title: Drought, Mutualism Breakdown, and Landscape-Scale Degradation of Seagrass Beds.
abstract: In many marine ecosystems, biodiversity critically depends on foundation species such as corals and seagrasses that engage in mutualistic interactions [1-3]. Concerns grow that environmental disruption of marine mutualisms exacerbates ecosystem degradation, with breakdown of the obligate coral mutualism ("coral bleaching") being an iconic example [2, 4, 5]. However, as these mutualisms are mostly facultative rather than obligate, it remains unclear whether mutualism breakdown is a common risk in marine ecosystems, and thus a potential accelerator of ecosystem degradation. Here, we provide evidence that drought triggered landscape-scale seagrass degradation and show the consequent failure of a facultative mutualistic feedback between seagrass and sulfide-consuming lucinid bivalves that in turn appeared to exacerbate the observed collapse. Local climate and remote sensing analyses revealed seagrass collapse after a summer with intense low-tide drought stress. Potential analysis-a novel approach to detect feedback-mediated state shifts-revealed two attractors (healthy and degraded states) during the collapse, suggesting that the drought disrupted internal feedbacks to cause abrupt, patch-wise degradation. Field measurements comparing degraded patches that were healthy before the collapse with patches that remained healthy demonstrated that bivalves declined dramatically in degrading patches with associated high sediment sulfide concentrations, confirming the breakdown of the mutualistic seagrass-lucinid feedback. Our findings indicate that drought triggered mutualism breakdown, resulting in toxic sulfide concentrations that aggravated seagrass degradation. We conclude that external disturbances can cause sudden breakdown of facultative marine mutualistic feedbacks. As this may amplify ecosystem degradation, we suggest including mutualisms in marine conservation and restoration approaches.
authors.affiliation: Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, Texel, the Netherlands.
authors.forename: Jimmy
authors.initials: J
authors.lastname: de Fouw
authors.affiliation: Department of Environmental Science, Institute for Water and Wetland Research, Radboud University, Heyendaalseweg 135, 6525 AJ Nijmegen, the Netherlands; Aquatic Ecology and Environmental Biology Group, Institute for Water and Wetland Research, Radboud University, Heyendaalseweg 135, 6525 AJ Nijmegen, the Netherlands.
authors.forename: Laura L
authors.initials: LL
authors.lastname: Govers
authors.affiliation: Conservation Ecology, Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, P.O. Box 11103, 9700 CC Groningen, the Netherlands; Department of Estuarine and Delta Systems, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 140, 4400 CA Yerseke, the Netherlands.
authors.forename: Johan
authors.initials: J
authors.lastname: van de Koppel
authors.affiliation: Department of Estuarine and Delta Systems, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 140, 4400 CA Yerseke, the Netherlands.
authors.forename: Jim
authors.initials: J
authors.lastname: van Belzen
authors.affiliation: Department of Geodesy and Geo-Information, Vienna University of Technology, Gusshausstrasse 27-29, 1040 Vienna, Austria; Laboratory of Hydrology and Water Management, Ghent University, Coupure Links 653, 9000 Ghent, Belgium.
authors.forename: Wouter
authors.initials: W
authors.lastname: Dorigo
authors.affiliation: Conservation Ecology, Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, P.O. Box 11103, 9700 CC Groningen, the Netherlands.
authors.forename: Mohammed A
authors.initials: MA
authors.lastname: Sidi Cheikh
authors.affiliation: Conservation Ecology, Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, P.O. Box 11103, 9700 CC Groningen, the Netherlands.
authors.forename: Marjolijn J A
authors.initials: MJ
authors.lastname: Christianen
authors.affiliation: Conservation Ecology, Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, P.O. Box 11103, 9700 CC Groningen, the Netherlands.
authors.forename: Karin J
authors.initials: KJ
authors.lastname: van der Reijden
authors.affiliation: Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, Texel, the Netherlands; Conservation Ecology, Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, P.O. Box 11103, 9700 CC Groningen, the Netherlands.
authors.forename: Matthijs
authors.initials: M
authors.lastname: van der Geest
authors.affiliation: Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, Texel, the Netherlands; Conservation Ecology, Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, P.O. Box 11103, 9700 CC Groningen, the Netherlands.
authors.forename: Theunis
authors.initials: T
authors.lastname: Piersma
authors.affiliation: Aquatic Ecology and Environmental Biology Group, Institute for Water and Wetland Research, Radboud University, Heyendaalseweg 135, 6525 AJ Nijmegen, the Netherlands; B-WARE Research Centre, Radboud University, Mercator 3, Toernooiveld 1, 6525 ED Nijmegen, the Netherlands.
authors.forename: Alfons J P
authors.initials: AJ
authors.lastname: Smolders
authors.affiliation: Conservation Ecology, Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, P.O. Box 11103, 9700 CC Groningen, the Netherlands.
authors.forename: Han
authors.initials: H
authors.lastname: Olff
authors.affiliation: Aquatic Ecology and Environmental Biology Group, Institute for Water and Wetland Research, Radboud University, Heyendaalseweg 135, 6525 AJ Nijmegen, the Netherlands.
authors.forename: Leon P M
authors.initials: LP
authors.lastname: Lamers
authors.affiliation: Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, Texel, the Netherlands.
authors.forename: Jan A
authors.initials: JA
authors.lastname: van Gils
authors.affiliation: Aquatic Ecology and Environmental Biology Group, Institute for Water and Wetland Research, Radboud University, Heyendaalseweg 135, 6525 AJ Nijmegen, the Netherlands; Conservation Ecology, Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, P.O. Box 11103, 9700 CC Groningen, the Netherlands. Electronic address: t.vanderheide@science.ru.nl.
authors.forename: Tjisse
authors.initials: T
authors.lastname: van der Heide
mesh_terms: D035961:Alismatales / Q000502:physiology*; D000818:Animals; D049872:Bivalvia / Q000502:physiology*; D057231:Climate Change; D055864:Droughts; D017753:Ecosystem; D013559:Symbiosis