Biological Invasions

, Volume 17, Issue 6, pp 1799–1816 | Cite as

Changes in habitat complexity resulting from sequential invasions of a rocky shore: implications for community structure

  • Saachi Sadchatheeswaran
  • George M. Branch
  • Tamara B. Robinson
Original Paper


Worldwide, marine rocky shores are being modified by alien species, but their successive impacts are rarely recorded. We documented sequential invasions of Marcus Island on the west coast of South Africa by comparing communities from 1980 (pre-invasion), 2001 (after invasion by the mussel Mytilus galloprovincialis) and 2012 (following invasions by another mussel, Semimytilus algosus, and the barnacle Balanus glandula). Their influence on habitat complexity was measured with a novel technique enabling retrospective calculation of historical complexity. In 1980, habitat complexity, invertebrate abundance and species richness decreased from the low-shore to the high-shore, but homogenised in 2001 after M. galloprovincialis elevated habitat complexity across most of the shore. In 2012, these variables returned to pre-invasion patterns, after M. galloprovincialis declined in the high-shore and was replaced there by B. glandula. With the first mussel invasion, several indigenous species extended up the intertidal, but retreated once M. galloprovincialis receded. Community composition differed significantly among nearly all years and zones, irrespective of whether the alien species were included in the analyses or not. Some once-dominant native species were negatively affected by the invasions: one indigenous mussel, Choromytilus meridionalis, disappeared by 2012, and another, Aulacomya atra, declined. The abundance of recruits of the limpet Scutellastra granularis rose and fell with the arrival and recession of M. galloprovincialis, but adults were adversely affected. Changes to habitat complexity induced by sequential invasions supported hypothesised changes in invertebrate abundance and species richness, but could not alone predict changes in community composition, which were also influenced by zonation.


Balanus glandula Ecosystem engineering Habitat complexity Mytilus galloprovincialis Semimytilus algosus South Africa 



Financial contributions by the DST-NRF Centre of Excellence for Invasion Biology, the Marine Research Institute, University of Cape Town (BASICs Programme) and the Andrew Mellon Foundation are gratefully acknowledged. Brendan Havenga is thanked for his help in the field. Thanks are due to Jennifer Ruesink, Divyalochany Thangavel and three anonymous reviewers for constructive and thoughtful comments.


  1. Barbarro JMF, Abad MJ (2013) Co-existence of two Mytilid species in a heterogeneous environment: mortality, growth and strength of shell and byssus attachment. Mar Ecol Prog Ser 467:115–128. doi: 10.3354/meps10122 CrossRefGoogle Scholar
  2. Barkai A, Branch GM (1988) Contrasts between the benthic communities of subtidal hard substrata at Marcus and Malgas Islands: a case of alternative stable states? S Afr J Mar Sci 7:117–137CrossRefGoogle Scholar
  3. Blender Foundation (2012) Blender 2.64. Retrieved October 13, 2012, from
  4. Borthagaray AI, Carranza A (2007) Mussels as ecological engineers: their contribution to species richness in a rocky littoral community. Acta Oecol 31:243–250. doi: 10.1016/j.actao.2006.10.008 CrossRefGoogle Scholar
  5. Bownes SJ, McQuaid CD (2006) Will the invasive mussel Mytilus galloprovincialis Lamarck replace the indigenous Perna perna L. on the south coast of South Africa? J Exp Mar Biol Ecol 338:140–151. doi: 10.1016/j.jembe.2006.07.006 CrossRefGoogle Scholar
  6. Bownes SJ, McQuaid CD (2010) Mechanisms of habitat segregation between an invasive (Mytilus galloprovincialis) and an indigenous (Perna perna) mussel: adult growth and mortality. Mar Biol 157:1799–1810. doi: 10.1007/s00227-010-1452-2 CrossRefGoogle Scholar
  7. Branch GM, Steffani CN (2004) Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamark). J Exp Mar Biol Ecol 300:189–215. doi: 10.1016/j.jembe.2003.12.007 CrossRefGoogle Scholar
  8. Branch GM, Odendaal F, Robinson TB (2008) Long-term monitoring of the arrival, expansion and effects of the alien mussel Mytilus galloprovincialis relative to wave action. Mar Ecol Prog Ser 370:171–183. doi: 10.3354/meps07626 CrossRefGoogle Scholar
  9. Branch GM, Odendaal F, Robinson TB (2010) Competition and facilitation between the alien mussel Mytilus galloprovincialis and indigenous species: moderation by wave action. J Exp Mar Biol Ecol 383:65–78. doi: 10.1016/j.jembe.2009.10.007 CrossRefGoogle 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. S Afr J Mar Sci 18:119–136. doi: 10.2989/025776197784160901 CrossRefGoogle Scholar
  11. Chao A (1987) Estimating the population size for capture–recapture data with unequal catchability. Biometrics 43:783–791CrossRefPubMedGoogle Scholar
  12. Commito JA, Boncavage EM (1989) Suspension-feeders and coexisting infauna: an enhancement counterexample. J Exp Mar Biol Ecol 125:33–42CrossRefGoogle Scholar
  13. Commito J, Rusignuolo B (2000) Structural complexity in mussel beds: the fractal geometry of surface topography. J Exp Mar Biol Ecol 225:133–152CrossRefGoogle Scholar
  14. Connell JH (1972) Community interactions on marine rocky intertidal shores. Annu Rev Ecol Evol Syst 3:169–192. doi: 10.1146/ CrossRefGoogle Scholar
  15. Creese R, Hooker S, DeLuca S, Wharton W (1997) Ecology and environmental impact of Musculista senhousia (Mollusca: Bivalvia: Mytilidae) in Tamaki Estuary, Auckland, New Zealand. N Z J Mar Fresh Res 31:225–236. doi: 10.1080/00288330.1997.9516760 CrossRefGoogle Scholar
  16. Crooks JA (1998) Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia. Mar Ecol Prog Ser 162:137–152CrossRefGoogle Scholar
  17. Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166. doi: 10.1043/j.1600-0706.2002.970201.x CrossRefGoogle Scholar
  18. Crooks JA, Khim HS (1999) Architectural vs. biological effects of a habitat-altering, exotic mussel, Musculista senhousia. J Exp Mar Biol Ecol 240:53–75CrossRefGoogle Scholar
  19. de Greef K, Griffiths CL, Zeeman Z (2013) Déjà vu? A second mytilid mussel, Semimytilus algosus, invades South Africa’s west coast. Afr J Mar Sci 35:307–313. doi: 10.2989/1814232X.2013.829789 CrossRefGoogle Scholar
  20. Firstater FN, Hidalgo FJ, Lomovasky BJ, Ramos E, Gamero P, Iribarne OO (2011) Habitat structure is more important than nutrient upwelling in modifying mussel bed assemblage in an upwelling area of the Peruvian coast. Helgol Mar Res 65:187–196. doi: 10.1007/s10152-010-0214-3 CrossRefGoogle Scholar
  21. Gestoso I, Arenas F, Rubal M, Veiga P, Peña M, Olabarria C (2013) Shifts from native to non-indigenous mussels: enhanced habitat complexity and its effects on faunal assemblages. Mar Env Res 90:85–95. doi: 10.1016/j.marenvres.2013.05.015 CrossRefGoogle Scholar
  22. Gotelli N, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391. doi: 10.1046/j.1461-0248.2001.00230.x CrossRefGoogle Scholar
  23. Griffiths R (1980) Filtration, respiration and assimilation in the black mussel Choromytilus meridionalis. Mar Ecol Prog Ser 3:63–70CrossRefGoogle Scholar
  24. Griffiths CL, Hockey PAR, van Erkom Schurink C, Le Roux PJ (1992) Marine invasive aliens on South African shores: implications for community structure and trophic functioning. S Afr J Mar Sci 12:713–722. doi: 10.2989/02577619209504736 CrossRefGoogle Scholar
  25. Guerra Á, Pascual S, Garci ME, Roura Á, Mucientes G, González ÁF (2013) The black-pygmy mussel Limnoperna securis in Galician Rias (north-eastern Atlantic): new records and first evidence of larval stages predation by copepods. Mar Biodivers Rec 6:1–7. doi: 10.1017/S1755267212001224 CrossRefGoogle Scholar
  26. Hammond W, Griffiths C (2006) Biogeographical patterns in the fauna associated with southern African mussel beds. Afr Zool 41:123–130. doi: 10.3377/1562-7020(2006)41[123:BPITFA]2.0.CO;2
  27. Harley CDG (2006) Effects of physical ecosystem engineering and herbivory on intertidal community structure. Mar Ecol Prog Ser 317:29–39. doi: 10.3354/meps317029 CrossRefGoogle Scholar
  28. Harley CDG, O’Riley JL (2011) Non-linear density-dependent effects of an intertidal ecosystem engineer. Oecologia 166:531–541. doi: 10.1007/s00442-010-1864-1 CrossRefPubMedGoogle Scholar
  29. Hockey PAR, van Erkom Schurink C (1992) The invasive biology of the mussel Mytilus galloprovincialis on the Southern African Coast. Trans R Soc S Afr 48:123–139. doi: 10.1080/00359199209520258 CrossRefGoogle Scholar
  30. Hoffman V, Pfaff MC, Branch GM (2012) Spatio-temporal patterns of larval supply and settlement of intertidal invertebrates reflect a combination of passive transport and larval behaviour. J Exp Mar Biol Ecol 418–419:83–90. doi: 10.1016/j.jembe.2012.03.008 CrossRefGoogle Scholar
  31. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386CrossRefGoogle Scholar
  32. Kovalenko KE, Thomaz SM, Warfe DM (2012) Habitat complexity: approaches and future directions. Hydrobiologia 685:1–17. doi: 10.1007/s10750-011-0974-z CrossRefGoogle Scholar
  33. Laird MC, Griffiths CL (2008) Present distribution and abundance of the introduced barnacle Balanus glandula Darwin in South Africa. Afr J Mar Sci 30:93–100. doi: 10.2989/AJMS.2008. CrossRefGoogle Scholar
  34. McKinney ML (1998) On predicting biotic homogenization: speciesarea patterns in marine biota. Glob Ecol Biogeogr Lett 7:297–301. doi: 10.1046/j.1466-822X.1998.00303.x CrossRefGoogle Scholar
  35. Mead A, Carlton JT, Griffiths CL, Rius M (2011) Revealing the scale of marine bioinvasions in developing regions: a South Africa assessment. Biol Invasions 13:1991–2008. doi: 10.1007/s10530-011-0016-9 CrossRefGoogle Scholar
  36. Menge BA, Foley MM, Pamplin J, Murphy G, Pennington C (2010) Supply-side ecology, barnacle recruitment, and rocky intertidal community dynamics: do settlement surface and limpet disturbance matter? J Exp Mar Biol Ecol 392:160–175. doi: 10.1016/j.jembe.2010.04.032 CrossRefGoogle Scholar
  37. Norling P, Kautsky N (2008) Patches of the mussel Mytilus sp. are islands of high biodiversity in subtidal sediment habitats in the Baltic Sea. Aquat Biol 4:89–98. doi: 10.3354/ab00096 CrossRefGoogle Scholar
  38. Pillay D, Branch GM (2011) Bioengineering effects of burrowing thalassinidean shrimps on marine softbottom ecosystems. Oceanogr Mar Biol Ann Rev 49:137–192Google Scholar
  39. Quinn G, Keough M (2002) Comparing groups or treatments—analysis of variance. In: Quinn G, Keough M (eds) Experimental design and data analysis for biologists. Cambridge University Press, New York, pp 173–188CrossRefGoogle Scholar
  40. Reaugh-Flower K, Branch GM, Harris JM, McQuaid CD, Currie B, Dye A, Robertson B (2011) Scale-dependent patterns and processes of intertidal mussel recruitment around southern Africa. Mar Ecol Prog Ser 434:101–119. doi: 10.3354/meps09169 CrossRefGoogle Scholar
  41. Ricciardi A, Whoriskey FG, Rasmussen JB (1997) The role of zebra mussel (Dreissena polymorpha) in structuring macroinvertebrate communities on hard substrata. Can J Fish Aquat Sci 54:2596–2608CrossRefGoogle Scholar
  42. Risk MJ (1972) Fish diversity on a coral reef in the Virgin Islands. Atoll Res Bull 193:1–6CrossRefGoogle Scholar
  43. Robinson TB, Branch GM, Griffiths CL, Govender A, Hockey PAR (2007a) Changes in South African rocky intertidal invertebrate community structure associated with the invasion of the mussel Mytilus galloprovincialis. Mar Ecol Prog Ser 340:163–171. doi: 10.3354/meps340163 CrossRefGoogle Scholar
  44. Robinson TB, Griffiths CL, Branch GM, Govender A (2007b) The invasion and subsequent die-off of Mytilus galloprovincialis in Langebaan Lagoon, South Africa: effects on natural communities. Mar Biol 152:225–232. doi: 10.1007/s00227-007-0697-x CrossRefGoogle Scholar
  45. Ruiz Sebastián C, Steffani CN, Branch GM (2002) Homing and movement patterns of a South African limpet Scutellastra argenvillei in an area invaded by an alien mussel Mytilus galloprovincialis. Mar Ecol Prog Ser 243:111–122. doi: 10.3354/meps243111 CrossRefGoogle Scholar
  46. Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr Comp Biol 42:780–789. doi: 10.1093/icb/42.4.780 CrossRefPubMedGoogle Scholar
  47. Steffani CN, Branch GM (2003) Spatial comparisons of populations of an indigenous limpet Scutellastra argenvillei and an alien mussel Mytilus galloprovincialis along a gradient of wave energy. Afr J Mar Sci 25:195–212. doi: 10.2989/18142320309504010 CrossRefGoogle Scholar
  48. Steffani CN, Branch GM (2005) Mechanisms and consequences of competition between an alien mussel, Mytilus galloprovincialis, and an indigenous limpet, Scutellastra argenvillei. J Exp Mar Biol Ecol 317:127–142. doi: 10.1016/j.jembe.2004.11.022 CrossRefGoogle Scholar
  49. Suchanek TH (1985) Mussels and their role in structuring rocky shore communities. In: Moore PG, Seed R (eds) The ecology of rocky coasts. Hodder and Stoughton, Sevenoaks, pp 70–96Google Scholar
  50. Thiel M, Ullrich N (2002) Hard rock versus soft bottom: the fauna associated with intertidal mussel beds on hard bottoms along the coast of Chile, and considerations on the functional role of mussel beds. Helgol Mar Res 56:21–30. doi: 10.1007/s10152-001-0098-3 CrossRefGoogle Scholar
  51. Thiesen BF (1972) Shell cleaning and deposit feeding in Mytilus edulis (Bivalvia). Ophelia 10:49–55CrossRefGoogle Scholar
  52. Thompson RC, Crowe TP, Hawkins SJ (2002) Rocky intertidal communities: past environmental changes, present status and predictions for the next 25 years. Environ Conserv 29:168–191CrossRefGoogle Scholar
  53. Tokeshi M (1995) Polychaete abundance and dispersion patterns in mussel beds: a non-trivial ‘infaunal’ assemblage on a pacific South American rocky shore. Mar Ecol Prog Ser 125:137–147. doi: 10.3354/meps125137 CrossRefGoogle Scholar
  54. Tokeshi M, Romero L (1995) Filling a gap: dynamics of space occupancy on a mussel-dominated subtropical rocky shore. Mar Ecol Prog Ser 119:167–176. doi: 10.3354/meps119167 CrossRefGoogle Scholar
  55. Tsuchiya M, Nishihira M (1985) Islands of Mytilus as a habitat for small intertidal animals: effect of island size on community structure 25:71–81Google Scholar
  56. Underwood AJ, Fairweather PG (1989) Supply-side ecology and benthic marine assemblages. Trends Ecol Evol 4:16–20CrossRefPubMedGoogle Scholar
  57. Valdivia N, Thiel M (2006) Effects of point-source nutrient addition and mussel removal on epibiotic assemblages in Perumytilus purpuratus beds. J Sea Res 56:271–283. doi: 10.1016/j.seares.2006.06.003 CrossRefGoogle Scholar
  58. van Erkom Schurink C, Griffiths CL (1991) A comparison of reproductive cycles and reproductive output in four southern African mussel species. Mar Ecol Prog Ser 76:123–134CrossRefGoogle Scholar
  59. van Erkom Schurink C, Griffiths CL (1993) Factors affecting relative rates of growth in four South African mussel species. Aquaculture 109:257–273CrossRefGoogle Scholar
  60. van Wesenbeeck BK, van de Koppel J, Herman PMJ, Bakker JP, Bouma TJ (2007) Biomechanical warfare in ecology; negative interactions between species by habitat modification. Oikos 116:742–750. doi: 10.1111/j.2007.0030-1299.15485.x CrossRefGoogle Scholar
  61. Wootton JT (1993) Indirect effects and habitat use in an intertidal community: interaction chains and interaction modifications. Am Nat 141:71–89CrossRefGoogle Scholar
  62. Wright JP, Jones CG, Flecker AS (2002) An ecosystem engineer, the beaver, increases species richness at the landscape level. Oecologia 132:96–101. doi: 10.1007/s00442-002-0929-1 CrossRefGoogle Scholar
  63. Zardi GI, Nicastro KR, McQuaid CD, Rius M, Porri F (2006) Hydrodynamic stress and habitat partitioning between indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussels: constraints of an evolutionary strategy. Mar Biol 150:79–88. doi: 10.1007/s00227-006-0328-y CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Saachi Sadchatheeswaran
    • 1
  • George M. Branch
    • 1
  • Tamara B. Robinson
    • 2
  1. 1.Department of Biological Sciences, Marine Research InstituteUniversity of Cape TownRondeboschSouth Africa
  2. 2.Department of Botany and Zoology, Centre for Invasion BiologyStellenbosch UniversityMatieland, StellenboschSouth Africa

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