Advertisement

Marine Biology

, Volume 162, Issue 12, pp 2493–2500 | Cite as

Forecasting invasions: resource use by mussels informs invasion patterns along the South African coast

  • Mhairi E. Alexander
  • Robyn Adams
  • Jaimie T. A. Dick
  • Tamara B. Robinson
Invasive Species - Original Paper
Part of the following topical collections:
  1. Invasive Species

Abstract

Invasive species are often more able to rapidly and efficiently utilise resources than natives, and comparing per capita resource use at different resource densities among invaders and trophically analogous natives could allow for reliable predictions of invasiveness. In South Africa, invasion by the Mediterranean mussel Mytilus galloprovincialis has transformed wave-exposed shores, negatively affecting native mussel species. Currently, South Africa is experiencing a second mussel invasion with the recent detection of the South American Semimytilus algosus. We tested per capita uptake of an algal resource by invading M. galloprovincialis, S. algosus, and the native Aulacomya atra at different algal concentrations and temperatures, representing the west and south coasts of South Africa, to examine whether their per capita resource use could be a predictor of their spread and subsequent invasiveness. Regardless of temperature, M. galloprovincialis was the most efficient consumer, significantly reducing algal cells compared to the other species when the resource was presented in both low and high starting densities. Furthermore, these findings aligned with a greater biomass of M. galloprovincialis on the shore in comparison with the other species. Resource use by the new invader S. algosus was dependent on the density of resource and, although this species was efficient at low algal concentrations at cooler temperatures, this pattern broke down at higher algal densities. This was once more reflected in lower biomass in surveys of this species along the cool west coast. We therefore forecast that S. algosus will be become established along the south coast; however, we also predict that M. galloprovincialis will maintain dominance on these shores.

Keywords

Algal Cell South Coast Capita Resource Algal Concentration Mussel Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We would like to thank H. Raven, S. Sadchatheeswaran and G. and M. Branch for assistance in field sampling, and R. Adams at the Centre of Analytical Facilities, Stellenbosch University, for assistance with flow cytometry. This study was funded by the DST-NRF Centre of Excellence for Invasion Biology.

References

  1. Alexander ME, Dick JTA, Weyl OLF et al (2014) Existing and emerging high impact invasive species are characterized by higher functional responses than natives. Biol Lett 10:2–6CrossRefGoogle Scholar
  2. Alexander ME, Raven HR, Robinson TB (2015) Foraging decisions of a native whelk, Trochia cinulata Linnaeus, and the effects of invasive mussels on prey choice. J Exp Mar Biol Ecol 470:26–33CrossRefGoogle Scholar
  3. Assis J, Zupan M, Nicastro KR, Zardi GI, McQuaid CD, Serrao EA (2015) Oceanographic conditions limit the spread of a marine invader along Southern African Shores. PLoS One 10(6):e0128124CrossRefGoogle Scholar
  4. Awad AA, Griffiths CL, Turpie JK (2002) Distribution of South African marine benthic invertebrates applied to the selection of priority conservation areas. Divers Distrib 8:129–145CrossRefGoogle Scholar
  5. Barrios-O’Neill D, Dick JTA, Emmerson MC et al (2013) Fortune favours the bold: a higher predator reduces the impact of a native but not an invasive intermediate predator. J Anim Ecol 83:693–701CrossRefGoogle Scholar
  6. Bax N, Williamson A, Aguero M et al (2003) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27:313–323CrossRefGoogle Scholar
  7. Bosman AL, Hockey PAR, Siegfried WR (1987) The influence of coastal upwelling on the functional structure of rocky intertidal communities. Oecologia 72:226–232CrossRefGoogle Scholar
  8. Branch GM, Griffiths CL (1988) The Benguela ecosystem part V. The coastal zone. Oceanogr Mar Biol 26:395–486Google Scholar
  9. 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 (Lamarck). J Exp Mar Biol Ecol 300:189–215CrossRefGoogle Scholar
  10. 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 Pog Ser 370:171–183CrossRefGoogle Scholar
  11. 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 383:65–78CrossRefGoogle Scholar
  12. Byers JE, Reichard S, Randall JM et al (2002) Directing research to reduce the impacts of nonindigenous species. Conserv Biol 16:630–640CrossRefGoogle Scholar
  13. Colautti RI, Grigorovich IA, MacIsaac HJ (2006) Propagule pressure: a null model for biological invasions. Biol Invasions 8:1023–1037CrossRefGoogle Scholar
  14. Dayton PK (1971) Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41:351–389CrossRefGoogle Scholar
  15. De Greef K, Griffiths CL, Zeeman Z (2013) Deja vu ? A second mytilid mussel, Semimytilus algosus, invades South Africa’s west coast. Afr J Mar Sci 35:37–41CrossRefGoogle Scholar
  16. Dick JTA, Gallagher K, Avlijas S et al (2013) Ecological impacts of an invasive predator explained and predicted by comparative functional responses. Biol Invasions 15:837–845CrossRefGoogle Scholar
  17. Dick JTA, Alexander ME, Jeschke J et al (2014) Advancing impact prediction and hypothesis testing using a comparative functional response approach. Biol Invasions 16:735–753CrossRefGoogle Scholar
  18. Fanslow DL, Nalepa TF, Lang GA (1995) Filtration rates of the zebra mussel (Dreissena polymorpha) on natural seston from Saginaw Bay, Lake Huron. J Great Lakes Res 21:489–500CrossRefGoogle Scholar
  19. Filgueira R, Fernández-reiriz MJ, Labarta U (2009) Clearance rate of the mussel Mytilus galloprovincialis. I. Response to extreme chlorophyll ranges. Cienc Mar 35:405–417CrossRefGoogle Scholar
  20. Grosholz E (2002) Ecological and evolutionary consequences. Trends Ecol Evol 17:22–27CrossRefGoogle Scholar
  21. Haure J, Penisson C, Bourgrier S, Baud JP (1998) Influence of temperature on clearance and oxygen rates of the flat oyster Ostrea edulis: determination of allometric coefficients. Aquaculture 169:211–224CrossRefGoogle Scholar
  22. Keller RP, Kocev D, Džeroski S (2011) Trait-based risk assessment for invasive species: high performance across diverse taxonomic groups, geographic ranges and machine learning/statistical tools. Divers Dist 17:451–461CrossRefGoogle Scholar
  23. Kulhanek SA, Ricciardi A, Leung B (2011) Is invasion history a useful tool for predicting the impacts of the world’ s worst aquatic invasive species ? Ecol Appl 21:189–202CrossRefGoogle Scholar
  24. Leffler AJ, James JJ, Monaco TA (2012) Temperature and functional traits influence differences in nitrogen uptake capacity between native and invasive grasses. Oecologia 171:51–60CrossRefGoogle Scholar
  25. Lucas AJ, Pitcher GC, Probyn TA, Kudela RM (2014) The influence of diurnal winds on phytoplankton dynamics in a coastal upwelling system off southwestern Africa. Deep sea Res Pt II 101:50–62CrossRefGoogle Scholar
  26. Mead A, Carlton JT, Griffiths CL, Rius M (2011) Revealing the scale of marine bioinvasions in developing regions: a South African re-assessment. Biol Invasions 13:1991–2008CrossRefGoogle Scholar
  27. Miller TE, Burns JH, Munguia P et al (2005) A critical review of twenty years use of the resource-ratio theory. Am Nat 165:439–448PubMedGoogle Scholar
  28. 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
  29. Murray CC, Gartner H, Gregr EJ, Chan K, Pakhomov E, Therriault TW (2014) Spatial distribution of marine invasive species: environmental, demographic and vector drivers. Divers Dist 20:824–836CrossRefGoogle Scholar
  30. Nelson G, Polito A (1987) Information on currents in the Cape Peninsula area, South Africa. S Afr J Mar Sci 5:287–304CrossRefGoogle Scholar
  31. Newell CR, Wildish D, MacDonald B (2001) The effects of velocity and seston concentration on the exhalant siphon area, valve gape and filtration rate of the mussel Mytilus edulis. J Exp Mar Biol Ecol 262:91–111CrossRefGoogle Scholar
  32. Parker IM, Simberloff D, Lonsdale WM et al (1999) Impact : toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19CrossRefGoogle Scholar
  33. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288CrossRefGoogle Scholar
  34. Ricciardi A (2003) Predicting the impacts of an introduced species from its invasion history : an empirical approach applied to zebra mussel invasions. Freshwater Biol 48:972–981CrossRefGoogle Scholar
  35. Riisgard HU, Kittner C, Seerup DF (2003) Regulation of opening state and filtration rate in filter-feeding bivalves (Cardium edule, Mytilus edulis, Mya arenaria) in response to low algal concentration. J Exp Mar Biol Ecol 284:105–127CrossRefGoogle Scholar
  36. Rilov G, Galil B (2009) Marine bioinvasions in the Mediterranean Sea—history, distribution and ecology. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 549–575CrossRefGoogle Scholar
  37. Robinson TB, Griffiths CL, McQuaid CD, Rius M (2005) Marine alien species of South Africa—status and impacts. Afr J Mar Sci 27:297–306CrossRefGoogle Scholar
  38. Robinson TB, Branch GM, Griffiths CL et al (2007) Changes in South African rocky intertidal invertebrate community structure associated with the invasion of the mussel Mytilus galloprovincialis. Mar Ecol Prog Ser 340:163–171CrossRefGoogle Scholar
  39. Ruiz GM, Fofonoff P, Hines AH, Grosholz ED (1999) Non-indigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions. Limnol Oceanogr 44:950–972CrossRefGoogle Scholar
  40. Sadchatheeswaran S, Branch GM, Robinson TB (2015) Changes in habitat complexity resulting from sequential invasions of a rocky shore: implications for community structure. Biol Invasions 17:1799–1816CrossRefGoogle Scholar
  41. Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  42. Schulte EH (1975) Influence of algal concentration and temperature on the filtration rate of Mytilus edulis. Mar Biol 30:331–341CrossRefGoogle Scholar
  43. Shinen JS, Morgan SG (2009) Mechanisms of invasion resistance: competition among intertidal mussels promotes establishment of invasive species and displacement of native species. Mar Ecol Prog Ser 383:187–197CrossRefGoogle Scholar
  44. Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Syst 40:81–102CrossRefGoogle Scholar
  45. Simberloff D, Martin J-L, Genovesi P et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66CrossRefGoogle Scholar
  46. Smit AJ, Roberts M, Anderson RJ et al (2013) A coastal seawater temperature dataset for biogeographical studies: large biases between in situ and remotely-sensed data sets around the coast of South Africa. PLoS One 8:e81944CrossRefGoogle Scholar
  47. Sousa R, Gutiérrez JL, Aldridge DC (2009) Non-indigenous invasive bivalves as ecosystem engineers. Biol Invasions 11:2367–2385CrossRefGoogle Scholar
  48. Steffani CN, Branch GM (2003) Growth rate, condition, and shell shape of Mytilus galloprovincialis: responses to wave exposure. Mar Ecol Prog Ser 246:197–209CrossRefGoogle Scholar
  49. Steffani CN, Branch GM (2005a) Mechanisms and consequences of competition between an alien mussel, Mytilus galloprovincialis, and an indigenous limpet, Scutellastra argenvillei. J Exp Mar Biol Ecol 317:127–142CrossRefGoogle Scholar
  50. Steffani CN, Branch GM (2005b) Growth rate, condition, and shell shape of Mytilus galloprovincialis: responses to wave exposure. Mar Ecol Prog Ser 246:197–209CrossRefGoogle Scholar
  51. 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
  52. Van Erkom Schurink C, Griffiths CL (1992) Physiological energetics of four South African mussel species in relation to body size, ration and temperature. Comp Biochem Phys A 101:779–789CrossRefGoogle Scholar
  53. Van Erkom Schurink C, Griffiths CL (1993) Factors affecting relative rates of growth in four South African mussel species. Aquaculture 109:257–273CrossRefGoogle Scholar
  54. Van Kleunen M, Dawson W, Schlaepfer D et al (2010) Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol Lett 13:947–958PubMedGoogle Scholar
  55. Wonham MJ, Carlton JT (2005) Trends in marine biological invasions at local and regional scales: the Northeast Pacific Ocean as a model system. Biol Invasions 7:369–392CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Mhairi E. Alexander
    • 1
    • 4
  • Robyn Adams
    • 1
  • Jaimie T. A. Dick
    • 2
    • 3
  • Tamara B. Robinson
    • 1
  1. 1.Department of Botany and Zoology, Centre for Invasion BiologyStellenbosch UniversityMatielandSouth Africa
  2. 2.Institute for Global Food Security, School of Biological SciencesQueen’s University BelfastBelfast, Northern IrelandUK
  3. 3.Queen’s University Marine Laboratory (QML)Portaferry, Co. Down, Northern IrelandUK
  4. 4.Institute of Biomedical and Environmental Health Research (IBEHR), School of Science and SportUniversity of the West of ScotlandPaisleyUK

Personalised recommendations