The ecological condition of vermetid platforms affects the cover of the alien seaweed Caulerpa cylindracea
DOI:
https://doi.org/10.3989/scimar.04984.06AKeywords:
rocky shores, phytobenthos, community composition, Caulerpa cylindracea, vermetid platforms, man-induced effects, MediterraneanAbstract
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.
Downloads
References
Adloff F., Jordà G., Somot S., et al. 2018. Improving sea level simulation in Mediterranean regional climate models. Clim. Dyn. 51: 1167-1178. https://doi.org/10.1007/s00382-017-3842-3
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. https://doi.org/10.1111/ddi.12301
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. https://doi.org/10.3989/ajbm.2381
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. https://doi.org/10.1016/j.ocecoaman.2018.12.019
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. https://doi.org/10.1016/j.marpolbul.2006.08.038 PMid:17045303
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. https://doi.org/10.3354/meps110009
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. https://doi.org/10.3354/meps214137
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. https://doi.org/10.3989/scimar.03669.21A
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. https://doi.org/10.1111/1365-2435.12815
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. https://doi.org/10.1016/S0025-326X(01)00150-3
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. https://doi.org/10.1890/09-1857.1 PMid:20836441
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. https://doi.org/10.1007/s10530-017-1442-0
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. https://doi.org/10.1016/j.ocecoaman.2017.04.014
Ceccherelli G., Piazzi L., Balata D. 2002. Spread of introduced Caulerpa species in macroalgal habitats. J. Exp. Mar. Biol. Ecol. 280: 1-11. https://doi.org/10.1016/S0022-0981(02)00336-2
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. https://doi.org/10.1007/s10530-014-0700-7
Cheminée A., Merigot B., Vanderklift M.A., et al. 2016. Does habitat complexity influence fish recruitment? Mediterr. Mar. Sci. 17: 39-46. https://doi.org/10.12681/mms.1231
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. https://doi.org/10.3354/meps07526
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. https://doi.org/10.3354/meps096093
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. https://doi.org/10.1016/j.tree.2007.07.001 PMid:17673330
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. https://doi.org/10.1080/09397140.2013.810885
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. https://doi.org/10.1007/698_2015_411
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. https://doi.org/10.3354/meps09053
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. https://doi.org/10.1007/s00227-004-1335-5
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. https://doi.org/10.1017/S0025315410001219
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. https://doi.org/10.2307/1940302
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. https://doi.org/10.3391/ai.2014.9.4.01
Klein J., Verlaque M. 2008. The Caulerpa racemosa invasion: a critical review. Mar. Pollut. Bull. 56: 205-225. https://doi.org/10.1016/j.marpolbul.2007.09.043 PMid:18061625
Laborel J., Kempf M. 1965. Formações de vermetos e algas calcárias nas costas do Brasil. Trabal. Inst. Ocean. UFPE 7/8: 33-50. https://doi.org/10.5914/tropocean.v7i1.2500
MacDougall A.S., Turkington R. 2005. Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86: 42-55. https://doi.org/10.1890/04-0669
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. https://doi.org/10.1016/j.marpolbul.2017.10.068 PMid:29108739
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. https://doi.org/10.3354/meps07400
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. https://doi.org/10.1007/s10530-015-0852-0
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. https://doi.org/10.1016/S0006-3207(03)00292-1
Milazzo M., Rodolfo-Metalpa R., San Chan V.B., et al. 2014. Ocean acidification impairs vermetid reef recruitment. Sci. Rep. 4: 1-7. https://doi.org/10.1038/srep04189 PMid:24577050 PMCid:PMC5379440
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. https://doi.org/10.1007/978-3-319-21012-4_9
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. https://doi.org/10.1007/s10530-015-0908-1
Munda I.M. 1993. Changes and degradation of seaweed stands in the Northern Adriatic. Hydrobiologia 260/261: 239-253. https://doi.org/10.1007/BF00049025
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. https://doi.org/10.1016/j.ecss.2005.03.010
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. https://doi.org/10.1007/s00227-016-2937-4
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 https://doi.org/10.1016/j.ecolind.2019.105556
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. https://doi.org/10.1016/j.marpolbul.2006.08.044 PMid:17049951
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. https://doi.org/10.1016/j.ecss.2015.05.004
Ponti M., Turicchia E., Ferro F., et al. 2018. The understorey of gorgonian forests in mesophotic temperate reefs. Aquat. Conserv. 28: 1153-1166. https://doi.org/10.1002/aqc.2928
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. https://doi.org/10.1023/B:BINV.0000034614.07427.96
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. https://doi.org/10.1007/978-3-540-79236-9_31
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. https://doi.org/10.1016/j.marpolbul.2005.04.009 PMid:15893332
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. https://doi.org/10.1007/BF00364323 PMid:28309299
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. https://doi.org/10.1016/j.marpolbul.2015.05.024 PMid:25986653
Sanz-Lázaro C. 2016. Climate extremes can drive biological assemblages to early successional stages compared to several mild disturbances. Sci. Rep. 6: 30607. https://doi.org/10.1038/srep30607 PMid:27527612 PMCid:PMC4985811
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. https://doi.org/10.2307/3545860
Templado J., Richter A., Calvo M. 2016. Reef building Mediterranean vermetid gastropods: disentangling the Dendropoma petraeum species complex. Mediterr. Mar. Sci. 17: 13-31. https://doi.org/10.12681/mms.1333
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. https://doi.org/10.12681/mms.14143
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. https://doi.org/10.1016/j.marenvres.2017.02.006 PMid:28237887
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. https://doi.org/10.1371/journal.pone.0047728 PMid:23110095 PMCid:PMC3478284
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. https://doi.org/10.1080/09670260310001612592
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. https://doi.org/10.1007/s12237-018-0408-5
Published
How to Cite
Issue
Section
License
Copyright (c) 2011 Consejo Superior de Investigaciones Científicas (CSIC)
This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the printed and online versions of this Journal are the property of Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.All contents of this electronic edition, except where otherwise noted, are distributed under a “Creative Commons Attribution 4.0 International” (CC BY 4.0) License. You may read here the basic information and the legal text of the license. The indication of the CC BY 4.0 License must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the published by the Editor, is not allowed.
