Dynamics of the seagrass Zostera noltei in a shallow Mediterranean lagoon exposed to chemical contamination and other stressors Diane Espel, Noël Diepens, Olivier Boutron, Evelyne Buffan-Dubau, Yves Chérain, Eric Coulet, Patrick Grillas, Anne Probst, Jérôme Silvestre, Arnaud Elger To cite this version: Diane Espel, Noël Diepens, Olivier Boutron, Evelyne Buffan-Dubau, Yves Chérain, et al.. Dy- namics of the seagrass Zostera noltei in a shallow Mediterranean lagoon exposed to chemical con- tamination and other stressors. Estuarine, Coastal and Shelf Science, Elsevier, 2019, 222, pp.1-12. 10.1016/j.ecss.2019.03.019. hal-02324534 HAL Id: hal-02324534 https://hal.archives-ouvertes.fr/hal-02324534 Submitted on 17 Jan 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Dynamics of the seagrass Zostera noltei in a shallow Mediterranean lagoon exposed to chemical contamination and other stressors Diane Espela, ∗, Noël J. Diepens b, Olivier Boutron c, Evelyne Buffan-Dubau a, Yves Chérain d, Eric Coulet d, Patrick Grillas c, Anne Probst a, Jérôme Silvestre a, Arnaud Elger a a EcoLab, Université de Toulouse, CNRS, INPT, UPS, Toulouse, France b Aquatic Ecology and Water Quality Management Group, Department of Environmental Sciences, Wageningen University, P.O. Box 47, 6700, AA, Wageningen, the Netherlands c Tour Du Valat, Research Institute for the Conservation of Mediterranean Wetlands, Le Sambuc, 13200, Arles, France d National Nature Reserve of Camargue, National Society for Nature Protection (SNPN), La Capeliere, 13200, Arles, France ∗ Corresponding author . E-mail address: [email protected] (D. Espel) How to cite this article : Espel D., Diepens N.J., Boutron O., Buffan-Dubau E., Chérain Y., Coulet E., Grillas P., Probst A., Silvestre J., Elger A. 2019. Dynamics of the seagrass Zostera noltei in a shallow Mediterranean lagoon exposed to chemical contamination and other stressors . Estuarine, Coastal and Shelf Science 222:1–12. doi: 10.1016/j.ecss.2019.03.019 Abstract Seagrass decline due to a variety of stressors has been observed worldwide. In the shallow Vaccarès lagoon, Camargue, France, the dominant macrophyte species, Zostera noltei, has suffered two major declines since 1996. The first decline was well explained by salinity and turbidity variations, while the second one could not be explained by these parameters. Other stressors such as chemical contamination, eutrophication or temperature increase could be explanatory variables for this most recent decline. The aim of our study was to understand, via scientific monitoring from 2011 to 2015, the influence of chemical contamination and its possible interactions with other biological and environmental pressures, on seagrass physiology and population dynamics in the Vaccarès lagoon. Multi-contamination by organic contaminants and trace metals was detected in the water and sediments, and their concentrations often exceeded environmental standards, particularly where seagrass regression was observed. Spatial variations in biological, environmental and chemical parameters in the lagoon were investigated by co-inertia analysis, which revealed significant relationships between environmental data, more particularly between contaminants, seagrass dynamics indices and biomarkers. Seagrass dynamics indices were negatively correlated with the concentrations of some herbicides in water (2,4- MCPA and bentazon) and with trace metals in sediments (arsenic). Rhizome starch contents in winter were negatively correlated with those herbicides and with several metals (arsenic, zinc, copper) in water and/or sediments. These results suggest that environmental contamination may play a role in seagrass decline. However, complementary investigations, such as monitoring over longer periods and additional toxicity tests, are required to address the causal link between contamination and seagrass decline. Keyword s: Seagrass dynamics, Multiple stressors, Coastal lagoon, Chemical contaminants, Zostera noltei https://doi.org/10.1016/j.ecss.2019.03.019 1. Introduction Seagrasses have a wide spatial distribution and are an important component of coastal ecosystems. They provide many essential ecosystem services such as sediment stabilization, nutrient cycling, a nursery for living organisms, high primary production (CO2 fixation), support for commercial fisheries and a source of food (Costanza et al., 1997; Orth et al., 2006; Waycott et al., 2009). However, seagrass decline has been observed worldwide, with a 29% decrease in the known extent of meadows since 1879, and has been ongoing at a rate of 110 km2 year−1 since 1980 (Bernard et al., 2007; WaycoN et al., 2009), potenOally affe ting the e osystem servi es provided. Apart from the highly flu tuating natural dynami s of seagrass meadows, whi h an 1 vary from enduring to transitory depending on the spe iesP traits (Kilminster et al., 2015), a variety of stressors for seagrasses have been identified. ,hese stressors an be divided in (1) natural pro esses su h as storms, old winters, sedimentation but also sediment resuspension aused by fre0uent wind, whi h redu es light availability, graHing by birds and ur hins and diseases and (2) anthropogeni pressures in luding invasive spe ies, eutrophi ation, dragging, a0ua ulture, dredging, brown tides, to4i ants, global limate hange and physi al and hydrologi al e osystem modifi ations (Charpentier et al., 2005J Orth et al., 2007J 1ay ott et al., 2009J Plus et al., 2010J Dos Santos et al., 2013J Diepens et al., 2017). Fig. 1. Location of the Vaccarès lagoon and samples stations in the study area (Camargue, South of France). Figure has been modified from Boutron et al. (2015). Fig. 2. Annual average cover (%) of Zostera meadow in the Vaccarès lagoon over all stations per year (grey bars), in comparison with salinity in July (circles) and December (triangles). Dark grey bars: average cover of 55 sampling stations, light grey bars: estimated cover using remote sensing. .n the south of /ran e, seagrass de line has been reported in the river deltas along the 3editerranean oast, espe ially in the 9a arEs lagoon, Camargue (/ig. 1). ,his shallow lagoon is among the most disturbed oastal e osystems be ause it is isolated by the Rh%ne River, dams and surrounding intensive agri ulture (mainly ri e). ,his is the main lagoon of the .le de Camargue, internationally re ogniHed as a biosphere reserve under the UNESCORs 3an and the Biosphere Programme, and as a RA3SAR site. ,he .le de Camargue is of global importan e for nesting, staging, and wintering water birds (S ott and Rose, 1997). Sin e 1993, its dominant ma rophyte spe ies, Fostera noltei (a.k.a. F. noltei, Iornemann, 1832), has shown e4treme variations in its average over with two maCor de lines in 1997 and 2008 (/ig. 2). ,he first de line was e4plained by a de rease in salinity, probably due to signifi ant rainfall and greater freshwater input, whi h aused an in rease in water turbidity (Charpentier et al., 2005). ,he other main fa tors ruling the spatial distribution of F. noltei are water depth and wave e4posure. Iowever, these abioti fa tors ould not e4plain the se ond de line (Charpentier et al., 2005). .t has been reported that poor water 0uality, and espe ially eutrophi ation, have a negative impa t on F. noltei at population and individual levels, and ould lead to regime shifts towards an algae dominated state (9aliela et al., 1992J 3 Glathery, 2001J Brun et al., 2002, 2008J Cardoso et al., 2005J CabaSo et al., 2008J Plus et al., 2001, 2010). /or e4ample, there were fewer 2 non-stru tural arbohydrates in rhiHomes at stations with a poor e ologi al 0uality status along the Atlanti oast of Portugal and Spain (Gar Ta-3arTn et al., 2013). 3oreover, hemi al mi4tures, in luding tra e metals and pesti ides, do impa t seagrasses at individual level (i.e. physiologi al and whole plant levels), and may be linked to population and ommunity effe ts (/lores et al., 2013J Negri et al., 2015J Unsworth et al., 2015J 1ilkinson et al., 2015J Diepens et al., 2017). Previous studies revealed the presen e of 25 different pesti ides in the surfa e water of the lagoon in 2005. Ri e ultivation was the maCor ontributor (90%) and the remaining 10% ame from the Rh%ne River (Comoretto et al., 2007). Considering ontaminant on entrations and their fate (e.g. adsorption to organi matter in sediment and bioa umulation) and effe ts, poor water and sediment 0uality ould be onsidered as a dire t ause of Fostera meadow de rease in the 9a arEs lagoon. Understanding seagrass dynami s and the influen e of multiple stressors on seagrasses at various levels of biologi al organisation is ru ial for environmental risk assessment and for preserving these valuable e osystems with integrated management strategies. ,he aim of the present study was to e4amine the role played by hemi al ontamination in the dynami s of Fostera meadows, taking into a ount possible intera tions with other environmental stressors. .t was hypothesised that some spatial patterns in the dynami s and physiology of Fostera ould be identified a ross the 9a arEs lagoon and tied in with ontamination gradients. 2. Material and methods ,o study temporal variation in the parameters monitored, we present data from 1980 to 2015 (,able 1, for details see supporting information ,ables S1 and S2). ,he earliest years on ern eelgrass over (1980A2015). Subse0uent attention was given to the potential effe ts of hemi al ontamination and environmental parameters fo using on the years 2011A2013 for inter-sites omparison.
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