Macrofaunal Functional Diversity Provides Resilience to Nutrient Enrichment in Coastal Sediments
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The degradation of ecosystems is often associated with losses of large organisms and the concomitant losses of the ecological functions they mediate. Conversely, the resilience of ecosystems to stress is strongly influenced by faunal communities and their impacts on processes. Denitrification in coastal sediments is a process that may provide ecosystem resilience to eutrophication by removing excess bioavailable nitrogen. Here, we conducted a large-scale field experiment to test the effect of macrofaunal community composition on denitrification in response to two levels of nutrient enrichment at 28 sites across a biologically heterogeneous sandflat. After 7 weeks of enrichment, we measured denitrification enzyme activity (DEA) along with benthic macrofaunal community composition and environmental variables. We normalised treatment site specific DEA values by those in ambient sediments (DEACN) to reveal the underlying response across the heterogeneous landscape. Nutrient enrichment caused reductions in DEACN as well as functional changes in the community; these were both more pronounced under the highest level of nutrient loading (on average DEACN was reduced by 34%). The degree of suppression of DEACN following moderate nitrogen loading was mitigated by a key bioturbating species, but following high nitrogen loading (which reduced the key species density) the abundance and diversity of other nutrient processing species were the most important factors alleviating negative effects. This study provides a prime example of the context-dependent role of biodiversity in maintaining ecosystem functioning, underlining that different elements of biodiversity can become important as stress levels increase. Our results emphasise that management and conservation strategies require a real-world understanding of the community attributes that facilitate nutrient processing and maintain resilience in coastal ecosystems.
Keywordsdenitrification benthic community nutrient processing eutrophication enzyme assay intertidal functional traits sandflat
We thank all those involved in field sampling and laboratory work, especially Barry Greenfield, Sarah Hailes, Lisa McCartain, Katie Cartner, Kelly Carter, Rosalie Carter, Carsten Dormann, Chris Eager, Laura Hines and Rebecca Gladstone-Gallagher. Special thanks to Judi Hewitt for advice with statistical analysis and two anonymous reviewers whose constructive comments improved the manuscript. This work was funded by the Marsden Fund, Royal Society of New Zealand (NIW1102) to SFT, a Marie-Curie International Outgoing Fellowship (FP7-PEOPLE-2011-IOF) to CK and CO1x1515 4.2.1 to SFT and CAP. EJD was funded by a University of Waikato Doctoral Scholarship. These funders had no role in the study design, interpretation or writing of this manuscript.
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Conflict of interest
The authors declare that they have no conflict of interest.
- Anthonisen AC, Loehr RC, Prakasam TBS, Srinath EG. 1976. Inhibition of nitrification by ammonia and nitrous acid. Water Pollution Control Federation 48:835–52.Google Scholar
- Arar E, Collins G. 1997. In vitro determination of chlorophyll a and pheophytin a in marine and freshwater algae by fluorescence. Cincinnati: National Exposure Research Laboratory, U.S. Environmental Protection Agency.Google Scholar
- Burnham KP, Anderson DR. 2002. Model selection and multimodel inference: a pratical information-theoretic approach. New York (NY): Springer.Google Scholar
- Clarke KR, Gorley RN. 2015. PRIMER v7: User manual/tutorial. Plymouth, 296 pp: PRIMER-E.Google Scholar
- Diaz RJ, Rosenberg R. 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. In: Ansell AD, Gibson RN, Barnes M, Eds. Oceanography and marine biology—an annual review, Vol. 33. London: UCL Press Ltd. p 245–303.Google Scholar
- Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S. 2013. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46.CrossRefGoogle Scholar
- Groffman PM, Holland EA, Myrold DD, Robertson GP. 1999. Denitrification. In: Robertson G, Bledsoe C, Coleman D, Sollins P, Eds. Standard soil methods for long term ecological research. Cary (NC): Oxford University Press. p 272–88.Google Scholar
- Henriksen K, Kemp WM. 1988. Nitrification in estuarine and coastal marine sediments. In: Blackburn TH, Sorensen J, Eds. Nitrogen cycling in coastal marine environments. New York: Wiley. p 207–49.Google Scholar
- Hines AH, Whitlatch RB, Thrush SF, Hewitt JE, Cummings VJ, Dayton PK, Legendre P. 1997. Nonlinear foraging response of a large marine predator to benthic prey: eagle ray pits and bivalves in a New Zealand sandflat. Journal of Experimental marine Biology and Ecology 216:191–210.CrossRefGoogle Scholar
- Jauffrais T, Drouet S, Turpin V, Mèlèder V, Jesus B, Cognie B, Raimbault P, Cosson RP, Decottignies P, Martin-Jèzèquel V. 2015. Growth and biochemical composition of a microphytobenthic diatom (Entomoneis paludosa) exposed to shorebird (Calidris alpina) droppings. Journal of Experimental Marine Biology and Ecology 469:83–92.CrossRefGoogle Scholar
- Nixon S. 1998. Enriching the sea to death. Scientific American 9:48–53.Google Scholar
- Pearson TH, Rosenberg R. 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanography and Marine Biology: An Annual Review 16:229–311.Google Scholar
- Singer JK, Anderson JB, Ledbetter MT, McCave IN, Jones KPN, Wright R. 1988. An assessment of analytical techniques for the size analysis of fine-grained sediments. Journal of Sedimentary Research 58:534–43.Google Scholar
- StatSoft Inc. 2012. STATISTICA (data analysis software system), version 11. www.statsoft.com.
- Thrush S, Hewitt J, Parkes S, Lohrer A, Pilditch C, Woodin SA, Wethey D, Chiantore M, Asnaghi V, De Juan S, Kraan C, Rodil I, Savage C, Van Colen C. 2014. Experimenting with ecosystem interaction networks in search of threshold potentials in real world marine ecosystems. Ecology 95:1451–7.CrossRefPubMedGoogle Scholar
- Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman D. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecological Applications 7:737–50.Google Scholar
- Volkenborn N, Meile C, Polerecky L, Pilditch CA, Norkko A, Norkko J, Hewitt JE, Thrush SF, Wethey DS, Woodin SA. 2012. Intermittent bioirrigation and oxygen dynamics in permeable sediments: an experimental and modeling study of three tellinid bivalves. Journal of Marine Research 70:794–823.CrossRefGoogle Scholar
- Yazdani Foshtomi M, Braeckman U, Derycke S, Sapp M, Van Gansbeke D, Sabbe K, Willems A, Vincx M, Vanaverbeke J. 2015. The link between microbial diversity and nitrogen cycling in marine sediments is modulated by macrofaunal bioturbation. PLoS ONE 10:e0130116.CrossRefPubMedPubMedCentralGoogle Scholar