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Wasting disease regulates long-term population dynamics in a threatened seagrass

  • Population ecology - Original research paper
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Abstract

The role of disease in the long-term dynamics of threatened species is poorly quantified, as well as being under-represented in ecology and conservation management. To understand persistent host–pathogen interaction operating in a vulnerable habitat, we quantified dynamics driving patterns of seagrass density using a longitudinal study in a relatively pristine site (Isles of Scilly, UK). Replicated samples of eelgrass (Zostera marina) density and wasting disease prevalence, presumably caused by Labyrinthula zosterae, were taken from five meadows at the height of the growing season, over the years 1997–2010. Data were used to parameterise a population dynamic model, incorporating density-dependent factors and sea temperature records. We found that direct density and disease-mediated feedback operate within a network of local populations. Furthermore, our results indicate that the strength of limitation to seagrass growth by disease was increased at higher temperatures. This modification of the coupled host–pathogen dynamics forms a novel hypothesis to account for dramatic die-backs of Z. marina widely reported elsewhere. Our findings highlight the importance of disease in structuring distributions of vulnerable species, as well as the application of population modelling in order to reveal ecological processes and prioritise future mechanistic investigation.

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References

  • Bonsall MB, Hastings A (2004) Demographic and environmental stochasticity in predator–prey metapopulation dynamics. J Anim Ecol 73:1043–1055

    Article  Google Scholar 

  • Bonsall MB, van der Meijden E, Crawley MJ (2003) Contrasting dynamics in the same plant–herbivore interaction. PNAS 100:14932–14936

    Article  PubMed  CAS  Google Scholar 

  • Bonsall MB, Hasan N, Nakamura K (2007) Density dependence and noise determine the long-term dynamics of two species of lady beetle (Coleoptera: Coccinellidae: Epilachninae) in the Indonesian tropics. Ecol Entomol 32:28–37

    Article  Google Scholar 

  • Buckley YM, Briese DT, Rees R (2003a) Demography and management of the invasive plant species Hypericum perforatum. I. Using multi-level mixed-effects models for characterizing growth, survival and fecundity in a long-term data set. J Appl Ecol 40:481–493

    Article  Google Scholar 

  • Buckley YM, Briese DT, Rees R (2003b) Demography and management of the invasive plant species Hypericum perforatum. II. Construction and use of an individual-based model to predict population dynamics and the effects of management strategies. J Appl Ecol 40:494–507

    Article  Google Scholar 

  • Bull JC, Kenyon EJ, Edmunds D, Cook KJ (2010) Recent loss of Gibraltar seagrasses. Bot Mar 53:89–91

    Article  Google Scholar 

  • Burdick DM, Short FT, Wolf J (1993) An index to asses and monitor the progression of wasting disease in eelgrass Zostera marina. Mar Ecol Prog Ser 94:83–90

    Article  Google Scholar 

  • Cambridge ML, Chiffings AW, Brittan C, Moore L, McComb AJ (1986) The loss of seagrass in cockburn sound, western Australia. II. Possible causes of seagrass decline. Aquat Bot 24:269–285

    Article  Google Scholar 

  • Chase JM, Abrams PA, Grover JP, Diehl S, Chesson P, Holt RD, Richards SA, Nisbet RM, Case TJ (2002) The interaction between predation and competition: a review and synthesis. Ecol Lett 5:302–315

    Article  Google Scholar 

  • Chesson P, Kuang JJ (2008) The interaction between predation and competition. Nature 456:235–238

    Article  PubMed  CAS  Google Scholar 

  • Clark JS (2007) Models for ecological data: an introduction. Princeton University Press, Princeton

    Google Scholar 

  • Cook KJ (2002) Isles of Scilly Zostera marina monitoring 2001: expedition report. Report to Natural England, Truro

    Google Scholar 

  • Costanza R, d’Arge R, de Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, O’Neill RV, Paruelo J, Raskin RG, Sutton P, van den Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260

    Article  CAS  Google Scholar 

  • Crawley MJ (2009) The R Book. Wiley, New York

    Google Scholar 

  • Damgaard C, Weiner J, Nagashima H (2002) Modelling individual growth and competition in plant populations: growth curves of Chenopodium album at two densities. J Ecol 90:666–671

    Article  Google Scholar 

  • den Hartog C (1987) Wasting disease and other dynamic phenomena in Zostera beds. Aquat Bot 27:3–14

    Article  Google Scholar 

  • den Hartog C (1989) Early records of wasting-disease-like damage patterns in eelgrass Zostera marina. Dis Aquat Organ 7:223–226

    Article  Google Scholar 

  • Dennis B, Taper ML (1994) Density dependence in time series observations of natural populations: estimation and testing. Ecol Monogr 64(2):205–224

    Article  Google Scholar 

  • Dennison WC (1987) Effects of light on seagrass photosynthesis, growth and depth distribution. Aquat Bot 27:15–26

    Article  Google Scholar 

  • Duarte CM (1991) Allometric scaling of seagrass form and productivity. Mar Ecol Prog Ser 77:289–300

    Article  Google Scholar 

  • Duarte CM, Chiscano CL (1999) Seagrass biomass and production: a reassessment. Aquat Bot 65:159–174

    Article  Google Scholar 

  • Duarte CM, Marbà N, Agawin N, Cebrián J, Enríquez S, Fortes MD, Gallegos ME, Merino M, Olesen B, Sand-Jensen K, Uri J, Vermaat J (1994) Reconstruction of seagrass dynamics age determinations and associated tools for the seagrass ecologist. Mar Ecol Prog Ser 107:195–209

    Article  Google Scholar 

  • Duarte CM, Middelburg J, Caraco N (2005) Major role of marine vegetation on the oceanic carbon cycle. Biogeosci 2:1–8

    Article  CAS  Google Scholar 

  • Fowler SL (1992) Marine monitoring in the Isles of Scilly. Report to Natural England, Truro

    Google Scholar 

  • García MB, Goñi D, Guzman D (2010) Living at the edge: local versus positional factors in the long-term population dynamics of an endangered orchid. Cons Biol 24:1219–1229

    Article  PubMed  Google Scholar 

  • Gillanders BM (2007) Seagrasses, fish and fisheries. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Dortrecht, pp 503–536

    Google Scholar 

  • Gillman MP, Dodd M (2000) Detection of delayed density dependence in an orchid population. J Ecol 88:204–212

    Article  Google Scholar 

  • Gonzalez-Andujar JL, Fernandez-Quintanilla C, Navarrete L (2006) Population cycles produced by delayed density dependence in an annual plant. Am Nat 168:318–322

    Article  PubMed  CAS  Google Scholar 

  • Green EP, Short FT (2003) World atlas of seagrasses. University of California Press, Berkeley

    Google Scholar 

  • Hily C, Raffin C, Brun A, den Hartog C (2002) Spatiotemporal variability of wasting disease symptoms in eelgrass meadows of Brittany (France). Aquat Bot 72:37–53

    Article  Google Scholar 

  • Kendrick GA, Duarte CM, Marbà N (2005) Clonality in seagrasses, emergent properties and seagrass landscapes. Mar Ecol Prog Ser 290:291–296

    Article  Google Scholar 

  • Loibel S, do Val JBR, Andrade MD (2006) Inference for the Richards growth model using Box and Cox transformation and bootstrap techniques. Ecol Model 191:501–512

    Article  Google Scholar 

  • Marbà N, Duarte CM, Cebrián J, Gallegos ME, Olesen B, Sand-Jensen K (1996) Growth and population dynamics of Posidonia oceanica on the Spanish Mediterranean coast: elucidating seagrass decline. Mar Ecol Prog Ser 137:203–213

    Article  Google Scholar 

  • Marsh JA, Dennison WC, Alberts RS (1986) Effects of temperature on photosynthesis and respiration in eelgrass (Zostera marina L.). J Exp Mar Biol Ecol 101:257–267

    Article  Google Scholar 

  • Moore KA, Short FT (2007) Zostera: biology, ecology and management. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Dortrecht, pp 361–386

    Google Scholar 

  • Moore KA, Wetzel RL, Orth RJ (1997) Seasonal pulses of turbidity and their relation to eelgrass (Zostera marina L.) survival in an estuary. J Exp Mar Biol Ecol 215:115–134

    Article  Google Scholar 

  • Muehlstein LK (1989) Perspectives on the wasting disease of eelgrass Zostera marina. Dis Aquat Org 7:211–221

    Article  Google Scholar 

  • Muehlstein LK, Porter D, Short FT (1991) Labyrinthula zosterae sp. nov., the causative agent of wasting disease in eelgrass, Zostera marina. Mycologia 83:180–191

    Article  Google Scholar 

  • Nejrup LB, Pedersen MF (2008) Effects of salinity and water temperature on the ecological performance of Zostera marina. Mar Ecol Prog Ser 88:239–246

    Google Scholar 

  • Olesen B, Sand-Jensen K (1994a) Biomass-density patterns in the temperate seagrass Zostera marina. Mar Ecol Prog Ser 109:283–291

    Article  Google Scholar 

  • Olesen B, Sand-Jensen K (1994b) Demography of shallow eelgrass (Zostera marina) populations: shoot dynamics and biomass development. J Ecol 82:379–390

    Article  Google Scholar 

  • Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S, Short FT, Waycott M, Williams SL (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996

    Article  Google Scholar 

  • Pergent G (1990) Lepidochronological analysis of the seagrass Posidonia oceanica (L.) Delile: a standardized approach. Aquat Bot 37:39–54

    Article  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-Plus. Springer, New York

    Book  Google Scholar 

  • Plus M, Deslous-Paolib J-M, Aubyc I, Dagaulta F (2001) Factors influencing primary production of seagrass beds (Zostera noltii Hornem.) in the Thau lagoon (French Mediterranean coast). J Exp Mar Biol Ecol 259:63–84

    Article  PubMed  Google Scholar 

  • Rasmussen E (1977) The wasting disease of eelgrass (Zostera marina) and its effects on environmental factors and fauna. In: McRoy CP, Helfferich C (eds) Seagrass ecosystems, a scientific perspective. Marcel Dekker, New York, pp 1–51

    Google Scholar 

  • Royama T (1992) Analytical population dynamics. Chapman & Hall, London

    Book  Google Scholar 

  • Rozenfeld AF, Arnaud-Haond S, Hernandez-García E, Eguíluz VM, Serrao EA, Duarte CM (2008) Network analysis identifies weak and strong links in a metapopulation system. PNAS 105:18824–18829

    Article  PubMed  Google Scholar 

  • Rueda JL, Marina P, Urra J, Salas C (2009) Changes in the composition and structure of a molluscan assemblage due to eelgrass loss in southern Spain (Alboran Sea). JMBA UK 89:1319–1330

    Google Scholar 

  • Short FT, Ibelings BW, den Hartog C (1988) Comparison of a current eelgrass disease to the wasting disease in the 1930s. Aquat Bot 30:295–304

    Article  Google Scholar 

  • Tomasko DA, Lapointe BE (1991) Productivity and biomass of Thalassia testudinum as related to water column nutrient availability and epiphyte levels: field observations and experimental studies. Mar Ecol Prog Ser 75:9–16

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful to a large number of volunteers, over many years, who have collected data and made financial contributions to the Isles of Scilly seagrass project. Further funding has been provided by Natural England. In particular, we thank Cyril Nicholas (Natural England) for expert local knowledge and logistical support. Finally, we thank Michael Bonsall (University of Oxford) and Charles Sheppard (University of Warwick) for useful comments during preparation of the manuscript.

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Authors and Affiliations

  1. School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK

    James C. Bull

  2. The Morgan Building, Wellcome Trust Genome Campus, Hinxton, Cambridge, CB10 1HH, UK

    Emma J. Kenyon

  3. Natural England, Pydar House, Pydar Street, Truro, TR1 1XU, UK

    Kevan J. Cook

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  1. James C. Bull
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  2. Emma J. Kenyon
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  3. Kevan J. Cook
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Correspondence to James C. Bull.

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Communicated by David Marcogliese.

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Bull, J.C., Kenyon, E.J. & Cook, K.J. Wasting disease regulates long-term population dynamics in a threatened seagrass. Oecologia 169, 135–142 (2012). https://doi.org/10.1007/s00442-011-2187-6

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  • DOI: https://doi.org/10.1007/s00442-011-2187-6

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