, Volume 818, Issue 1, pp 211–222 | Cite as

Adding early-stage engineering species affects advanced-stage organization of shallow-water fouling assemblages

  • Edson A. Vieira
  • Gustavo M. Dias
  • Augusto A. V. Flores
Primary Research Paper


Although commonly overlooked, processes determining early patterns of species assembly may affect community dynamics and diversity at advanced states. In this study, we followed richness and community structure in experimental units pioneered by single or multiple species, within a given functional group—colonial ascidians, arborescent, and encrusting bryozoans. We tested the hypotheses that richness and community structure are positively affected by founder-richness at more advanced stages, and that such effect may depend on the functional traits of founders (more or less prone to facilitate other species). More diverse founding assemblages of arborescent bryozoans led to richer communities after 1 and 5 months of succession, with no effects observed for the other functional groups. Assemblages started by a single species were dominated by space monopolizers (encrusting bryozoans), while the ones founded by two species were characterized by a higher abundance of engineering forms (arborescent bryozoans), which may provide a physically complex substrate suitable to both the attraction and protection of other species recruits. Both effects on advanced-stage richness and community structure reflect the importance of facilitation through founder diversity and functionality in community organization.


Historical contingency Ecologic function Facilitation Competition Diversity 



The authors thank the Staff at Centro de Biologia Marinha (CEBIMar-USP) and Yacht Club Ilhabela (YCI) for field assistance. Marcel O. Tanaka, Guilherme H. Pereira Filho, Rafael S. Oliveira, José R. Trigo, Fabiane Gallucci and two anonymous reviewers provided helpful suggestions on early versions of this manuscript. EAV thanks Fundação de Amparo à Pesquisa do Estado de São Paulo – FAPESP (Process #2012/18432-1) for the Award of a PhD Scholarship. This is a contribution of the Research Centre for Marine Biodiversity of the University of São Paulo (NP – Biomar/USP).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10750_2018_3612_MOESM1_ESM.docx (21 kb)
Supplementary material 1 (DOCX 21 kb)
10750_2018_3612_MOESM2_ESM.docx (23 kb)
Supplementary material 2 (DOCX 23 kb)
10750_2018_3612_MOESM3_ESM.docx (18 kb)
Supplementary material 3 (DOCX 18 kb)


  1. Adler, P. B., J. HilleRisLambers & J. M. Levine, 2007. A niche for neutrality. Ecology Letters 10: 95–104.CrossRefPubMedGoogle Scholar
  2. Allisson, G., 2004. The influence of species diversity and stress intensity on community resistance and resilience. Ecological Monographs 74: 117–134.CrossRefGoogle Scholar
  3. Almany, G. R., 2004. Priority effects in coral reef fish communities of the Great Barrier Reef. Ecology 85: 2872–2880.CrossRefGoogle Scholar
  4. Anderson, M. J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46.Google Scholar
  5. Beisner, B. E., D. T. Hyadon & K. Cuddington, 2003. Alternative stable states in ecology. Frontiers in Ecology and Environment 1: 376–382.CrossRefGoogle Scholar
  6. Breitburg, D. L., 1985. Development of a subtidal epibenthic community: factors affecting species composition and the mechanisms of succession. Oecologia 65: 173–184.CrossRefPubMedGoogle Scholar
  7. Bruno, J. F., J. J. Stachowicz & M. D. Bertness, 2003. Inclusion of facilitation into ecological theory. Trends in Ecology and Evolution 18: 119–125.CrossRefGoogle Scholar
  8. Bulleri, F., 2009. Facilitation research in marine systems: state of the art, emerging patterns and insights for future developments. Journal of Ecology 97: 1121–1130.CrossRefGoogle Scholar
  9. Bulleri, F. & M. G. Chapman, 2010. The introduction of coastal infrastructure as a driver of changes in marine environments. Journal of Applied Ecology 47: 26–35.CrossRefGoogle Scholar
  10. Cardinale, B. J., K. Nelson & M. A. Palmer, 2000. Linking species diversity to the functioning of ecosystems: on the importance of environmental context. Oikos 91: 175–183.CrossRefGoogle Scholar
  11. Carlton, J. T. & J. B. Geller, 1993. Ecological Roulette – the global transport of nonindigenous marine organisms. Science 261: 78–82.CrossRefGoogle Scholar
  12. Chang, C. & D. Marshall, 2017. Quantifying the role of colonization history and biotic interactions in shaping communities – a community transplant approach. Oikos 126: 204–211.CrossRefGoogle Scholar
  13. Chase, J. M., 2007. Drought mediates the importance of stochastic community assembly. Oecologia 104: 17430–17434.Google Scholar
  14. Chase, J. M. & J. A. Myers, 2011. Disentangling the importance of ecological niches from stochastic processes across scales. Philosophical Transactions of the Royal Society B 366: 2351–2363.CrossRefGoogle Scholar
  15. Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in community structure. Austral Ecology 18: 117–143.CrossRefGoogle Scholar
  16. Connell, J. H. & R. O. Slatyer, 1977. Mechanisms of succession in natural communities and their role in community stability and organization. American Naturalist 111: 1119–1144.CrossRefGoogle Scholar
  17. Dahms, H., S. Dobretsov & P. Qian, 2004. The effect of bacterial and diatom biofilms on the settlement of the bryozoan Bugula neritina. Journal of the Experimental Marine Biology and Ecology 313: 191–209.CrossRefGoogle Scholar
  18. De Meester, L., J. Vanoverbeke, L. J. Kilsdonk & M. C. Urban, 2016. Evolving perspectives on monopolization and priority effects. Trends in Ecology and Evolution 31: 136–146.CrossRefPubMedGoogle Scholar
  19. Dean, T. A. & L. E. Hurd, 1980. Development in an estuarine fouling community: the influence of early colonists on later arrivals. Oecologia 46: 295–301.CrossRefPubMedGoogle Scholar
  20. Edmunds, P. J., 2014. Landscape-scale variation in coral reef community structure in the United States Virgin Islands. Marine Ecology Progress Series 509: 137–152.CrossRefGoogle Scholar
  21. Fargione, J. E., C. S. Brown & D. Tilman, 2003. Community assembly and invasion: an experimental test of neutral versus niche processes. Proceedings of the National Academy of Sciences of USA 100: 8916–8920.CrossRefGoogle Scholar
  22. Fukami, T., 2015. Historical contingency in community assembling: integrative niches, species pools, and priority effects. Annual Review of Ecology Evolution and Systematics 46: 1–23.CrossRefGoogle Scholar
  23. Griffin, J. N., V. Mendez, A. F. Johnson, S. R. Jenkins & A. Foggo, 2009. Functional diversity predicts overyielding effect of species combination on primary productivity. Oikos 118: 37–44.CrossRefGoogle Scholar
  24. Guillemot, N., M. Kulbicki, P. Chabanet & L. Vigliola, 2011. Functional redundancy patterns reveal non-random assembly rules in a species-rich marine assemblage. PLoS ONE 6: e26735.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hart, D. D., 1992. Community organization in streams: the importance of species interactions, physical factors, and chance. Oecologia 91: 220–228.CrossRefPubMedGoogle Scholar
  26. Hart, S. P. & D. J. Marshall, 2009. Spatial arrangement affects population dynamics and competition independent of community composition. Ecology 90: 1485–1491.CrossRefPubMedGoogle Scholar
  27. Hata, T., J. S. Madin, V. R. Cumbo, M. Denny, J. Figueiredo, S. Harii, C. J. Thomas & A. H. Baird, 2017. Coral larvae are poor swimmers and require fine-scale reef structure to settle. Scientific Reports 7: 2249.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hay, M. E., 2009. Marine chemical ecology: chemical signals and cues structure marine populations, communities and ecosystems. Annual Review of Marine Science 1: 193–212.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hooper, D. U., F. F. Chapin III, J. J. Ewel, A. Hector, P. Inchausti, S. Lavorel, J. H. Lawton, D. M. Lodge, S. Naeem, B. Schmid, H. Setälä, A. J. Symstad, J. Vandermeer & D. A. Wardle, 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75: 3–35.CrossRefGoogle Scholar
  30. Jackson, J. B. C. & L. Buss, 1975. Allelopathy and spatial competition among coral reef invertebrates. Proceedings of the National Academy of Science of USA 72: 5160–5163.CrossRefGoogle Scholar
  31. Jones, C. G., J. H. Lawton & M. Shachak, 1994. Organisms as ecosystem engineers. Oikos 69: 373–386.CrossRefGoogle Scholar
  32. Jurgens, L. & B. Gaylord, 2016. Edge effects reverse facilitation by a widespread foundation species. Scientific Reports. Scholar
  33. Kay, A. M. & M. J. Keough, 1981. Occupation of patches in the epifaunal community on pier pilings and the bivalve Pinna bicolor ar Edithburgh, South Australia. Oecologia 48: 123–130.CrossRefPubMedGoogle Scholar
  34. Keough, M. J., 1984. Kin-recognition and the spatial distribution of larvae of the bryozoan Bugula neritina (L.). Evolution 38: 142–147.CrossRefPubMedGoogle Scholar
  35. Kittelmann, S. & T. Harder, 2005. Species- and site-specific bacterial communities associated with four bryozoans from the North Sea, Germany. Journal of Experimental Marine Biology and Ecology 327: 201–209.CrossRefGoogle Scholar
  36. Klingbeil, B. T. & M. R. Willig, 2016. Community assembly in temperate forest birds: habitat filtering, interspecific interactions and priority effects. Evolutionary Ecology 30: 703–722.CrossRefGoogle Scholar
  37. Koehl, M. A. R., 1982. The interaction of moving water and sessile organisms. Scientific American 274: 124–134.CrossRefGoogle Scholar
  38. Koehl, M. A. R., 1984. How do benthic organisms withstand moving water? American Zoologist 24: 57–70.CrossRefGoogle Scholar
  39. Kondoh, M., 2003. Foraging adaptation and the relationship between food-web complexity and stability. Science 299: 1388–1391.CrossRefPubMedGoogle Scholar
  40. Levine, J. M. & J. HilleRisLambers, 2009. The importance of niches for the maintenance of species diversity. Nature 461: 254–257.CrossRefPubMedGoogle Scholar
  41. Loreau, M., S. Naeem, P. Inchausti, J. Bengtsson & J. P. Grime, 2001. Ecology: biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294: 804–808.CrossRefPubMedGoogle Scholar
  42. MacArthur, R. H., 1972. Geographical Ecology. Harper and How, New York.Google Scholar
  43. Maida, M., P. W. Sammarco & J. C. Coll, 2001. Effects of soft corals on scleratinian coral recruitment. II: allelopathy, spat survivorship and reef community structure. Marine Ecology 22: 397–414.CrossRefGoogle Scholar
  44. Menge, B. A. & J. P. Sutherland, 1987. Community regulation – variation in disturbance, competition, and predation in relation to environmental-stress and recruitment. American Naturalist 130: 730–757.CrossRefGoogle Scholar
  45. Mineur, F., E. J. Coo, D. Minchin, K. Bohn, A. MacLeod & C. A. Maggs, 2012. Changing coasts: marine aliens and artificial structures. Oceanography and Marine Biology 50: 189–233.CrossRefGoogle Scholar
  46. Moore, J. W., J. L. Ruesink & K. A. McDonald, 2004. Impact of supply-side ecology on consumer-mediated coexistence: evidence from a meta-analysis. American Naturalist 163: 480–487.CrossRefPubMedGoogle Scholar
  47. Nandakumar, K., 1996. Importance of timing of panel exposure on the competitive outcome and succession of sessile organisms. Marine Ecology Progress Series 131: 191–203.CrossRefGoogle Scholar
  48. Oricchio, F. T., A. A. V. Flores & G. M. Dias, 2016a. The importance of predation and predator size on the development and structure of a subtropical fouling community. Hydrobiologia 776: 209–219.CrossRefGoogle Scholar
  49. Oricchio, F. T., G. Pastro, E. A. Vieira, A. A. V. Flores, F. Z. Gibran & G. M. Dias, 2016b. Distinct community dynamics at two artificial habitats in a recreational marina. Marine Environmental Research. Scholar
  50. Osman, R. W., 1977. Establishment and development of a marine epi-faunal community. Ecological Monographs 47: 37–63.CrossRefGoogle Scholar
  51. Osman, R. W., P. Munguia, R. B. Witlatch, R. N. Zajac & J. Hamilton, 2010. Thresholds and multiple community states in marine fouling communities: integrating natural history with management strategies. Marine Ecology Progress Series 413: 277–289.CrossRefGoogle Scholar
  52. Paine, R. T., 1966. Food web complexity and species diversity. American Naturalist 100: 65–75.CrossRefGoogle Scholar
  53. Perea, R. & L. Gil, 2014. Shrubs facilitating seedling performance on ungulate-dominated systems: biotic versus abiotic mechanisms of plant facilitation. European Journal of Forest Research 133: 525–534.CrossRefGoogle Scholar
  54. Russ, G. R., 1980. Effects of predation by fishes, competition, and structural complexity of the substratum on the establishment of a marine epifaunal community. Journal of Experimental Marine Biology and Ecology 42: 55–69.CrossRefGoogle Scholar
  55. Sharp, J. H., M. K. Winson, S. Wade, P. Newman, B. Bullimore, K. Lock, M. Burton, R. Gibbs & J. S. Porter, 2008. Differential microbial fouling on the marine bryozoan Pentapora fascialis. Journal of the Marine Biological Association of the United Kingdom 88: 705–710.CrossRefGoogle Scholar
  56. Shea, K. & P. Chesson, 2002. Community ecology theory as a framework for biological invasions. Trends in Ecology and Evolution 17: 170–176.CrossRefGoogle Scholar
  57. Srivastava, D. S. & M. Vellend, 2005. Biodiversity-ecosystem function research: is it relevant to conservation? Annual Review of Ecology, Evolution and Systematics 36: 267–294.CrossRefGoogle Scholar
  58. Stachowicz, J. J., 2001. Mutualism, facilitation and the structure of ecological communities. BioScience 51: 235–246.CrossRefGoogle Scholar
  59. Stachowicz, J. J. & J. E. Byrnes, 2006. Species diversity, invasion success and ecosystem functioning: disentangling the influence of resource competition, facilitation and extrinsic factors. Marine Ecology Progress Series 311: 251–262.CrossRefGoogle Scholar
  60. Stachowicz, J. J., R. B. Whitlatch & R. W. Osman, 1999. Species diversity and invasion resistance in a marine ecosystem. Science 286: 1577–1579.CrossRefPubMedGoogle Scholar
  61. Stachowicz, J. J., H. Fried, R. W. Osman & R. B. Whitlatch, 2002. Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83: 2575–2590.CrossRefGoogle Scholar
  62. Stachowicz, J. J., J. F. Bruno & J. E. Duffy, 2007. Consequences of biodiversity for marine communities and ecosystems. Annual Review of Ecology, Evolution and Systematics 38: 739–766.CrossRefGoogle Scholar
  63. Stachowicz, J. J., M. Graham, M. E. S. Bracken & A. I. Szoboszlai, 2008. Diversity enhances cover and stability of seaweed assemblages: the role of heterogeneity and time. Ecology 89: 3008–3019.CrossRefGoogle Scholar
  64. Stoecker, D., 1980. Relationships between chemical defense and ecology in benthic ascidians. Marine Ecology Progress Series 3: 257–265.CrossRefGoogle Scholar
  65. Sutherland, J. P., 1978. Functional roles of Schizoporella and Styela in the fouling community at Beaufort North Carolina. Ecology 59: 257–264.CrossRefGoogle Scholar
  66. Sutherland, J. P. & R. H. Karlson, 1977. Development and stability of the fouling community at Beaufort, North Carolina. Ecological Monographs 47: 425–446.CrossRefGoogle Scholar
  67. Tilman, D., 2001. Functional diversity. In Levin, S. A. (ed.), Encyclopedia of Biodiversity. Academic, San Diego.Google Scholar
  68. Trowbridge, W. B., 2007. The role of stochasticity and priority effects in floodplain restoration. Ecological Applications 17: 1312–1324.CrossRefPubMedGoogle Scholar
  69. Valdivia, N., K. de la Haye, S. R. Jenkins, S. A. Kimmance, R. C. Thompson & M. Molis, 2008. Functional composition, but not richness, affected the performance of sessile suspension-feeding assemblages. Journal of Sea Research. Scholar
  70. Vellend, M., 2008. Effects of diversity on diversity: consequences of competition and facilitation. Oikos 117: 1075–1085.CrossRefGoogle Scholar
  71. Vellend, M., 2010. Conceptual synthesis in community ecology. The Quarterly Review of Biology 85: 183–206.CrossRefPubMedGoogle Scholar
  72. Vieira, E. A., L. F. L. Duarte & G. M. Dias, 2012. How the timing of predation affects composition and diversity of species in a marine sessile community? Journal of Experimental Marine Biology and Ecology 412: 126–133.CrossRefGoogle Scholar
  73. Vieira, E. A., G. M. Dias & A. A. V. Flores, 2016. Effects of predation depend on successional stage and recruitment rate in shallow benthic assemblages of the Southwestern Atlantic. Marine Biology 163: 1–12.CrossRefGoogle Scholar
  74. Vieira, E. A., A. A. V. Flores & G. M. Dias, 2018. Persistence and space preemption explain species-specific founder effects on the organization of marine sessile communities. Ecology and Evolution. Scholar
  75. Vogt, J., Y. Lin, A. Pranchai, P. Frohberg, U. Mehlig & U. J. Berger, 2014. The importance of conspecific facilitation during recruitment and regeneration: a case study in degraded mangroves. Basic and Applied Ecology. Scholar
  76. Wahl, M., H. Link, N. Alexandridis, J. C. Thomason, M. Cifuentes, M. J. Costello, B. A. P. da Gama, K. Hillock, A. J. Hobday, M. J. Kaufmann, S. Keller, P. Kraufvelin, I. Krüger, L. Lauterbach, B. L. Antunes, M. Molis, M. Nakaoka, J. Nyström, Z. Radzi, B. Stochausen, M. Thiel, T. Vence, A. Weseloh, M. Whittle, L. Wiesmann, L. Wunderer, T. Yamakita & M. Lenz, 2011. Re-structuring of marine communities exposed to environmental change: a global study on the interactive effects of species and functional richness. PLoS ONE 6: e19514.CrossRefPubMedPubMedCentralGoogle Scholar
  77. Walls, J. T., D. A. Ritz & A. J. Blackman, 1993. Fouling, surface bacteria and antibacterial agents of four bryozoan species found in Tasmania, Australia. Journal of Experimental Marine Biology and Ecology 169: 1–13.CrossRefGoogle Scholar
  78. Walters, L. J. & D. S. Wethey, 1996. Settlement and early post-settlement survival of sessile marine invertebrates on topographically complex surfaces: the importance of refuge dimensions and adult morphology. Marine Ecology Progress Series 137: 161–171.CrossRefGoogle Scholar
  79. Yang, H., L. Jiang, L. Li, A. Li, M. Wu & S. Wan, 2012. Diversity-dependent stability under mowing and nutrient addition: evidence from a 7-year grassland experiment. Ecology Letters 15: 619–626.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Programa de Pós-Graduação em Ecologia, Instituto de BiologiaUniversidade Estadual de Campinas (UNICAMP)CampinasBrazil
  2. 2.Centro de Ciências Naturais e HumanasUniversidade Federal do ABC (UFABC)São Bernardo do CampoBrazil
  3. 3.Centro de Biologia MarinhaUniversidade de São Paulo (USP)São SebastiãoBrazil

Personalised recommendations