The ecological condition of vermetid platforms affects the cover of the alien seaweed Caulerpa cylindracea

  1. Terradas-Fernández, Marc 1
  2. Valverde-Urrea, Miguel 1
  3. Casado-Coy, Nuria 1
  4. Sanz-Lazaro, Carlos 2
  1. 1 Departamento de Ciencias del Mar y Biología Aplicada, Facultad de Ciencias, Universidad de Alicante
  2. 2 Departamento de Ecología, Universidad de Alicante - Multidisciplinary Institute for Environmental Studies (MIES), Universidad de Alicante
Revista:
Scientia Marina

ISSN: 0214-8358

Año de publicación: 2020

Volumen: 84

Número: 2

Páginas: 1-11

Tipo: Artículo

DOI: 10.3989/SCIMAR.04984.06A DIALNET GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Scientia Marina

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Resumen

The seaweed Caulerpa cylindracea Sonder is one of the most important invaders on Mediterranean rocky shores. However, many driving pressures affecting its spread are poorly understood and seem to involve the interactions between abiotic and biotic factors. We studied the invasiveness of C. Cylindracea on two shallow vermetid platforms with a con­trasting ecological status on which C. Cylindracea was first detected simultaneously 15 years ago. The cover values of C. Cylindracea and the other macroalgal species were assessed for one year, embracing the whole platform width. Caulerpa cylindracea cover was higher on the platform that had a low ecological status, especially during warmer months at the outer seaward margin. The ecological status of the overstory of native species seems to be a key point conditioning the success of C. Cylindracea invasiveness on these platforms.

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Información de financiación

This work was partially funded by the project GRE14-19 of the University of Alicante. We are thankful to Alberto Baraza, Aitor Navarro, Ana Belen Jodar, Lotte Krüger, Luís Enrique Alcaraz, Carlos Botana and Leticia Asensio for their help in the fieldwork. We are also thankful to J. Zubcoff for statistical advice. Ivan Egea helped us to improve the English grammar and two anonymous reviewers contributed to the improvement of the manuscript. C. S. was supported as “In-vestigador Distinguido” by the University of Alicante (Ref. UATALENTO 17-11).

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Referencias bibliográficas

  • Adloff F., Jordà G., Somot S., et al. 2018. Improving sea level simulation in Mediterranean regional climate models. Clim. Dyn. 51: 1167-1178.
  • Aguilar J. 2009. Seguimiento de la comunidad fitoplanctónica influenciada por actividades antrópicas en la bahía de Alicante (SE de la península ibérica). MSc. thesis, Univ. Alicante.
  • Airoldi L. 2003. The effects of sedimentation on rocky coast assemblages. Oceanogr. Mar. Biol. Annu. Rev. 41: 161-236.
  • Airoldi L., Turon X., Perkol-Finkel S., et al. 2015. Corridors for aliens but not for natives: effects of marine urban sprawl at a regional scale. Divers. Distrib. 21: 755-768.
  • Altamirano M., Andreakis N., Souza-Egipsy V., et al. 2014. First record of Caulerpa cylindracea (Caulerpaceae, Chlorophyta) in Andalusia (Southern Spain). An. Jar. Bot. Mad. 71: e007 2014.
  • Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, 244 pp.
  • Aranda A., Gras D., Guillén J.E., et al. 1994. Estudio bionómico de la Bahía de Alicante. Inst. Ecol. Lit, Ayuntamiento de Alicante, 172 pp.
  • Badreddine A., Milazzo M., Saab M.A.A., et al. 2019. Threatened biogenic formations of the Mediterranean: Current status and assessment of the vermetid reefs along the Lebanese coastline (Levant basin). Ocean Coast Manage.169: 137-146.
  • Balistreri P., Mannino A.M. 2017. Preliminary data on the occurrence of alien macroalgae in the vermetid reef along the coasts of Favignana Island (Southern Tyrrhenian Sea). Biodiversity J. 8: 105-112.
  • Ballesteros E., Torras X., Pinedo S., et al. 2007. A new methodology based on littoral community cartography dominated by macroalgae for the implementation of the European Water Framework Directive. Mar. Poll. Bull. 55: 172-180.
  • Benedetti-Cecchi L., Cinelli F. 1994. Recovery of patches in an assemblage of geniculate coralline algae: variability at different successional stages. Mar. Ecol. Prog. Ser. 110: 9-18.
  • Benedetti-Cecchi L., Pannacciulli F., Bulleri F., et al. 2001. Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Mar. Ecol. Prog. Ser. 214: 137-150.
  • Bertocci I., Araújo R., Incera M., et al. 2012. Benthic assemblages of rock pools in northern Portugal: seasonal and between-pool variability. Sci. Mar. 76: 781-789.
  • Bertocci I., Domínguez Godino J.A., Freitas C., et al. 2017. Compounded perturbations in coastal areas: contrasting responses to nutrient enrichment and the regime of storm-related disturbance depend on life-history traits. Funct. Ecol. 31: 1122-1134.
  • Boudouresque C.F., Meinesz A., Ribera M.A., et al. 1995. Spread of the green alga Caulerpa taxifolia (Caulerpales, Chlorophyta) in the Mediterranean: possible consequences of a major ecological event. Sci. Mar. 59: 21-29.
  • Boudouresque C.F., Verlaque M. 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar. Poll. Bull. 44: 32-38.
  • Bulleri F., Balata D., Bertocci I., et al. 2010. The seaweed Caulerpa racemosa on Mediterranean rocky reefs: from passenger to driver of ecological change. Ecology 91: 2205-2212.
  • Bulleri F., Benedetti-Cecchi L., Ceccherelli G., et al. 2017. A few is enough: a low cover of a non-native seaweed reduces the resilience of Mediterranean macroalgal stands to disturbances of varying extent. Biol. Invasions 19: 2291-2305.
  • Cantasano N., Pellicone G., Di Martino V. 2017. The spread of Caulerpa cylindracea in Calabria (Italy) and the effects of shipping activities. Ocean Coast Manag. 144 : 51-58.
  • Ceccherelli G., Piazzi L., Balata D. 2002. Spread of introduced Caulerpa species in macroalgal habitats. J. Exp. Mar. Biol. Ecol. 280: 1-11.
  • Ceccherelli G., Pinna S., Cusseddu V., et al. 2014. The role of disturbance in promoting the spread of the invasive seaweed Caulerpa racemosa in seagrass meadows. Biol. Invasions 16: 2737-2745.
  • Cheminée A., Merigot B., Vanderklift M.A., et al. 2016. Does habitat complexity influence fish recruitment? Mediterr. Mar. Sci. 17: 39-46.
  • Clarke K., Gorley R. 2015. PRIMER v7: User Manual/Tutorial. PRIMER-E, Plymouth, 296 pp.
  • Connell S.D., Russell B.C., Turner D.J., et al. 2008. Recovering a lost baseline: missing kelp forests on a metropolitan coast. Mar. Ecol. Prog. Ser. 360: 63-72.
  • Dethier M.N., Graham E.S., Cohen S., et al. 1993. Visual versus random-point percent cover estimations: ‘objective’ is not always better. Mar. Ecol. Prog. Ser. 96: 93-100.
  • Didham R.K., Tylianakis J.M., Gemmell N.J., et al. 2007. Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol. Evol. 22: 489-496.
  • Enguix A.M., Argente J., Chicharro J., et al. 2014. Estacionalidad y colonización de Caulerpa racemosa var. cylindracea en espacios naturales protegidos marinos de la Comunidad Valenciana. Chron. Nat. 4: 21-33.
  • Galil B.S. 2013. Going going gone: the loss of a reef building gastropod (Mollusca: Caenogastropoda: Vermetidae) in the southeast Mediterranean Sea. Zool. Middle East 59: 179-182.
  • García M., Weitzmann B., Pinedo S., et al. 2015. First report on the distribution and impact of marine alien species in Coastal Benthic assemblages along the Catalan Coast. In: Munné A., Ginebreda A., Prat N. (eds), Experiences from Ground, Coastal and Transitional Water Quality Monitoring. Springer, pp. 249-270.
  • Gennaro P., Piazzi L. 2011. Synergism between two anthropic impacts: Caulerpa racemosa var. cylindracea invasion and seawater nutrient enrichment. Mar. Ecol. Prog. Ser. 427: 59-70.
  • Gorgula S.K., Connell S.D. 2004. Expansive covers of turf-forming algae on human-dominated coast: the relative effects of increasing nutrient and sediment loads. Mar. Biol. 145: 613-619.
  • Guerra-García J.M., Cabezas M.P., Baeza-Rojano E., et al. 2011. Spatial patterns and seasonal fluctuations of intertidal macroalgal assemblages from Tarifa Island, southern Spain: relationship with associated Crustacea. J. Mar. Biol. Assoc. U.K. 91: 107-116.
  • Huenneke L.F., Hamburg S.P., Koide R., et al. 1990. Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71: 478-491.
  • Katsanevakis S., Wallentinus I., Zenetos A., et al. 2014. Impacts of invasive alien marine species on ecosystem services and biodiversity: a pan-European review. Aquat. Invasions 9: 391-423.
  • Klein J., Verlaque M. 2008. The Caulerpa racemosa invasion: a critical review. Mar. Pollut. Bull. 56: 205-225.
  • Laborel J., Kempf M. 1965. Formações de vermetos e algas calcárias nas costas do Brasil. Trabal. Inst. Ocean. UFPE 7/8: 33-50.
  • MacDougall A.S., Turkington R. 2005. Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86: 42-55.
  • Mancuso F.P., Strain E.M.A., Piccioni E., et al. 2018. Status of vulnerable Cystoseira populations along the Italian infralittoral fringe, and relationships with environmental and anthropogenic variables. Mar. Poll. Bull. 129: 762-771.
  • Mangialajo L., Chiantore M., Cattaneo-Vietti R. 2008. Loss of fucoid algae along a gradient of urbanisation, and structure of benthic assemblages. Mar. Ecol. Prog. Ser. 358: 63-74.
  • Marín-Guirao L., Bernardeau-Esteller J., Ruiz J.M., et al. 2015. Resistance of Posidonia oceanica seagrass meadows to the spread of the introduced green alga Caulerpa cylindracea: assessment of the role of light. Biol. Invasions 17: 1989-2009.
  • Milazzo M., Badalamenti F., Riggio S., et al. 2004. Patterns of algal recovery and small-scale effects of canopy removal as a result of human trampling on a Mediterranean rocky shallow community. Biol. Conserv. 117: 191-202.
  • Milazzo M., Rodolfo-Metalpa R., San Chan V.B., et al. 2014. Ocean acidification impairs vermetid reef recruitment. Sci. Rep. 4: 1-7.
  • Milazzo M., Fine M., La Marca E.C., et al. 2016. Drawing the Line at Neglected Marine Ecosystems: Ecology of Vermetid Reefs in a Changing Ocean. In: Rossi S., Bramanti L., Gori A., et al. (eds), Marine Animal Forests. Springer International Publishing AG, Switzerland, pp. 345-367.
  • Montefalcone M., Morri C., Parravicini V., et al. 2015. A tale of two invaders: divergent spreading kinetics of the alien green algae Caulerpa taxifolia and Caulerpa cylindracea. Biol. Invasions 17: 2717-2728.
  • Munda I.M. 1993. Changes and degradation of seaweed stands in the Northern Adriatic. Hydrobiologia 260/261: 239-253.
  • Pena-Martín C., Fernanz J.C.C., Crespo M.B., et al. 2003. Caulerpa racemosa (Forssk.) J. Agardh (Caulerpaceae, Chlorophyceae), nueva para la flora de Alicante. Anales Jard. Bot. Madrid 60: 448-449.
  • Piazzi L., Balata D., Ceccherelli G., et al. 2005. Interactive effect of sedimentation and Caulerpa racemosa var. cylindracea invasion on macroalgal assemblages in the Mediterranean Sea. Estuar. Coast. Shelf Sci. 64: 467-474.
  • Piazzi L., Balata D., Bulleri F., et al. 2016. The invasion of Caulerpa cylindracea in the Mediterranean: the known, the unknown and the knowable. Mar. Biol. 163: 161.
  • Pinedo S., Ballesteros E. 2019. The role of competitor, stress-tolerant and opportunist species in the development of indexes based on rocky shore assemblages for the assessment of ecological status. Ecol. Indic. 107: 105556
  • Pinedo S., García M., Satta M.P., et al. 2007. Rocky-shore communities as indicators of water quality: a case study in the Northwestern Mediterranean. Mar. Poll. Bull. 55: 126-135.
  • Pinedo S., Arévalo R., Ballesteros E. 2015. Seasonal dynamics of upper sublittoral assemblages on Mediterranean rocky shores along a eutrophication gradient. Est. Coast. Shelf Sci. 161: 93-101.
  • Ponti M., Turicchia E., Ferro F., et al. 2018. The understorey of gorgonian forests in mesophotic temperate reefs. Aquat. Conserv. 28: 1153-1166.
  • Ramos-Esplà A., Vázquez M., Izquierdo A. 2008. Cartografía de las formaciones de vermétidos en la Comunidad Valenciana y evaluación de su estado de conservación. D.G. Biodiversidad-Generalitat Valenciana, CIMAR-Universidad de Alicante, 120 pp.
  • Ramos-Esplà A, Vázquez M, Izquierdo A, et al. 2011. Estudio del estado de conservación de las comunidades bentónicas de substrato duro en la franja litoral de la Comunidad Valenciana, en aplicación de la Directiva Marco del Agua. D.G. Biodiversidad- Generalitat Valenciana, CIMAR-Universidad de Alicante, 91 pp.
  • Rilov G., Benayahu Y., Gasith A. 2004. Prolonged lag in population outbreak of an invasive mussel: a shifting-habitat model. Biol. Invasions 6: 347-364.
  • Rilov G., Galil B. 2009. Marine Bioinvasions in the Mediterranean Sea - History, Distribution and Ecology. In: Rilov G., Crooks J.A. (eds), Biological invasions in marine ecosystems. Springer, Berlin, pp. 549-575.
  • Ruitton S., Javel F., Culioli J.M., et al. 2005. First assessment of the Caulerpa racemosa (Caulerpales, Chlorophyta) invasion along the French Mediterranean coast. Mar. Poll. Bull. 50:1061-1068.
  • Ruiz J.M., Marín-Guirao L., Bernardeau-Esteller J., et al. 2011. Spread of the invasive alga Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) along the Mediterranean Coast of the Murcia region (SE Spain). Anim. Biodivers. Conserv. 34: 73-82.
  • Safriel U.N. 1975. The role of vermetid gastropods in the formation of Mediterranean and Atlantic reefs. Oecologia 20: 85-101.
  • Samperio-Ramos G., Olsen Y.S., Tomas F., et al. 2015. Ecophysiological responses of three Mediterranean invasive seaweeds (Acrothamnion preissii, Lophocladia lallemandii and Caulerpa cylindracea) to experimental warming. Mar. Poll. Bull. 96: 418-423.
  • Sanz-Lázaro C. 2016. Climate extremes can drive biological assemblages to early successional stages compared to several mild disturbances. Sci. Rep. 6: 30607.
  • Soto J. 1987. Estudio florístico, corológico, autoecológico y sinecológico de las algas bentónicas marinas del Sureste de la Península Ibérica. PhD thesis, Univ. Málaga, 507 pp.
  • Steneck R.S., Dethier M.N. 1994. A functional group approach to the structure of algal-dominated communities. Oikos. 69: 476-498.
  • Templado J., Richter A., Calvo M. 2016. Reef building Mediterranean vermetid gastropods: disentangling the Dendropoma petraeum species complex. Mediterr. Mar. Sci. 17: 13-31.
  • Terradas-Fernández M., Botana-Gómez C., Valverde-Urrea M., et al. 2018. The dynamics of phytobenthos and its main drivers on abrasion platforms with vermetids (Alicante, Southeastern Iberian Peninsula). Mediterr. Mar. Sci. 19: 58-68.
  • Uyà M., Maggi E., Mori G., et al. 2017. Carry over effects of nutrient addition on the recovery of an invasive seaweed from the winter die-back. Mar. Environ. Res. 126: 37-44.
  • Varela-Alvarez E., Garreta A.G., Lluch J.R., et al. 2012. Mediterranean species of Caulerpa are polyploid with smaller genomes in the invasive ones. PLoS ONE 7: e47728.
  • Verlaque M., Durand C., Huisman J.M., et al. 2003. On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta). Eur. J. Phycol. 38: 325-339.
  • Zamir R., Alpert P., Rilov G. 2018. Increase in Weather Patterns Generating Extreme Desiccation Events: Implications for Mediterranean Rocky Shore Ecosystems. Est. Coasts 41: 1868-1884.
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