. – Density-frequency distributions of Cystoseira s.l. species (n=2885).

The size class frequency distribution of T. ballesterosii is unimodal but non-normal (K-S, d=0.5, p<0.0001), with a prevalence of small individuals (g1=1.376) (Fig. 5). The mean length of the main axis is 4.7±3.8 cm (±SD, n=2603), with a maximum length of 26 cm obtained for three individuals, and 90% of the population ranging between 0.5 and 9 cm. The T. cf. elegans population shows two peaks at 2 and 7 cm and does not follow a normal distribution either (K-S, d=0.84, p<0.0001) (Fig. 6). The mean length of the main axis is 5.3±3.1 cm (±SD, n=92), with a maximum length of 14 cm.

figure5

Full size image

Fig. 5. – Size frequency distribution of Treptacantha ballesterosii starting at the class interval of 1 cm (main axes measuring 0.1-1 cm) (n=2603).

figure6

Full size image

Fig. 6. – Size frequency distribution of Treptacantha cf. elegans starting at the class interval of 1 cm (main axes measuring 0.1-1 cm) (n=92).

Treptacantha ballesterosii, the most abundant macroalga, shows a slight but very significant positive relationship with C. caespitosa abundance (p=0.0005, n=202) (Fig. 7A). No significant relationship was found between T. cf. elegans densities and C. caespitosa abundance (p=0.64, n=52) (Fig. 7B). In contrast, densities of C. brachycarpa decline when C. caespitosa abundance increases (p=0.02, n=65) (Fig. 7C).

figure7

Full size image

Fig. 7. – Relationship between the densities of the different species of Cystoseira s.l. and Cladocora caespitosa abundance: Treptacantha ballesterosii (A), Treptacantha cf. elegans (B) and Carpodesmia brachycarpa (C).

DISCUSSIONTop

We have identified and characterized a new Mediterranean habitat constituted by a mixture of C. caespitosa colonies and T. ballesterosii stands. This kind of habitat is not reported in the EUNIS (Moss 2008Moss D. 2008. EUNIS habitat classification - a guide for users. European Topic Center on Biological Diversity.) or RAC/SPA (UNEP-MAP-RAC/SPA 2006UNEP-MAP-RAC/SPA. 2006. Classification of benthic marine habitat types for the Mediterranean region. 15 pp.) habitat classification lists or in the Spanish List of Marine Habitats (Templado et al. 2012Templado J., Ballesteros E., et al. 2012. Guía interpretativa. Inventario español de hábitats marinos. Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, 229 pp.). Both the EUNIS and RAC/SPA lists only consider a “facies with Cladocora caespitosa” (III.6.1.14) and up to 12 associations with Cystoseira s.l. Furthermore, the Spanish List of Marine Habitats only lists two habitats harbouring C. caespitosa (i.e. 0301041408 “Infralittoral rock, moderately illuminated, without Fucales with C. caespitosa”, and 0301041607 “Infralittoral rock with low hydrodynamism, poorly lit dominated by invertebrates with Cladocora caespitosa”) and 19 habitats with Cystoseira s.l. We therefore suggest a new habitat type to be included in the Spanish List of Marine Habitats named “Infralittoral rock with low hydrodynamism, moderately lit, with Cladocora caespitosa and Treptacantha ballesterosii” and numbered 03010503.

The coexistence of C. caespitosa and Cystoseira s.l. has been previously reported at several Mediterranean sites: the Columbretes Islands (Kersting and Linares 2012Kersting D.K., Linares C. 2012. Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar. Ecol. 33: 427-436.) and the Balearic Islands (Kersting et al. 2017Kersting D.K., Cebrian E., Verdura J., et al. 2017. A new Cladocora caespitosa population with unique ecological traits. Medit. Mar. Sci. 18: 38-42., Ballesteros and Pons-Fita 2020Ballesteros E., Pons-Fita A. 2020. Corals and macroalgae can sometimes coexist. Frontiers Ecol. Environm. 18: 150.) in the western Mediterranean and Cyprus in the eastern Mediterranean Sea (Jiménez et al. 2016Jiménez C., Hadjioannou L., Petrou A., et al. 2016. Mortality of the scleractinain coral Cladocora caespitosa during a warming event in the Levantine Sea (Cyprus). Region. Environm. Change 16: 1963-1973.). However, none of these studies described the seaweed assemblages in terms of densities and stand size.

The population and individual sizes estimated in this study are very noteworthy for both the coral and the macroalgae. We have estimated a total area of C. caespitosa of 387.5 m2, which is rather outstanding considering the 650 m2 reported from Veliko Jezero lake (Mljet National Park, Adriatic Sea), which hosts the most compact reef of C. caespitosa known to date (Kružić and Požar-Domac 2003Kružić P., Požar-Domac A. 2003. Banks of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic Sea. Coral Reefs 22: 536.), and the 2900 m2 covered by this coral in the Columbretes Islands (NW Mediterranean Sea), the most extensive C. caespitosa–covered area known in the Mediterranean Sea (Kersting and Linares 2012Kersting D.K., Linares C. 2012. Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar. Ecol. 33: 427-436.). The mean coral cover of 33.7% obtained in Es Banc, although lower than that found in Veliko Jezero lake, is slightly higher than the 31% found in the Bay of Piran (Schiller 1993Schiller C. 1993. Ecology of the symbiotic coral Cladocora caespitosa (L.) (Faviidae, Scleractinia) in the Bay of Piran (Adriatic Sea): I. Distribution and biometry. Mar. Ecol. 14: 205-219.) and much higher than the 20% from Espardelló islet (Kersting et al. 2017Kersting D.K., Cebrian E., Verdura J., et al. 2017. A new Cladocora caespitosa population with unique ecological traits. Medit. Mar. Sci. 18: 38-42.) and the 7% found in the Columbretes Islands (Kersting and Linares 2012Kersting D.K., Linares C. 2012. Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar. Ecol. 33: 427-436.).

Mean colony size is also higher than at other sites reported, such as the Bay of Piran, La Spezia and Espardelló islet (Schiller 1993Schiller C. 1993. Ecology of the symbiotic coral Cladocora caespitosa (L.) (Faviidae, Scleractinia) in the Bay of Piran (Adriatic Sea): I. Distribution and biometry. Mar. Ecol. 14: 205-219., Peirano et al. 2001Peirano A., Morri C., Bianchi C.N., et al. 2001. Biomass, carbonate standing stock and production of the mediterranean coral Cladocora caespitosa (L.). Facies 44: 75-80., Kersting et al. 2017Kersting D.K., Cebrian E., Verdura J., et al. 2017. A new Cladocora caespitosa population with unique ecological traits. Medit. Mar. Sci. 18: 38-42.). Es Banc holds some very large colonies (>100 cm), similar to Columbretes (Kersting and Linares 2012Kersting D.K., Linares C. 2012. Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar. Ecol. 33: 427-436.), but these are present in reduced numbers. However, Columbretes has twice the mean colony size of Es Banc (31.48 cm average diameter) (Kersting and Linares 2012Kersting D.K., Linares C. 2012. Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar. Ecol. 33: 427-436.), which may be related to depth and sea-floor morphology, since water motion and other disturbances related to exceptional storms are minimized with depth and hydrodynamic shelter (Schiller 1993Schiller C. 1993. Ecology of the symbiotic coral Cladocora caespitosa (L.) (Faviidae, Scleractinia) in the Bay of Piran (Adriatic Sea): I. Distribution and biometry. Mar. Ecol. 14: 205-219., Kersting and Linares 2012Kersting D.K., Linares C. 2012. Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar. Ecol. 33: 427-436.). In fact, Es Banc and Columbretes show different types of spatial coral colony development. In Columbretes, coral colonies are large, but their distribution is patchy and highly associated with sea-floor morphology, with large areas almost devoid, or with a very low density, of colonies (Kersting and Linares 2012Kersting D.K., Linares C. 2012. Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar. Ecol. 33: 427-436.). In contrast, coral colonies in Es Banc form a wide irregular carpet that covers the rocky bottom. This encrusting ecotype, which has been attributed mainly to mechanical stress from waves and currents (Riedl 1964Riedl R. 1964. Die Erscheinungen der Wasserbewegung und ihre Wirkung auf Sedentarier im mediterranen Felslitoral. Helgol. Wiss. Meeresunters. 10: 155-186.), is also present in other localities in concurrence with macroalgae (e.g. Espardelló [Kersting et al. 2017Kersting D.K., Cebrian E., Verdura J., et al. 2017. A new Cladocora caespitosa population with unique ecological traits. Medit. Mar. Sci. 18: 38-42.], Vulcano [O. Ocaña, pers. comm.]). Other large colonies forming reef-like structures are reported from Veliko Jezero lake (Mjlet, Croatia) (Kružić and Požar-Domac 2002Kružić P., Požar-Domac A. 2002. Skeleton growth rates of coral bank of Cladocora caespitosa (Anthozoa, Scleractinia) in lake Veliko jezero (Mljet National Park). Period. Biol. 104: 123-129., 2003Kružić P., Požar-Domac A. 2003. Banks of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic Sea. Coral Reefs 22: 536.), but the conditions of this site are extremely sheltered and not comparable to those of other localities located in open sea areas. Large C. caespitosa colonies are almost absent in Piran and La Spezia (Schiller 1993Schiller C. 1993. Ecology of the symbiotic coral Cladocora caespitosa (L.) (Faviidae, Scleractinia) in the Bay of Piran (Adriatic Sea): I. Distribution and biometry. Mar. Ecol. 14: 205-219., Peirano et al. 1998Peirano A., Morri C., Mastronuzzi G., et al. 1998. The coral Cladocora caespitosa (Anthozoa, Scleractinia) as a bioherm builder in the Mediterranean Sea. Mem. descritt. Carta Geol. Italia 52: 59-74., 2001Peirano A., Morri C., Bianchi C.N., et al. 2001. Biomass, carbonate standing stock and production of the mediterranean coral Cladocora caespitosa (L.). Facies 44: 75-80.). Small colonies (<10 cm) are very abundant, in agreement with other localities (Rodolfo-Metalpa et al. 2005Rodolfo-Metalpa R., Bianchi C.N., Peirano A., et al. 2005. Tissue necrosis and mortality of the temperate coral Cladocora caespitosa. Ital. J. Zool. 72: 271-276., Kersting and Linares 2012Kersting D.K., Linares C. 2012. Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar. Ecol. 33: 427-436., Kersting et al. 2017Kersting D.K., Cebrian E., Verdura J., et al. 2017. A new Cladocora caespitosa population with unique ecological traits. Medit. Mar. Sci. 18: 38-42.).

The population of T. ballesterosii from Es Banc is also outstanding. Mean density reaches 206 individuals m–2, which is very high when compared with densities reported from Scandola Marine Reserve (Parc Naturel Régional de Corse, France), where T. ballesterosii var. compressa (as Cystoseira spinosa var. compressa) shows densities of 28 individuals m–2 at 26-29 m depth, decreasing to 3 individuals m–2 between 38 and 50 m depth (Ballesteros et al. 1998Ballesteros E., Sala E., Garrabou J., et al. 1998. Community structure and frond size distribution of a deep water stand of Cystoseira spinosa (Phaeophyta) in the Northwestern Mediterranean. Eur. J. Phycol. 33: 121-128., 2009Ballesteros E., Garrabou J., Hereu B., et al. 2009. Deep-water stands of Cystoseira zosteroides C. Agardh (Fucales, Ochrophyta) in the Northwestern Mediterranean: Insights into assemblage structure and population dynamics. Estuar. Coast. Shelf. Sci. 82: 477-484.). Hereu et al. (2009)Hereu B., Mangialajo L., Ballesteros E., et al. 2009. On the occurrence, structure and distribution of deep-water Cystoseira (Phaeophyceae) populations in the Port-Cros National Park (north-western Mediterranean). Eur. J. Phycol. 43: 263-273. found T. ballesterosii v. compressa densities ranging from 0 to 7 individuals m–2 between 35 and 47 m depth in Port-Cros National Park (France). However, thallus length of T. ballesterosii is much lower in Es Banc than in Scandola and Port-Cros deep waters, where mean lengths of 7 to 16 cm have been reported (Ballesteros et al. 1998Ballesteros E., Sala E., Garrabou J., et al. 1998. Community structure and frond size distribution of a deep water stand of Cystoseira spinosa (Phaeophyta) in the Northwestern Mediterranean. Eur. J. Phycol. 33: 121-128., Hereu et al. 2009Hereu B., Mangialajo L., Ballesteros E., et al. 2009. On the occurrence, structure and distribution of deep-water Cystoseira (Phaeophyceae) populations in the Port-Cros National Park (north-western Mediterranean). Eur. J. Phycol. 43: 263-273.). The shape of the size class distribution of T. ballesterosii population in Es Banc is close to a negative exponential function, which has been associated with populations at equilibrium (Lorimer 1985Lorimer C.G. 1985. Methodological considerations in the analysis of forest disturbance history. Can. J. For. Res. 15: 200-213., Edmonds et al. 1993Edmonds R.L., Thomas T.B., Maybury K.P. 1993. Tree populations dynamics, growth, and mortality in old-growth forests in the Western Olympic Mountains, Washington. Can. J. For. Res. 23: 512-519., Berg and Hemrick 1994Berg E.E., Hemrick J.L. 1994. Spatial and genetic structure of two sandhill oaks: Quercus laevis and Quercus margaretta (Fagaceae). Am. J. Bot. 81: 7-14.), where small size individuals are very abundant and the abundances progressively decline at increasing sizes. In contrast, Ballesteros et al. (1998)Ballesteros E., Sala E., Garrabou J., et al. 1998. Community structure and frond size distribution of a deep water stand of Cystoseira spinosa (Phaeophyta) in the Northwestern Mediterranean. Eur. J. Phycol. 33: 121-128. and Hereu et al. (2009)Hereu B., Mangialajo L., Ballesteros E., et al. 2009. On the occurrence, structure and distribution of deep-water Cystoseira (Phaeophyceae) populations in the Port-Cros National Park (north-western Mediterranean). Eur. J. Phycol. 43: 263-273. found log-normal distributions of size classes of T. ballesterosii v. compressa in Scandola and Port-Cros. Other deep-water Cystoseira s.l. populations (Carpodesmia zosteroides, Treptacantha funkii) also follow log-normal distributions (Hereu et al. 2009Hereu B., Mangialajo L., Ballesteros E., et al. 2009. On the occurrence, structure and distribution of deep-water Cystoseira (Phaeophyceae) populations in the Port-Cros National Park (north-western Mediterranean). Eur. J. Phycol. 43: 263-273., Ballesteros et al. 2009Ballesteros E., Garrabou J., Hereu B., et al. 2009. Deep-water stands of Cystoseira zosteroides C. Agardh (Fucales, Ochrophyta) in the Northwestern Mediterranean: Insights into assemblage structure and population dynamics. Estuar. Coast. Shelf. Sci. 82: 477-484., Navarro et al. 2011Navarro L., Ballesteros E., Linares C., et al. 2011. Spatial and temporal variability of deep-water algal assemblages in the Northwestern Mediterranean: The effects of an exceptional storm. Estuar. Coast. Shelf. Sci. 95: 52-58.), which must be related either to unpredictable episodes of recruitment or to the dense canopy of large individuals that must inhibit the recruitment of new individuals.

In Es Banc, the shape distribution of size classes in T. cf. elegans population showing two peaks might indicate uneven recruitment events depending on the year, as has already been reported in other Cystoseira s.l. populations (e.g. Ballesteros et al. 1998Ballesteros E., Sala E., Garrabou J., et al. 1998. Community structure and frond size distribution of a deep water stand of Cystoseira spinosa (Phaeophyta) in the Northwestern Mediterranean. Eur. J. Phycol. 33: 121-128., 2009Ballesteros E., Garrabou J., Hereu B., et al. 2009. Deep-water stands of Cystoseira zosteroides C. Agardh (Fucales, Ochrophyta) in the Northwestern Mediterranean: Insights into assemblage structure and population dynamics. Estuar. Coast. Shelf. Sci. 82: 477-484., Hereu et al. 2009Hereu B., Mangialajo L., Ballesteros E., et al. 2009. On the occurrence, structure and distribution of deep-water Cystoseira (Phaeophyceae) populations in the Port-Cros National Park (north-western Mediterranean). Eur. J. Phycol. 43: 263-273.) and other fucoids (e.g. Deysher and Norton 1982Deysher L., Norton T.A. 1982. Dispersal and colonization in Sargassum muticum (Yendo) Fensholt. J. Exp. Mar. Biol. Ecol. 56: 179-195., Dayton et al. 1984Dayton P.K., Currie V., Gerrodette T., et al. 1984. Patch dynamics and stability of some California kelp communities. Ecol. Monogr. 54: 253-289., Fernández et al. 1990Fernández C., Gutiérrez L.M., Rico J.M. 1990. Ecology of Sargassum muticum on the north coast of Spain. Preliminary observations. Bot. Mar. 33: 423-428.).

Another result of this study is the discovery of a positive relationship between C. caespitosa cover and the density of T. ballesterosii, which challenges the predicted competition for space between corals and macroalgae (McCook et al. 2001McCook L., Jompa J., Diaz-Pulido G. 2001. Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19: 400-417.). This contrasts with reports of growth limitation of C. caespitosa by soft algae (Peirano et al. 1998Peirano A., Morri C., Mastronuzzi G., et al. 1998. The coral Cladocora caespitosa (Anthozoa, Scleractinia) as a bioherm builder in the Mediterranean Sea. Mem. descritt. Carta Geol. Italia 52: 59-74.) or the competition between C. caespitosa and macroalgae (Codium) found in other localities (Kružić and Benković 2008Kružić P., Benković L. 2008. Bioconstructional features of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic Sea (Croatia). Mar. Ecol. 29: 125-139.). In fact, the positive interaction between C. caespitosa and T. ballesterosii points to a possible facilitation mechanism. We suggest the hypothesis that the recruitment or survival of T. ballesterosii might be enhanced by the presence of C. caespitosa, but colonies do not seem to be affected by the presence of algal thalli. Treptacantha cf. elegans shows a neutral relationship while the relationship with C. brachycarpa is negative, probably due to the caespitose habit of this species, which cannot progress inside a coral colony. These results launch a wide array of possible open discussions on coral-macroalgae interactions.

In conclusion, here we report on a new habitat type for the Mediterranean Sea, which is co-dominated by an endemic colonial coral and an endemic canopy-forming alga. Both the coral and the macroalga show large cover and abundance, challenging the theory of competitive exclusion between these two functional groups (photosyntethic organisms versus photo-suspension feeders) in the marine benthos. Moreover, the fact that this habitat is dominated by species of high vulnerability and included in red lists and international conventions merits a special monitoring project and proper management actions in order to ensure its persistence over the years.

ACKNOWLEDGEMENTSTop

We are grateful to the managers of the Freus d’Eivissa i Formentera Marine Reserve for diving permissions and research authorization and to Bàrbara Terrasa and the managers and rangers of the Ses Salines Natural Park for lodging facilities. The authors also acknowledge the help provided by Javi Asensio in parking and transportation issues and the technical support provided by the Vell Marí Diving Centre. Information provided by one of the referees (Dr Óscar Ocaña) is also acknowledged.

REFERENCESTop

Arévalo R., Pinedo S., Ballesteros E. 2007. Changes in the composition and structure of Mediterranean rocky-shore commnities following a gradient of nutrient enrichment: descriptive study and test of proposed methods to assess water quality regarding macroalgae. Mar. Pollut. Bull. 55: 104-113.
https://doi.org/10.1016/j.marpolbul.2006.08.023

Ballesteros E. 1988. Estructura y dinámica de la comunidad de Cystoseira mediterranea Sauvageau en el Mediterráneo Noroccidental. Inv. Pesq. 52: 313-334.

Ballesteros E. 1990a. Structure and dynamics of the community of Cystoseira zosteroides (Turner) C. Agardh (Fucales, Phaeophyceae) in the north-western Mediterranean. Sci. Mar. 54: 217-229.

Ballesteros E. 1990b. Structure and dynamics of the Cystoseira caespitosa Sauvageau (Fucales, Phaeophyceae) community in the North-Western Mediterranean. Sci. Mar. 54: 155-168.

Ballesteros E., Pons-Fita A. 2020. Corals and macroalgae can sometimes coexist. Frontiers Ecol. Environm. 18: 150.
https://doi.org/10.1002/fee.2183

Ballesteros E., Sala E., Garrabou J., et al. 1998. Community structure and frond size distribution of a deep water stand of Cystoseira spinosa (Phaeophyta) in the Northwestern Mediterranean. Eur. J. Phycol. 33: 121-128.
https://doi.org/10.1080/09670269810001736613

Ballesteros E., Garrabou J., Hereu B., et al. 2009. Deep-water stands of Cystoseira zosteroides C. Agardh (Fucales, Ochrophyta) in the Northwestern Mediterranean: Insights into assemblage structure and population dynamics. Estuar. Coast. Shelf. Sci. 82: 477-484.
https://doi.org/10.1016/j.ecss.2009.02.013

Berg E.E., Hemrick J.L. 1994. Spatial and genetic structure of two sandhill oaks: Quercus laevis and Quercus margaretta (Fagaceae). Am. J. Bot. 81: 7-14.
https://doi.org/10.1002/j.1537-2197.1994.tb15402.x

Bianchi C.N., Corsini-Foka M., Morri C., et al. 2014. Thirty years after-dramatic change in the coastal marine habitats of Kos Island (Greece), 1981-2013. Medit. Mar. Sci. 15: 482-497.
https://doi.org/10.12681/mms.678

Blanfuné A., Boudouresque C.F., Verlaque M., et al. 2016. The fate of Cystoseira crinita, a forest-forming Fucale (Phaeophyceae, Stramenopiles), in France (North Western Mediterranean Sea). Estu. Coast. Shelf. Sci. 181: 196-208.
https://doi.org/10.1016/j.ecss.2016.08.049

Blanfuné A., Boudouresque C.F., Verlaque M., et al. 2019. The ups and downs of a canopy-forming seaweed over a span of more than one century. Sci. Rep. 9: 5250.
https://doi.org/10.1038/s41598-019-41676-2

Boudouresque C.F. 1971. Recherches de bionomie analytique, structurale et expérimentale sur les peuplements benthiques sciaphiles de Méditerranée occidentale (fraction algale): la sous-strate sciaphile des peuplements des grandes Cystoseira de mode battu. Bull. Mus. Natl. Hist. Nat. Marseille 31: 79-104.

Boudouresque C.F. 1972. Recherches de bionomie analytique, structurale et expérimentale sur les peuplements benthiques sciaphiles de Méditerranée Occidentale (fraction algale): le sous-strate sciaphile d’un peuplement photophile de mode calme, le peuplement à Cystoseira crinita. Bull. Mus. Nat. Hist. Nat. Marseille 32: 253-263.

Boudouresque C.F. 2004. Marine biodiversity in the Mediterranean: status of species, populations and communities. Trav. Sci. Parc Nat. Port-Cros 20: 97-146.

Bruno de Sousa C., Cox C.J., Brito L., et al. 2019. Improved phylogeny of brown algae Cystoseira (Fucales) from the Atlantic-Mediterranean region based on mitochondrial sequences. PLoS ONE 14: e0210143.
https://doi.org/10.1371/journal.pone.0210143

Casado-Amezúa P., Kersting D.K., Linares C., et al. 2015. Cladocora caespitosa. The IUCN Red List of Threatened Species 2015: e.T133142A75872554
https://doi.org/10.2305/IUCN.UK.2015-2.RLTS.T133142A75872554.en

Cheminée A., Sala E., Pastor J., et al. 2013. Nursery value of Cystoseira forests for Mediterranean rocky reef fishes. J. Exp. Mar. Biol. Ecol. 442: 70-79.
https://doi.org/10.1016/j.jembe.2013.02.003

Cheminée A., Pastor J., Bianchimani O., et al. 2017. Juvenile fish asemblages in temperate rocky reefs are shaped by the presence of macroalgae canopy and its three dimensional structure. Sci. Rep. 7: 14638.
https://doi.org/10.1038/s41598-017-15291-y

Cormaci M., Furnari G. 1999. Changes of the benthic algal flora of the Tremiti Islands (southern Adriatic) Italy. Hydrobiologia 398-399: 75-79.
https://doi.org/10.1023/A:1017052332207

Cormaci M., Furnari G., Catra M., et al. 2012. Flora marina bentonica del Mediterraneo: Phaeophyceae. Accad. Gioenia Boll. 45: 1-508.

Dayton P.K., Currie V., Gerrodette T., et al. 1984. Patch dynamics and stability of some California kelp communities. Ecol. Monogr. 54: 253-289.
https://doi.org/10.2307/1942498

Deysher L., Norton T.A. 1982. Dispersal and colonization in Sargassum muticum (Yendo) Fensholt. J. Exp. Mar. Biol. Ecol. 56: 179-195.
https://doi.org/10.1016/0022-0981(81)90188-X

Draisma S.G., Ballesteros E., Rousseau F., et al. 2010. DNA sequence data demonstrate the polyphyly of the genus Cystoseira and other Sargassaceae genera (Phaeophyceae). J. Phycol. 46: 1329-1345.
https://doi.org/10.1111/j.1529-8817.2010.00891.x

Edmonds R.L., Thomas T.B., Maybury K.P. 1993. Tree populations dynamics, growth, and mortality in old-growth forests in the Western Olympic Mountains, Washington. Can. J. For. Res. 23: 512-519.
https://doi.org/10.1139/x93-069

El Kateb A., Stalder C., Neururer C., et al. 2016. Correlation between pollution and decline of Scleractinian Cladocora caespitosa (Linnaeus, 1758) in the Gulf of Gabes. Heliyon 2: e00195.
https://doi.org/10.1016/j.heliyon.2016.e00195

English S., Wilkinson C., Baker V. (eds). 1997. Survey manual for tropical marine resources. Australian Institute of Marine Science, Townsville, Australia, 390 pp.

Fernández C., Gutiérrez L.M., Rico J.M. 1990. Ecology of Sargassum muticum on the north coast of Spain. Preliminary observations. Bot. Mar. 33: 423-428.
https://doi.org/10.1515/botm.1990.33.5.423

Giaccone G., Bruni A. 1973. Le Cistoseire e la vegetazione sommersa del Mediterraneo. Atti Ist. Veneto Sci. Lett. Arti 131: 59-103.

Gianni F., Bartolini F., Airoldi L., et al. 2013. Conservation and restoration of marine forests in the Mediterranean Sea and the potential role of Marine Protected Areas. Adv. Oceanogr. Limnol. 4: 83-101.
https://doi.org/10.1080/19475721.2013.845604

Hereu B., Mangialajo L., Ballesteros E., et al. 2009. On the occurrence, structure and distribution of deep-water Cystoseira (Phaeophyceae) populations in the Port-Cros National Park (north-western Mediterranean). Eur. J. Phycol. 43: 263-273.
https://doi.org/10.1080/09670260801930330

Jiménez C., Hadjioannou L., Petrou A., et al. 2016. Mortality of the scleractinain coral Cladocora caespitosa during a warming event in the Levantine Sea (Cyprus). Region. Environm. Change 16: 1963-1973.
https://doi.org/10.1007/s10113-014-0729-2

Kersting D.K., Linares C. 2012. Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar. Ecol. 33: 427-436.
https://doi.org/10.1111/j.1439-0485.2011.00508.x

Kersting D.K., Linares C. 2019. Living evidence of a fossil survival strategy raises hope for warming-affected corals. Sci. Adv. 5: eaax2950.
https://doi.org/10.1126/sciadv.aax2950

Kersting D.K., Bensoussan N., Linares C. 2013. Long-term responses of the endemic reef-builder Cladocora caespitosa to Mediterranean warming. PLoS ONE 8: e70820.
https://doi.org/10.1371/journal.pone.0070820

Kersting D.K., Teixidó N., Linares C. 2014a. Recruitment and mortality of the temperate coral Cladocora caespitosa: implications for the recovery of endangered populations. Coral Reefs 33: 403-407.
https://doi.org/10.1007/s00338-014-1144-3

Kersting D.K., Ballesteros E., De Caralt S., et al. 2014b. Invasive macrophytes in a marine reserve (Columbretes Islands, NW Mediterranean): spread dynamics and interactions with the endemic scleractinian coral Cladocora caespitosa. Biol. Inv. 16: 1599-1610.
https://doi.org/10.1007/s10530-013-0594-9

Kersting D.K., Ballesteros E., Bensoussan N., et al. 2014c. Long-term monitoring of Cladocora caespitosa reefs in the Columbretes Islands: From mapping to population dynamics and threats. In Bouafif C., Langar H., et al. (eds), Proceedings of the Second Mediterranean Symposium of coralligenous and other calcareous bioconcretions (Portoroz, Slovenia, 29-30 October 2014). RAC/SPA publ., Tunis. pp. 89-94.

Kersting D.K., Cebrian E., Casado C., et al. 2015. Experimental evidence of the synergistic effects of warming and invasive algae on a temperate reef-builder coral. Sci. Rep. 5: 18635.
https://doi.org/10.1038/srep18635

Kersting D.K., Cebrian E., Verdura J., et al. 2017. A new Cladocora caespitosa population with unique ecological traits. Medit. Mar. Sci. 18: 38-42.
https://doi.org/10.12681/mms.1955

Kružić P., Benković L. 2008. Bioconstructional features of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic Sea (Croatia). Mar. Ecol. 29: 125-139.
https://doi.org/10.1111/j.1439-0485.2008.00220.x

Kružić P., Požar-Domac A. 2002. Skeleton growth rates of coral bank of Cladocora caespitosa (Anthozoa, Scleractinia) in lake Veliko jezero (Mljet National Park). Period. Biol. 104: 123-129.

Kružić P., Požar-Domac A. 2003. Banks of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic Sea. Coral Reefs 22: 536.
https://doi.org/10.1007/s00338-003-0345-y

Kružić P., Požar-Domac A. 2007. Impact of tuna farming on the banks of the coral Cladocora caespitosa in the Adriatic Sea. Coral Reefs 26: 665.
https://doi.org/10.1007/s00338-007-0237-7

Lorimer C.G. 1985. Methodological considerations in the analysis of forest disturbance history. Can. J. For. Res. 15: 200-213.
https://doi.org/10.1139/x85-038

Mariani S., Cefalì M.E., Chappuis E., et al. 2019. Past and present of Fucales from shallow and sheltered shores in Catalonia. Reg. Stud. Mar. Sci. 32: 100824.
https://doi.org/10.1016/j.rsma.2019.100824

McCook L., Jompa J., Diaz-Pulido G. 2001. Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19: 400-417.
https://doi.org/10.1007/s003380000129

Morri C., Peirano A., Bianchi C.N., et al. 1994. Present day bioconstructions of the hard coral, Cladocora caespitosa (L.) (Anthozoa, Scleractinia), in the Eastern Ligurian Sea (NW Mediterranean). Biol. Mar. Medit. 1: 371-373.

Morri C., Peirano A., Bianchi C.N., et al. 2000. Cladocora caespitosa: A colonial zooxanthellate Mediterranean coral showing constructional ability. Reef Encounter 27: 22-25.

Moss D. 2008. EUNIS habitat classification - a guide for users. European Topic Center on Biological Diversity.
https://eionet.europa.eu/etcs/etc-bd/

Munda M. 1974. Changes and succession in the benthic algal associations of slightly polluted habitats. Rev. Int. Oceanogr. Med. 34: 37-52.

Navarro L., Ballesteros E., Linares C., et al. 2011. Spatial and temporal variability of deep-water algal assemblages in the Northwestern Mediterranean: The effects of an exceptional storm. Estuar. Coast. Shelf. Sci. 95: 52-58.
https://doi.org/10.1016/j.ecss.2011.08.002

Orellana S., Hernández M., Sansón M. 2019. Diversity of Cystoseira sensu lato (Fucales, Phaeophyceae) in the eastern Atlantic and Mediterranean based on morphological and DNA evidence, including Carpodesmia gen. emend. and Treptacantha gen. emend. Eur. J. Phycol. 54: 447-465.
https://doi.org/10.1080/09670262.2019.1590862

Peirano A., Morri C., Mastronuzzi G., et al. 1998. The coral Cladocora caespitosa (Anthozoa, Scleractinia) as a bioherm builder in the Mediterranean Sea. Mem. descritt. Carta Geol. Italia 52: 59-74.

Peirano A., Morri C., Bianchi C.N., et al. 2001. Biomass, carbonate standing stock and production of the mediterranean coral Cladocora caespitosa (L.). Facies 44: 75-80.
https://doi.org/10.1007/BF02668168

Riedl R. 1964. Die Erscheinungen der Wasserbewegung und ihre Wirkung auf Sedentarier im mediterranen Felslitoral. Helgol. Wiss. Meeresunters. 10: 155-186.
https://doi.org/10.1007/BF01626105

Rodolfo-Metalpa R., Bianchi C.N., Peirano A., et al. 2005. Tissue necrosis and mortality of the temperate coral Cladocora caespitosa. Ital. J. Zool. 72: 271-276.
https://doi.org/10.1080/11250000509356685

Rodríguez-Prieto C., Ballesteros E., Boisset F., et al. 2013. Guía de las macroalgas y fanerógamas marinas del Mediterráneo Occidental. Ediciones Omega, Barcelona, 656 pp.

Sala E., Ballesteros E. 1997. Partitioning of space and food resources by three fishes of the genus Diplodus (Sparidae) in a Mediterranean rocky infralittoral ecosystem. Mar. Ecol. Prog. Ser. 152: 273-283.
https://doi.org/10.3354/meps152273

Sala E., Boudouresque C.F., Harmelin-Vivien M. 1998. Fishing, trophic cascades, and the structure of algal assemblages: evaluation of an old but untested paradigm. Oikos 82: 425-439.
https://doi.org/10.2307/3546364

Sales M., Ballesteros E. 2010. Long-term comparison of algal assemblages dominated by Cystoseira crinita (Fucales, Heterokontophyta) from Cap Corse (Corsica, North Western Mediterranean). Eur. J. Phycol. 45: 404-412.
https://doi.org/10.1080/09670262.2010.498585

Sales M., Cebrian E., Tomas F., et al. 2011. Pollution impacts and recovery potential in three species of the genus Cystoseira (Fucales, Heterokontophyta). Estuar. Coast. Shelf. Sci. 92: 347-357.
https://doi.org/10.1016/j.ecss.2011.01.008

Sant N. 2003. Algues bentòniques mediterrànies: comparació de mètodes de mostreig, estructura de comunitats i variació en la resposta fotosintètica. Ph.D. Thesis, Universitat de Barcelona, 250 pp.

Sant N., Chappuis E., Rodríguez-Prieto C., et al. 2017. Cost-benefit of three different methods for studying Mediterranean rocky benthic assemblages. Sci. Mar. 81: 129-138.
https://doi.org/10.3989/scimar.04463.04A

Schiller C. 1993. Ecology of the symbiotic coral Cladocora caespitosa (L.) (Faviidae, Scleractinia) in the Bay of Piran (Adriatic Sea): I. Distribution and biometry. Mar. Ecol. 14: 205-219.
https://doi.org/10.1111/j.1439-0485.1993.tb00480.x

Sokal R.R., Rohlf F.J. 1995. Biometry: the principles and practice of statistics in biological research. W.H. Freeman and Co., New York, USA, 887 pp.

Teixidó N., Gambi M.C., Parravacini V., et al. 2018. Functional biodiversity loss along natural CO2 gradients. Nat. Comm. 9: 5149.
https://doi.org/10.1038/s41467-018-07592-1

Templado J., Ballesteros E., et al. 2012. Guía interpretativa. Inventario español de hábitats marinos. Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, 229 pp.

Thibaut T., Pinedo S., Torras X., et al. 2005. Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France, North-western Mediterranean). Mar. Pollut. Bull. 50: 1472-1489.
https://doi.org/10.1016/j.marpolbul.2005.06.014

Thibaut T., Blanfuné A., Markovic L., et al. 2014. Unexpected abundance and long-term relative stability of the brown alga Cystoseira amentacea, hitherto regarded as a threatened species, in the north-western Mediterranean Sea. Mar. Pollut. Bull. 89: 305-323.
https://doi.org/10.1016/j.marpolbul.2014.09.043

Thibaut T., Blanfuné A., Boudouresque C.F., et al. 2015. Decline and local extinction of Fucales in French Riviera: the harbinger of future extinctions? Medit. Mar. Sci. 16: 206-224.
https://doi.org/10.12681/mms.1032

Thibaut T., Blanfuné A., Boudouresque C.F., et al. 2016. Unexpected temporal stability of Cystoseira and Sargassum forests in Port-Cros, one of the oldest Mediterranean marine National Parks. Crypt. Algol. 37: 61-91.
https://doi.org/10.7872/crya/v37.iss1.2016.61

UNEP/MAP/RAC-SPA. 2006. Classification of benthic marine habitat types for the Mediterranean region. 15 pp.

UNEP/MAP/RAC-SPA. 2013. Protocol concerning specially protected areas and biological diversity in the Mediterranean. Annex II. List of endangered or threatened species. 7 pp.

Zabala M., Ballesteros E. 1989. Surface-dependent strategies and energy flux in benthic marine communities or, why corals do not exist in the Mediterranean. Sci. Mar. 53: 1-15.

Zibrowius H. 1982. Taxonomy in ahermatypic scleractinian corals. Palaeont. Amer. 54: 80-85.



Copyright (c) 2011 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.


Contact us scimar@icm.csic.es

Technical support soporte.tecnico.revistas@csic.es