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Local benthic assemblages in shallow rocky reefs find refuge in a marine protected area at Madeira Island

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Abstract

The patterns of variability in the composition and structure of benthic communities along two depth strata (5 and 10 m) and the presence of sea urchins in structuring the subtidal rocky reefs were quantified in a long-established coastal marine protected area (Garajau MPA) and in two size equivalent and contiguous impacted areas (one highly urbanized and other with high fishing pressure) at Madeira Island (northeast Atlantic). Results suggest i) the MPA could be acting as a refuge for local biodiversity, ii) communities from the highly fished area could be suffering an impoverishment of local biodiversity, and iii) communities from the highly urbanized area would be enriched by the establishment of opportunistic species. These findings support that the level of human-pressure likely plays an important role in the composition of benthic communities in this insular ecosystem, although this was more relevant at the shallower stratum where the key grazer Diadema africanum explained 65% of the variance of benthic assemblages. It is suggested that this MPA small dimension and proximity to human impacted areas are limiting the survival of predators of the D. africanum.

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References

  • Abecasis RC, Schmidt L, Longnecker N, Clifton J (2013) Implications of community and stakeholder perceptions of the marine environment and its conservation for MPA management in a small Azorean island. Ocean Coast Manag 84:208–219

    Article  Google Scholar 

  • Airoldi L, Bulleri F (2011) Anthropogenic disturbance can determine the magnitude of opportunistic species responses on marine urban infrastructures. PLoS One 6:e22985

    Article  Google Scholar 

  • Alves FMA, Chícharo LM, Serrão E, Abreu D (2001) Algal cover and sea urchin spatial distribution at Madeira Island (NE Atlantic). Sci Mar 65:383–392

    Article  Google Scholar 

  • Alves FMA, Chícharo LM, Serrão E, Abreu D (2003) Grazing by Diadema antillarum (Philippi) upon algal communities on rocky substrates. Sci Mar 67:307–311

    Article  Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+for PRIMER: Guide to Software and Statistical Methods. Primer-E, Plymouth

  • Andrade CA, Albuquerque FM (1995) Fish assemblages associated with bottom habitats on the south coast of Madeira. Bol Mus Mun Funchal (Suppl) 4:9–20

  • Aucelli PPC, Matano F, Salvini R, Schiattarella M (2018) Coastal changes, from past records to future trends: proxy analysis, modelling, and monitoring. J Coast Conserv 22:821–825. https://doi.org/10.1007/s11852-018-0623-z

    Article  Google Scholar 

  • Augier H (1985) Première contribution à l’étude et à la cartographie des biocenoses marines benthiques de l’Ile de Madère. Bol Mus Mun Funchal 37:86–129

    Google Scholar 

  • Baioni D (2011) Human activity and damaging landslides and floods on Madeira Island. Nat Hazards Earth Syst Sci 11:3035–3046

    Article  Google Scholar 

  • Batista MI, Cabral HN (2016) An overview of marine protected areas in SW Europe: factors contributing to their management effectiveness. Ocean Coast Manag 132:15–23

    Article  Google Scholar 

  • Baynes TW, Szmant AM (1989) Effect of current on the sessile benthic community structure of an artificial reef. Bull Mar Sci 44:545–566

    Google Scholar 

  • Bianchi CN, Morri C, Sartoni G, Wirtz P (1998) Sublittoral epibenthic communities around Funchal (Ilha da Madeira, NE Atlantic). Bol Mus Mun Funchal (Suppl) 5:59–80

  • Canning-Clode J, Fofonoff P, McCann L, Carlton JT, Ruiz G (2013) Marine invasions on a subtropical island: fouling studies and new records in a recent marina on Madeira Island (eastern Atlantic Ocean). Aquat Invasions 8:261–270

    Article  Google Scholar 

  • Castrejón M, Charles A (2013) Improving fisheries co-management through ecosystem-based spatial management: the Galapagos marine reserve. Mar Policy 38:235–245

    Article  Google Scholar 

  • Cicin-Sain B, Belfiore S (2005) Linking marine protected areas to integrated coastal and ocean management: a review of theory and practice. Ocean Coast Manag 48:847–868

    Article  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community. Austral Ecol 18:117–143

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: User manual/tutorial. PRIMER-E, Plymouth

  • Clemente S, Hernández JC (2008) Influence of wave exposure and habitat complexity in determining spatial variation of the sea urchin Diadema aff. antillarum (Echinoidea: Diadematidae) populations and macroalgal cover (Canary Islands-eastern Atlantic Ocean). Rev Biol Trop 56:229–254

    Google Scholar 

  • Clemente S, Hernández JC, Rodríguez A, Brito A (2010) Identifying keystone predators and the importance of preserving functional diversity in sublittoral rocky-bottom areas. Mar Ecol Prog Ser 413:55–67

    Article  Google Scholar 

  • Clemente S, Hernández JC, Brito A (2011) Context-dependent effects of marine protected areas on predatory interactions. Mar Ecol Prog Ser 437:119–133

    Article  Google Scholar 

  • Clemente S, Lorenzo-Morales SJ, Mendoza JC, López C, Sangil C, Alves F, Kaufmann M, Hernández JC (2014) Mass mortality of the sea urchin Diadema africanum in the subtropical eastern Atlantic archipelagos: the role of waterborne bacteria in a warming ocean. Mar Ecol Prog Ser 506:1–14

    Article  Google Scholar 

  • Day J, Dudley N, Hockings M, Holmes G, Laffoley D, Stolton S, Wells S (2012) Guidelines for applying the IUCN protected area management categories to marine protected areas. IUCN, Gland, Switzerland

  • DREM (2017) Madeira em Números Direção Regional de Estatística da Madeira. https://estatistica.madeira.gov.pt/. Accessed 10 May 2018

  • Elliot M (2011) Marine science and management means tackling exogenic unmanaged pressures and endogenic managed pressures – a numbered guide. Mar Pollut Bull 62:651–655

    Article  Google Scholar 

  • Elliot M (2014) Integrated marine science and management: wading through the morass. Mar Pollut Bull 86:1–4

    Article  Google Scholar 

  • Foster NL, Rees S, Langmead O, Griffiths C, Oates J, Attrill MJ (2017) Assessing the ecological coherence of a marine protected area network in the Celtic seas. Ecosphere 8:e01688

    Article  Google Scholar 

  • Friedlander AM, Ballesteros E, Beets J, Berkenpas E, Gaymer CF, Gorny M, Sala E (2013) Effects of isolation and fishing on the marine ecosystems of Easter Island and Salas y Gómez, Chile. Aquat Conserv 23:515–531

    Article  Google Scholar 

  • Friedlander AM, Ballesteros E, Clemente S, Gonçalves EJ, Estep A, Rose P, Sala E (2017) Contrasts in the marine ecosystem of two Macaronesian islands: a comparison between the remote Selvagens reserve and Madeira Island. PLoS One 12:e0187935

    Article  Google Scholar 

  • Gestoso I, Ramalhosa P, Oliveira P, Canning-Clode J (2017) Marine protected communities against biological invasions: a case study from an offshore island. Mar Pollut Bull 119:72–80

    Article  Google Scholar 

  • González-Delgado S, Lozano-Bilbao E, Alcázar-Treviño J (2018) Habitat preference of Anemonia sulcata in intertidal pools in the north-East Atlantic. Majorensis 14:7–11

    Google Scholar 

  • Guidetti P (2006) Marine reserves reestablish lost predatory interactions and cause community changes in rocky reefs. Ecol Appl 16:963–976

    Article  Google Scholar 

  • Halpern BS, Walbridge S, Selkoe K, Kappel C (2008) A global map of human impact on marine ecosystems. Science 319:948–952

    Article  Google Scholar 

  • Hawkins JE, Roberts CM (2004) Effects of artisanal fishing on Caribbean coral reefs. Conserv Biol 18:215–226

    Article  Google Scholar 

  • Hermida M, Delgado J (2016) High trophic level and low diversity: would Madeira benefit from fishing down? Mar Policy 73:130–137

    Article  Google Scholar 

  • Hernández JC, Gil-Rodriguez MC, Herrera-López G, Brito A (2007) Diet of the “key herbivore” Diadema antillarum in two contrasting habitats in the Canary Islands (Eastern-Atlantic). Vieraea 35:109–120

    Google Scholar 

  • Hernández JC, Clemente S, Sangil C, Brito A (2008a) The key role of the sea urchin Diadema aff antillarum in controlling macroalgae assemblages throughout the Canary Islands (eastern subtropical Atlantic): a spatio-temporal approach. Mar Environ Res 66:259–270

    Article  Google Scholar 

  • Hernández JC, Clemente S, Sangil C, Brito A (2008b) Actual status of the sea urchin Diadema aff antillarum populations and macroalgal cover in marine protected areas compared to a highly fished area (Canary Islands - eastern Atlantic Ocean). Aquat Conserv Mar Freshwat Ecosyst 18:1091–1108

    Article  Google Scholar 

  • INE (2012) Censos 2011 Resultados Definitivos - Autonomous Region of Madeira. Statistics Portugal. https://estatistica.madeira.gov.pt/. Accessed 15 May 2018

  • Jiao N-Z, Chen D-K, Luo Y-M, Huang X-P, Zhang R, Zhang H-B, Jiang Z-J, Zhang F (2015) Climate change and anthropogenic impacts on marine ecosystems and countermeasures in China. Adv Clim Chang Res 6:118–125

    Article  Google Scholar 

  • Johnson J, Stevens I (2000) A fine resolution model of the eastern North Atlantic between the Azores, the Canary Islands and the Gibraltar Strait. Deep-Sea Res I 47:875–899

    Article  Google Scholar 

  • Kappel CV (2005) Losing pieces of puzzle: threats to marine, estuarine, and diadromous species. Front Ecol Environ 3:275–282

    Article  Google Scholar 

  • Kingsford M, Battershill C (1998) Studying temperate marine environments: a handbook for ecologists. In: Canterbury University press. Christchurch, New Zealand

    Google Scholar 

  • Klügel A, Schwarz S, Bogaard P, Hoernle K, Wohlgemuth-Ueberwasser CC, Köster J (2009) Structure and evolution of the volcanic rift zone at Ponta de São Lourenço, eastern Madeira. Bull Volcanol 71:671–685

    Article  Google Scholar 

  • Kohler KE, Gill SM (2006) Coral point count with excel extensions (CPCe): a visual basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32:1259–1269

    Article  Google Scholar 

  • Ledoyer M (1967) Aperçu sur la faune vagile de quelques biotopes de l’archipel de Madère Comparaison avec les biotopes Mediterraneens homologues. Arq Mus Bocage (Serie 2) 1:415–424

  • Levring T (1974) The marine algae of the archipelago of Madeira. Bol Mus Mun Funchal 28:5–111

    Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • McCay BJ, Jones PJS (2011) Marine protected areas and the governance of marine ecosystems and fisheries. Conserv Biol 25:1130–1133

    Article  Google Scholar 

  • McLeod E, Salm R, Green A, Almany J (2009) Designing marine protected area networks to address the impacts of climate change. Front Ecol Environ 7:362–370

    Article  Google Scholar 

  • Micheli F, Benedetti-Cecchi L, Gambaccini S, Bertocci I, Borsini C, Osio GC, Romano F (2005) Cascading human impacts, marine protected areas, and the structure of Mediterranean reef assemblages. Ecol Monogr 75:81–102

    Article  Google Scholar 

  • Miller RJ, Adams AJ, Ebersole JP, Ruiz E (2007) Evidence for positive density-dependent effects in recovering Diadema antillarum populations. J Exp Mar Biol Ecol 349:215–222

    Article  Google Scholar 

  • Mortensen T (1940) A monograph of the Echinoidea III, 1 Aulodonta. CA Reitzel, Copenhagen

    Google Scholar 

  • Nettleton JC (2012) Tracking environmental trends in the Great Bay estuarine system: an examination of water quality and nuisance macroalgal blooms. In: PhD Thesis. University of New Hampshire, Durham

    Google Scholar 

  • New AL, Jia Y, Coulibaly M, Dengg J (2001) On the role of the Azores current in the ventilation of the North Atlantic Ocean. Prog Oceanogr 48:163–194

    Article  Google Scholar 

  • Oliveira P, Pereira PT (2008) Who values what in a tourism destination? The case of Madeira Island. Tour Econ 14:155–168

    Article  Google Scholar 

  • Paine RT (1980) Food webs, linkage, interaction strength, and community infrastructure. J Anim Ecol 49:667–685

    Article  Google Scholar 

  • Palomo I, Martín-López B, Potschin M, Haines-Young R, Montes C (2013) National Parks, buffer zones and surrounding lands: mapping ecosystem service flows. Ecosyst Serv 4:104–116

    Article  Google Scholar 

  • Pawlik J (1992) Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr Mar Biol Annu Rev 30:273–335

    Google Scholar 

  • Pinnegar JK, Polunin NVC, Francour P, Badalamenti F, Chemello R, Harmelin-Vivien ML, Hereu B, Milazo M, Zabala M, D’Anna G, Pipitone C (2000) Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management. Environ Conserv 27:179–200

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/. Accessed 11 Nov 2017

  • Ribeiro C (2008) Comparison of rocky reef fish communities among protected, unprotected and artificial habitats in Madeira Island coastal waters using underwater visual techniques. PhD thesis, Universidade de Lisboa, Portugal

  • Ribeiro C, Almeida AJ, Araújo R, Biscoito M, Freitas M (2005) Fish assemblages of Cais do Carvão Bay (Madeira Island) determined by the visual census technique. J Fish Biol 67:1568–1584

    Article  Google Scholar 

  • Roberts CM, Hawkins JP, Gell FR (2005) The role of marine reserves in achieving sustainable fisheries. Philos Trans Royal Soc B Biol Sci 360:123–132

    Article  Google Scholar 

  • Sala E (2004) The past and present topology and structure of Mediterranean subtidal rocky-shore food webs. Ecosystems 7:333–340

    Article  Google Scholar 

  • Sala E, Boudouresque CF, Harmelin-Vivien ML (1998) Fishing, trophic cascades, and the structure of algal assemblages: evaluation of an old but untested paradigm. Oikos 82:425–439

    Article  Google Scholar 

  • Sala I, Caldeira RMA, Estrada-Allis SN, Froufe E, Couvelard X (2013) Lagrangian transport pathways in the Northeast Atlantic and their environmental impact. Limnol Oceanog Fluids Environ 3:40–60

    Article  Google Scholar 

  • Salm RV, Clarck J, Siirila E (2000) Marine and coastal protected areas: a guide for planners and managers. IUCN, Washington DC

    Book  Google Scholar 

  • Sandrini-Neto L, Camargo MG (2010) GAD: an R package for ANOVA designs from general principles. http://www.r-project.org. Accessed 27 Oct 2017

  • Sangil C, Clemente S, Martín-García L, Hernández JC (2012) No-take areas as an effective tool to restore urchin barrens on subtropical rocky reefs. Estuar Coast Shelf Sci 112:207–215

    Article  Google Scholar 

  • Sangil C, Martins GM, Hernández JC, Alves F, Neto AI, Ribeiro C et al (2018) Shallow subtidal macroalgae in the North-Eastern Atlantic archipelagos (Macaronesian region): a spatial approach to community structure. Eur J Phycol 53:83–98

    Article  Google Scholar 

  • Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M et al (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57:573–583

    Article  Google Scholar 

  • Stachowicz JJ, Fried H, Osman RW, Whitlatch R (2002) Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83:2575–2590

    Article  Google Scholar 

  • Tegner MJ, Dayton PK (2000) Ecosystem effects of fishing in kelp forest fishing in kelp forest communities. ICES J Mar Sci 57:579–589

    Article  Google Scholar 

  • Tuya F, Boyra A, Sánchez-Jerez P, Barbera C, Haround RJ (2004a) Relationships between rocky-reef fish assemblages, the sea urchin Diadema antillarum and macroalgae throughout the Canarian archipelago. Mar Ecol Prog Ser 278:157–169

    Article  Google Scholar 

  • Tuya F, Boyra A, Sánchez-Jerez P, Barbera C, Haroun RJ (2004b) Can one species determine the structure of the benthic community on a temperate rocky reef? The case of the long-spined sea-urchin Diadema antillarum (Echinodermata: Echinoidea) in the eastern Atlantic. Hydrobiologia 519:211–214

    Article  Google Scholar 

  • Tuya F, Haroun R, Boyra A, Sánchez-Jerez P (2005) Sea urchin Diadema antillarum: different functions in the structure and dynamics of reefs on both sides of the Atlantic. Mar Ecol Prog Ser 302:307–310

    Article  Google Scholar 

  • Tuya F, Cisneros-Aguirre J, Ortega-Borges L, Haroun RJ (2007) Bathimetric segregation of sea urchins on reefs on the Canarian archipelago: role of flow-induce forces. Estuar Coast Shelf Sci 73:481–488

    Article  Google Scholar 

  • Wirtz P (2007) The return of the yellow grouper - annual migration and return to the same site by a xanthistic Mycteroperca fusca (Pisces Serranidae). Aqua Intern J Ichthyol 13:31–34

    Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall, London

    Google Scholar 

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Acknowledgments

We thank Catarina Alves, Jorge Alves, Luís Dias, Cláudia Delgado, Helena Kaufmann, and Filipe Henriques for their collaboration during the sampling surveys, and Serviço do Parque Natural da Madeira (as IFCN since 2016) and Frente MarFunchal for logistical support. This study was partially supported by the Oceanic Observatory of Madeira for funding the CR postdoctoral grant throughout the project M1420-01-0145-FEDER-000001-OOM, and by ARDITI - Madeira’s Regional Agency for the Development of Research, Technology and Innovation, for funding the FA and IG postdoctoral grants throughout the Project Madeira M1420-09-5369-FSE-000001. JCC was supported by a starting grant in the framework of the 2014 FCT Investigator Programme (IF/01606/2014/CP1230/CT0001).

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Authors and Affiliations

  1. MARE, Marine and Environmental Sciences Centre, Quinta do Lorde Marina, Caniçal, Madeira, Portugal

    Filipe Alves, João Canning-Clode & Ignacio Gestoso

  2. CIIMAR-Madeira, Interdisciplinary Centre of Marine and Environmental Research of Madeira, Funchal, Madeira, Portugal

    Filipe Alves, Cláudia Ribeiro & Manfred Kaufmann

  3. OOM, Oceanic Observatory of Madeira, Madeira Tecnopolo, Funchal, Portugal

    Filipe Alves & Cláudia Ribeiro

  4. Department of Oceanography and Fisheries, IMAR, Centre of the University of the Azores, Horta, Azores, Portugal

    João Canning-Clode

  5. Smithsonian Environmental Research Center, Edgewater, NJ, USA

    João Canning-Clode & Ignacio Gestoso

  6. CCMAR, Centro de Ciências do Mar, Campus de Gambelas, Faro, Portugal

    Cláudia Ribeiro

  7. Faculty of Life Sciences, Marine Biology Station of Funchal, University of Madeira, Funchal, Portugal

    Manfred Kaufmann

  8. CIIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Porto, Portugal

    Manfred Kaufmann

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  1. Filipe Alves
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  2. João Canning-Clode
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  4. Ignacio Gestoso
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Correspondence to Filipe Alves.

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Alves, F., Canning-Clode, J., Ribeiro, C. et al. Local benthic assemblages in shallow rocky reefs find refuge in a marine protected area at Madeira Island. J Coast Conserv 23, 373–383 (2019). https://doi.org/10.1007/s11852-018-0669-y

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