Impact of intertidal oyster trestle cultivation on the Ecological Status of benthic habitats

Highlights

• The IQI is suitable for assessing ES in Irish intertidal environments.

• The IQI has potential as a tool for the management of intertidal oyster cultivation.

• Cultivation activities at access routes had a significant negative impact on ES.

• The IQI has potential for assessing habitat conservation status in Natura 2000 sites.

Abstract

A considerable number of Ireland’s shellfish production areas co-occur with or are adjacent to Natura 2000 sites which are protected under European legislation. To investigate the general interaction between trestle oyster cultivation and the surrounding intertidal environment, six sites were selected within designated Natura 2000 sites. At each trestle site three Treatment areas were sampled. One Treatment area corresponded to potential impacts associated with cultivation activities occurring at trestle structures (designated the Trestle Treatment) while one Treatment area corresponded to potential impacts due to cultivation activities occurring along access routes (the Access Treatment). An area not subject to any known anthropogenic activity was used as a control (the Control Treatment). Potential impacts associated with Trestle Treatment areas included changes in sediment total organic matter (TOM) levels underneath trestles due to the bio-deposition of faecal/pseudofaecal material while the predominant impact associated with Access Treatment areas was compaction of sediments due to heavy vehicle traffic. In this study, macrobenthic communities at the sites were highly variable and exhibited low levels of diversity which prevented the detection of general effects of cultivation activity on community structure, diversity and secondary production. To overcome this variability, the Infaunal Quality Index (IQI) was used to assess impacts on Ecological Status (ES) of benthic communities (sensu Water Framework Directive). Relative to Control and Trestle Treatment areas, activities occurring at Access Treatment areas had a significant negative impact on ES. This study highlights the potential of the IQI for the management of aquaculture activity and provides validation for the use of the IQI in Irish intertidal environments. This study also highlights the IQI as a potential tool for assessing the conservation status of designated habitats in Natura 2000 sites.

Introduction

The impact of different modes of shellfish cultivation on benthic habitats and associated communities have been well documented in the literature (for review see McKindsey et al., 2011, Gallardi, 2014) and are largely attributable to the bio-deposition of pseudofaecal and faecal material by cultured organisms (Crawford et al., 2003, McKindsey et al., 2011). The impact of the increased flux of organic material to the seabed on benthic communities around aquaculture facilities is well studied and broadly follows the Pearson and Rosenberg (1978) generalised model of organic enrichment and oxygen deficiency (McKindsey et al., 2011). Pearson and Rosenberg (1978) showed that the structure of benthic communities changed in a predictable fashion in relation to distance from sources of disturbance. As disturbance increases benthic communities exhibit declines in diversity, abundance and biomass with stress sensitive, large bodied, infaunal deposit feeders becoming increasingly replaced by stress tolerant, small bodied, opportunistic species. The level of impact associated with suspended shellfish cultivation facilities on the subtidal benthic environmental can vary considerably (Crawford et al., 2003, McKindsey et al., 2011). For instance, some studies have recorded significant increases in the abundance of species tolerant to high organic loading (Tenore et al., 1982), reductions in bottom oxygen concentrations and the formation of extensive bacterial mats under aquaculture structures (Cranford et al., 2009, Dahlbäck and Gunnarsson, 1981, Souchu et al., 1998). While the effects of suspended shellfish cultivation activity are generally most severe directly underneath and in the immediate vicinity of cultivation structures, previous studies have reported significant enrichment of sediment can extend into the surrounding environment (e.g. Borja et al., 2009a). In general, the shifts in community structure reported in Borja et al. (2009a) were typical of organic enrichment. Other subtidal studies reported no significant effect of suspended shellfish cultivation on benthic infaunal communities (Crawford et al., 2003) or only minimal effects on sediment chemical fluxes (e.g. Baudinet et al., 1990) and community structure (e.g. Chamberlain et al., 2001). Similarly, studies investigating the interaction of shellfish cultivation in intertidal areas have reported varying levels of impact. Castel et al. (1989) reported that organic enrichment and low bottom oxygen concentrations associated with bottom “parc” cultivation of Crassostrea gigas at Arcachon, France resulted in significant decreases in the relative diversity and abundance of macrobenthic species with an allied increase in the meiobenthic species. Similar effects of off-bottom oyster trestle cultivation were observed in intertidal macrobenthic communities in the River Exe estuary, Devon, England (Nugues et al., 1996). In contrast, a study at an extensive intertidal oyster trestle farm in Dungarvan Harbour, on the southwest coast of Ireland, showed no evidence of organic enrichment (De Grave et al., 1998). The absence of organic enrichment was attributed to the high dissipative nature of the site acting to effectively prevent the accumulation of pseudofaecal and faecal material in the vicinity of the culture structures. However, the study did report significant changes in the relative abundance of surficial and shallow burrowing fauna along access track lanes used by heavy vehicles to access the farm. Mallet et al. (2006) also identified erosion associated with wave action as a reason for no observed difference in organic enrichment between oyster culture and control locations.

In Ireland, a considerable number of shellfish production areas co-occur with or are adjacent to Natura 2000 sites which are protected under European legislation. Natura 2000 sites include Special Areas of Conservation (SACs) designated due to their significant ecological importance for species and habitats protected under the Habitats Directive (HD; Council Directive, 92/43/EEC) and Special Protected Areas (SPAs) designated for the protection of bird species protected under the Birds Directive (BD; Council Directive, 2009/409/EEC). Under Article 6(3) of the HD Appropriate Assessment (AA) is required to be conducted for any project or plan that is likely to have a significant effect on a designated European Natura 2000 site. To this end, AAs have been carried out at a number of Ireland’s Natura sites to assess likely impacts of existing and proposed aquaculture activities on conservation features within the protected sites (e.g. Marine Institute, 2011, Marine Institute, 2013). Despite Ireland’s proactive approach to monitoring and assessment there remains some doubt concerning the level of impact of intertidal shellfish cultivation activities on the benthic environment. The development of a systematic approach to assess and compare the impacts associated with cultivation activity on different habitat types across multiple geographical sites is therefore required. Typically, investigations assessing anthropogenic impacts on benthic habitats produce complex data matrices describing species abundance and local environmental conditions (e.g. sediment characteristics, ecological disturbances) at a series of sites (Elliot, 1994, Clarke and Warwick, 2001, Clarke and Gorley, 2006, Whomersley et al., 2010). To simplify, summarise, quantify and communicate complex ecological information a range of benthic indicators have been developed to detect and compare change in the quality of benthic subtidal habitats and communities (Borja et al., 2000, Borja et al., 2009a, Borja et al., 2009b, Clarke and Warwick, 2001, Elliot, 1994, Mackie, 2009, Phillips et al., 2014, Prior et al., 2004, Quintino et al., 2006, Rosenberg et al., 2004, Whomersley et al., 2010). Indicators include the AZTI Marine Biotic Index (AMBI; Borja et al., 2000), the Multivariate-AZTI Marine Biotic Index (M-AMBI; Borja et al., 2007, Muxika et al., 2007) and the Infaunal Quality Index (IQI; Phillips et al., 2014, Prior et al., 2004, Mackie, 2009). Like many benthic indices the AMBI, the M-AMBI and the IQI are largely dependent on the Pearson-Rosenberg (1978) model for organic enrichment. The AMBI is a single metric index which is calculated based on the proportions of five Ecological Groups (EG) to which benthic species are allocated depending on their tolerance to disturbance (Borja et al., 2007, Muxika et al., 2007). The assignment of species to EG in the AMBI is based on the extensive literature describing North Atlantic species and, where the existing literature is lacking, consensus expert judgement (Teixeira et al., 2010). Based on AMBI index values benthic communities are classified as undisturbed, slightly disturbed, moderately disturbed, heavily disturbed or extremely disturbed (Muxika et al., 2007). In Ireland the IQI is used as a tool for monitoring change in Ecological Status (ES) of benthic habitats under the European Water Framework Directive (WFD; Council Directive, 2000/60/EC) (e.g. Prior et al., 2004, Borja et al., 2007, EPA, 2011, Forde et al., 2012, Forde et al., 2013, Kennedy et al., 2011, Phillips et al., 2014). Metrics used in the calculation of the IQI include the AMBI, Simpson’s evenness diversity index (1−λ′) and the number of invertebrate taxa (S). Before ES assessments can be made reference conditions for the IQI component metrics must be described. Within the IQI tool reference conditions are set with regard to habitat physico-chemical conditions and sampling techniques associated with the sample. For each sample monitoring data for each component are compared to their reference conditions to derive an Ecological Quality Ratio (EQR). EQR values range between 0 and 1, with High status represented by values close to 1 and Bad status close to 0. The EQR scale is sub-divided into five ES classes by assigning a numerical value to each of the class boundaries. The ES classes are High, Good, Moderate, Poor and Bad.

Previous studies have highlighted the ability of AMBI-based methodologies to successfully discriminate the responses of macrobenthic communities to a wide range of natural and anthropogenic environmental impacts including aquaculture, in both coastal and transitional waters, and throughout different regions. The majority of studies investigating the impact of finfish and shellfish aquaculture using AMBI-based indictors have focussed on subtidal habitats (e.g. Aguado-Giménez et al., 2007, Borja et al., 2009a, Callier et al., 2008, Sanz-Lázaro and Marín, 2006) while the indicators remain relatively untested in the intertidal. However, a number of recent studies have highlighted the potential of AMBI-based indicators for assessing anthropogenic impacts on intertidal habitats and communities (e.g. Bouchet and Sauriau, 2008, Fitch and Crowe, 2010). In the current study the IQI is used to assess the general impact of oyster trestle cultivation activity on the ES classification (sensu the WFD) of macrobenthic communities at six intertidal sites around the Irish coast. In addition to highlighting the IQI as a tool for the management of shellfish cultivation activity this study provides possible validation for the use of the IQI in Irish intertidal environments and for assessing the conservation status of designated habitats in Natura 2000 sites.

This study serves two broad purposes;

• Given that the literature can be somewhat conflicted in relation to the impact of intertidal oyster trestle cultivation on surrounding habitats and associated communities, this study was initiated to examine the influence of cultivation activities on habitat sediment characteristics and macrobenthic community structure, diversity and secondary production at a range of sites around the Irish coast. The sites were chosen because they are considered representative of larger scale production areas which are typically large intertidal sand flats. The study examined habitat and community characteristics in areas subject to interaction with oyster trestles and site access routes as well as control locations not subject to any known anthropogenic activity.

• To test the applicability of the WFD IQI EQR for the assessment of the putative impacts of shellfish cultivation on intertidal habitats and associated communities. Using the IQI, the outputs of this study comparing the impacts associated with cultivation activities on habitats across a range of geographical areas will inform the further development of a systematic approach to measure and assess ES in intertidal areas.