Hostname: page-component-848d4c4894-ndmmz Total loading time: 0 Render date: 2024-05-03T20:16:09.866Z Has data issue: false hasContentIssue false

Invasive green algae in a western Mediterranean Marine Protected Area: interaction of photophilous sponges with Caulerpa cylindracea

Published online by Cambridge University Press:  06 March 2020

R. Manconi*
Affiliation:
Department of Veterinary Medicine, University of Sassari, Sassari, Italy
A. Padiglia
Affiliation:
Department of Veterinary Medicine, University of Sassari, Sassari, Italy Department for the Earth, Environment and Life Sciences, University of Genova, Genova, Italy
B. M. Padedda
Affiliation:
Department of Architecture, Design and Urban Planning, University of Sassari, Sassari, Italy
R. Pronzato
Affiliation:
Department for the Earth, Environment and Life Sciences, University of Genova, Genova, Italy
*
Author for correspondence: R. Manconi, E-mail: renata.manconi@uniss.it

Abstract

We report on the relationships between some conspicuous Mediterranean photophilous sponge species and Caulerpa cylindracea, a non-indigenous species. A diversification of defence strategies and behaviour is highlighted in target species belonging to different orders of Demospongiae from a western Mediterranean Marine Protected Area (NW Sardinian Sea). Caulerpa cylindracea displays a strongly invasive behaviour during body colonization of the Irciniidae Sarcotragus spinosulus and Ircinia retidermata (order Dictyoceratida). These sponges possess pre-adaptive defensive morpho-functional and physiological traits enabling them to partly withstand algal invasion. Also Aplysina aerophoba (order Verongiida) seems to be able to control colonization. Successful anti-Caulerpa strategies characterize the rarely affected Crambe crambe (order Poecilosclerida). Species-specific competitive strategies are displayed at different levels of body architecture, behaviour and physiology by native sponge species. The invasion patterns on sponges, the invasion dynamics in 2016–2017 and topographic distribution of C. cylindracea on S. spinosulus confirm this algal species as a threat, with potential long-term effects on sponge assemblages. Data suggest other kinds of poorly investigated synergic stressors affecting these habitat-forming species. Defence strategies of sponge species take the form of: (1) passive deterrence by morpho-functional pre-adaptive traits as growth form, biomass amount, surface traits, and microhabitat within the sponges' aquiferous system; (2) active physiological defence, whereby the morphology/anatomy of the sponge body is adapted to control invaders, by body remodelling and regenerative processes within the aquiferous system and at the sponge surface; (3) presumed active chemical defence by exudation processes of bioactive compounds.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bakus, G and Green, G (1974) Toxicity in sponges and holothurians: a geographic pattern. Science 185, 951953.CrossRefGoogle ScholarPubMed
Baldacconi, R and Corriero, G (2009) Effects of the spread of the alga Caulerpa racemosa var. Cylindracea on the sponge assemblage from coralligenous concretions of the Apulian coast (Ionian Sea, Italy). Marine Ecology 30, 337345.CrossRefGoogle Scholar
Becerro, MA, Thacker, RW, Turon, X, Uriz, MJ and Paul, VJ (2003) Biogeography of sponge chemical ecology: comparisons of tropical and temperate defenses. Oecologia 135, 91101.CrossRefGoogle ScholarPubMed
Bell, JJ (2008) The functional roles of marine sponges. Estuarine and Coastal Shelf Science 79, 341353.CrossRefGoogle Scholar
Belton, GS, P'homme van Reine, WF, Huisman, JM, Draisma, SGA and Gurgel, CFD (2014) Resolving phenotypic plasticity and species designation in the morphology challenging Caulerpa racemosa-peltata complex (Caulerpaceae, Chlorophyta). Journal of Phycology 50, 3254.10.1111/jpy.12132CrossRefGoogle Scholar
Bianchi, CN, Morri, C and Pronzato, R (2014) The other side of rarity: recent habitat expansion and increased abundance of the horny sponge Ircinia retidermata (Demospongiae: Dictyoceratida) in the southeast Aegean. Italian Journal of Zoology 81, 564570.10.1080/11250003.2014.920929CrossRefGoogle Scholar
Boudouresque, CF and Verlaque, M (2012) An overview of species introduction and invasion processes in marine and coastal lagoon habitats. CBM–Cahiers de Biologie Marine 53, 309.Google Scholar
Boury-Esnault, N (1976) Morphogénése expérimentale des papilles inhalantes des eponge Polymastia mamillaris (Muller). Archives de zoologie expérimentale et générale 117, 181196.Google Scholar
Braekman, JC and Daloze, D (1986) Chemical defence in sponges. Pure and Applied Chemistry 58, 357364.CrossRefGoogle Scholar
Brunelli, M, Garcia-Gil, M, Mozzachiodi, R, Scuri, MR, Traina, G and Zaccardi, ML (2000) Neurotoxic effects of caulerpenyne. Progress in Neuro-Psychopharmacology & Biological Psychiatry 24, 939954.CrossRefGoogle ScholarPubMed
Bulut, H (2018) MVTests: Multivariate Hypothesis Tests. R package version 1.0. https://CRAN.R-project.org/package=MVTests.Google Scholar
Bulleri, F, Alestra, T, Ceccherelli, G, Tamburello, L, Pinna, S, Sechi, N and Benedetti-Cecchi, L (2011) Determinants of Caulerpa racemosa distribution in the north-western Mediterranean. Marine Ecology Progress Series 431, 5567.CrossRefGoogle Scholar
Cadeddu, B, Ledda, FD, Padiglia, A and Manconi, R (2014) Biodiversity of Capo Caccia-Isola Piana MPA: faunistic update on Porifera. Biologia Marina Mediterranea 21, 228229.Google Scholar
Caronni, S, Calabretti, C, Delaria, MA, Bernardi, G, Navone, A, Occhipinti-Ambrogi, A, Panzalis, P and Ceccherelli, G (2015) Consumer depletion alters seagrass resistance to an invasive macroalga. PLoS ONE 10, e0115858.CrossRefGoogle Scholar
Casu, D, Ceccherelli, G, Palomba, D, Curini Galletti, M and Castelli, A (2006) Effetto immediato della rimozione di Caulerpa racemosa sullo zoobenthos dell'infralitorale superficiale roccioso di Porto Torres (Nord Sardegna). In XV Meeting of the Italian Society of Ecology, pp. 13.Google Scholar
Connell, JH (1978) Diversity in tropical rain forests and coral reefs. Science 199, 13021310.CrossRefGoogle ScholarPubMed
Corriero, G, Pierri, C, Accoroni, S, Alabiso, G, Bavestrello, G, Barbone, E, Bastianini, M, Bazzoni, AM, Bernardi Aubry, F, Boero, F, Buia, MC, Cabrini, M, Camatti, E, Cardone, F, Cataletto, B, Cattaneo Vietti, R, Cecere, E, Cibic, T, Colangelo, P, De Olazabal, A, D'onghia, G, Finotto, S, Fiore, N, Fornasaro, D, Fraschetti, S, Gambi, MC, Giangrande, A, Gravili, C, Guglielmo, R, Longo, C, Lorenti, M, Lugliè, A, Maiorano, P, Mazzocchi, MG, Mercurio, M, Mastrototaro, F, Mistri, M, Monti, M, Munari, C, Musco, L, Nonnis-Marzano, C, Padedda, BM, Patti, FP, Petrocelli, A, Piraino, S, Portacci, G, Pugnetti, A, Pulina, S, Romagnoli, T, Rosati, I, Sarno, D, Satta, CT, Sechi, N, Schiaparelli, S, Scipione, B, Sion, L, Terlizzi, A, Tirelli, V, Totti, C, Tursi, A, Ungaro, N, Zingone, A, Zupo, V and Basset, A (2016) Ecosystem vulnerability to alien and invasive species: a case study on marine habitats along the Italian coast. Aquatic Conservation: Marine and Freshwater Ecosystems 26, 392409.CrossRefGoogle Scholar
Cottalorda, JM, Gratiot, J, Mannoni, PA, de Vaugelas, J and Meinesz, A (2008) Suivi de l'invasion des algues introduites Caulerpa taxifolia et Caulerpa racemosa en Méditerranée: situation devant les côtes françaises au 31 décembre 2007. EA 4228 ECOMERS. Université de Nice-Sophia Antipolis publ., France.Google Scholar
De Luca, M, Pascucci, V, Gazale, V, Ruiu, A, Massetti, L and Cossu, A (2018) Marine benthic forms of the Marine Protected Area Capo Caccia-Isola Piana (Sardinia, Italy). Journal of Maps 14, 421427.CrossRefGoogle Scholar
Duckworth, AR and Battershill, CN (2001) Population dynamics and chemical ecology of New Zealand Demospongiae Latrunculia sp. nov. and Polymastia croceus (Poecilosclerida: Latrunculiidae: Polymastiidae). New Zealand Journal of Marine and Freshwater Research 35, 935949.CrossRefGoogle Scholar
Erickson, AA, Paul, VJ, Van Alstyne, KL and Kwiatkowski, LM (2006) Palatability of macroalgae that use different types of chemical defenses. Journal of Chemical Ecology 32, 18831895.CrossRefGoogle ScholarPubMed
Fazzi, R, Bortulo, S and Manconi, R (2014) Studio preliminare sulla colonizzazione di poriferi da parte di Caulerpa cylindracea nella Area Marina Protetta Capo Caccia-Isola Piana. In Proceedings of Fifth International Symposium on Monitoring of Mediterranean Coastal Areas: Problems and Measurement Techniques, Livorno, Italy.Google Scholar
Funayama, N (2018) The cellular and molecular bases of the sponge stem cell systems underlying reproduction, homeostasis and regeneration. International Journal of Developmental Biology 62, 513525.CrossRefGoogle ScholarPubMed
Gaino, E and Pronzato, R (1989) Ultrastructural evidence of bacterial damage to Spongia officinalis fibres (Porifera, Demospongiae). Disease of Aquatic Organisms 6, 6774.10.3354/dao006067CrossRefGoogle Scholar
Gaino, E, Pronzato, R, Corriero, G and Buffa, P (1992) Mortality of commercial sponges: incidence in two Mediterranean areas. Italian Journal of Zoology 59, 7985.Google Scholar
Gaino, E, Manconi, R and Pronzato, R (1995) Organizational plasticity as a successful conservative tactic in sponges. Animal Biology 4, 3143.Google Scholar
Gambi, MC, Giangrande, A, Chessa, LA, Manconi, R and Scardi, M (1989) Distribution and ecology of polychaetes in the foliar stratum of a Posidonia oceanica bed in the bay of Porto Conte (N.W. Sardinia). In Boudouresque, CF, Meinesz, A, Fresi, E and Gravez, V (eds), International Workshop on Posidonia Beds. Marseille: GIS Posidonie Publication, 2, pp. 175187.Google Scholar
Gambi, MC, Giangrande, A, Martinelli, M and Chessa, LA (1995) Polychaetes of a Posidonia oceanica bed off Sardinia (Italy): spatio-temporal distribution and feeding guild analysis. Scientia Marina 59, 129141.Google Scholar
Harvey, WH (1858) Nereis boreali-americana. Part III. Chlorospermae. Smithsonian Contributions to Knowledge 10, 140 pp.Google Scholar
Jousson, O, Pawlowski, J, Zaninetti, L, Zechman, FW, Dini, F, Di Guiseppe, G, Woodfield, R, Millar, A and Meinesz, A (2000) Invasive alga reaches California. Nature 408, 157158.CrossRefGoogle ScholarPubMed
Klein, J (2007) Impact de Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) sur les communautés macrophytiques en Méditerranée nord-occidentale (Thèse de doctorat). Université Aix-Marseille II, France.Google Scholar
Klein, J and Verlaque, M (2008) The Caulerpa racemosa invasion: a critical review. Marine Pollution Bulletin 56, 205225.CrossRefGoogle ScholarPubMed
Maj, RLC and Taramelli, E (1989) Mysidacea of Posidonia oceanica (L.) Delile beds in Torvaldiga (Latium) and Porto Conte (Sardinia). In Boudouresque, CF, Meinesz, A, Fresi, E and Gravez, V (eds), International Workshop on Posidonia Beds. Marseille: GIS Posidonie Publication, 2, pp. 203206.Google Scholar
Manconi, R, Ledda, FD, Ortu, MF, Serusi, A, Stocchino, GA, Corso, G and Pronzato, R (2005) Spongicoltura integrata nell'AMP ‘Capo Caccia-Isola piana’: il caso di Aplysina aerophoba (Aplysinidae: Verongida). Biologia Marina Mediterranea 12, 191194.Google Scholar
Manconi, R, Ledda, FD, Serusi, A, Corso, G and Stocchino, GA (2009) Sponges of marine caves: notes on the status of the Mediterranean palaeoendemic Petrobiona massiliana (Porifera: Calcarea: Lithonida) with new records from Sardinia. Italian Journal of Zoology 76, 306315.CrossRefGoogle Scholar
Manconi, R, Cadeddu, B, Ledda, F and Pronzato, R (2013) An overview of the Mediterranean cave-dwelling horny sponges (Porifera, Demospongiae). ZooKeys 281, 168.CrossRefGoogle Scholar
Mollo, E, Cimino, G and Ghiselin, MT (2015) Alien biomolecules: a new challenge for natural product chemists. Biological Invasions 17, 941950.CrossRefGoogle Scholar
Montefalcone, M, Albertelli, G, Morri, C and Bianchi, CN (2010) Pattern of wide-scale substitution within Posidonia oceanica meadows of NW Mediterranean Sea: invaders are stronger than natives. Aquatic Conservation: Marine and Freshwater Ecosystems 20, 507515.10.1002/aqc.1128CrossRefGoogle Scholar
Montefalcone, M, Morri, C, Parravicini, V and Bianchi, CN (2015) A tale of two invaders: divergent spreading kinetics of the alien green algae Caulerpa taxifolia and Caulerpa cylindracea. Biological Invasion 17, 27172728.CrossRefGoogle Scholar
Murray, PM, Moane, S, Collins, C, Beletskaya, T, Thomas, OP, Duarte, AWF, Nobre, FS, Owoyemi, IO, Pagnocca, FC, Sette, LD, McHugh, E, Causse, E, Pérez-López, P, Feijoo, G, Moreira, MT, Rubiolo, J, Leiròs, M, Botana, LM, Pinteus, S, Alves, C, Horta, A, Pedrosa, R, Jeffryes, C, Agathos, SN, Allewaert, C, Verween, A, Vyverman, W, Laptev, I, Sineoky, S, Bisio, A, Manconi, R, Ledda, F, Marchi, M, Pronzato, R and Walsh, DJ (2013) Sustainable production of biologically active molecules of marine based origin. New Biotechnology 30, 839850.CrossRefGoogle ScholarPubMed
Nizamuddin, M (1991) The Green Marine Algae of Libya. Bern: Elga Publ., 227 pp.Google Scholar
Otero, M, Cebrian, E, Francour, P, Galil, B and Savini, D (2013) Monitoring Marine Invasive Species in Mediterranean Marine Protected Areas (MPAS): A Strategy and Practical Guide for Managers. Malaga: IUCN, 136.Google Scholar
Ould-Ahmed, N and Meinesz, A (2007) First record of the invasive alga Caulerpa racemosa (Caulerpales, Chlorophyta) on the coast of Algeria. Cryptogamie Algologie 28, 303305.Google Scholar
Padiglia, A, Cadeddu, B, Bertolino, M, Demurtas, D, Manconi, R and Pronzato, R (2015) Sponges of Posidonia oceanica meadows in two marine protected areas (Sardinia Sea). Biologia Marina Mediterranea 22, 105106.Google Scholar
Padiglia, A, Cadeddu, B, Ledda, FD, Bertolino, M, Costa, G, Pronzato, R and Manconi, R (2018 a) Biodiversity assessment in Western Mediterranean Marine Protected Areas (MPAs): Porifera of Posidonia oceanica Meadows (Asinara Island MPA) and submerged caves (Capo Caccia – Isola Piana MPA) of NW Sardinia. European Journal of Zoology 85, 409422.CrossRefGoogle Scholar
Padiglia, A, Ledda, FD, Padedda, BM, Pronzato, R and Manconi, R (2018 b) Long-term experimental in situ farming of Crambe crambe (Demospongiae: Poecilosclerida). PeerJ 6, e4964.CrossRefGoogle Scholar
Papini, A, Mosti, S and Santosuosso, U (2013) Tracking the origin of the invading Caulerpa (Caulerpales, Chlorophyta) with geographic profiling: a criminological technique for a killer alga. Biological Invasions 15, 16131621. https://doi.org/10.1007/s10530-012-0396-5CrossRefGoogle Scholar
Pawlik, JR, Chanas, B, Toonen, RJ and Fenical, W (1995) Defenses of Caribbean sponges against predatory reef fish. 1. Chemical deterrency. Marine Ecology Progress Series 127, 183194.CrossRefGoogle Scholar
Piazzi, L and Balata, D (2009) Invasion of alien macroalgae in different Mediterranean habitats. Biological Invasions 11, 193204.CrossRefGoogle Scholar
Piazzi, L, Meinesz, A, Verlaque, M, Akçali, B, Antolić, B, Argyrou, M, Balata, D, Ballesteros, E, Calvo, S, Cinelli, F, Cirik, S, Cossu, A, D'archino, F, Djellouli, AS, Javel, F, Lanfranco, E, Mifsud, C, Pala, D, Panayotidis, P, Peirano, A, Pergent, G, Petrocelli, A, Ruitton, S, Žuljević, A and Ceccherelli, G (2005) Invasion of Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) in the Mediterranean Sea: an assessment of the spread. Cryptogamie Algologie 26, 189202.Google Scholar
Piazzi, L, Balata, D, Bulleri, F, Gennaro, P and Ceccherelli, G (2016) The invasion of Caulerpa cylindracea in the Mediterranean: the known, the unknown and the knowable. Marine Biology 163, 114.CrossRefGoogle Scholar
Piazzi, L, Gennaro, P, Atzori, F, Cadoni, N, Cinti, MF, Frau, F and Ceccherelli, G (2018) ALEX index enables detection of alien macroalgae invasions across habitats within a marine protected area. Marine Pollution Bulletin 128, 318323.CrossRefGoogle ScholarPubMed
Raniello, R, Lorenti, M, Brunet, C and Buia, MC (2004) Photosynthetic plasticity of an invasive variety of Caulerpa racemosa in a coastal Mediterranean area: light harvesting capacity and seasonal acclimation. Marine Ecology Progress Series 271, 113120.CrossRefGoogle Scholar
Raniello, R, Mollo, E, Lorenti, M, Gavagnin, M and Buia, MC (2007) Phytotoxic activity of caulerpenyne from the Mediterranean invasive variety of Caulerpa racemosa: a potential allelochemical. Biological Invasions 9, 361368.CrossRefGoogle Scholar
R Core Team (2013) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.Google Scholar
Rocha, FD, Soares, AR, Houghton, PJ, Pereira, RC, Kaplan, MAC and Teixeira, VL (2007) Potential cytotoxic activity of some Brazilian seaweeds on human melanoma cells. Phytotherapy Research: An International Journal Devoted to Pharmacological and Toxicological Evaluation of Natural Product Derivatives 21, 170175.CrossRefGoogle ScholarPubMed
Ruitton, S, Verlaque, M and Boudouresque, CF (2005) Seasonal changes of the introduced Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) at the northwest limit of its Mediterranean range. Aquatic Botany 82, 5570.CrossRefGoogle Scholar
Russo, GF, Chessa, LA, Vinci, D and Fresi, E (1991) Molluscs of Posidonia oceanica beds in the bay of Porto Conte (North-Western Sardinia): zonation pattern, seasonal variability and geographical comparison. Posidonia Newsletter 4, 514.Google Scholar
Simpson, TL (1984) The Cell Biology of Sponges. New York, NY: Springer-Verlag.CrossRefGoogle Scholar
Storr, JF (1976) Field observations of sponge reactions as related to their ecology. In Harrison, FW and Cowden, RR (eds), Aspects of Sponge Biology. New York, NY: Academic Press, pp. 277282.CrossRefGoogle Scholar
Streftaris, N and Zenetos, A (2006) Alien marine species in the Mediterranean – the 100 ‘Worst Invasives’ and their impact. Mediterranean Marine Science 7, 87118.CrossRefGoogle Scholar
Ternon, E, Zarate, L, Chenesseau, S, Croué, J, Dumollard, R, Suzuki, MT and Thomas, OP (2016) Spherulization as a process for the exudation of chemical cues by the encrusting sponge C. crambe. Scientific Reports 6, 29474.CrossRefGoogle ScholarPubMed
Tsoukatou, M, Hellio, C, Vagias, C, Harvala, C and Roussis, V (2002) Chemical defense and antifouling activity of three Mediterranean sponges of the genus Ircinia. Zeitschrift für Naturforschung C 57, 161171.CrossRefGoogle ScholarPubMed
Tsurumi, M and Reiswig, HM (1997) Sexual vs asexual reproduction in an oviparous rope-form sponge, Aplysina cauliformis (Porifera; Verongida). Invertebrate Reproduction & Development 32, 19.10.1080/07924259.1997.9672598CrossRefGoogle Scholar
Uriz, MJ, Becerro, MA, Tur, JM and Turon, X (1996 a) Location of toxicity within the Mediterranean sponge Crambe crambe (Demospongiae: Poecilosclerida). Marine Biology 124, 583590.10.1007/BF00351039CrossRefGoogle Scholar
Uriz, MJ, Turon, X, Becerro, MA and Galera, J (1996 b) Feeding deterrence in sponges: the role of toxicity, physical defenses, energetic contents, and life-history traits. Journal of Experimental Marine Biology and Ecology 205, 187204.CrossRefGoogle Scholar
Verlaque, M, Boudouresque, CF, Meinesz, A and Gravez, V (2000) The Caulerpa racemosa complex (Caulerpales, Ulvophyceae) in the Mediterranean Sea. Botanica Marina 43, 4968.10.1515/BOT.2000.005CrossRefGoogle Scholar
Verlaque, M, Durand, C, Huisman, JM, Boudouresque, CF and le Parco, Y (2003) On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta). European Journal of Phycology 38, 325329.CrossRefGoogle Scholar
Wilkinson, DM (1999) The disturbing history of intermediate disturbance. Oikos 84, 145147.CrossRefGoogle Scholar
Withgott, J (2002) California tries to rub out the monster of the lagoon. Science 295, 22012202.CrossRefGoogle Scholar
Womersley, HBS (1984) The Marine Benthic Flora of South Australia. Part I. Adelaide: South Australian Government Printing Division.Google Scholar
Wulff, JL (1991) Asexual fragmentation, genotype success, and population dynamics of erect branching sponges. Journal of Experimental Marine Biology and Ecology 149, 227247.CrossRefGoogle Scholar
Žuljević, A, Antolić, B and Onofri, V (2003) First record of Caulerpa racemosa (Caulerpales: Chlorophyta) in the Adriatic Sea. Journal of the Marine Biological Association of the United Kingdom 83, 711712.10.1017/S0025315403007689hCrossRefGoogle Scholar
Žuljević, A, Thibaut, T, Despalatovic, M, Cottalorda, J-M, Nikolic, V, Cvitkovic, I and Antolić, B (2011) Invasive alga Caulerpa racemosa var. cylindracea makes a strong impact on the Mediterranean sponge Sarcotragus spinosulus. Biological Invasions 13, 23032308.CrossRefGoogle Scholar