Marine Biodiversity

, Volume 49, Issue 6, pp 2709–2723 | Cite as

Intertidal assemblages across boulders and rocky platforms: a multi-scaled approach in a subtropical island

  • Eva CacabelosEmail author
  • Ignacio Gestoso
  • Patrício Ramalhosa
  • Léa Riera
  • Ana I. Neto
  • João Canning-Clode
Original Paper


Rocky intertidal communities have proved to be tractable systems for experimental ecology, contributing much to our general understanding of population and community ecology. Physical environmental factors are usually considered strong structuring elements for these assemblages. In this study, we adopted a mixed model sampling design to study the effects of substratum type and shore orientation (i.e. different wave exposure) on intertidal assemblages of Madeira Island (NE Atlantic) across time. We included both macrofauna and macroalgae and compare their abundance and distribution in boulders and rocky platforms on north and south coasts of the island. Generally, assemblages moderately differed between boulders and rocky platforms whereas orientation had little influence on the distribution of most taxa. A high variability was observed across a range of spatial and temporal scales, suggesting that interactions of both physical variables and biological parameters may be influencing distribution of intertidal organisms. The results obtained provide pioneer quantitative data on intertidal assemblages of Madeira.


Madeira Hierarchical design Substratum type Hydrodynamics Benthos Macroalgae Gastropods Intertidal communities Functional groups 



Authors are grateful to Nahir Abraín and Lurdes Ferreira for their assistance during field surveys and to Drs. Gustavo Martins and Juan Moreira for their helpful comments. Finally, this study had the support of Fundação para a Ciência e Tecnologia (FCT), through the strategic project UID/MAR/04292/2019 granted to MARE. The manuscript was substantially improved through the comments and suggestions of two anonymous reviewers. This is contribution #42 from the Smithsonian’s MarineGEO network.

Funding information

EC and IG were financially supported by post-doctoral grants in the framework of the 2015 ARDITI Grant Programme Madeira 14-20 (Project M1420-09-5369-FSE-000001). PR was financially supported by the Oceanic Observatory of Madeira Project (M1420-01-0145-FEDER-000001-Observatório Oceânico da Madeira-OOM), co-financed by the Madeira Regional Operational Programme (Madeira 14-20), under the Portugal 2020 strategy, through the European Regional Development Fund (ERDF). JCC was supported by a starting grant in the framework of the 2014 FCT Investigator Programme (IF/01606/2014/CP1230/CT0001). Additional funding was provided from National Funds through FCT-Fundação para a Ciência e a Tecnologia, under the projects UID/BIA/00329/2013, 2015-2018 and UID/BIA/00329/2019, and DRCT-M1.1.a/005/Funcionamento-C/2016.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

No animal testing was performed during this study.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable.

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Supplementary material

12526_2019_1000_MOESM1_ESM.docx (43 kb)
ESM 1 (DOCX 42 kb)
12526_2019_1000_Fig9_ESM.png (233 kb)
Fig. S1

Low level. a, Mean (+SE, per quadrat) number of Patella spp. across locations and sampling times, and b, across sites (showing differences between the substratum types (for further details see Tables S1 and S2). (PNG 233 kb)

High Resolution Image (TIF 49 kb)
12526_2019_1000_Fig10_ESM.png (467 kb)
Fig. S2

Mid level. Mean (+SE, per quadrat) a, cover of sessile organisms across time showing differences between the substratum types, b, across locations, showing differences between the substratum types, and c, total number of motile fauna across sites, showing differences between the substratum types. (PNG 466 kb)

High Resolution Image (TIF 117 kb)
12526_2019_1000_Fig11_ESM.png (239 kb)
Fig. S3

Mid level. Mean (+SE, per quadrat) cover of Chthamalus, a, across locations, and, b, across time, showing differences between the substratum types, and c, number of Melarhaphe across sites, showing differences between the substratum types. (PNG 239 kb)

High Resolution Image (TIF 54 kb)
12526_2019_1000_Fig12_ESM.png (350 kb)
Fig. S4

High level. Mean (+SE, per quadrat) a, total counts of motile fauna, and b, cover of sessile organisms across time, showing differences between the substratum types and orientations, c, number of taxa, d, number of Phorcus and, e, Melarhaphe across locations and sampling times showing differences between the substratum types. (PNG 350 kb)

High Resolution Image (TIF 68 kb)


  1. Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of varianceGoogle Scholar
  2. Anderson MJ (2014) Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef Stat Ref Online:1–15Google Scholar
  3. Arrontes J (1999) On the evolution of interactions between marine mesoherbivores and algae. Bot Mar 42:137e155Google Scholar
  4. Benedetti-Cecchi L, Acunto S, Bulleri F, Cinelli F (2000) Population ecology of the barnacle Chthamalus stellatus in the Northwest Mediterranean. Mar Ecol Prog Ser 198:157–170Google Scholar
  5. Benedetti-Cecchi L, Pannacciulli F, Bulleri F, Moschella PS, Airoldi L, Relini G, Cinelli F (2001) Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Mar Ecol Prog Ser 214:137–150Google Scholar
  6. Benedetti-Cecchi L, Iacopo B, Micheli F, Maggi E, Fosella T, Vaselli S (2003) Implications of spatial heterogeneity for management of marine protected areas (MPAs): examples from assemblages of rocky coasts in the Northwest Mediterranean. Mar Environ Res 55:429–458PubMedGoogle Scholar
  7. Bertness MD, Callaway R (1994) Positive interaction in communities. Trends Ecol Evol 9:191–193Google Scholar
  8. Bornet E (1892) Les algues de P.-K.-a. Schousboe. Mémoires de la Société des Sciences Naturelles et Mathématiques de Cherbourg 28:165–376Google Scholar
  9. Branch GM, Thompson RC, Crowe TP, Castilla JC, Langmead O, Hawkins SJ (2008) Rocky intertidal shores: prognosis for the future. In: Polunin N (ed) Aquatic ecosystems. Cambridge University Press, Trends and Global Prospects, pp 209–225Google Scholar
  10. Bustamante RH, Branch GM, Eekhout S (1997) The influences of physical factors on the distribution and zonation patterns of south African rocky-shore communities. South African J Mar Sci 18:119–136Google Scholar
  11. Cacabelos E, Martins GM, Thompson R, Prestes ACL, Azevedo JMN, Neto AI (2016) Material type and roughness influence structure of inter-tidal communities on coastal defenses. Mar Ecol 37:801–812Google Scholar
  12. Caldeira RMA, Groom S, Miller P, Pilgrim D, Nezlin NP (2002) Sea-surface signatures of the island mass effect phenomena around Madeira Island, Northeast Atlantic. Remote Sens Environ 80:336–360Google Scholar
  13. Chapman MG, Tolhurst TJ, Murphy RJ, Underwood AJ (2010) Complex and inconsistent patterns of variation in benthos, micro-algae and sediment over multiple spatial scales. Mar Ecol Prog Ser 398:33–47Google Scholar
  14. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, PRIMER-E. edGoogle Scholar
  15. Connolly RM, Roughgarden J (1999) Theory of marine communities: competition, predation, and recruitment-dependent interaction strength. Ecol Monogr 66:277–296Google Scholar
  16. Cruz-Motta JJ (2007) Análisis espacial de las comunidades tropicales intermareales asociadas a los litorales rocosos de Venezuela. Ciencias Marinas 33(2):133–148Google Scholar
  17. Daudin FM (1800) Receuil de mémoires et de notes sur des espèces inédites ou peu connues de Mollusques, de vers et de zoophytes. xviii & 19-50. Fuchs & Treuttel et Wurtz. ParisGoogle Scholar
  18. de Vasconcelos ERTPP, Vasconcelos JB, Reis TN, Concentino ALM, Mallea AJA, Martins GM, Neto AI, Fujii MT (2019) Macroalgal responses to coastal urbanization: relative abundance of indicator species. J Appl Phycol 31(2):893–903Google Scholar
  19. Ferreira S (2011) Contributo para o estudo das Macroalgas do Intertidal da ilha da Madeira. Diversidade, Distribuição e Sazonalidade. Dissertação de mestrado, Universidade da Madeira, Portugal, 112 ppGoogle Scholar
  20. Firth LB, Thompson RC, White FJ, Schofield M, Skov MW, Hoggart SPG, Jackson J, Knights AM, Hawkins SJ (2013) The importance of water-retaining features for biodiversity on artificial intertidal coastal defence structures. Divers Distrib 19:1275–1283Google Scholar
  21. Fraschetti S, Terlizzi A, Benedetti-Cecchi L (2005) Patterns of distribution of marine assemblages from rocky shores: evidence of relevant scales of variation. Mar Ecol Prog Ser 296:13–29Google Scholar
  22. Gaspar R, Pereira L, Neto JM (2017) Intertidal zonation and latitudinal gradients on macroalgal assemblages: species, functional groups and thallus morphology approaches. Ecol Indic 81:90–103Google Scholar
  23. Griffin JN, Jenkins SR, Gamfeldt L, Jones D, Hawkins SJ, Thompson RC (2009) Spatial heterogeneity increases the importance of species richness for an ecosystem process. Oikos 118:1335–1342Google Scholar
  24. Hawkins SJ, Corte-Real HBSM, Pannacciulli FG, Weber LC, Bishop JDD (2000) Thoughts on the ecology and evolution of the intertidal biota of the Azores and other Atlantic islands. Hydrobiologia 440:3–17Google Scholar
  25. Hawkins SJ, Moore PJ, Burrows MT, Poloczanska E, Mieszkowska N et al (2008) Complex interactions in a rapidly changing world: responses of rocky shore communities to recent climate change. Clim Res 37:123–133Google Scholar
  26. Jenkins SR (2005) Larval habitat selection, not larval supply, determines settlement patterns and adult distribution in two chthamalid barnacles. J Anim Ecol 74:893–904Google Scholar
  27. King PP (1832) Description of the Cirrhipeda, Conchifera and Mollusca, in a collection formed by the officers of H.M.S. adventure and beagle employed between the years 1826 and 1830 in surveying the southern coasts of South America, including the straits of Magalhaens and the coast of Tierra del Fuego. Zool J 5:332–349Google Scholar
  28. Kohler KE, Gill S (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 32:1259–1269Google Scholar
  29. Kroeker KJ, Gambi MC, Micheli F (2013) Community dynamics and ecosystem simplification in a high-CO2 ocean. Proc Natl Acad Sci 110:12721–12726PubMedGoogle Scholar
  30. Kützing FT (1843) Phycologia generalis: oder Anatomie. Physiologie und Systemkunde der tange. 458 ppGoogle Scholar
  31. Lamouroux JVF (1809) Observations sur la physiologie des algues marines, et description de cinq nouveaux genres de cette famille. N Bull Soc phil Paris 1(20):330–333Google Scholar
  32. Lamouroux JVF (1812) Extrait d'un mémoire sur la classification des polypiers coralligènes non entièrement pierreux. N Bull Soc phil Paris 3:181–188Google Scholar
  33. Le Hir M, Hily C (2005) Macrofaunal diversity and habitat structure in intertidal boulder fields. Biodivers Conserv 14:233Google Scholar
  34. Leclerc JC (2018) Patterns of spatial variability between contrasting substrata: a boulder-field study. Mar Ecol Prog Ser 597:23–38Google Scholar
  35. Linnaeus C (1753) Species plantarum, exhibentes plantas rite cognitas ad genera relatas cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. StockholmGoogle Scholar
  36. Linnaeus C (1758) Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Editio decima, reformata. Laurentius Salvius: Holmiae. 824 ppGoogle Scholar
  37. Linnaeus C (1767) Systema naturae per regna tria naturae: secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Laurentii Salvii. 1327 ppGoogle Scholar
  38. Little C, Kitching JA (1996) The biology of rocky shores. Oxford University Press, LondonGoogle Scholar
  39. Lubchenco J, Olson A, Brubaker L, Carpenter SR, Holland MM (1991) The sustainable biosphere initiative: an ecological research agenda. Ecology 72:371–412Google Scholar
  40. Maggi E, Cappiello M, Del Corso A, Lenzarini F, Peroni E, Benedetti-Cecchi L (2016) Climate-related environmental stress in intertidal grazers: scaling-up biochemical responses to assemblage-level processes. PeerJ4:e2533Google Scholar
  41. Martins GM, Thompson RC, Hawkins SJ, Neto AI, Jenkins SR (2008) Rocky intertidal community structure in oceanic islands: scales of spatial variability. Mar Ecol Prog Ser 345:15–24Google Scholar
  42. Martins GM, Amaral AF, Wallenstein FM, Neto AI (2009) Influence of a breakwater on nearby rocky intertidal community structure. Mar Environ Res 67PubMedGoogle Scholar
  43. Martins GM, Prestes ACL, Neto AI (2013a) Population structure in high shore littorinids: contrast between riprap and rocky shores. World Congress of Malacology, Ponta DelgadaGoogle Scholar
  44. Martins GM, Patarra RF, Álvaro NV, Prestes ACL, Neto AI (2013b) Effects of coastal orientation and depth on the distribution of subtidal benthic assemblages. Mar Ecol 34:289–297Google Scholar
  45. Martins GM, Neto AI, Cacabelos E (2016) Ecology of a key ecosystem engineer on hard coastal infrastructure and natural rocky shores. Mar Environ Res 113:88–94PubMedGoogle Scholar
  46. McGuinness KA (1987) Disturbance and organisms on boulders - I. patterns in the environment and the community. Oecologia 71(3):409–419PubMedGoogle Scholar
  47. McGuinness KA, Underwood AJ (1986) Habitat structure and the nature of communities on intertidal boulders. J Exp Mar Bio Ecol 104:97–123Google Scholar
  48. McQuaid C, Branch G (1984) Influence of sea temperature, substratum and wave exposure on rocky intertidal communities: an analysis of faunal and floral biomass. Mar Ecol Prog Ser 19:145–151Google Scholar
  49. Menge BA, Daley BA, Lubchenco J, Sanford E, Dahlhoff E, Halpin PM, Hudson G, Burnaford JL (1999) Top-down and bottom-up regulation of New Zealand rocky interdial communities. Ecol Monogr 69:297–330Google Scholar
  50. Menge BA, Lubchenco J, Bracken MES, Chan F, Foley MM, Freldenberg TL, Gaines SD, Hudson G, Krenz C, Leslie H, Menge DNL, Russell R, Webster MS (2003) Coastal oceanography sets the pace of rocky intertidal community dynamics. Proc Natl Acad Sci USAmerica 100:12229–12234Google Scholar
  51. Miller LP, Harley CDG, Denny MW (2009) The role of temperature and desiccation stress in limiting the local-scale distribution of the owl limpet, Lottia gigantea. Funct Ecol 23(4):756–767Google Scholar
  52. Molina-Montenegro MA, Muñoz AA, Badano EI, Morales BW, Fuentes KM, Cavieres LA (2005) Positive associations between macroalgal species in a rocky intertidal zone and their effects on the physiological performance of Ulva lactuca. Mar Ecol 292:173–180Google Scholar
  53. Nardo GD (1834) De novo genere Algarum cui nomen est Hildbrandtia prototypus. Isis von Oken 1834:675–676Google Scholar
  54. Neto AI (2000) Ecology and dynamics of two intertidal algal communities on the littoral of the island of São Miguel (Azores). Hydrobiologia 432:135–147Google Scholar
  55. Neto AI (2001) Macroalgal species diversity and biomass of subtidal communities of São Miguel (Azores). Helgol Mar Res 55:101–111Google Scholar
  56. Neto AI, Tittley I (1995) Structure and zonation of algal turf communities on the Azores: an numerical approach. Bol Mus Mun Funchal 4:487–504Google Scholar
  57. Poli JX (1791) Testacea vtrivsqve Siciliae eorvmqve historia et anatome tabvlis aeneis illvstrata. Ex Regio Typographeio, Parmae 5:1–303Google Scholar
  58. Risso A (1826-1827). Histoire naturelle des principales productions de l'Europe Méridionale et particulièrement de celles des environs de Nice et des Alpes Maritimes. Paris, Levrault 3(XVI): 1-480Google Scholar
  59. Robles CD, Alvarado MA, Desharnais RA (2001) The shifting balance of littoral predator-prey interaction in regimes of hydrodynamic stress. Oecologia 128:142–152PubMedGoogle Scholar
  60. Sangil C, Martins G, Hernández J, Alves F, Neto AI, Ribeiro C, León-Cisneros K, Canning-Clode J, Rosas-Alquicira E, Mendoza J, Tittley I, Wallenstein F, Couto RP, Kaufmann M (2018) Shallow subtidal macroalgae in the North-Eastern Atlantic archipelagos (Macaronesian region): a spatial approach to community structure. Eur J Phycol 53Google Scholar
  61. Sanz-Lázaro C (2016) Climate extremes can drive biological assemblages to early successional stages compared to several mild disturbances. Sci Rep 6:1–9Google Scholar
  62. Scherner F, Antunes Horta P, Cabral de Oliveira E, Simonassi JC, Hall-Spencer JM, Chow F, Nunes JMC, Barreto Pereira SM (2013) Coastal urbanization leads to remarkable seaweed species loss and community shifts along the SW Atlantic. Mar Pollut Bull 76:106–115PubMedGoogle Scholar
  63. Simpson TJS, Smale DA, McDonald JI, Wernberg T (2017) Large scale variability in the structure of sessile invertebrate assemblages in artificial habitats reveals the importance of local-scale processes. J Exp Mar Bio Ecol 494:10–19Google Scholar
  64. Sousa R, Vasconcelos J, Henriques P, Pinto AR, Delgado J, Riera R (2019) Long-term population status of two harvested intertidal grazers (Patella aspera and Patella candei), before (1996–2006) and after (2007–2017) the implementation of management measures. J Sea Res 144:33–38Google Scholar
  65. Steneck RS, Dethier MN (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498Google Scholar
  66. Stephenson TA, Stephenson A (1949) The universal features of zonation between the tidemarks on rocky coasts. J Ecol 38:289–305Google Scholar
  67. Thompson TL, Glenn EP (1994) Plaster standards to measure water motion. Limnol Oceanogr 39:1768–1779Google Scholar
  68. Thompson RC, Wilson BJ, Tobin ML, Hill AS, Hawkins SJ (1996) Biologically generated habitat provision and diversity of rocky shore organisms at a hierarchy of spatial scales. J Exp Mar Bio Ecol 202:73–84Google Scholar
  69. Thompson RC, Crowe TP, Hawkins SJ (2002) Rocky intertidal communities: past environmental changes, present status and predictions for the next 25 years. Environ Conserv 29:168–191Google Scholar
  70. Tomanek L, Helmuth B (2002) Physiological ecology of rocky intertidal organisms: a synergy of concepts. Integr Comp Biol 42:771–775PubMedGoogle Scholar
  71. Tucker L, Griffiths CL, Schroeter F, Vetter HD (2017) Boulder shores in South Africa – a distinct but poorly documented coastal habitat type. Afr J Mar Sci 39(2):193–202Google Scholar
  72. Tuya F, Haroun RJ (2006) Spatial patterns and response to wave exposure of shallow water algal assemblages across the Canarian archipelago: a multiscaled approach. Mar Ecol Prog Ser 311:15–28Google Scholar
  73. Underwood AJ (1980) The effects of grazing by gastropods and physical factors on the upper limits of distribution of intertidal macroalgae. Oecologia 46:201–213PubMedGoogle Scholar
  74. Underwood AJ (1997) Experiments in ecology. Cambridge University Press, CambridgeGoogle Scholar
  75. Underwood AJ (2000) Experimental ecology of rocky intertidal habitats what are we learning? J Exp Mar Bio Ecol 250:51–76PubMedGoogle Scholar
  76. Underwood AJ, Chapman MG, Connell SD (2000) Observation in ecology: you can’t make progress on process without understanding the patterns. J Exp Mar Bio Ecol 20:97–115Google Scholar
  77. Veiga P, Rubal M, Vieira R, Arenas F, Sousa-Pinto I (2013) Spatial variability in intertidal macroalgal assemblages on the north Portuguese coast: consistence between species and functional group approaches. Helgol Mar Res 67:191–201Google Scholar
  78. Wallenstein FM, Neto AI (2006) Intertidal rocky shore biotopes of the Azores: a quantitative approach. Helgol Mar Res 60:196–206Google Scholar
  79. Wallenstein FM, Neto AI, Álvaro NV, Santos CI (2008) Algae-based biotopes of the Azores (Portugal): spatial and seasonal variation. Aquat Ecol 42:547–559Google Scholar
  80. Williams SL, Bracken MES, Jones E (2013) Additive effects of physical stress and herbivores on intertidal seaweed diversity. Ecology 94:1089–1101PubMedGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung 2019

Authors and Affiliations

  1. 1.MARE–Marine and Environmental Sciences CentreQuinta do Lorde MarinaCaniçalPortugal
  2. 2.cE3c–Centre for Ecology, Evolution and Environmental Changes/Azorean Biodiversity Group, Faculty of Sciences and Technology, Department of BiologyUniversity of AzoresAzoresPortugal
  3. 3.Smithsonian Environmental Research CenterEdgewaterUSA
  4. 4.OOM—Oceanic Observatory of MadeiraAgência Regional para o Desenvolvimento da Investigação Tecnologia e InovaçãoFunchalPortugal
  5. 5.Faculté des SciencesUniversité Montpellier IIMontpellierFrance
  6. 6.Centre of IMAR of the University of the AzoresHortaPortugal

Personalised recommendations