Can benthic foraminifera serve as proxies for changes in benthic macrofaunal community structure? Implications for the definition of reference conditions
Introduction
Most benthic macro-invertebrate species are sedentary, making them dependent on the local environmental conditions. Living at the sediment-water interface, they integrate aquatic as well as sediment conditions. Their communities show dramatic changes in their composition in response to organic matter loads (Pearson and Rosenberg, 1978; Bouchet and Sauriau, 2008), oxygen depletion (Rosenberg et al., 2002), oil spills (Gray et al., 1990), sewage (Glémarec and Hily, 1981), heavy metals (Olsgard and Gray, 1995) and physical disturbance (Lavesque et al., 2009). Tolerant species thrive at the early stages of the perturbation, followed by highly tolerant opportunistic species when the perturbation becomes severe (Glémarec and Hily, 1981). Hence, macrofauna are routinely used in environmental bio-monitoring studies (e.g. Warwick, 1986; Grall and Glémarec, 1997; Borja et al., 2003; Bouchet and Sauriau, 2008). In response to the implementation of marine legislation such as the Water Framework Directive (WFD), the Clean Water Act, and the Marine Strategy Framework Directive (MSFD), numerous indices based on macrofauna have been established for assessing the ecological quality status (EcoQ, see review in Pinto et al., 2009). Most of the indices developed to assess the EcoQ of marine systems are based on the indicative value of macrofaunal species. They have been classified into 5 ecological groups of sensitivity to disturbances from sensitive to first-order opportunistic species (Glémarec and Hily, 1981; Borja et al., 2000). Lately, concerns arose about these indices (see review in Spilmont, 2013). One of the main concerns is the definition of reliable reference conditions for benthic macrofaunal communities. This is a crucial point since in the European Water Framework Directive (WFD), reference conditions are mandatory to assess the EcoQ. According to the WFD, the reference conditions (also called “high” status) are defined as “for any surface water body type reference conditions or high ecological status is a state in the present or in the past where there are no, or only very minor, changes to the values of the hydromorphological, physico-chemical, and biological quality elements which would be found in the absence of anthropogenic disturbance” (Common implementation strategy for the Water Framework Directive (2000/60/EC), Guidance Document No.5, transitional and coastal waters – typology, reference conditions and classification systems p. 106). Assessment of environmental quality is based on the extent of deviation from these reference conditions, following the definitions in the WFD (www.ec.europa.eu/environment/water/marine.htm). Most of the coastal areas are modified or have been modified by human activities (Diaz and Rosenberg, 2008). Hence, EcoQ assessment within the WFD is facing issues to determine true reference condition (Nielsen et al., 2003; Elliott and Quintino, 2007). As for benthic macrofauna, since there is almost no data from pre-impact time, reference conditions have to be determine using today's communities, which is an issue considering the aforementioned degradation of coastal areas.
There is an increasing interest in the use of benthic foraminifera to characterize the health of marine systems (e.g. Alve, 1995; Scott et al., 2001; Mojtahid et al., 2006; Bouchet et al., 2007; Frontalini et al., 2009). Lately, indices to use benthic foraminifera routinely to assess EcoQs have been proposed (Hallock et al., 2003; Alve et al., 2009; Bouchet et al., 2012; Barras et al., 2014; Dimiza et al., 2016). Specifically, benthic foraminiferal species were assigned to ecological groups (EGs) according to their sensitivity/tolerance to increasing organic matter enrichment (Alve et al., 2016; Jorissen et al., 2018), inspired by work on benthic macrofauna to develop the AMBI index (Glémarec and Hily, 1981; Borja et al., 2000). It led to the development of the Foram-AMBI to assess the ecological quality status of marine systems. In these studies, the response of species along a gradient of enrichment in organic matter allowed their classification into groups of different sensitivity. Five ecological groups were defined: sensitive (EG1), indifferent (EG2), tolerant (EG3), second-order opportunistic (EG4) and first-order (most) opportunistic (EG5). The AMBI and the Foram-AMBI are computed based on the proportion of the different ecological groups in the species community, allowing assessment of ecological quality status.
Benthic foraminifera leave an easily accessible and abundant fossil record, which allows reconstruction of the characteristics and timing of historical environmental variations (e.g. Alve, 1991; Hayward et al., 2004; Dolven et al., 2013; Polovodova Asteman et al., 2015; Francescangeli et al., 2016). Consequently, it is possible to trace the record of human-induced disturbance over decades or centuries. Indeed, in a pilot study, Alve et al. (2009) suggested that in situ reference conditions can be established using fossil benthic foraminiferal assemblages from dated sediment cores. For example, by comparing the “background” fossil foraminiferal assemblages to the modern living foraminiferal assemblages at the same site, it would be possible to determine if a site is naturally anoxic or has become anoxic with recent human influence. This kind of temporal, in situ monitoring is not possible with soft-bottom sediment macrofauna because they do not leave abundant or, for most species, any fossil records. Benthic foraminifera may thus provide a powerful tool for defining habitat-specific, in situ reference conditions for soft-bottom coastal and transitional waters. Although the response of macrofauna and foraminifera species to environmental gradients may partly differ (Mojtahid et al., 2008), the few studies comparing the two groups have indicated that their responses to environmental changes are basically similar (Schafer et al., 1975, 1995; Klitgaard-Kristensen and Buhl-Mortensen, 1999; Bouchet, 2007; Denoyelle et al., 2010; Dolven et al., 2013; Hess et al., 2013; Wlodarska-Kowalczuk et al., 2013). For instance, benthic foraminiferal and macrofaunal communities showed similar response to oil-based drill mud disposal with tolerant and opportunistic species dominating in the vicinity of the disposal area (Denoyelle et al., 2010). Furthermore, calcareous foraminifera can be reliable indicators for variability in density, diversity and species composition of benthic macrofauna in the Artic at Svalbard (Wlodarska-Kowalczuk et al., 2013). Hence, it is reasonable to suggest that macrofaunal and foraminiferal species with similar sensitivity to environmental changes may show co-occurrence. This would be of great interest when it comes to the definition of reference conditions. It is reasonable to think that fossil benthic foraminifera could be used as proxies to define reference conditions for benthic macrofauna communities. Further baseline studies are however necessary to validate such a hypothesis. It is thus urgent to quantify the level of correlation between the distribution patterns of these two groups in other environments.
In the present study, living benthic foraminifera and macrofauna were investigated in fjordic systems along the Norwegian Skagerrak coast to assess to which degree their responses to major driving environmental factors correspond. This work is part of a comprehensive project (PES), which includes both foraminifera and macrofauna collected at the same sites at the same time. An understanding of the driving forces of the benthic foraminifera communities, expressed as species diversity, was partly achieved in a previous analysis of the same data set (Bouchet et al., 2012, 2013). The present paper aims (i) to determine the driving environmental factors of both the benthic foraminiferal and macrofaunal community structures, (ii) to identify indicator species of both normal and poor environmental conditions, (iii) to compare species assignment in EG from this study to the existing Foram-AMBI and AMBI species lists, and (iv) to assess the correlation between benthic foraminiferal and macrofaunal community patterns to identify the potential of benthic foraminifera to serve as a proxy for benthic macrofauna in environmental assessments.
Section snippets
Study area and sampling sites
In August 2008, 27 stations from 11 silled basins along the Norwegian Skagerrak coast, NE North Sea (Fig. 1), were sampled for bottom water, sedimentological, biogeochemical and faunal analyses. Stations between 23 and 204 m water depth were selected to provide an oxygen gradient with stable temperature (5–6 °C; occasionally 8–9 °C at <40 m depth) and salinity (33–34) conditions (Table 1; see Bouchet et al., 2012 for further details) using information from previous studies (Buhl-Mortensen et
Environmental conditions at sampling stations
Depth-below threshold (DBT), bottom-water dissolved oxygen concentration, sediment grain size and sediment organics were rather different among the stations (Table 1). Sandnesfjord, Eidangerfjord, Risørbassenget (R60), Topdalsfjord, Groosefjord, Frierfjord (except F70) and Indre Hvaler have rather shallow DBT below 50 m, whereas the other fjords have DBT up to 169 m. In Kristiansandsfjord there is no sill. High (normoxic) bottom-water oxygen concentrations (>2 mL O2.L−1) characterized stations
Discussion
In the present study, patterns of distribution of foraminiferal and macrofaunal species are best explained by the variables of TOC and DBT. Along the same lines, deep-water renewal and oxygenation in a fjord depend on DBT as well as on the supply of organic matter (i.e., impacts oxygen consumption). DBT will, however, also represent the influence of other variables, e.g. pigments, different organic components and temperature, that increase or decrease due to the gradually changing conditions
Acknowledgment
We are grateful to the crew of the R/V Trygve Braarud; S Holm, J. Sundøy and T.E. Baade. Nina Reuss is warmly thanked for the analysis of pigment samples. Thanks are also due to M. Hollerbach, and J. Håvardstun for assistance during fieldwork, and Y. Descatoire for graphics. This study was supported by the Norwegian Research Council-funded project PES (no. 184870) “Paleoecological reconstructions of marine soft-bottom Ecologic Status and in situ reference conditions: calibrating benthic
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