Advertisement

Sun coral invasion of shallow rocky reefs: effects on mobile invertebrate assemblages in Southeastern Brazil

  • Rodrigo Silva
  • Catarina Vinagre
  • Marcelo V. Kitahara
  • Isabela V. Acorsi
  • Damián Mizrahi
  • Augusto A. V. FloresEmail author
Original Paper

Abstract

Invasive engineering species impact local biodiversity and ecosystem services as they often change habitat complexity while displacing native species, ultimately altering fundamental processes such as secondary production and the energy flow through trophic levels. The sun corals Tubastraea coccinea and T. tagusensis have successfully invaded reef habitats along the Brazilian coast, drastically reducing the diversity of benthic fouling invertebrates and macroalgae at places where colonies had taken large fractions of the available space. Yet, there is no consistent information on the effects of this invasion on assemblages of mobile invertebrates. We sampled shallow vertical reef areas at Búzios Island, SP, Brazil, and compared univariate and multivariate attributes of these assemblages at different levels of sun-coral cover (no cover, half and full cover), at two sites separated by a few km, and two areas within sites separated by several tens of meters. Consistent declines of overall abundance and biomass with increasing coral cover were found at one sampled site, while richness responded only to small-scale heterogeneity with no sun-coral effects. Changes in assemblage structure were area-specific, but similarity analyses most often grouped no coral and half coral cover, leaving aside full coral plots. Tanaids, ostracods and harpacticoid copepods were among the most important groups where sun corals were absent or covering only half of the reef habitat. However, these groups became almost absent in coral saturated habitats. Polychaetes also contributed substantially to dissimilarities, but effects on this group were less clear. Overall, results suggest a negative tipping point between partial to nearly full coral cover, especially at sites where physically complex macroalgae, capable to retain sediments and hence the invertebrates therein, are displaced by the establishment and growth of sun-coral colonies. As important prey for reef fishes, the collapse of small crustacean populations may alter whole-reef ecosystem functioning and negatively impact local fisheries.

Keywords

Ecosystem engineer Alternative stable states Exotic species Space monopolization Habitat complexity 

Notes

Acknowledgements

The valuable and constructive criticism of three anonymous referees greatly improved this paper. We sincerely thank reviewers for their time and dedication. We also thank the technical staff at the CEBIMar/USP, especially Joseilto M. de Oliveira and Eduardo Honuma for their support in the field. This study was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico, as a research grant to AAVF and CV (CNPq 400614/2014-6), and by the Research Centre for Marine Biodiversity of the University of São Paulo (NP-Biomar/USP).

Supplementary material

10530_2018_1903_MOESM1_ESM.pdf (2 kb)
Supplementary material 1 (PDF 1 kb)
10530_2018_1903_MOESM2_ESM.pdf (2 kb)
Supplementary material 2 (PDF 1 kb)

References

  1. Airoldi L (2003) The effects of sedimentation on rocky coast assemblages. Oceanogr Mar Biol 41:161–236Google Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  3. Araújo FG, Rodrigues FL, Teixeira-Neves TP, Vieira JP, Azevedo MCC, Guedes APP, Garcia AM, Pessanha ALM (2018) Regional patterns in species richness and taxonomic diversity of the nearshore fish community in the Brazilian coast. Estuar Coast Shelf Sci 208:9–22CrossRefGoogle Scholar
  4. Arvanitidis C, Koukouras A (1994) Polychaete fauna associated with the coral Cladocora caespitosa (L.) in the eastern Mediterranean. Mem Mus Natl Hist 162:347–353Google Scholar
  5. Aued AW, Smith F, Quimbayo JP, Cândido DV, Longo GO, Ferreira CEL, Witman JD, Floeter SR, Segal B (2018) Large-scale patterns of benthic marine communities in the Brazilian province. PLoS ONE 13(6):e0198452CrossRefGoogle Scholar
  6. Barroso CX, Lotufo TMC, Mathews-Cascon H (2016) Biogeography of Brazilian prosobranch gastropods and their Atlantic relationships. J Biogeogr 43:2477–2488CrossRefGoogle Scholar
  7. Benkendorfer G, Soares-Gomes A (2009) Biogeography and biodiversity of gastropod molluscs from the eastern Brazilian continental shelf and slope. Lat Am J Aquat Res 37:143–159CrossRefGoogle Scholar
  8. Berghe WV, Bergmans M (1981) Differential food preference in three co-occurring species of Tisbe (Copepoda, Harapaticoida). Mar Ecol Prog Ser 4:213–219CrossRefGoogle Scholar
  9. Berthelsen AK, Hewitt AK, Taylor RB (2015) Coralline turf-associated fauna are affected more by spatial variability than by host species identity. Mar Biodivers 45:689–699CrossRefGoogle Scholar
  10. Calado L, Gangopadhyay A, da Silveira ICA (2006) A parametric model for the Brazil current meanders and eddies off southeastern Brazil. Geohpys Res Lett 33:1–5Google Scholar
  11. Castro CB, Pires DO (2001) Brazilian coral reefs: what we already know and what is still missing. Bull Mar Sci 69:357–371Google Scholar
  12. Ciotti AM, Garcia CAE, Jorge DSF (2010) Temporal and meridional variability of satellite-estimates of surface chlorophyll concentration over the Brazilian continental shelf. Pan-Am J Aquat Sci 5:236–253Google Scholar
  13. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143CrossRefGoogle Scholar
  14. Clarke KR, Green H (1988) Statistical design and analysis for a ‘biological effects’ study. Mar Ecol Prog Ser 46:213–226CrossRefGoogle Scholar
  15. Cox CB, Moore PD (2000) Biogeography: an ecological and evolutionary approach, 6th edn. Blackwell Science, Oxford, p 298Google Scholar
  16. Danielopol DL, Baltanás A, Bonaduce G (1996) The darkness syndrome in subsurface-shallow and deep-sea dwelling Ostracoda (Crustacea). Biosyst Ecol Ser 11:123–143Google Scholar
  17. De Paula AF, Creed JC (2005) Spatial distribution and abundance of nonindigenous coral genus Tubastraea (Cnidaria, Scleractinia) around Ilha Grande, Brazil. Braz J Biol 65:661–673CrossRefGoogle Scholar
  18. Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237–263CrossRefGoogle Scholar
  19. Eggersten L, Ferreira CEL, Fontoura L, Kautsy N, Gullstrom M, Berkstrom C (2017) Seaweed beds support more juvenile reef fish than seagrass beds in a south-western Atlantic tropical seascape. Estuar Coast Shelf Sci 196:97–108CrossRefGoogle Scholar
  20. Floeter SR, Krohling W, Gasparini JL, Ferreira CEL, Zalmon IR (2007) Reef fish community structure on coastal islands of the southeastern Brazil: the influence of exposure and benthic cover. Environ Biol Fish 78:147–160CrossRefGoogle Scholar
  21. Fontes RFC, Castro BM (2017) Currents on the continental shelf adjacent to the Laje de Santos (SP, Brazil). Braz J Oceanogr 65:595–604CrossRefGoogle Scholar
  22. Garrabou J, Ballesteros E, Zabala M (2002) Structure and dynamics of North-western Mediterranean rocky benthic communities along a depth gradiente. Estuar Coast Shelf Sci 55:493–508CrossRefGoogle Scholar
  23. Gobin J (2010) Free-living marine polychaetes (Annelida) inhabiting hard-bottom substrates in Trinidad and Tobago, West Indies. Rev Biol Trop 58:147–157PubMedGoogle Scholar
  24. Hutchings PA (1981) Polychaete recruitment onto dead coral substrates at Lizard Island, Great Barrier Reef, Australia. Bull Mar Sci 31:410–423Google Scholar
  25. Jacobucci GB, Vieira EA, Leite FPP (2018) Influence of a narrow depth gradient on the spatial structure of Sargassum peracarid aseemblages. Mar Biodivers.  https://doi.org/10.1007/s12526-018-0885-6 CrossRefGoogle Scholar
  26. Jones CG, Lawton JH, Shachac M (1994) Organisms as ecosystem engineers. Oikos 69:373–386CrossRefGoogle Scholar
  27. Kohn AJ, Lloyd MC (1973) Polychaetes of truncated reef limestone substrates on Eastern Indian Ocean coral reefs: diversity, abundance, and taxonomy. Int Rev Gesamt Hydrobiol 58:369–399CrossRefGoogle Scholar
  28. Leão ZM, Ginsburg RN (1997) Living reefs surrounded by siliciclastic sediments: the Abrolhos coastal reefs, Bahia, Brazil. In: Proceedings of 8th International Coral Reef Symposium, Panamá 2:1767–1772Google Scholar
  29. Leite FPP, Turra A (2003) Temporal variation in Sargassum biomass, Hypnea epiphytism and associated fauna. Braz Arch Biol Technol 46:665–671CrossRefGoogle Scholar
  30. Manté C, Dauvin JC, Durbec JP (1995) Statistical method for selecting representative species in multivariate analysis of long-term changes of marine communities applications to a microbenthic community from the Bay of Morlaix. Mar Ecol Prog Ser 120:243–250CrossRefGoogle Scholar
  31. Mbahinzireki G, Uiblein F, Winkler H (1991) Microhabitat selection of ostracods in relation to predation and food. Hydrobiologia 222:115–119CrossRefGoogle Scholar
  32. McCloskey LR (1970) The dynamics of the community associated with a marine scleractinian coral. Int Rev ges Hydrobiol 55:13–81CrossRefGoogle Scholar
  33. Méthot G, Hudon C, Gagnon P, Pinel-Alloul B, Armellin A, Poirier AMT (2012) Macroinvertebrate size–mass relationships: how specific should they be? Freshw Sci 31:750–764CrossRefGoogle Scholar
  34. Milne R, Griffiths C (2014) Invertebrate biodiversity associated with algal turfs on a coral-dominated reef. Mar Biodivers 44:181–188CrossRefGoogle Scholar
  35. Miranda RJ, Cruz ICS, Barros F (2016) Effects of the alien coral Tubastraea tagusensis on native coral. Mar Biol 163:1–12CrossRefGoogle Scholar
  36. Miranda RJ, Nunes JACC, Mariano-Neto EM, Sippo JZ, Barros F (2018) Do invasive corals alter coral reef processes? An empirical approach evaluating reef fish trophic interactions. Mar Environ Res 138:19–27CrossRefGoogle Scholar
  37. Mizrahi D, Navarrete SA, Flores AAV (2014) Uneven abundance of the invasive sun coral over habitat patches of different orientation: an outcome of larval or later benthic processes? J Exp Mar Biol Ecol 452:22–30CrossRefGoogle Scholar
  38. Mizrahi D, Pereira SF, Navarrete SA, Flores AAV (2017) Allelopathic effects on the sun coral invasion: facilitation, inhibition and patterns of local biodiversity. Mar Biol 164:139CrossRefGoogle Scholar
  39. Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492CrossRefGoogle Scholar
  40. Munro C (2013) Diving. In: Eleftheriou A (ed) Methods for the study of marine benthos, 4th edn. John Wiley & Sons, West Sussex, pp 125–173CrossRefGoogle Scholar
  41. Neckles HA, Wetzel RL, Orth RJ (1993) Relative effects of nutrient enrichment and grazing on epiphyte-macrophyte (Zostera marina L) dynamics. Oecologia 93:285–295CrossRefGoogle Scholar
  42. Nelson AL, Coull BC (1989) Selection of meiobenthic prey by juvenile spot (Pisces): an experimental study. Mar Ecol Prog Ser 53:51–57CrossRefGoogle Scholar
  43. Nogueira JMM, Martin GS (2002) Species of Syllis Savigny in Lamarck, 1818 (Polychaeta: Syllidae) living in corals in the state of São Paulo, Southeastern Brazil. Beaufortia 52:57–93Google Scholar
  44. Nogueira JMM, Martin GS, Amaral ACZ (2001) Description of five new species of Exogoninae Rioja, 1925 (Polychaeta: Syllidae) associated with the stony coral Mussismilia hispida (Verrill, 1868) in São Paulo State, Brazil. J Nat Hist 35:1773–1794CrossRefGoogle Scholar
  45. Oigman-Pszcol SS, Figueiredo MAO, Creed JC (2004) Distribution of benthic communities on the tropical rocky subtidal of Armação dos Búzios, Southeastern Brazil. PSZN Mar Ecol 25:173–190CrossRefGoogle Scholar
  46. Pereira PHC, Barros B, Zemoi R, Ferreira BP (2014) Ontogenetic diet changes and food partitioning of Haemulon spp coral reef fishes, with a review of the genus diet. Rev Fish Biol Fisher 25:245–260CrossRefGoogle Scholar
  47. Pinto CSC, Souza-Santos LP, Santos PJP (2001) Development and population dynamics of Tisbe biminiensis (Copepoda: Harpacticoida) reared on different diets. Aquaculture 198:253–267CrossRefGoogle Scholar
  48. Porter SN, Branch GM, Sink KJ (2013) Biogeographic patterns on shallow subtidal reefs in the western Indian Ocean. Mar Biol 160:1271–1283CrossRefGoogle Scholar
  49. Rocha RM, Vieira LM, Migotto AE, Amaral ACZ, Ventura RR, Serejo CS, Pitombo FB, Santos KC, Simone LRL, Tavares M, Lopes RM, Pinheiro U, Marques AC (2013) The need of more rigorous assessments of marine species introductions: a counter example from the Brazilian coast. Mar Pollut Bull 67:241–243CrossRefGoogle Scholar
  50. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176CrossRefGoogle Scholar
  51. Silva AG, de Paula AF, Fleury BG, Creed JC (2014) Eleven years of range expansion of two invasive corals (Tubastraea coccinea and Tubastraea tagusensis) through the southwest Atlantic (Brazil). Estuar Coastl Shelf Sci 141:9–16CrossRefGoogle Scholar
  52. Stachowicz JJ, Fried H, Osman RW, Whitlatch RB (2002) Biodiversity, invasion resistance, and marine function: reconciling patterns and process. Ecology 83:2575–2590CrossRefGoogle Scholar
  53. Stech JL, Lorenzetti JA (1992) The response of the South Brazil Bight to the passage of wintertime cold fronts. J Geophys Res 97:9507–9520CrossRefGoogle Scholar
  54. Tano S, Eggertsen M, Wikström SA, Berkström C, Buriyo AS, Halling C (2016) Tropical seaweed beds are important habitats for mobile invertebrate epifauna. Estuar Coast Shelf Sci 183:1–12CrossRefGoogle Scholar
  55. Vermeij GJ (1978) Biogeography and adaptation: patterns of marine life. Harvard University Press, CambridgeGoogle Scholar
  56. Vieira EA, Dias GM, Flores AAV (2016) Effects of predation depend on successional stage and recruitment rate in shallow benthic assemblages of the Southwestern Atlantic. Mar Biol 163:87CrossRefGoogle Scholar
  57. Vinagre C, Silva R, Mendonça V, Flores AAV, Baeta A, Marques JC (2018) Food web organization following the invasion of habitat-modifying Tubastraea spp. corals appears to favour the invasive borer bivalve Leiosolenus aristatus. Ecol Ind 85:1204–1209CrossRefGoogle Scholar
  58. Witman JD, Dayton PK (2001) Rocky subtidal communities. In: Gaines SD, Hay ME (eds) Marine Community Ecology (Bertness, MD. Sinauer Associates, Sunderland, pp 339–366Google Scholar
  59. Wouters JM, Gusmão JB, Mattos G, Lana P (2018) Polychaete functional diversity in shallow habitats: shelter from the storm. J Sea Res 135:18–30CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.MARE—Marine and Environmental Sciences CentreUniversidade de Lisboa, Faculdade de CiênciasLisbonPortugal
  2. 2.Universidade Federal de São PauloSantosBrazil
  3. 3.Centro de Biologia MarinhaUniversidade de São PauloSão SebastiãoBrazil

Personalised recommendations