Benthic foraminifera to assess ecological quality statuses: The case of salmon fish farming
Introduction
During the last 30 years, aquaculture in marine waters has greatly increased partly driven by the need for greater self-sufficiency in marine food production (Holmer, 2010). However, it is now widely acknowledged that activities related to aquaculture cause environmental disturbances (Bouchet and Sauriau, 2008, Carvalho et al., 2006, Chamberlain et al., 2001). Numerous studies have demonstrated that aquaculture degrades both sedimentary characteristics and benthic communities (Bouchet and Sauriau, 2008, Karakassis et al., 2002, La Rosa et al., 2004, Mazzola et al., 2000, Dauvin et al., 2020), which ultimately leads to decreased ecological quality statuses (Bouchet and Sauriau, 2008, Muxika et al., 2005). Previous studies show that the impacts of fish farms are essentially localised and depend mainly on aquaculture and environmental factors such as fish density, start date of activities, water depth, initial sea bottom site characteristics and hydrodynamic regime (Black, 2001, Karakassis et al., 2002, Yokoyama et al., 2006, Dauvin et al., 2020).
The Rade de Cherbourg (RdC), the second largest artificial roadstead in the world, is located on the north coast of the Cotentin Peninsula (Normandy, France) and hosts the only open marine water French salmon farm since the begining of 1990 s. Sediments directly below the cages are characterized by a moderated and localized increase in mud, organic carbon and nitrogen content (Kempf et al., 2002, Baux et al., 2017, Dauvin et al., 2020). Both the high hydrodynamic regime in the RdC and the acceleration of currents under the cages (Poizot et al., 2016) may often enhance the dispersion of excess organic waste from the salmon fish farm and limit long term accumulation of organic matter (OM). Hence, there are most likely a shift between periods of accumulation and then dispersion of the sediment under the cages. Accumulated OM under salmon farms may leads to anoxia in the sediment (Nickell et al., 2003), hence generate further constraints on the related benthic communities. So far, only two studies described the soft bottom macrobenthic communities and the associated habitats in the RdC (Andres et al., 2020, Baux et al., 2017) and no information is available on meiobenthic communities. In addition, the salmon cages in the RdC have been shown to induce high to moderate Ecological Quality status (EcoQs), but only on the basis of a macrobenthic community assessment (Dauvin et al., 2020). There is consequently a need to monitor other components of the benthic ecosystem, an absolute prerequisite to assess the health status of the RdC in general, and in relation to salmon farming in particular.
There is now a plethora of biological quality elements (BQE) used to assess the health of benthic ecosystem — sensu stricto EcoQs — for instance, benthic macrofauna (Borja et al., 2000), fish (Coates et al., 2007), seagrass (Krause-Jensen et al., 2005), macro-algae (Ar Gall et al., 2016), and more recently, benthic foraminifera (Bouchet et al., 2012). Note that over the last 20 years, benthic macrofauna has been by far the most widely used BQE to assess EcoQs (Birk et al., 2012, Borja et al., 2000, Bouchet and Sauriau, 2008, Dauvin, 2018, Dauvin et al., 2007, Pinto et al., 2009, Rombouts et al., 2013). Recent developments in benthic foraminiferal biotic indices (Bouchet et al., 2012, Alve et al., 2016, Dimiza et al., 2016) provide, however, further opportunities for the development and implementation of this meiobenthic group as an acknowledged biological quality element within marine legislations for EcoQs assessment.
Benthic foraminifera have increasingly been acknowledged as indicators of human-induced stresses (e.g. Alve, 1995, Francescangeli et al., 2016, Polovodova Asteman et al., 2015), such as oil spills (Morvan et al., 2004), heavy metals (Armynot du Châtelet et al., 2004), urban sewage (Melis et al., 2016), and aquaculture (Bouchet et al., 2007, Debenay et al., 2015, Vidovic et al., 2014). Specifically, fish farms induce clear shifts in the community structure of benthic foraminifera (Pochon et al., 2015), promote tolerant species (Angel et al., 2000) and lead to moderate to poor EcoQs (Bouchet et al., 2018a). In Norwegian fjords, benthic foraminiferal communities significantly correlate with benthic macrofauna communities, indicating that foraminifera can also be considered as good indicators of environmental conditions (Bouchet et al., 2018b). Foraminiferal indices based either on diversity (Alve et al., 2009, Bouchet et al., 2013, Bouchet et al., 2012) and on the sensitivity of species to organic pollution (Alve et al., 2016, Barras et al., 2014, Dimiza et al., 2016, Jorissen et al., 2018), have been designed and successfully applied to assess EcoQs of benthic habitats (Alve et al., 2019, Bouchet et al., 2018a, Bouchet et al., 2012, Damak et al., 2020, Dijkstra et al., 2017, Dolven et al., 2013, El Kateb et al., 2020, Francescangeli et al., 2016, Melis et al., 2016). Alve et al. (2019) further demonstrated that foraminifera and macrofauna have similar indicator efficiency by applying multimetric index based on foraminifera (NQIf) as an alternative, which is an adaptation of the Norwegian Quality Index (NQI), an internationally intercalibrated macrofauna index. Based on their results, Alve et al. (2019) recommended the inclusion of foraminifera as Biological Quality Element within the European Water Framework Directive’s guidelines (WFD). In a study of Italian transitional waters, benthic foraminifera have further been shown to be more accurate than benthic macrofauna to assess EcoQs (Bouchet et al., 2018a). Considering the difficulties to assess EcoQs in naturally stressed ecosystems (Dauvin, 2007, Dauvin and Ruellet, 2009, Elliott and Quintino, 2007), foraminifera may be a relevant alternative to macrofauna (Hess et al., in press). Because of their potential to reconstruct palaeo-environments (Alve, 1991, Alve et al., 2009, Hayward et al., 2004), an unique feature compared to benthic macrofauna (except for molluscs; Poirier et al., 2009), foraminifera are also good candidates to establish objective and reliable reference conditions (Dolven et al., 2013, Francescangeli et al., 2016). In short, benthic foraminifera may be a relevant complement to benthic macrofauna to assess EcoQs. These two groups exhibit similar features. Both are benthic and sedentary organisms, their distribution patterns depending directly on the environmental conditions. Furthermore, foraminiferal and macrofaunal community compositions in SE Norwegian fjords were significantly correlated suggesting that benthic foraminiferal distribution patterns mirror those of benthic macrofauna (Bouchet et al., 2018b). Intercalibration of benthic foraminiferal and macrofaunal biotic indices further confirm the complementarity of these two groups (Alve et al., 2019). Hence, this study was designed to discuss the relative strength of the classical macrofauna tool and the “newcomers” benthic foraminifera one to assess ecological quality statuses in the RdC in the context of salmon fish farming.
In this context, the present study aims at (1) monitoring the impact of a salmon fish farm on ecological quality statuses (EcoQs) of the Rade of Cherbourg based on a benthic foraminiferal biotic index, (2) comparing EcoQs assessment results between benthic foraminifera and benthic macrofauna, and (3) assessing the potential for benthic foraminifera to become an alternate biological quality element.
Section snippets
Sedimentological, foraminiferal and macrofaunal sampling
For the present study, thirteen stations (Fig. 1) were sampled in June 2015 in the RdC by scuba-diving using a push corer (diameter: 9.8 cm, layer: 0–1 cm, n = 3). Stations from S17 to S24 were away the salmon fish farm in the RdC, while stations from S25 to S28 and S30 were directly under the salmon cages (Fig. 1). The geographical positions of the stations were determined using a RTK Global Position System (GPS ASHTECH Promark 120, accuracy better than 10 cm). The study stations were visited
Environmental parameters
Results for the fine fraction (<63 µm) and total organic carbon (TOC) percentages were summarized in the Table 2. The average percentage of the fine fraction represented 33 ± 7% outside the farm and 21 ± 5% under the salmon cages. There was no difference between the two areas (t-test, p > 0.05). Total organic carbon average contents in the sediment remained low in the RdC, 0.72 ± 0.16% and 0.45 ± 0.05%, respectively outside the farm and under the cages. There was no difference between the two
Effects of salmon fish farm on the benthic ecosystem health in the RdC
Our results did not reveal any specific accumulation of silt sediments nor organic matter due to the presence of the salmon farm in the RdC. This fact confirmed previous studies that showed only a moderate impact on the sediment characteristics in the RdC (Dauvin et al., 2020, Kempf et al., 2002). Specifically, the semi-diurnal megatidal regime of the Rade de Cherbourg (5–8 m tidal range from neap to spring tide) likely limits any long term accumulation of OM under the cages, with tidal current
Conclusion
This work confirmed that benthic foraminifera are reliable to evaluate EcoQs in the context of salmon fish farm as the indices used for the macrofauna. Hence, this study represents a further step towards the official inclusion of benthic foraminifera in the list of biological quality elements. Comparison with macrofauna confirmed that these two groups, that share similar features, have the same response to pollution. However, differences in the reported EcoQs might suggest that
CRediT authorship contribution statement
Vincent M.P. Bouchet: Conceptualization, Data curation, Formal analysis, Writing - original draft. Noémie Deldicq: Investigation, Visualization, Formal analysis, Writing - review & editing. Noémie Baux: Investigation, Formal analysis, Writing - review & editing. Jean-Claude Dauvin: Writing - review & editing. Jean-Philippe Pezy: Data curation, Writing - review & editing. Laurent Seuront: Formal analysis, Writing - review & editing. Yann Méar: Resources, Writing - review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The authors thank A. Baffreau and Q. Bachelet for their help in field and laboratory macrofauna works. We are grateful to crews of the “GMG Saumon de France” and N.O. Côtes de la Manche (CNRS-INSU) vessels. We are thankful to Helena Adão, guest editor of the special Issue of Ecological Indicators entitled: “SeventIMCO, the 17th International Meiofauna Conference: Meiofauna in a changing world” and to two anonymous reviewers; their comments greatly help improving this paper.
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