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Ecosystems

, Volume 22, Issue 1, pp 49–63 | Cite as

Sandy Beaches as Biogeochemical Hotspots: The Metabolic Role of Macroalgal Wrack on Low-productive Shores

  • Iván F. RodilEmail author
  • Mariano Lastra
  • Jesús López
  • Ana P. Mucha
  • Joana P. Fernandes
  • Sara V. Fernandes
  • Celia Olabarria
Article
  • 203 Downloads

Abstract

Sandy beaches, which represent the most common type of land–sea interface, harbor distinctive biotic communities and regulate the flow of energy between marine and terrestrial ecosystems. Accumulations of sea wrack on sandy beaches are of crucial importance for recycling beach nutrients and for regulating trophic connectivity and coastal functioning. We investigated the role of beaches as biogeochemical hotspots by examining the metabolic activity in accumulations of different species of wrack on two exposed beaches affected by different levels of human pressure. Experimental wrack patches provided large amounts of different sedimentary nutrients over time due to remineralization of the algae. Unsurprisingly, the variation in the nutrients present in the beach sediments was related to the species of wrack considered. Macroalgal wrack was metabolically very active and supported high respiration rates represented by intense CO2 fluxes. Importantly, we demonstrated that the wrack metabolic rate differed significantly depending on the algal species considered. Different macrofauna and bacterial assemblages were identified in the different wrack patches and on the different beaches. We suggest that human activities such as beach grooming can modify the wrack-associated communities, thus contributing to the variability in the biogeochemical processes and metabolic rates. Significant changes in the type and amount of wrack deposited on beaches can change fundamental processes related to the marine-terrestrial transfer of nutrients and energy and to the marine-atmospheric transfer of CO2 emissions, with ecological consequences for nearshore environments.

Keywords:

bacterial assemblages benthic macrofauna CO2 emissions metabolic hotspots non-native species nutrient inputs 

Notes

Acknowledgements

We thank B. Araujo, P. de Pedro, and L. Gestoso for field and laboratory assistance. We also thank F. Barreiro, for providing some of the photographs included in this paper, and P. Lucena-Moya for comments in an early version of this manuscript. The constructive comments of two anonymous reviewers and the handling editor improved the final version of this manuscript. This study was funded by the IACOBUS European cooperation program, the Portuguese Foundation for Science and Technology (SFRH/ BPD/ 87042/ 2012) and the Galician Government (GRC2013/0049). IFR is supported by strategic research funding for collaboration between the University of Helsinki and Stockholm University.

Supplementary material

10021_2018_253_MOESM1_ESM.docx (6.6 mb)
Supplementary material 1 (DOCX 6732 kb)

References

  1. Anderson MJ, Gorley RN, Clarke KR. 2008. PERMANOVA + for FRIMER: guide to software and statistical methods. Plymouth, UK: PRIMER-E.Google Scholar
  2. Barott KL, Rodriguez-Brito B, Janouškovec J, Marhaver KL, Smith JE, Keeling P. 2011. Microbial diversity associated with four functional groups of benthic reef algae and the reef − building coral Montastraea annularis. Environ Microbiol 13:1192–204.CrossRefGoogle Scholar
  3. Barreiro F, Gómez M, Lastra M, López J, De la Huz R. 2011. Annual cycle of wrack supply to sandy beaches: effect of the physical environment. Marine Ecol Prog Ser 433:65–74.CrossRefGoogle Scholar
  4. Barreiro F, Gómez M, López J, Lastra M, De la Huz R. 2013. Coupling between macroalgal inputs and nutrients outcrop in exposed sandy beaches. Hydrobiologia 700:73–84.CrossRefGoogle Scholar
  5. Bishop M, Coleman MA, Kelaher BP. 2010. Cross-habitat impacts of species decline: response of estuarine sediment communities to changing detrital resources. Oecologia 163:517–25.CrossRefGoogle Scholar
  6. Bucholc K, Szymczak-Żyła M, Lubecki L, Zamojska A, Hapter P, Tjernström E, Kowalewska G. 2014. Nutrient content in macrophyta collected from southern Baltic Sea beaches in relation to eutrophication and biogas production. Sci Total Environ 473–474:298–307.CrossRefGoogle Scholar
  7. Byrnes JE, Reed DC, Cardinale BJ, Cavanaugh KC, Holbrook SJ, Schmitt RJ. 2011. Climate-driven increases in storm frequency simplify kelp forest food webs. Glob Change Biol 17:2513–24.CrossRefGoogle Scholar
  8. Cardinale M, Brusetti L, Quatrini P, Borin S, Puglia AM, Rizzi A, Zanardini E, Sorlini C, Corselli C, Daffonchio D. 2004. Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl Environ Microbiol 70:6147–56.CrossRefGoogle Scholar
  9. Clarke KR, Gorley RN. 2006. PRIMER v6: User Manual/Tutorial. Plymouth: PRIMER-E. p 192.Google Scholar
  10. Colombini I, Chelazzi L. 2003. Influence of marine allochthonous input on sandy beach communities. Oceanogr Mar Biol: Ann Rev 41:115159.Google Scholar
  11. Coupland GT, Duarte CM, Walker DI. 2007. High metabolic rates in beach cast communities. Ecosystems 10:1341–50.CrossRefGoogle Scholar
  12. Cowles A, Hewitt JE, Taylor RB. 2009. Density, biomass and productivity of small mobile invertebrates in a wide range of coastal habitats. Mar Ecol Prog Ser 384:175–85.CrossRefGoogle Scholar
  13. Crawley KR, Hyndes GA, Vanderklift MA, Revill AT, Nichols PD. 2009. Allochthonous brown algae are the primary food source for consumers in a temperate, coastal environment. Mar Ecol Prog Ser 376:33–44.CrossRefGoogle Scholar
  14. De la Huz R, Lastra M, Junoy J, Castellanos C, Vieitez JM. 2005. Biological impacts of oil pollution and cleaning in the intertidal zone of exposed sandy beaches: preliminary study of the “Prestige” oil spill. Estuar Coast Shelf Sci 65:19–29.CrossRefGoogle Scholar
  15. Dugan JE, Hubbard DM, McCrary MD, Pierson MO. 2003. The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed sandy beaches of southern California. Estuar Coast Shelf Sci 58:25–40.CrossRefGoogle Scholar
  16. Dugan JE, Hubbard DM, Page HM, Schimel JP. 2011. Marine macrophyte wrack inputs and dissolved nutrients in beach sands. Estuar Coast 34:839–50.CrossRefGoogle Scholar
  17. Duggins EO, Eckman JE. 1997. Is kelp detritus a good food for suspension feeders? Effects of kelp species, age and secondary metabolites. Mar Biol 128:489–95.CrossRefGoogle Scholar
  18. García-Robledo E, Corzo A, García de Lomas J, van Bergeijk S. 2008. Biogeochemical effects of macroalgal decomposition on intertidal microbenthos: a microcosm experiment. Mar Ecol Prog Ser 356:139–51.CrossRefGoogle Scholar
  19. Hanisak M. 1993. Nitrogen release from decomposing seaweeds: species and temperature effects. J Appl Phycol 5:175–81.CrossRefGoogle Scholar
  20. Ince R, Hyndes GA, Lavery PS, Vanderklift MA. 2007. Marine macrophytes directly enhance abundances of sandy beach fauna through provision of food and habitat. Estuar Coast Shelf Sci 74:77–86.CrossRefGoogle Scholar
  21. Inglis G. 1989. The colonisation and degradation of stranded Macrocystis pyrifera (L.) C. Ag. by the macrofauna of a New Zealand sandy beach. J Exp Mar Biol Ecol 125:203–17.CrossRefGoogle Scholar
  22. Koop K, Griffiths CL. 1982. The relative significance of bacteria, meio- and macrofauna on an exposed sandy beach. Mar Biol 66:295–300.CrossRefGoogle Scholar
  23. Koop K, Newell RC, Lucas MI. 1982. Microbial regeneration of nutrients from the decomposition of macrophyte debris on the shore. Mar Ecol Prog Ser 9:91–6.CrossRefGoogle Scholar
  24. Krause-Jensen D, Duarte CM. 2016. Substantial role of macroalgae in marine carbon sequestration. Nat Geosci 9:737–42.CrossRefGoogle Scholar
  25. Krumhansl KA, Scheibling RE. 2012. Detrital subsidy from subtidal kelp beds is altered by the invasive green alga Codium fragile spp. fragile. Mar Ecol Progr Ser 456:73–85.CrossRefGoogle Scholar
  26. Langsrud Ø. 2003. ANOVA for unbalanced data: use Type II instead of Type III sums of squares. Stat Comput 13:163–7.CrossRefGoogle Scholar
  27. Lastra M, Page HM, Dugan JE, Hubbard DM, Rodil IF. 2008. Processing of allochthonous macrophyte subsidies by sandy beach consumers: estimates of feeding rates and impacts on food resources. Mar Biol 154:163–74.CrossRefGoogle Scholar
  28. Lavery PS, McMahon K, Weyers J, Boyce MC, Oldham CE. 2013. Release of dissolved organic carbon from seagrass wrack and its implications for trophic connectivity. Mar Ecol Progr Ser 494:121–33.CrossRefGoogle Scholar
  29. Lenth RV. 2016. Least-squares means: the R package lsmeans. J Stat Softw 69(1):1–33.CrossRefGoogle Scholar
  30. Malm T, Råberg S, Fell S, Carlsson P. 2004. Effects of beach cast cleaning on beach quality, microbial food web, and littoral macrofaunal biodiversity. Estuar Coast Shelf Sci 60:339–47.CrossRefGoogle Scholar
  31. McClain ME, Boyer EW, Dent CL, Gergel SE, Grimm NB, Groffman PM, Hart SC, Harvey JW, Johnston CA, Mayorga E, McDowell WH, Pinay G. 2003. Biogeochemical hotspots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6:310–12.CrossRefGoogle Scholar
  32. Mews M, Zimmer M, Jelinski DE. 2006. Species-specific decomposition rates of beach-cast wrack in Barkley Sound, British Columbia, Canada. Mar Ecol Progr Ser 328:155–60.CrossRefGoogle Scholar
  33. Olabarria C, Lastra M, Garrido J. 2007. Succession of macrofauna on macroalgal wrack of an exposed sandy beach: effects of patch size and site. Mar Environ Res 63(1):19–40.CrossRefGoogle Scholar
  34. Olabarria C, Incera M, Garrido J, Rodil IF, Rossi F. 2009. Intraspecific diet shift in Talitrus saltator inhabiting exposed sandy beaches. Estuar Coast Shelf Sci 84:282–8.CrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. Orr M, Zimmer M, Jelinski DE, Mews M. 2005. Wrack deposition on different beach types: spatial and temporal variation in the pattern of subsidy. Ecology 86:1496–507.CrossRefGoogle Scholar
  37. Park K-J, Kim BY, Park SK, Lee J-H, Kim YS, Choi HG, Nam KW. 2012. Morphological and biochemical differences in three Undaria pinnatifida populations in Korea. Algae 27(3):189–96.CrossRefGoogle Scholar
  38. Pelletier AJD, Jelinski DE, Treplin M, Zimmer M. 2011. Colonisation of beachcast macrophyte wrack patches by talitrid amphipods: a primer. Estuar Coast 34:863–71.CrossRefGoogle Scholar
  39. Quijón PA, Tummon Flynn P, Duarte C. 2017. Beyond negative perceptions: The role of some marine invasive species as trophic subsidies. Mar Pollut Bull 116(1–2):538–9.CrossRefGoogle Scholar
  40. Ranjard L, Poly F, Lata J-C, Mougel C, Thioulouse J, Nazaret S. 2001. Characterization of bacterial and fungal soil communities by automated ribosomal intergenic spacer analysis fingerprints: biological and methodological variability. Appl Environ Microbiol 67:4479–87.CrossRefGoogle Scholar
  41. R Development Core Team. 2016. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  42. Rodil IF, Olabarria C, Lastra M, López 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.CrossRefGoogle Scholar
  43. Rodil IF, Olabarria C, Lastra M, Arenas F. 2015a. Combined effects of wrack identity and solar radiation on associated beach macrofaunal assemblages. Mar Ecol Progr Ser 531:167–78.CrossRefGoogle Scholar
  44. Rodil IF, Fernandes JP, Mucha AP. 2015b. Disentangling the effects of solar radiation, wrack macroalgae and beach macrofauna on associated bacterial assemblages. Mar Environ Res 112:104–12.CrossRefGoogle Scholar
  45. Russell TL, Sassoubre LM, Zhou C, French-Owen D, Hassaballah A, Boehm AB. 2014. Impacts of beach wrack removal via grooming on surf zone water quality. Environ Sci Technol 48:2203–11.CrossRefGoogle Scholar
  46. Schlacher TA, Schoeman DS, Dugan JE, Lastra M, Jones A, Scapini F, McLachlan A. 2008. Sandy beach ecosystems: key features, sampling issues, management challenges and climate change impacts. Mar Ecol 29(S1):70–90.CrossRefGoogle Scholar
  47. Smetacek V, Zingone A. 2013. Green and golden seaweed tides on the rise. Nature 504:84–8.CrossRefGoogle Scholar
  48. Spiller DA, Piovia-Scott J, Wright AN, Yang LH, Takimoto G, Schoener TW, Iwata T. 2010. Marine subsidies have multiple effects on coastal food webs. Ecology 91:1424–34.CrossRefGoogle Scholar
  49. Sosik EA, Simenstad CA. 2013. Isotopic evidence and consequences of the role of microbes in macroalgae detritus-based food webs. Mar Ecol Progr Ser 494:107–19.CrossRefGoogle Scholar
  50. Suárez-Jiménez R, Hepburn CD, Hyndes GA, McLeod RJ, Taylor RB, Hurd CL. 2017. Importance of the invasive macroalga Undaria pinnatifida as trophic subsidy for a beach consumer. Mar Biol 164:113.CrossRefGoogle Scholar
  51. Tait LW, South PM, Lilley SA, Thomsen MS, Schiel DR. 2015. Assemblage and understory carbon production of native and invasive canopy-forming macroalgae. J Exp Mar Biol Ecol 469:10–17.CrossRefGoogle Scholar
  52. Trevathan-Tackett SM, Macreadie PI, Sanderman J, Baldock J, Howes JM, Ralph PJ. 2017. A global assessment of the chemical recalcitrance of seagrass tissues: implications for long-term carbon sequestration. Front Plant Sci 8:925.CrossRefGoogle Scholar
  53. Williams PLB, del Giorgio PA. 2005. Respiration in aquatic systems: history and background. The global significance of respiration in aquatic systems: from single cells to the biosphere. In: del Giorgio PA, Williams PLB, Eds. Respiration in aquatic ecosystems. Oxford: Oxford University Press. p 1–17.Google Scholar
  54. Williams SL, Smith JE. 2007. A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Ann Rev Ecol Syst 38:327–59.CrossRefGoogle Scholar
  55. Xu M, Qi Y. 2001. Soil-surface CO2 efflux and its spatial and temporal variations in a young ponderosa pine plantation in northern California. Glob Change Biol 7:667–77.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Tvärminne Zoological Station, University of HelsinkiHelsinkiFinland
  2. 2.Baltic Sea Centre, Stockholm UniversityStockholmSweden
  3. 3.Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of PortoPortoPortugal
  4. 4.Department of Ecology and Animal BiologyUniversity of VigoVigoSpain

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