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Parasitism as a determinant of community structure on intertidal flats

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Abstract

The burrowing and movement ability of the New Zealand cockle Austrovenus stutchburyi is reduced when infected by echinostome trematodes. Previous experimental evidence from a single site suggests that this parasite-induced behavioural change of a key bivalve can affect the structure of the surrounding benthic community. By using multiple regression analyses on data collected from 17 intertidal flats, we here show that cockle parasitism is associated with macrozoobenthic community structure on a larger spatial scale. Regressions were performed for animal abundance, biomass, species diversity and species richness separately, entering cockle parasitism (infection intensity), presence/absence of ghost shrimps (Callianassa filholi), cockle density, primary producer abundance and organic content, particle size, sorting coefficient and gravel content of the substrate as predictors. Next to ghost shrimps, cockle parasitism was the best predictor of animal abundance by affecting (mainly positively) 8 of the 49 most widespread species significantly. Cockle parasitism was also associated with the biomass of anthozoans (positively), nemerteans (negatively) and bivalves (positively), whereas overall animal biomass was positively related to the sorting coefficient of the substrate. Species diversity was positively associated with cockle parasitism and gravel content of the substrate. Species richness was significantly associated with cockle parasitism (positively), ghost shrimps (negatively) and abundance of primary producers (positively) in combination. The impact of cockle parasitism on benthic community structure is believed governed directly or indirectly by (1) reduced sediment disturbance, (2) increased surface structural complexity and (3) availability of larval trematodes as an additional food source.

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References

  • Admiraal W (1984) The ecology of estuarine sediment-inhabiting diatoms. Prog Phycol Res 3:269–322

    Google Scholar 

  • Allison FR (1979) Life-cycle of Curtuteria australis n.sp. (Digenea, Echinostomatidae, Himasthlinae), intestinal parasite of the South Island pied oystercatcher. N Z J Zool 6:13–20

    Article  Google Scholar 

  • Amaral ACZ, Denadai MR, Turra A, Rizzo AE (2003) Intertidal macrofauna in Brazilian subtropical tide-dominated sandy beaches. J Coast Res 35:S446–S455

    Google Scholar 

  • Babirat C, Mouritsen KN, Poulin R (2004) Equal partnership: two trematode species, not one, manipulate the burrowing behaviour of the New Zealand cockle, Austrovenus stutchburyi. J Helminthol 78:195–199

    Article  CAS  Google Scholar 

  • Ballard HR (1990) MacRSA: Macintosh application program for rapid sediment analysis. University of Otago, Dunedin

    Google Scholar 

  • Berkenbusch K, Rowden AA (1999) Factors influencing sediment turnover by the burrowing ghost shrimps Callianassa filholi (Decapoda: Thalassinidea). J Exp Mar Biol Ecol 238:283–292

    Article  Google Scholar 

  • Berkenbusch K, Rowden AA, Probert PK (2000) Temporal and spatial variation in macrofauna community composition imposed by ghost shrimps Callianassa filholi bioturbation. Mar Ecol Prog Ser 192:249–257

    Article  Google Scholar 

  • Branch GM, Pringle A (1987) The impact of the sand prawn Callianassa kraussi Stebbing on sediment turnover and bacteria, meiofauna, and benthic microflora. J Exp Mar Biol Ecol 107:219–235

    Article  Google Scholar 

  • Buchanan JB (1984) Sediment analysis. In: Holme NA, McIntyre AD (eds) Methods for the study of marine benthos, 2nd edn. Blackwell, Oxford, pp 41–65

    Google Scholar 

  • Butler S, Bird FL (2007) Estimating density of intertidal ghost shrimps using counts of burrow openings. Is the method reliable? Hydrobiologia 589:303–314

    Article  Google Scholar 

  • Byers JE, Blakeslee AMH, Linder E, Cooper AB, Maguire TJ (2008) Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology 89:439–451

    Article  Google Scholar 

  • Combes C (1996) Parasites, biodiversity and ecosystem stability. Biodivers Conserv 5:953–962

    Article  Google Scholar 

  • Currie DR, Small KJ (2006) The influence of dry-season conditions on the bottom dwelling fauna of an east Australian sub-tropical estuary. Hydrobiologia 560:345–361

    Article  Google Scholar 

  • Flach EC (1995) The influence of the cockle, Cerastoderma edule, on the macrozoobenthic community of tidal flats in the Wadden Sea. Mar Ecol 17:87–98

    Article  Google Scholar 

  • Fredensborg BL, Mouritsen KN, Poulin R (2006) Relating bird host distribution and spatial heterogeneity in trematode infections in an intertidal snail: from small to large scale. Mar Biol 149:275–283

    Article  Google Scholar 

  • Fujii T (2007) Spatial patterns of benthic macrofauna in relation to environmental variables in an intertidal habitat in the Humber estuary, UK: Developing a tool for estuarine shoreline management. Estuar Coast Shelf Sci 75:101–119

    Article  Google Scholar 

  • Gross K, Cardinale BJ (2007) Does species richness drive community production or vice versa? Reconciling historical and contemporary paradigms in competitive communities. Am Nat 170:207–220

    Article  Google Scholar 

  • Hopper JV, Poulin R, Thieltges DW (2008) Buffering role of the intertidal anemone Anthopleura aureoradiata in cercarial transmission from snails to crabs. J Exp Mar Biol Ecol 367:303–314

    Article  Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957

    Article  Google Scholar 

  • Krebs CJ (1999) Ecological methodology, 2nd edn. Addison-Welsey, Menlo Park

    Google Scholar 

  • Lefèvre T, Lebarbenchon C, Gauthier-Clerc M, Missé D, Poulin R, Thomas F (2009) The ecological significance of manipulative parasites. Trends Ecol Evol 24:41–48

    Article  Google Scholar 

  • Lepitzki DAW, Scott ME, McLaughlin JD (1994) Influence of storage and examination methods on the recovery and size of metacercariae of Cyathocotyle bushiensis and Spaeridotrema pseudoglobulus (Digenea). J Parasitol 80:454–460

    Article  CAS  Google Scholar 

  • Lorentzen CJ (1967) Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol Oceanogr 12:343–346

    Article  Google Scholar 

  • Martorelli SR, Poulin R, Mouritsen KN (2006) A new cercaria and metacercaria of Acanthoparyphium (Echinostomatidae) found in an intertidal snail Zeacumantus subcarinatus (Batillaridae) from New Zealand. Parasitol Int 55:163–167

    Article  Google Scholar 

  • Minchella DJ, Scott ME (1991) Parasitism: a cryptic determinant of animal community structure. Trends Ecol Evol 6:250–254

    Article  CAS  Google Scholar 

  • Mouritsen KN (2002) The parasite-induced surfacing behaviour in the cockle Austrovenus stutchburyi: a test of an alternative hypothesis and identification of potential mechanisms. Parasitology 124:521–528

    CAS  PubMed  Google Scholar 

  • Mouritsen KN (2004) Intertidal facilitation and indirect effects: causes and consequences of crawling in the New Zealand cockle. Mar Ecol Prog Ser 271:207–220

    Article  Google Scholar 

  • Mouritsen KN, Haun SCB (2008) Community regulation by herbivore parasitism and density: trait-mediated indirect interactions in the intertidal. J Exp Mar Biol Ecol 367:236–246

    Article  Google Scholar 

  • Mouritsen KN, Poulin R (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124:S101–S117

    PubMed  Google Scholar 

  • Mouritsen KN, Poulin R (2003a) Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator’s nightmare. Int J Parasitol 33:1043–1050

    Article  Google Scholar 

  • Mouritsen KN, Poulin R (2003b) The mud flat anemone-cockle association: mutualism in the intertidal zone? Oecologia 135:131–137

    Article  Google Scholar 

  • Mouritsen KN, Poulin R (2005a) Parasites boost biodiversity and change animal community structure by trait-mediated indirect effects. Oikos 108:344–350

    Article  Google Scholar 

  • Mouritsen KN, Poulin R (2005b) Parasitism can influence the intertidal zonation of non-host organisms. Mar Biol 148:1–11

    Article  Google Scholar 

  • Mouritsen KN, Poulin R (2006) A parasite indirectly impacts both abundance of primary producers and biomass of secondary producers in an intertidal benthic community. J Mar Biol Assoc UK 86:221–226

    Article  Google Scholar 

  • Mouritsen KN, Mouritsen LT, Jensen KT (1998) Change of topography and sediment characteristics on an intertidal mud-flat following mass-mortality of the amphipod Corophium volutator. J Mar Biol Assoc UK 78:1167–1180

    Article  Google Scholar 

  • Pillay D, Branch GM, Forbes AT (2007) Effects of Callianassa kraussi on microbial biofilms and recruitment of macrofauna: a novel hypothesis for adult-juvenile interactions. Mar Ecol Prog Ser 347:1–14

    Article  Google Scholar 

  • Posey MH (1986) Changes in a benthic community associated with dense beds of a burrowing deposit feeder, Callianassa californiensis. Mar Ecol Prog Ser 31:15–22

    Article  Google Scholar 

  • Posey MH, Alphin TD, Cahoon L (2006) Benthic community responses to nutrient enrichment and predator exclusion: influence of background nutrient concentrations and interactive effects. J Exp Mar Biol Ecol 330:105–118

    Article  CAS  Google Scholar 

  • Reise K (1985) Tidal flat ecology. An experimental approach to species interactions. Springer, Berlin

    Book  Google Scholar 

  • Siebert T, Branch GM (2005) Interactions between Zostera capensis and Callianassa kraussi: influences on community composition of eelgrass and sandflats. Afr J Mar Sci 27:357–373

    Article  Google Scholar 

  • Snelgrove PVR, Butman CA (1994) Animal sediment relationships revisited—cause and effect. Oceanogr Mar Biol 32:111–177

    Google Scholar 

  • Sousa WP (1991) Can models of soft-sediment community structure be complete without parasites? Am Zool 31:821–830

    Article  Google Scholar 

  • Stewart MJ, Creese RG (2002) Transplants of intertidal shellfish for enhancement of depleted populations: preliminary trials with the New Zealand little neck clam. J Shellfish Res 21:21–27

    Google Scholar 

  • Thieltges DW, Jensen KT, Poulin R (2008a) The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135:407–426

    CAS  PubMed  Google Scholar 

  • Thieltges DW, de Montaudouin X, Fredensborg B, Jensen KT, Koprivnikar J, Poulin R (2008b) Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems. Mar Ecol Prog Ser 372:147–155

    Article  Google Scholar 

  • Thomas F, Poulin R (1998) Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology 116:431–436

    Article  Google Scholar 

  • Thomas F, Renaud F, de Meeûs T, Poulin R (1998) Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone? Proc R Soc Lond B 265:1091–1096

    Article  Google Scholar 

  • Thomas F, Adamo S, Moore J (2005) Parasitic manipulation: where are we and where should we go? Behav Processes 68:185–199

    Article  Google Scholar 

  • Valiela I (1995) Marine ecological processes. Springer, Berlin

    Book  Google Scholar 

  • Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100

    Article  Google Scholar 

  • Whitlatch RB, Hines AH, Thrush SF, Hewitt JE, Cummings V (1997) Benthic faunal responses to variation in patch density and patch size of a suspension-feeding bivalve. J Exp Mar Biol Ecol 216:171–189

    Article  Google Scholar 

  • Wood CL, Byers JE, Cottingham KL, Altman I, Donahue MJ, Blakeslee AMH (2007) Parasites alter community structure. Proc Natl Acad Sci 104:9335–9339

    Article  CAS  Google Scholar 

  • Ysebaert T, Herman PMJ (2002) Spatial and temporal variation in benthic macrofauna and relationships with environmental variables in an estuarine, intertidal soft-sediment environment. Mar Ecol Prog Ser 244:105–124

    Article  Google Scholar 

  • Ziebis W, Forster S, Huettel M, Jørgensen BB (1996) Complex burrows of the mud shrimp Callianassa truncata and their geochemical impact in the sea bed. Nature 382:619–622

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Gerd Banke, Brian Fredensborg, Karina Holmes, Maureen Howard, Susan Lusseau, Matthew McArthur and Kate Steger for technical assistance. The Danish Natural Science Research Council (KNM), the Marsden Fund and a James Cook Research Fellowship from the Royal Society of New Zealand (RP) provided funding.

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Authors and Affiliations

  1. Department of Biological Sciences, Marine Ecology, Aarhus University, Finlandsgade 14, 8200, Aarhus N, Denmark

    Kim N. Mouritsen

  2. Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand

    Robert Poulin

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  1. Kim N. Mouritsen
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  2. Robert Poulin
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Correspondence to Kim N. Mouritsen.

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Communicated by U. Sommer.

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Mouritsen, K.N., Poulin, R. Parasitism as a determinant of community structure on intertidal flats. Mar Biol 157, 201–213 (2010). https://doi.org/10.1007/s00227-009-1310-2

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