Identifying benthic macrofaunal assemblages and indicator taxa of intertidal boulder fields in the south of the Bay of Biscay (northern Basque coast). A framework for future monitoring

Abstract

The French southern marine subregion of the Bay of Biscay presents local environmental features explaining the presence of specific communities in remarkable habitats. The aim of the study is, for the first time, to assess benthic macrofaunal assemblages and to identify indicator species of each assemblage within intertidal boulder field habitats in this marine subregion.

Mobile boulders were sampled with a stratified random sampling design in upper and lower midlittoral zones in March–June 2015. Sessile (in percentage cover) and mobile macrofauna (in abundance) communities were identified and counted within 0.1 m² quadrats. Ecological function and precision between the two groups were found dissimilar thus species richness, abundance, macrofauna distribution and indicator species/taxa of sessile and mobile macrofauna were analyzed separately. 78 species/taxa of macrofauna were recorded. A restricted list of 12 singletons (8 for mobile and 4 for sessile macrofauna) and 33 combinations of species/taxa were identified as significant indicators of each assemblage. Species ecological features (food webs, signs of disturbance, alien species, biogeographical range limit) were also considered as additional selection criteria. Therefore, species with a high ecological interest but not considered statistically as valid indicators were also highlighted.

Thus, this work constitutes a framework for future monitoring of the Basque intertidal rocky shore and could be used as an alternative to sampling the entire biodiversity. It also meets the MSFD requirements (e.g. take into account marine subregion specificities; integrate the metric “macrofauna” and supports several descriptors as the D1 “Biodiversity” and D6 “Seafloor integrity”).

Introduction

Over the last decades, investigations and monitoring of biological communities, used as bio-indicators, have been carried out worldwide to assess continental and marine ecosystems. Those were undertaken in different contexts either in the prospect of a global climatic change Barange (2003), Thompson et al. (2002) or to evaluate ecological status of water bodies (e.g., European Water Framework Directory (WFD)) ( European Commission, 2000; Borja et al. (2013), Guinda et al. (2008)). Indeed, ecological indicators are useful to monitor environmental changes and assess ecological management and conservation Cairns et al. (1993), Legendre and Legendre (1998), Marques et al. (2009), Siddig et al. (2016). They provide information to understand the environment and its ecological status while highlighting changes in the environment by giving, for example, early warning signals (Cairns et al., 1993). The identification of indicator species is commonplace in ecology and biogeography because they add ecological meaning to studied sites and their use is an alternative to sampling the entire biodiversity (Legendre and Legendre, 2012).

Nowadays, there is a large number of survey methods used to study the intertidal benthic environment. Various tools have been developed to analyze rocky shore communities data (e.g., Borja et al., 2013; Borja and Dauer, 2008; Clarke, 1993; Dauer, 1993; Panayotidis et al., 2004; Rombouts et al., 2013). Macroalgal communities, which are one of the dominant groups of hard substrata, are often used as bioindicators (for instance to assess the water quality of coastal waters for the WFD Ar Gall et al. (2016), Ar Gall and Le Duff (2014), Ballesteros et al. (2007), Díez et al. (2012), Orfanidis et al. (2001). More recently, the European Marine Strategy Framework Directive ( European Commission, 2008, MSFD) has proposed a set of indicators (e.g. characteristic and opportunistic species) in order to assess the environmental status of marine habitats (Teixeira et al., 2016). But, assessment and monitoring programs must be achieved and adapted to the level of marine subregions while integrating and supporting the monitoring requirements imposed by other EU legislation, such as the Habitats Directive (92/43/EEC), Birds Directive (2009/147/EC) and international agreements (Patrício et al., 2016). Moreover, the MSFD emphasized significant deficiencies Berg et al. (2015), Heiskanen et al. (2016), Queirós et al. (2016), Teixeira et al. (2014), in particular from the Basque Country (southern Bay of Biscay subregion) (Borja et al., 2011).

A great number of studies (including studies carried out on the national scale) highlighted the bathymetric zonation of benthic communities (species richness and diversity patterns) in the intertidal systems (e.g., Ballesteros, 1992; Bellan and Bellan-Santini, 1972; Bellan-Santini, 1966; Bouchet and Tardy, 1976; Fischer-Piette and Duperier, 1960; Folin, 1903; Hondt, d’; Murray et al., 2006; Ortea, 1979; Thompson et al., 2002; Underwood, 1981; Van Den Hoek and Donze, 1966). The relevance of studying benthic macrofauna in intertidal boulder fields is widely documented throughout the world Archambault and Bourget (1996), Grayson and Chapman (2004), Hiscock et al. (2005), Kuklinski et al. (2006), Sousa (1979). Within this habitat, macroalgal communities are ephemeral due to boulder instability. Sessile macrofauna are distributed in a patchwork of successional stages (Sousa, 1979). Most French studies on macrofauna are conducted in Brittany Bernard (2012), Guillaumont et al. (2009), Le Hir and Hily (2005). Surprisingly, few studies have been undertaken in the northern Basque coast (France) while high hydrodynamic pressure may occasionally disrupt the bathymetric zonation of benthic communities. Since 2008, solely macroalgae surveys have been carried out to assess the ecological status on platforms within the WFD (Casamajor (de) et al., 2016). A macrofauna inventory is currently conducted on the Basque coast but without considering the habitat type such as platforms and boulders (Castège et al., 2014). By contrast, many studies have been carried out on platforms and other habitats in the southern Basque coast (Spain) Aguirrezabalaga et al. (1986), Aroca et al. (1984), Artica (1978), Borja et al. (2004), Elosegui (1985), Elosegui et al. (1987), Gorostiaga et al. (2004).

The marine subregion “Bay of Biscay” shows environmental specificities. In France, thirty percent of this coastal zone is composed by rocky substrata (Chust et al., 2009). The northern Basque coast constitutes a smaller rocky area (around 15 km long; Chust et al., 2009) in comparison with the Brittany’s coastline or the southern Basque coast (around 135 km long; Borja and Collins, 2004). Within the intertidal zone, taxa live in heterogeneous habitats listed in the Habitats Directive Annex I as boulder fields, platforms and rock pools (EUR 27, July 2007, European Commission). This zone, with considerable spatial and temporal variations of environmental components (temperature, salinity), is especially sensitive because impacts are concentrated. Communities are thus subject to environmental conditions which create a stressful habitat. It is due to mesotidal conditions, with a magnitude between 1.85 and 3.85 m (Augris et al., 2009), energetic waves Abadie et al. (2005), Bajjouk et al. (2015), freshwater input caused by rainfall and a dense river system (Winckel et al., 2004) and coast orientation (exposition to swell, slope). Urban sprawl and summer overcrowding also explain the increased anthropogenic pressures on the coastline Cearreta et al. (2004), Chust et al. (2009), Le Treut (2013). All those parameters in this region, considered as a heritage area Augris et al. (2009), Casamajor (de) and Lalanne (2016), justify the presence of specific communities in these remarkable habitats (Borja et al., 2004).

The aim of the study is therefore: (i) to describe macrofauna assemblages of the boulder field habitat that is poorly known in the southern marine subregion of the Bay of Biscay, (ii) to identify, for the first time, indicator species/taxa of this habitat which could be used to detect time changes and as an alternative to an exhaustive sampling of biodiversity and (iii) to provide a framework for future monitoring. Lastly, this study bridges the data gap emphasized by the MSFD on rocky-shore macrofauna communities notably in this specific area.