Modification of benthic food web structure by recovering seagrass meadows, as revealed by trophic markers and mixing models

Jankowska, E.; De Troch, M.; Michel, Loïc; Lepoint, Gilles; Włodarska-Kowalczuk, M.

doi:10.1016/j.ecolind.2018.02.054

Article (Scientific journals)

Modification of benthic food web structure by recovering seagrass meadows, as revealed by trophic markers and mixing models

Jankowska, E.; De Troch, M.; Michel, Loïc et al.

2018 • In Ecological Indicators, 90, p. 28-37

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/221262

DOI
10.1016/j.ecolind.2018.02.054

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

emilia ecol indic.pdf

Publisher postprint (992 kB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Ecosystem functioning; Fatty acids; Food web ecology; Recovery; Seagrass meadows; Stable isotopes; Trophic markers; Animals; Biogeochemistry; Biological materials; Ecology; Isotopes; Mixing; Organic compounds; Plants (botany); Food webs; Ecosystems; Animalia; Bacteria (microorganisms); Invertebrata; Zostera marina

Abstract :

[en] Seagrass meadows are among the most diverse and productive coastal ecosystems in the world. Currently, the accelerating loss of these habitats is recognized worldwide. In the southern Baltic Sea, a natural recovery of Zostera marina meadows has occurred after a dramatic reduction within the last century. The aim of this study is to understand if and how the recovering eelgrass meadows affect the functioning of benthic ecosystems. The trophic links within the benthic food webs in the seagrass meadows and bare sandy bottoms were depicted and compared. The trophic connections were examined by combining stable isotope (SI) composition (δ13C, δ15N) and fatty acid (FA) profiles of meio- and macrofauna consumers and of potential food sources (particulate organic matter, surface sediment organic matter, epiphytes, microphytobenthos/bacteria and macrophytes) in a Bayesian mixing model framework (MixSIAR). Significantly higher amounts of the FA bacterial marker (C18:1ɷ7) were observed in meiofauna (approximately 40%) than in the macrofauna (1% on average), suggesting that bacteria are an important part of the meiofauna diet. The mixing model results indicated that the benthic consumers in the vegetated habitat utilized more food sources (e.g., epiphytes in the diets of meiofauna and macrofaunal grazers) and thus had a more diverse diet. Macrofaunal omnivores relied to a larger degree on animal-derived organic matter in vegetated habitat, which could be linked to higher invertebrate prey availability. The results highlight the importance of recovering seagrass meadows in driving the mechanisms responsible for food web organization. Any type of change to the state of seagrass meadows is crucial to the functioning and stability of marine ecosystems. © 2018

Disciplines :

Environmental sciences & ecology
Aquatic sciences & oceanology

Author, co-author :

Jankowska, E.; Institute of Oceanology Polish Academy of Sciences, Powstańców Warszawy 55, Sopot, Poland

De Troch, M.; Ghent University, Biology Department, Marine Biology, Krijgslaan 281 – S8, Ghent, Belgium

Michel, Loïc ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique

Lepoint, Gilles ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique

Włodarska-Kowalczuk, M.; Institute of Oceanology Polish Academy of Sciences, Powstańców Warszawy 55, Sopot, Poland

Language :

English

Title :

Modification of benthic food web structure by recovering seagrass meadows, as revealed by trophic markers and mixing models

Publication date :

2018

Journal title :

Ecological Indicators

ISSN :

1470-160X

eISSN :

1872-7034

Publisher :

Elsevier B.V., Netherlands

Volume :

Pages :

28-37

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

POIS.05.01.00-00-205/09-00, ERDF, European Regional Development Fund

Available on ORBi :

since 13 March 2018

Statistics

Number of views

71 (8 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Abdulkadir, S., Tsuchiya, M., One-step method for quantitative and qualitative analysis of fatty acids in marine animal samples. J. Exp. Mar. Biol. Ecol. 354 (2008), 1–8.
Anderson, M.J., Gorley, R.N., Clarke, K.R., PERMANOVA for PRIMER: Guide to Software and Statistical Methods. 2008, PRIMER-E Ltd, Plymouth.
Baeta, A., Valiela, I., Rossi, F., Pinto, R., Richard, P., Niquil, N., Marques, J.C., Eutrophication and trophic structure in response to the presence of the eelgrass Zostera noltii. Mar. Biol. 156:10 (2009), 2107–2120.
Boström, Ch., Baden, S., Bockelmann, A.-Ch., Dromph, K., Fredriksen, S., Gustafsson, C., Krause-Jensen, D., Möller, T., Laurentius Nielsen, S., Olesen, B., Olsen, J., Pihl, L., Rinde, E., Distribution, structure and function of Nordic eelgrass (Zostera marina) ecosystems: implications for coastal management and conservation. Aquat. Conserv. Mar. Freshwater Ecosyst. 3 (2014), 410–434, 10.1002/aqc.2424.
Budge, S.M., Parrish, C.C., Lipid biogeochemistry of plankton, settling matter and sediments in Trinity Bay, Newfoundland. II. Fatty acids. Org. Geochem. 29 (1998), 1547–1559.
Budge, S.M., Iverson, S.J., Koopman, H.N., Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar. Mammal Sci. 22 (2006), 759–801.
Dalsgaard, J., St. John, M., Kattner, G., Müller-Navarra, D., Hagen, W., Fatty acid trophic markers in the pelagic marine environment. Adv. Mar. Biol. 46 (2003), 225–340.
Danovaro, R., Croce, Della, N., Fabiano, M., Biochemical composition of particulate organic matter and bacterial dynamics at the sediment – water interface in a Mediterranean seagrass system. Hydrobiology 363 (1998), 241–251.
De Troch, M., Steinarsdóttir, M.B., Chepurnov, V., Grazing on diatoms by harpacticoid copepods: species-specific density-dependent uptake and microbial gardening. Aquat. Microb. Ecol. 39 (2005), 135–144.
De Troch, M., Chepurnov, V., Gheerardyn, H., Vanreusel, A., Ólafsson, E., Is diatom size selection by harpacticoid copepods related to grazer body size?. J. Exp. Mar. Biol. Ecol. 332 (2006), 1–11.
De Troch, M., Vergaerde, I., Cnudde, C., Vanormelingen, P., Vyverman, W., Vincx, M., The taste of diatoms: the role of diatom growth phase characteristics and associated bacteria for benthic copepod grazing. Aquat. Microb. Ecol. 67 (2012), 47–58.
Gartner, A., Tuya, F., Lavery, P.S., McMahon, K., Habitat preferences of macroinvertebrate fauna among seagrasses with varying structural forms. J. Exp. Mar. Biol. Ecol. 439 (2013), 143–151.
Giere, O., Meiobenthology. The Microscopic Motile Fauna of Aquatic Sediments, second ed., 2009 528 pp.
Guckert, J.B., Antworth, C.P., Nichols, P.D., White, D.C., Phospholipid ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol. Ecol. 31 (1985), 147–158.
Hedges, J.I., Stern, J.H., Carbon and nitrogen determinations of carbonate-containing solids. Limnol. Oceanogr. 29 (1984), 657–663.
Hemminga, M.A., Duarte, C.M., Seagrass Ecology. 2000, Cambridge University Press, Cambridge, 298.
Hoshika, A., Sarker, M.J., Ishida, S., Mishima, Y., Takai, N., Food web analysis of an eelgrass (Zostera marina L.) meadow and neighbouring sites in Mitsukuchi Bay (Seto Inland Sea, Japan) using carbon and nitrogen stable isotope ratios. Aquat. Bot. 85:3 (2006), 191–197.
Jankowska, E., Włodarska-Kowalczuk, M., Kotwicki, L., Balazy, P., Kuliński, K., Seasonality in vegetation biometrics and its effects on sediment characteristics and meiofauna in Baltic seagrass meadows. Estuarine Coast. Shelf Sci. 139 (2014), 159–170.
Jankowska, E., Jankowska, K., Włodarska-Kowalczuk, M., Seagrass vegetation and meiofauna enhance the bacterial abundance in the Baltic Sea sediments (Puck Bay). Environ. Sci. Pollut. Res. 22:18 (2015), 14372–14378.
Jankowska, E., Michel, L.N., Zaborska, A., Włodarska-Kowalczuk, M., Sediment carbon sink in low density temperate eelgrass meadows (Baltic Sea). J. Geophys. Res. Biogeosci., 121, 2016, 10.1002/2016JG003424.
Jaschinski, S., Brepohl, D., Sommer, U., Carbon sources and trophic structure in an eelgrass Zostera marina bed, based on stable isotope and fatty acid analyses. Mar. Ecol. Prog. Ser. 358:1 (2008), 103–114.
Kelly, J.R., Scheibling, R.E., Fatty acids as dietary tracers in benthic food webs. Mar. Ecol. Prog. Ser. 446 (2012), 1–22.
Kruk-Dowigałło, L., Long term changes in the structure of underwater meadows of the Puck lagoon. Acta Ichtiol. Piscatoria, XXI Supplement, 1991.
Lebreton, B., Richard, P., Galois, R., Radenac, G., Pfléger, C., Guillou, G., Mornet, F., Blanchard, G.F., Trophic importance of diatoms in an intertidal Zostera noltii seagrass bed: Evidence from stable isotope and fatty acid analyses. Estuar. Coast. Shelf Sci. 92:1 (2011), 140–153.
Lebreton, B., Richard, P., Galois, R., Radenac, G., Brahmia, A., Colli, G., Grouazel, M., André C., Guillou, G., Blanchard, G.F., Food sources used by sediment meiofauna in an intertidal Zostera noltii seagrass bed: a seasonal stable isotope study. Mar. Biol. 159 (2012), 1537–1550.
Leduc, D., Probert, P.K., Duncan, A., A multi-method approach for identifying meiofaunal trophic connections. Mar. Ecol. Prog. Ser. 383 (2009), 95–111.
Leduc, D., Probert, P.K., Frew, R.D., Hurd, C.L., Macroinvertebrate diet in intertidal seagrass and sandflat communities: a study using C, N, and S stable isotopes. New Zealand. J. Mar. Freshwater Res. 40:4 (2006), 615–629.
Lepoint, G., Nyssen, F., Gobert, S., Dauby, P., Bouquegneau, J.M., Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Mar. Biol. 136 (2000), 513–518.
McCutchan, J.H., Lewis, W.M., Kendall, C., McGrath, C.C., Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102 (2003), 378–390.
Michel, L.N., Dauby, P., Gobert, S., Graeve, M., Nyssen, F., Thelen, N., Lepoint, G., Dominant amphipods of Posidonia oceanica seagrass meadows display considerable trophic diversity. Mar. Ecol. 36:4 (2015), 969–981.
Miller, D.C., Geii, R.J., MacIntyre, H.L., Geider, R.J., MacIntyre, H.L., Microphytobenthos: the ecological role of the “secret garden” of unvegetated, shallow-water marine habitats. II. Role in sediment stability and shallow-water food webs. Estuaries, 19(2), 1996, 202.
Moksnes, P.O., Gullström, M., Tryman, K., Baden, S., Trophic cascades in a temperate seagrass community. Oikos 117:5 (2008), 763–777.
Nelson, M.M., Leighton, D.L., Phleger, C.F., Nichols, P.D., Comparison of growth and lipid composition in the green abalone, Haliotis fulgens, provided specific macroalgal diets. Compar. Biochem. Physiol. Part B: Biochem. Mol. Biol. 131 (2002), 695–712.
Nowacki, J., Stany wód. Zatoka Pucka, K., (eds.) Korzeniewski red, 1993, Fundacja Rozwoju Uniwersytetu Gdańskiego, Gdańsk, 206–221.
Ouisse, V., Riera, P., Migne, A., Leroux, C., Davoult, D., Freshwater seepages and ephemeral macroalgae proliferation in an intertidal bay: I effect on benthic community structure and food web. Estuarine Coast. Shelf Sci. 91 (2011), 272–281.
Ouisse, V., Riera, P., Migné A., Leroux, C., Davoult, D., Food web analysis in intertidal Zostera marina and Zostera noltii communities in winter and summer. Mar. Biol. 159:1 (2012), 165–175.
Richoux, N.B., Froneman, P.W., Trophic ecology of dominant zooplankton and macrofauna in a temperate, oligotrophic South African estuary: a fatty acid approach. Mar. Ecol. Prog. Ser. 357 (2008), 121–137.
Søreide, J.E., Falk-Petersen, S., Hegseth, E.N., Hop, H., Carroll, M.L., Hobson, K.A., Blachowiak-Samolyk, K., Seasonal feeding strategies of Calanus in the high-Arctic Svalbard region. Deep Sea Res. Part II 55 (2008), 2225–2244.
Stock B.C., & Semmens B.X. (2013). MixSIAR GUI User Manual. Version 3.1. https://github.com/brianstock/MixSIAR. doi: 10.5281/zenodo.56159.
Vafeiadou, A.M., Materatski, P., Adão, H., Troch, M., Moens, T., Food sources of macrobenthos in an estuarine seagrass habitat (Zostera noltii) as revealed by dual stable isotope signatures. Mar. Biol. 160:9 (2013), 2517–2523.
Vafeiadou, A.M., Materatski, P., Adão, H., De Troch, M., Moens, T., Resource utilization and trophic position of nematodes and harpacticoid copepods in and adjacent to Zostera noltii beds. Biogeosciences 11:14 (2014), 4001–4014.
Vizzini, S., Sara, G., Michener, R.H., Mazzola, A., The role and contribution of the seagrass Posidonia oceanica (L.) Delite organic matter for secondary consumers as revealed by carbon and nitrogen stable isotopes analysis. Acta Oecol. 23 (2002), 277–285.
Waycott, M., Duarte, C., Carruthers, T., Orth, R.J., Dennison, W.C., Olyarnik, S., Calladine, A., Fourqurean, J.W., Hesk, K.L., Hughes, A.R., Kendrick, G.A., Kenworthy, W.J., Short, F.T., Williams, L., Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proce. Natl. Acad. Sci. 106 (2009), 12377–12381.
Węsławski, J.M., Kryla-Straszewska, L., Piwowarczyk, J., Urbański, J., Warzocha, J., Kotwicki, L., Wiktor, J., Habitat modelling limitations – Puck Bay, Baltic Sea – a case study. Oceanologia 55:1 (2013), 167–183.
Włodarska-Kowalczuk, M., Jankowska, E., Kotwicki, L., Balazy, P., Evidence of season-dependency in vegetation effects on Macrofauna in temperate seagrass meadows (Baltic Sea). PLoS One, 9(7), 2014, e100788, 10.1371/journal.pone.0100788.