Skip to main content

Advertisement

SpringerLink
Log in

Replacement of native seagrass with invasive algal detritus: impacts to estuarine sediment communities

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Biological invasions modify the quality and supply of detrital subsidies to aquatic and terrestrial ecosystems. Where the invader has very different traits to native species, major changes in associated consumer communities may result, as a consequence of differences in their nutritional value and effects on the sedimentary habitat. We assessed how the replacement of seagrasses with the invasive alga Caulerpa taxifolia in modified Australian estuaries influences invertebrate communities of mudflats that are subsidized by detritus from submerged aquatic vegetation. Two months after experimental enrichment of sediments with high (60 g dry weight per 0.25 m2 plot) or low (30 g dry weight) quantities of either non-native C. taxifolia or native Posidonia australis or Zostera capricorni detritus, there were positive effects of detrital addition on invertebrate abundance that occurred irrespective of the resource added. By 4 months after addition, however, detritus from invasive C. taxifolia had produced effects on benthic communities that could not be replicated by detritus from either of the native seagrasses. Plots receiving the high loading of C. taxifolia detritus contained fewer invertebrates than plots of the other treatments, perhaps due to the induction of sediment hypoxia. The pattern, however, reversed at low detrital loading, with the plots receiving 30 g of C. taxifolia containing more invertebrates and more taxa than the other plots, presumably due to the greater resource availability for detritivores. Our results demonstrate that replacement of native seagrass with invasive algal detritus can have large impacts on sediment-dwelling communities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawaii. Oecologia 141:612–619

    Article  PubMed  Google Scholar 

  • Alonso A, González-Muñoz N, Castro-Díez P (2010) Comparison of leaf decomposition and macroinvertebrate colonization between exotic and native trees in a freshwater ecosystem. Ecol Res 25:647–653

    Article  Google Scholar 

  • Amade P, Lemée R (1998) Chemical defense of the Mediterranean alga Caulerpa taxifolia: variations in caulerpenyne production. Aquat Toxicol 43:287–300

    Article  CAS  Google Scholar 

  • Ashton IW, Hyatt LA, Howe KM, Gurevitch J, Lerdau MT (2005) Invasive species accelerate decomposition and litter nitrogen loss in a mixed deciduous forest. Ecol Appl 15:1263–1272

    Article  Google Scholar 

  • Baumgartner FA, Motti CA, de Nys R, Paul NA (2009) Feeding preferences and host associations of specialist marine herbivores align with quantitative variation in seaweed secondary metabolites. Mar Ecol Prog Ser 396:1–12

    Article  CAS  Google Scholar 

  • Beesley PL, Ross GJB, Wells A (1998) Mollusca: the southern synthesis. Fauna of Australia, volume 5, parts A and B. CSIRO Publishing, Melbourne

    Google Scholar 

  • Beesley PL, Ross GJB, Glasby CJ (2000) Polychaetes and allies: the southern synthesis. Fauna of Australia, volume 4A. Polychaeta, Myzostomidia, Pogonophora, Echiura, Sipuncula. CSIRO Publishing, Melbourne

    Google Scholar 

  • Bishop MJ, Kelaher BP (2007) Impacts of detrital enrichment on estuarine assemblages: disentangling effects of frequency and intensity of disturbance. Mar Ecol Prog Ser 341:25–36

    Article  Google Scholar 

  • Bishop MJ, Kelaher BP (2008) Non-additive, identity-dependent effects of detrital species mixing on soft-sediment communities. Oikos 117:531–542

    Article  Google Scholar 

  • Bishop MJ, Kelaher BP, Alquezar RA, York PH, Ralph PJ, Skilbeck CG (2007) Trophic cul-de-sac, Pyrazus ebeninus, limits trophic transfer through an estuarine detritus-based food web. Oikos 116:427–438

    Article  Google Scholar 

  • Bishop MJ, Coleman MA, Kelaher BP (2010) Cross-habitat impacts of species decline: response of estuarine sediment communities to changing detrital resources. Oecologia 163:517–525

    Article  PubMed  Google Scholar 

  • Blair JM, Parmelee RW, Beare MH (1990) Decay rates, nitrogen fluxes, and decomposer communities of single- and mixed-species foliar litter. Ecology 71:1976–1985

    Article  Google Scholar 

  • Bolam SG, Fernandes TF, Read P, Raffaelli D (2000) Effects of macroalgal mats on intertidal sandflats: an experimental study. J Exp Mar Biol Ecol 249:123–137

    Article  PubMed  Google Scholar 

  • Boudouresque C-F, Meinesz A, Ribera MA, Ballesteros E (1995) Spread of the green alga Caulerpa taxifolia (Caulerpales, Chlorophyta) in the Mediterranean: possible consequences of a major ecological event. Sci Mar 59:21–29

    Google Scholar 

  • Casu D, Ceccherelli G, Sechi N, Rumolo P, Gianluca S (2009) Caulerpa racemosa var. cylindracea as a potential source of organic matter for benthic consumers: evidences from stable isotope analysis. Aquat Ecol 43:1023–1029

    Article  CAS  Google Scholar 

  • Cebrián J (1999) Patterns in the fate of production in plant communities. Am Nat 154:449–468

    Article  PubMed  Google Scholar 

  • Ceccherelli G, Cinelli F (1997) Short-term effects of nutrient enrichment of the sediment and interactions between the seagrass Cymodocea nodosa and the introduced green alga Caulerpa taxifolia in a Mediterranean bay. J Exp Mar Biol Ecol 217:165–177

    Article  Google Scholar 

  • Ceccherelli G, Cinelli F (1999) A pilot study of nutrient enriched sediments in a Cymodocea nodosa bed invaded by the introduced alga Caulerpa taxifolia. Bot Mar 42:409–417

    Article  CAS  Google Scholar 

  • De Villéle X, Verlaque M (1995) Changes and degradation in a Posidonia oceanica bed invaded by the introduced tropical alga Caulerpa taxifolia in the north western Mediterranean. Bot Mar 38:79–87

    Google Scholar 

  • Enriquez S, Duarte CM, Sand-Jensen K (1993) Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C:N:P content. Oecologia 94:457–471

    Article  Google Scholar 

  • Fernades MB, Deveney MR (2008) The effect of substrate cover on sediment chemistry and morphology: seagrasses versus the invasive seaweed Caulerpa taxifolia. In: Deveney MR, Rowling KP, Wiltshire KH, Manning CE, Fernandes MB, Collings GJ, Tanner JE (eds) Caulerpa taxifolia (M. Vahl.) C. Agardh: environmental risk assessment. South Australian Research and Development Institute, Adelaide, pp 82–95

    Google Scholar 

  • Findlay S, Tenore K (1982) Nitrogen source for a detritivore: detritus substrate versus associated microbes. Science 218:371–373

    Article  PubMed  CAS  Google Scholar 

  • Gessner MO (1991) Differences in processing dynamics of fresh and dried leaf litter in a freshwater ecosystem. Freshwat Biol 26:387–398

    Article  CAS  Google Scholar 

  • Godbold JA, Solan M, Killham K (2009) Consumer and resource diversity effects on marine macroalgal decomposition. Oikos 118:77–86

    Article  Google Scholar 

  • Godoy O, Castro-Díez P, Van Logtestijn RSP, Cornelissen JHC, Valladres F (2010) Leaf litter traits of invasive species slow down decomposition compared to Spanish natives: a broad phylogenetic comparison. Oecologia 162:781–790

    Article  PubMed  Google Scholar 

  • Heip CHR, Goosen NK, Herman PMJ, Krokamp J, Middelburg JJ, Soetaert K (1995) Production and consumption of biological particles in temperate tidal estuaries. Oceanogr Mar Biol Annu Rev 33:1–149

    Google Scholar 

  • Industry and Investment NSW (2009) NSW control plan for the noxious marine alga Caulerpa taxifolia. Industry and Investment NSW, Orange, August 2009

  • Jaubert JM, Chisholm JRM, Ducrot D, Ripley HT, Roy L, Passeron-Seitre G (1999) No deleterious alterations in Posidonia beds in the Bay of Menton (France) eight years after Caulerpa taxifolia colonization. J Phycol 35:1113–1119

    Article  Google Scholar 

  • Jaubert JM, Chisholm JRM, Minghelli-Roman A, Marchioretti M, Morrow JH, Ripley HT (2003) Re-evaluation of the extent of Caulerpa taxifolia development in northern Mediterranean using airborne spectrographic sensing. Mar Ecol Prog Ser 263:75–82

    Article  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae, and natural phytoplankton. Biochem Physiol Pflanz 167:191–194

    CAS  Google Scholar 

  • Kelaher BP, Levinton JS (2003) Variation in detrital enrichment causes spatio-temporal variation in soft-sediment assemblages. Mar Ecol Prog Ser 261:85–97

    Article  Google Scholar 

  • Kristensen E (1994) Decomposition of macroalgae, vascular plants and sediment detritus in seawater: use of stepwise thermogravimetry. Biogeochemistry 26:1–24

    Article  Google Scholar 

  • Leff LG, McArthur JV (1989) The effect of leaf pack composition on processing: a comparison of mixed and single species packs. Hydrobiologia 182:219–224

    Article  Google Scholar 

  • Lemée R, Pesando D, Durand-Clément M, Dubreuill A, Meinesz A, Guerriero A, Pietra F (1993) Preliminary survey of toxicity of the green alga Caulerpa taxifolia introduced into the Mediterranean. J Appl Phycol 5:485–493

    Article  Google Scholar 

  • Levin LA, Neira C, Grosholz ED (2006) Invasive cordgrass modifies wetland trophic function. Ecology 87:419–432

    Article  PubMed  Google Scholar 

  • Lopes RJ, Pardal MA, Marques JC (2000) Impact of macroalgae blooms and wader predation on intertidal macroinvertebrates—experimental evidence in the Mondego estuary (Portugal). J Exp Mar Biol Ecol 249:165–179

    Article  PubMed  Google Scholar 

  • MacIntyre HL, Geider RJ, Miller DC (1996) Microphytobenthos: the ecological role of the “secret garden” of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 19:186–201

    Article  Google Scholar 

  • Macreadie PI, Allen K, Kelaher BP, Ralph PJ, Skilbeck CG (2012) Paleoreconstruction of estuarine sediments reveal human-induced weakening of coastal carbon sinks. Glob Change Biol 18:891–901

    Article  Google Scholar 

  • Meinesz A, Belsher T, Thibaut T, Antolic B, Mustapha KB, Boudouresque CF, Chiaverini D, Cinelli F, Cottalorda JM, Djellouli A, El Abed A, Orestano C, Grau AM, Ivesa L, Jaklin A, Langar H, Massuti-Pascual E, Peirano A, Tunesi L, de Vaugelas J, Zavodnik N, Zuljevic A (2001) The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean. Biol Invasions 3:201–210

    Article  Google Scholar 

  • Melville AJ, Connolly R (2003) Spatial analysis of stable isotope data to determine primary sources of nutrition for fish. Oecologia 136:499–507

    Article  PubMed  Google Scholar 

  • Moore JC, Berlow EL, Coleman DC, de Ruiter PC, Dong Q, Hastings A, Johnson NC, McCann KS, Melville K, Morin PJ, Nadelhoffer K, Rosemond AD, Post DM, Sabo JL, Scow KM, Vanni MJ, Wall DH (2004) Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600

    Article  Google Scholar 

  • Norkko A, Bonsdorff E (1996) Population responses of coastal zoobenthos to stress induced by drifting algal mats. Mar Ecol Prog Ser 140:141–151

    Article  Google Scholar 

  • Oakes JM, Bautista MD, Jones WB, Maher D, Eyre BD (2011) Carbon self-utilisation may assist Caulerpa taxifolia invasion. Limnol Oceanogr 56:1824–1831

    Article  Google Scholar 

  • Olabarria C, Incera M, Garrido J, Rossi F (2010) The effect of wrack composition and diversity on macrofaunal assemblages in intertidal marine sediments. J Exp Mar Biol Ecol 396:18–26

    Article  Google Scholar 

  • Oliver I, Beattie AJ (1996) Invertebrate morphospecies as surrogates for species: a case study. Conserv Biol 10:99–109

    Article  Google Scholar 

  • Page HM, Lastra M, Rodil IF, Briones MJI, Garrido J (2010) Effects of non-native Spartina patens on plant and sediment organic matter carbon incorporation into the local invertebrate community. Biol Invas 12:3825–3838

    Article  Google Scholar 

  • Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Ann Rev Ecol Syst 28:289–316

    Article  Google Scholar 

  • Preisler A, de Beer D, Lichtschlag A, Lavik A, Lavik G, Boetius A, Barker Jørgensen B (2007) Biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment. ISME J 1:341–353

    PubMed  CAS  Google Scholar 

  • Rodil IF, Olabarria C, Lastra M, Lopez J (2008) Differential effects of native and invasive algal wrack on macrofaunal assemblages inhabiting exposed sandy beaches. J Exp Mar Biol Ecol 358:1–13

    Article  Google Scholar 

  • Rossi F (2006) Small-scale burial of macroalgal detritus in marine sediments: Effects of Ulva spp. on the spatial distribution of macrofauna assemblages. J Exp Mar Biol Ecol 332:84–95

    Article  Google Scholar 

  • Rossi F (2007) Surface feeders recycle buried macro-algal detritus. Use of dual-labelling experiments in the field. Mar Biol 150:1073–1081

    Article  CAS  Google Scholar 

  • Rossi F, Incera M, Callier M, Olabarria C (2011) Effects of detrital non-native and native macroalgae on the nitrogen and carbon cycling in intertidal sediments. Mar Biol 158:2705–2715

    Article  CAS  Google Scholar 

  • Rublee PA (1982) Seasonal distribution of bacteria in salt-marsh sediments in North Carolina. Est Coast Shelf Sci 15:67–74

    Article  Google Scholar 

  • Scanes P, Coade G, Doherty M, Hill R (2007) Evaluation of the utility of water quality based indicators of estuarine lagoon condition in NSW, Australia. Est Coast Shelf Sci 74:306–319

    Article  Google Scholar 

  • Schaffelke B, Smith JE, Hewitt CL (2006) Introduced macroalgae: a growing concern. J Appl Phycol 18:529–541

    Article  Google Scholar 

  • Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. Univ of California Press, Berkeley

    Google Scholar 

  • Taylor SL, Bishop MJ, Kelaher BP, Glasby TM (2010) Impacts of detritus from the invasive alga Caulerpa taxifolia on a soft sediment community. Mar Ecol Prog Ser 420:43–81

    Article  Google Scholar 

  • Thrush SF (1986) The sublittoral macrobenthic community structure of an Irish sea-lough: effect of decomposing accumulations of seaweed. J Exp Mar Biol Ecol 96:199–212

    Article  Google Scholar 

  • Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Short FT, Williams SL (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Nat Acad Sci 106:12377–12381

    Article  PubMed  CAS  Google Scholar 

  • Whitcraft CR, Levin LA, Talley D, Crooks JA (2008) Utilization of invasive tamarisk by salt marsh consumers. Oecologia 158:259–272

    Article  PubMed  Google Scholar 

  • Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. An Rev Ecol Evol Syst 38:327–359

    Article  Google Scholar 

  • Winer BJ (1971) Statistical principles in experimental design, 2nd edn. McGraw-Hill Kogakusha, Tokyo

    Google Scholar 

  • Wright JT, Byers JE, Koukoumaftsis LP, Ralph PJ, Gribben PE (2010) Native species behaviour mitigates the impact of habitat-forming invasive seaweed. Oecologia 163:527–534

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank M. Cole and S. Taylor for assistance with field work and sample processing. Two anonymous reviewers provided helpful comments that improved the quality of this paper. This study was funded by an Australian Research Council Discovery Grant to B. P. K. and a Hermon Slade Foundation Grant to B. P. K. and M. J. B. The experiments comply with the current laws of Australia.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Macquarie University, North Ryde, NSW, 2109, Australia

    Melanie J. Bishop

  2. Batemans Marine Park, PO Box 341, Narooma, NSW, 2546, Australia

    Brendan P. Kelaher

Authors
  1. Melanie J. Bishop
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brendan P. Kelaher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Melanie J. Bishop.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bishop, M.J., Kelaher, B.P. Replacement of native seagrass with invasive algal detritus: impacts to estuarine sediment communities. Biol Invasions 15, 45–59 (2013). https://doi.org/10.1007/s10530-012-0267-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-012-0267-0

Keywords

Search

Navigation