macrobenthos; Black Sea; trait distribution model; functional biodiversity; ecosystem functions; spatial mapping
Abstract :
[en] Benthic biodiversity is of global significance for the provision of ecosystem services and the mediation of global biogeochemical cycles. The lack of detailed spatial distributions of the functions and vulnerabilities of the benthos critically prevents us from protecting benthic biodiversity and its functioning in the context of increasing human perturbations and climate change. Here, we propose a multidisciplinary approach to bridging in situ benthic data to the maps of macrobenthic functions and vulnerabilities at the scale of the northwestern shelf of the Black Sea. Our findings show that oxygen availability is a key driver of the functional trait composition of macrozoobenthic communities. Shallower well-oxygenated areas support high biomixing and bioirrigation on muddier-sandier substrata and high biodeposition on coarser substrata associated with mussel reef communities. In contrast, at depleted oxygen areas at the edge of the shelf, macrobenthic communities are functionally impoverished with only a combination of a few typical opportunistic traits, and those communities have a negligible impact on ecosystem functions. Mapping of vulnerabilities and functions of benthic communities can support marine management strategies aligned with the United Nations Sustainable Development Goal 14: Life Below Water.
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Chevalier, Séverine ; Université de Liège - ULiège > Département d'astrophysique, géophysique et océanographie (AGO) > MAST (Modeling for Aquatic Systems) ; UGent - Universiteit Gent
Beauchard, Olivier; the Royal Netherlands Institute for Sea Research (NIOZ) > Estuarine & Delta Systems (EDS)
Vandenbulcke, Luc ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS)
Teaca, Adrian; National Research and Development Institute for Marine Geology and Geoecology (GeoEcoMar) > Department of Biology and Ecology
Begun, Tatiana; National Research and Development Institute for Marine Geology and Geoecology (GeoEcoMar) > Department of Biology and Ecology
Todorova, Valentina; Institute of Oceanology - Bulgarian Academy of Sciences (IO-BAS)
Soetaert, Karline; the Royal Netherlands Institute for Sea Research > Estuarine & Delta Systems (EDS)
Grégoire, Marilaure ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS)
Language :
English
Title :
Trait modeling to predict benthic functions and vulnerabilities across black sea seascapes
D.C. Rhoads Organism-sediment relations on the muddy sea floor Oceanogr. Mar. Biol. Annu. Rev. 12 263 300 1:CAS:528:DyaE28Xmt1emug%3D%3D
E. Kristensen et al. What is bioturbation? The need for a precise definition for fauna in aquatic sciences Mar. Ecol. Prog Ser. 446 285 302 2012MEPS.446.285K 10.3354/meps09506
F.J.R. Meysman O.S. Galaktionov B. Gribsholt J.J. Middelburg Bioirrigation in permeable sediments: advective pore-water transport induced by burrow ventilation Limnol. Oceanogr. 51 1 142 156 2006LimOc.51.142M 10.4319/lo.2006.51.1.0142
E. Kristensen G. Liebezeit S. Dittmann I. Kröncke Organic matter diagenesis at the oxic/anoxic interface in coastal marine sediments, with emphasis on the role of burrowing animals Life at Interfaces and Under Extreme Conditions. Developments in Hydrobiology Springer 10.1007/978-94-011-4148-2_1 151
F. Mermillod-Blondin The functional significance of bioturbation and biodeposition on biogeochemical processes at the water–sediment interface in freshwater and marine ecosystems J. N Am. Benthol Soc. 30 3 770 778 10.1899/10-121.1
G. Graf R. Rosenberg Bioresuspension and biodeposition: a review J. Mar. Syst. 11 3–4 269 278 10.1016/S0924-7963(96)00126-1
A. Norkko J.E. Hewitt S.F. Thrush T. Funnell Benthic-pelagic coupling and suspension-feeding bivalves: linking site-specific sediment flux and biodeposition to benthic community structure Limnol. Oceanogr. 46 8 2067 2072 2001LimOc.46.2067N 10.4319/lo.2001.46.8.2067
G.R. Lopez J.S. Levinton Ecology of Deposit-Feeding animals in marine sediments Q. Rev. Biol. 62 3 235 260 10.1086/415511
R.C. Aller Carbonate dissolution in nearshore terrigenous muds: the role of physical and biological reworking J. Geol. 90 1 79 95 1982JG...90..79A 1:CAS:528:DyaL38XhtVOmtbs%3D 10.1086/628652
K. Norling R. Rosenberg S. Hulth A. Grémare E. Bonsdorff Importance of functional biodiversity and species-specific traits of benthic fauna for ecosystem functions in marine sediment Mar. Ecol. Prog Ser. 332 11 23 2007MEPS.332..11N 1:CAS:528:DC%2BD2sXkslKhs7s%3D 10.3354/meps332011
M. Solan P. Batty M.T. Bulling J.A. Godbold How biodiversity affects ecosystem processes: implications for ecological revolutions and benthic ecosystem function Aquat. Biol. 2 3 289 301 10.3354/ab00058
Díaz, S, Fargione, J, Iii, F. S. C. & Tilman, D. Biodiversity loss threatens human Well-Being. PLOS Biol. 4 (8). https://doi.org/10.1371/journal.pbio.0040277 (2006). e277.
T.S. Bianchi et al. What global biogeochemical consequences will marine animal–sediment interactions have during climate change? Elem. Sci. Anth 9 1 00180 1328512 10.1525/elementa.2020.00180
F. Olsgard M.T. Schaanning S. Widdicombe M.A. Kendall M.C. Austen Effects of bottom trawling on ecosystem functioning J. Exp. Mar. Biol. Ecol. 366 1–2 123 133 10.1016/j.jembe.2008.07.036
S. Dı́az M. Cabido Vive La différence: plant functional diversity matters to ecosystem processes Trends Ecol. Evol. 16 11 646 655 10.1016/S0169-5347(01)02283-2
T.R.E. Southwood Habitat, the Templet for ecological strategies? J. Anim. Ecol. 46 2 336 10.2307/3817
C.B. Cogan B.J. Todd P. Lawton T.T. Noji The role of marine habitat mapping in ecosystem-based management ICES J. Mar. Sci. 66 9 2033 2042 10.1093/icesjms/fsp214
P.V.R. Snelgrove S.F. Thrush D.H. Wall A. Norkko Real world biodiversity–ecosystem functioning: a seafloor perspective Trends Ecol. Evol. 29 7 398 405 10.1016/j.tree.2014.05.002 24932849
C.J. Brown J.A. Sameoto S.J. Smith Multiple methods, maps, and management applications: purpose made seafloor maps in support of ocean management J. Sea Res. 72 1 13 2012JSR..72..1B 10.1016/j.seares.2012.04.009
D.P. Tittensor et al. Global patterns and predictors of marine biodiversity across taxa Nature 466 1098 1101 2010Natur.466.1098T 1:CAS:528:DC%2BC3cXptl2rsrY%3D 10.1038/nature09329 20668450
X. Morin W. Thuiller Comparing niche-and process‐based models to reduce prediction uncertainty in species range shifts under climate change Ecology 90 5 1301 1313 10.1890/08-0134.1 19537550
J. Franklin Species distribution models in conservation biogeography: developments and challenges Divers. Distrib. 19 10 1217 1223 10.1111/ddi.12125
A. Guisan N.E. Zimmermann Predictive habitat distribution models in ecology Ecol. Model. 135 2–3 147 186 10.1016/S0304-3800(00)00354-9
Costello, M. J. et al. A census of marine biodiversity knowledge, resources, and future challenges. PLoS ONE. 5 (8). https://doi.org/10.1371/journal.pone.0012110 (2010). e12110.
M. Townsend et al. Overcoming the challenges of data scarcity in mapping marine ecosystem service potential Ecosyst. Serv. 8 44 55 10.1016/j.ecoser.2014.02.002
J.P. Rodríguez L. Brotons J. Bustamante J. Seoane The application of predictive modelling of species distribution to biodiversity conservation Divers. Distrib. 13 3 243 251 10.1111/j.1472-4642.2007.00356.x
V. Gerovasileiou et al. Habitat mapping in the European Seas-is it fit for purpose in the marine restoration agenda? M Policy 106 103521 10.1016/j.marpol.2019.103521
S.A. Gignoux-Wolfsohn et al. New framework reveals gaps in US ocean biodiversity protection One Earth 7 1 31 43 10.1016/j.oneear.2023.12.014
P.Y. Le Traon et al. From observation to information and users: the copernicus marine service perspective Front. Mar. Sci. 6 234 2019pcqm.book...T 10.3389/fmars.2019.00234
Kendzierska, H. & Janas, U. Functional diversity of macrozoobenthos under adverse oxygen conditions in the southern Baltic Sea. Sci. Rep. 14(1), 8946 (2024). (2024). https://doi.org/10.1038/s41598-024-59354-3
Villnäs, A, Norkko, J, Lukkari, K, Hewitt, J. & Norkko, A. Consequences of increasing hypoxic disturbance on benthic communities and ecosystem functioning. PLoS ONE. 7 (10). https://doi.org/10.1371/journal.pone.0044920 (2012). e44920.
M. Bon et al. Functional changes in benthic macrofaunal communities along a natural gradient of hypoxia in an upwelling system Mar. Pollut Bull. 164 112056 1:CAS:528:DC%2BB3MXis1Kku7s%3D 10.1016/j.marpolbul.2021.112056 33517087
A.S. Pacheco et al. Functional diversity of marine macrobenthic communities from Sublittoral soft-sediment habitats off Northern Chile Helgol. Mar. Res. 65 3 413 424 2011HMR..65.413P 10.1007/s10152-010-0238-8
H.K. Kindsvater M. Mangel J.D. Reynolds N.K. Dulvy Ten principles from evolutionary ecology essential for effective marine conservation Ecol. Evol. 6 7 2125 2138 10.1002/ece3.2012 27069573 4782246
J. Friedrich et al. Investigating hypoxia in aquatic environments: diverse approaches to addressing a complex phenomenon Biogeosciences 11 4 1215 1259 2014BGeo..11.1215F 10.5194/bg-11-1215-2014
L. Mee J. Friedrich M.T. Gomoiu Restoring the black sea in times of uncertainty Oceanography 18 2 100 111 10.5670/oceanog.2005.45
O. Beauchard S. Mestdagh L. Koop T. Ysebaert P. Herman Benthic synecology in a soft sediment shelf: habitat contrasts and assembly rules of life strategies Mar. Ecol. Prog Ser. 682 31 50 2022MEPS.682..31B 10.3354/meps13928
M.J.L. Holbrook J.P. Grassle The effect of low density on the development of simultaneous hermaphroditism in male capitella species I (polychaeta) Biol. Bull. 166 1 103 109 10.2307/1541434
S. Chevalier O. Beauchard A. Teacă K. Soetaert M. Grégoire Partial recovery of macrozoobenthos on the Northwestern shelf of the black sea Mar. Pollut Bull. 207 116857 1:CAS:528:DC%2BB2cXhvV2itLbO 10.1016/j.marpolbul.2024.116857 39216251
T. Stevens L. Mee J. Friedrich D. Aleynik G. Minicheva Partial recovery of Macro-Epibenthic assemblages on the North-West shelf of the black sea Front. Mar. Sci. 6 474 10.3389/fmars.2019.00474
Begun, T, Teaca, A. & Gomoiu, M. T. State of Macrobenthos within Modiolus phaseolinus biocoenosis from Romanian Black Sea Continental shelf. GeoEcoMarina 16 (1), 5–18 (2010).
V. Surugiu Polychaete research in the black sea Rom J. Aquat. Ecol. 1 1 101 122
A. Teacă T. Begun M.T. Gomoiu G.M. Paraschiv The present state of the epibiontic populations to the biocenosis of stone mussels in the shallow water off the Romanian black sea Coast Geo-Eco-Marina 12 53 66
S.G. Bolam et al. Differences in biological traits composition of benthic assemblages between unimpacted habitats Mar. Environ. Res. 126 1 13 2017rdrd.book...B 1:CAS:528:DC%2BC2sXivFWhtbs%3D 10.1016/j.marenvres.2017.01.004 28214628
N.T. Breine et al. Structural and functional diversity of soft-bottom macrobenthic communities in the Southern North sea Estuar. Coast Shelf Sci. 214 173 184 2018ECSS.214.173B 10.1016/j.ecss.2018.09.012
J. Bremner S.I. Rogers C.L.J. Frid Matching biological traits to environmental conditions in marine benthic ecosystems J. Mar. Syst. 60 3 302 316 10.1016/j.jmarsys.2006.02.004
A. Norkko A. Villnäs J. Norkko S. Valanko C. Pilditch Size matters: implications of the loss of large individuals for ecosystem function Sci. Rep. 3 1 2646 2013NatSR..3.2646N 10.1038/srep02646 24025973 6505624
L.A. Levin et al. Effects of natural and human-induced hypoxia on coastal benthos Biogeosciences 6 10 2063 2098 2009BGeo..6.2063L 1:CAS:528:DC%2BC3cXltVCkug%3D%3D 10.5194/bg-6-2063-2009
Van Colen, C. et al. Organism-sediment interactions govern post-hypoxia recovery of ecosystem functioning. PLoS ONE7(11), e49795. https://doi.org/10.1371/journal.pone.0049795
J.J. Beukema The efficiency of the Van Veen grab compared with the Reineck box sampler ICES J. Mar. Sci. 35 3 319 327 10.1093/icesjms/35.3.319
S. Martini et al. Functional trait-based approaches as a common framework for aquatic ecologists Limnol. Oceanogr. 66 3 965 994 2021LimOc.66.965M 10.1002/lno.11655
O. Beauchard et al. Assessing sea floor functional biodiversity and vulnerability Mar. Ecol. Prog Ser. 708 21 43 2023MEPS.708..21B 10.3354/meps14270
A.M. Queirós et al. A bioturbation classification of European marine infaunal invertebrates Ecol. Evol. 3 11 3958 3985 10.1002/ece3.769 24198953 3810888
A. Wrede J. Beermann J. Dannheim L. Gutow T. Brey Organism functional traits and ecosystem supporting services – A novel approach to predict bioirrigation Ecol. Indic. 91 737 743 10.1016/j.ecolind.2018.04.026
M. Gogina et al. Towards benthic ecosystem functioning maps: quantifying bioturbation potential in the German part of the Baltic sea Ecol. Indic. 73 574 588 10.1016/j.ecolind.2016.10.025
Bolam, S. G, Cooper, K. & Downie, A. Mapping marine benthic biological traits to facilitate future sustainable development. Ecol. Appl. 33 (7). https://doi.org/10.1002/eap.2905 (2023). e2905.
M. Miatta A.E. Bates P.V.R. Snelgrove Incorporating biological traits into conservation strategies Annu. Rev. Mar. Sci. 13 1 421 443 2021ARMS..13.421M 10.1146/annurev-marine-032320-094121
M. Nenciu V. Niță A. Teacă A. Popa T. Begun An assessment of potential beam trawling impact on North-Western black sea benthic habitats aiming at a sustainable fisheries management Water 15 12 2241 10.3390/w15122241
A. Capet F.J.R. Meysman I. Akoumianaki K. Soetaert M. Grégoire Integrating sediment biogeochemistry into 3D oceanic models: A study of benthic-pelagic coupling in the black sea Ocean. Model. 101 83 100 2016OcMod.101..83C 10.1016/j.ocemod.2016.03.006
A. Capet J.M. Beckers M. Grégoire Drivers, mechanisms and long-term variability of seasonal hypoxia on the black sea Northwestern shelf – is there any recovery after eutrophication? Biogeosciences 10 6 3943 3962 2013BGeo..10.3943C 1:CAS:528:DC%2BC2cXjtVWhu7c%3D 10.5194/bg-10-3943-2013
J. Friedrich et al. Benthic nutrient cycling and diagenetic pathways in the North-western black sea Estuar. Coast Shelf Sci. 54 3 369 383 2002ECSS..54.369F 1:CAS:528:DC%2BD38XktlaltLc%3D 10.1006/ecss.2000.0653
Todorova, V. & Konsulova, T. Manual for quantitative sampling and sample treatment of marine soft-bottom macrozoobenthic. Inst Oceanol. Bulg. Acad. Sci. (IO-BAS): Varna Bulg (2005). www.blacksea-commission.org
S. Chevalier et al. A macrozoobenthic data set of the black sea Northwestern shelf Sci. Data 12 957 10.1038/s41597-025-05311-2 40483280 12145434
S.A. Ciliberti et al. Monitoring and forecasting the ocean state and biogeochemical processes in the black sea: recent developments in the copernicus marine service J. Mar. Sci. Eng. 9 10 1146 10.3390/jmse9101146
M. Grégoire C. Raick K. Soetaert Numerical modeling of the central black sea ecosystem functioning during the eutrophication phase Prog Oceanogr. 76 3 286 333 2008PrOce.76.286G 10.1016/j.pocean.2008.01.002
M. Grégoire K. Soetaert Carbon, nitrogen, oxygen and sulfide budgets in the black sea: A biogeochemical model of the whole water column coupling the oxic and anoxic parts Ecol. Modell 221 19 2287 2301 1:CAS:528:DC%2BC3cXhtVKlurzE 10.1016/j.ecolmodel.2010.06.007
O. Beauchard H. Veríssimo A.M. Queirós P.M.J. Herman The use of multiple biological traits in marine community ecology and its potential in ecological indicator development Ecol. Indic. 76 81 96 10.1016/j.ecolind.2017.01.011
F. Murtagh P. Legendre Ward’s hierarchical agglomerative clustering method: which algorithms implement ward’s criterion? J. Classif. 31 274 295 3277707 10.1007/s00357-014-9161-z
S. Lavorel et al. Assessing functional diversity in the field – methodology matters! Funct. Ecol. 22 1 134 147 10.1111/j.1365-2435.2007.01339.x
S. Dray et al. Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation Ecology 95 1 14 21 10.1890/13-0196.1 24649641
P. Legendre R. Galzin M.L. Harmelin-Vivien Relating behavior to habitat: solutions to the fourth-corner problem Ecology 78 2 547 562 10.1890/0012-9658(1997)078[0547:RBTHST]2.0.CO;2
S. Dray A.B. Dufour D. Chessel The ade4 package-II: Two-table and K-table methods R News 7 2 47 52
S. Dray P. Legendre Testing the species Traits–Environment relationships: the Fourth-Corner problem revisited Ecology 89 12 3400 3412 10.1890/08-0349.1 19137946
C.J.F. ter Braak A. Cormont S. Dray Improved testing of species traits–environment relationships in the fourth-corner problem Ecology 93 7 1525 1526 10.1890/12-0126.1 22919899
Y. Benjamini Y. Hochberg Controlling the false discovery rate: a practical and powerful approach to multiple testing J. R Stat. Soc. Ser. B Stat. Methodol. 57 1 289 300 1325392 10.1111/j.2517-6161.1995.tb02031.x
Dong, C. et al. Recent Developments in Artificial Intelligence in Oceanography. Ocean-Land-Atmos Res. 1–26 (2022). (2022). https://doi.org/10.34133/2022/9870950
R. Lou Z. Lv S. Dang T. Su X. Li Application of machine learning in ocean data Multimed Syst. 29 1815 1824 10.1007/s00530-020-00733-x
F. Pedregosa et al. Scikit-learn: machine learning in python J. Mach. Learn. Res. 12 2825 2830 2854348
Phil et al. Scitools/cartopy: REL: V0.24.1. v0.24.1, Zenodo, 8 octobre 2024, https://doi.org/10.5281/zenodo.13905945
R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2024).
