Good-Moderate boundary setting for the environmental status assessment of the macrozoobenthos communities with the Benthic Quality Index (BQI) in the south-western Baltic Sea.

The status assessment of the macrofauna community under the European Marine Strategy Framework Directive (MSFD) requires threshold values that mark the transition from good to moderate conditions (G-M boundaries). Using the example of the Benthic Quality Index (BQI) in the south-western Baltic Sea, we demonstrate the possibilities and restrictions of i) defining G-M boundaries using reference areas, historical data and a statistical method and ii) the subsequent evaluation of the resulting G-M boundaries using disturbance data. The historical data from the period 1911 to 1929 proved to be unsuitable for defining G-M boundaries due to their data quality. The G-M boundaries calculated using the statistical method delineated high disturbance values more reliably than those based on reference areas. We conclude that disturbance data are very useful to evaluate G-M boundaries for their suitability, but data on all state conditions are needed.

Substrate Heterogeneity as a Trigger for Species Diversity in Marine Benthic Assemblages.

Many studies show that habitat complexity or habitat diversity plays a major role in biodiversity throughout different spatial scales: as structural heterogeneity increases, so does the number of available (micro-) habitats for the potential species inventory. The capability of housing species (even rare species) increases rapidly with increasing habitat heterogeneity. However, habitat complexity is not easy to measure in marine sublittoral sediments. In our study, we came up with a proposal to estimate sublittoral benthic habitat complexity using standard underwater video techniques. This tool was subsequently used to investigate the effect of habitat complexity on species richness in comparison to other environmental parameters in a marine protected area situated in the Fehmarn Belt, a narrow strait in the southwestern Baltic Sea. Our results show that species richness is significantly higher in heterogeneous substrates throughout all considered sediment types. Congruently, the presence of rare species increases with structural complexity. Our findings highlight the importance of the availability of microhabitats for benthic biodiversity as well as of the study area for regional ecosystem functioning.

High-resolution history of oxygen depletion in the SW Baltic Sea since the mid-19th century as revealed by bivalve shells.

The Baltic Sea serves as a model region to study processes leading to oxygen depletion. Reconstructing past low-oxygen occurrences, specifically hypoxia, is crucial to understand current ecological disturbances and developing future mitigation strategies. The history of dissolved oxygen (DO) concentration in some Baltic Sea basins has been investigated in previous studies, but temporally well-constrained, inter-annual and better resolved DO reconstructions are still scarce. Here, we present precisely dated, high-resolution DO record since the mid-19th century reconstructed from Mn/Cashell values of Arctica islandica (Bivalvia) collected in the Mecklenburg Bight. According to the data, this area experienced similar low oxygenation during the second half of the 19th century and the late 20th century, but DO variability increased: A 12-15-yr oscillation prevailed in the 19th century, but a 4-6-year period dominated in the late 20th century. Shortly after the onset of the Industrial Revolution around 1850, Mn/Cashell values increased, indicating a DO decrease, probably caused by strong anthropogenic nutrient input. More recently, phosphate levels and inflows of oxygen-rich North Sea water have been identified as major factors controlling the bottom water oxygenation. For example, the increase in DO in the mid-1990s was linked to the decrease in phosphate content and several Major Baltic Inflows. The strong Ba/Cashell rise between the 1860s and the turn of the century most likely reflects changes in diatom community structure rather than a bloom of mass phytoplankton. This is supported by largely unchanged Mn/Cashell and shell growth. Decadal and multi-decadal cycles of shell growth rate correlated strongly with the Atlantic Multidecadal Variability, likely reflecting changes in atmospheric circulation patterns, precipitation rate and riverine nutrient supply. To further improve the management and protection of ecosystems in the Baltic Sea, a larger number of such high-resolution retrospective studies covering long periods of time and large regions are needed.

Habitats and Biotopes in the German Baltic Sea.

To maintain or enhance biodiversity and sea floor integrity, mapping benthic habitats is a mandatory requirement in compliance with the Marine Strategy Framework Directive (MSFD). The EU Commission Decision distinguishes between Broad Habitat Types (BHTs) and Other Habitat Types (OHTs). At the regional level, biotopes in the Baltic Sea region are classified according to the HELCOM underwater biotope and habitat classification (HUB). In this study, the habitats and their benthic communities were mapped for the entire German Baltic Sea at a high spatial resolution of 1 km. In two nature conservation areas of the Exclusive Economic Zone (EEZ) as well as selected focus areas in the coastal waters, the resolution we provide is even more detailed at 50 × 50 m. Hydroacoustic data recording and benthological surveys (using bottom grabs, underwater towing camera technology, and diver sampling) helped identify biotopes in high resolution. Based on these data, together with additional data acquired since 2010 (a total of over 7000 stations and transect sections), we were able to spatially delineate benthic biotopes and their communities via predictive habitat modelling. The results are provided as full-coverage maps each for BHT, OHT, and HUB (9 classes of BHTs, 5 classes of OHTs, and 84 classes of HUB) with a level of spatial detail that does not yet exist for the Baltic Sea, and they form an essential basis for future monitoring, status assessments, and protection and management measures.

Benthic Macrofauna Community Bioirrigation Potential (BIPc): Regional Map and Utility Validation for the South-Western Baltic Sea.

Benthic community bioirrigation potential (BIPc), an index developed to quantify the anticipated capacity of macrofauna to influence the solute exchange at the sediment-water interface, was calculated for the south-western Baltic Sea. This index can be regarded as an effect trait that is useful for predicting ecosystem processes impacted by animal burrow ventilation. The special feature, and presumably an advantage, of BIPc, compared to alternative recently developed benthic macrofauna-based bioirrigation indices, lies in its ability to distinguish the taxa-specific score values between diffusion- and advection-dominated sediment systems. The usefulness of the BIPc index was compared against the estimates of the well-established community bioturbation potential index (BPc). The BIPc index displayed a moderately but significantly stronger correlation with estimates of irrigation rates derived from tracer experiments. Using a random forest machine learning approach and a number of available relevant environmental predictor layers, we have modelled and mapped the spatial differences in this ecosystem functioning expression. The key species contributing to bioirrigation potential in the study area were identified. The interannual variation in BIPc was assessed on a small exemplary dataset. The scores required to calculate the index, that were assigned to 120 taxa dominating abundance and biomass in the region, are provided for reuse. The utility, temporal variability and uncertainty of the distribution estimate are discussed.

A new amphipod species of the bathyal genus Dautzenbergia Chevreux, 1900 (Amphipoda, Calliopioidea, Pontogeneiidae) associated with cold-water corals off Angola.

A new species of pontogeneiid amphipod, Dautzenbergia concavipalma sp. nov., is described from cold-water corals off Angola. This is only the second observation of this genus in the South Atlantic. Important morphological characters in combination, which define the new species from its congeners, occur especially in the shape and size of gnathopod 1-2 propodus, the smooth pereopod dactyls, the shape of the basis of pereopod 7 and the telson shape with narrow cleft. The taxon is fully described and figured and is compared with known species of the genus. A key to Dautzenbergia species is also given.

Transcriptional response of key metabolic and stress response genes of a nuculanid bivalve, Lembulus bicuspidatus from an oxygen minimum zone exposed to hypoxia-reoxygenation.

Benthic animals inhabiting the edges of marine oxygen minimum zones (OMZ) are exposed to unpredictable large fluctuations of oxygen levels. Sessile organisms including bivalves must depend on physiological adaptations to withstand these conditions. However, as habitats are rather inaccessible, physiological adaptations of the OMZ margin inhabitants to oxygen fluctuations are not well understood. We therefore investigated the transcriptional responses of selected key genes involved in energy metabolism and stress protection in a dominant benthic species of the northern edge of the Namibian OMZ, the nuculanid clam Lembulus bicuspidatus,. We exposed clams to normoxia (~5.8 ml O2 l-1), severe hypoxia (36 h at ~0.01 ml O2 l-1) and post-hypoxic recovery (24 h of normoxia following 36 h of severe hypoxia). Using newly identified gene sequences, we determined the transcriptional responses to hypoxia and reoxygenation of the mitochondrial aerobic energy metabolism (pyruvate dehydrogenase E1 complex, cytochrome c oxidase, citrate synthase, and adenine nucleotide translocator), anaerobic glycolysis (hexokinase (HK), phosphoenolpyruvate carboxykinase (PEPCK), phosphofructokinase, and aldolase), mitochondrial antioxidants (glutaredoxin, peroxiredoxin, and uncoupling protein UCP2) and stress protection mechanisms (a molecular chaperone HSP70 and a mitochondrial quality control protein MIEAP) in the gills and the labial palps of L. bicuspidatus. Exposure to severe hypoxia transcriptionally stimulated anaerobic glycolysis (including HK and PEPCK), antioxidant protection (UCP2), and quality control mechanisms (HSP70 and MIEAP) in the gills of L. bicuspidatus. Unlike UCP2, mRNA levels of the thiol-dependent mitochondrial antioxidants were not affected by hypoxia-reoxygenation stress. Transcript levels of marker genes for aerobic energy metabolism were not responsive to oxygen fluctuations in L. bicuspidatus. Our findings highlight the probable importance of anaerobic succinate production (via PEPCK) and mitochondrial and proteome quality control mechanisms in responses to oxygen fluctuations of the OMZ bivalve L.bicuspidatus. The reaction of L.bicuspidatus to oxygen fluctuations implies parallels to that of other hypoxia-tolerant bivalves, such as intertidal species.

Methodological elements for optimising the spatial monitoring design to support regional benthic ecosystem assessments.

Benthic habitat condition assessments are a requirement under various environmental directives. The Marine Strategy Framework Directive (MSFD), for example, challenges member states in a European sea region to perform comparable assessments of good environmental status and improve coherence of their monitoring programmes by 2020. Currently, North Sea countries operate independent monitoring programmes using nationally defined assessment areas. Lack of an agreed OSPAR or EU scale monitoring method and programme has been identified as a priority science need. This paper proposes a method for the development of a coherent and efficient spatial sampling design for benthic habitats on regional level and gives advice on optimal monitoring effort to get more accurate assessments. We use ecologically relevant assessment areas (strata) across national borders and test spatial sample allocation methods. Furthermore, we investigate the number of samples needed in each stratum to reduce the variance for estimating mean number of taxa and abundance. The stratification needs to take into account the spatial heterogeneity of the entire ecosystem. The total sample effort is optimal when sample allocation takes into account the size and benthic variability within those strata. Change point analysis helps to find a balance between sampling effort and precision of the benthic parameter estimate. A joint sampling design for the North Sea could be generated by combining current efforts, and where needed adapting existing national programmes. This serves a coordinated, region-wide, benthic condition status assessment and strengthens regional cooperation to fulfil multiple monitoring tasks, with a scientifically underpinned common approach.

Cold-water corals off Angola as refuge for a new Aeginella species (Crustacea: Amphipoda: Caprellidae).

A new species of caprellid amphipod, Aeginella corallina sp. nov., is described from cold-water corals off Angola. This is the first observation of this genus in the South-Atlantic. The taxon is fully described and figured and is compared with the only known species of the genus, A. spinosa, occurring in deep waters of the northern hemisphere. Both species can be clearly differentiated on the basis of the following characters: (1) pereonite 1 is provided with a large dorsal acute projection in A. spinosa, while this projection is lacking in A. corallina; (2) gnathopod 2 propodus has an acute projection distally which is lacking in A. corallina; (3) the palm of the gnathopod 2 propodus in males is densely setose and it is provided with two distal projections in A. corallina while it is scarcely setose and with less developed projections in A. spinosa; (4) distal article of the mandibular palp is provided by a setal formula of 1-x-1, being x=10-12, in A. spinosa, while in A. corallina x=2-3, and the formula 1-x-1 is not so evident and it could be considered as 1-x-0. (Zoobank: urn:lsid:zoobank.org:act:3D7EB67D-88F2-40D8-99C1-7D62F44F7163).

A new species of Ledoyerella, L. kunensis sp. nov. (Amphipoda, Senticaudata, Kamakidae) from South West Africa.

A new species of kamakid amphipod, Ledoyerella kunensis sp. nov., is described from waters off Namibia and Angola. This is the first record of this genus in the Atlantic. The taxon is fully described and figured and is compared with the other known species of the genus occurring in waters of the Indian and Pacific Ocean.

Benefits and shortcomings of non-destructive benthic imagery for monitoring hard-bottom habitats.

Hard-bottom habitats with complex topography and fragile epibenthic communities are still not adequately considered in benthic monitoring programs, despite their potential ecological importance. While indicators of ecosystem health are defined by major EU directives, methods commonly used to measure them are deficient in quantification of biota on hard surfaces. We address the suitability of seafloor imaging for monitoring activities. We compared the ability of high-resolution imagery and physical sampling methods (grab, dredge, SCUBA-diving) to detect taxonomic and functional components of epibenthos. Results reveal that (1) with minimal habitat disturbance on large spatial scales, imagery provides valuable, cost-effective assessment of rocky reef habitat features and community structure, (2) despite poor taxonomic resolution, image-derived data for habitat-forming taxa might be sufficient to infer richness of small sessile and mobile fauna, (3) physical collections are necessary to develop a robust record of species richness, including species-level taxonomic identifications, and to establish a baseline.

Biotope map of the German Baltic Sea.

Full-coverage maps on the distribution of marine biotopes are a necessary basis for Nature Conservation and Marine Spatial Planning. Yet biotope maps do not exist in many regions. We are generating the first full-coverage biotope map for the German Baltic Sea according to the HELCOM Underwater biotope and habitat classification system (HUB). Species distribution modelling is applied to create full-coverage spatial information of biological features. The results of biomass modelling of twelve target taxa and presence/absence modelling of three target taxa enabled the identification of biological levels up to HUB level 6. Environmental data on bathymetry, light penetration depth and substrate are used to identify habitat levels. HUB biotope levels were combined with HUB habitat levels to create a biotope map. Altogether, 68 HUB biotopes are identified in the German Baltic Sea. The new biotope map combining substrate characteristics and biological communities will facilitate marine management in the area.

Verifying a biotope classification using benthic communities--an analysis towards the implementation of the European Marine Strategy Framework Directive.

The HELCOM Red List biotopes project proposed a Baltic Sea wide classification consisting of six levels: The HELCOM Underwater biotopes/habitats classification system (HELCOM HUB). We present a case study from the south-western Baltic Sea where we tested the applicability of this system. More than 500 sampling stations were analyzed regarding macrozoobenthic communities and their linkage to environmental parameters. Based on the analyses of biotic and abiotic data, 21 groups were assigned to 13 biotopes of the classification. For some biotopes varying states of communities were recognized. Even though not all abiotic parameters are considered directly in the hierarchy of the classification in general, all soft-bottom communities could be allocated to a corresponding biotope. The application of the HELCOM HUB for the south-western Baltic Sea is feasible, in regard to the implementation of the European Marine Strategy Framework Directive as well as the Baltic Sea Action Plan.

On the myths of indicator species: issues and further consideration in the use of static concepts for ecological applications.

The use of static indicator species, in which species are expected to have a similar sensitivity or tolerance to either natural or human-induced stressors, does not account for possible shifts in tolerance along natural environmental gradients and between biogeographic regions. Their indicative value may therefore be considered at least questionable. In this paper we demonstrate how species responses (i.e. abundance) to changes in sediment grain size and organic matter (OM) alter along a salinity gradient and conclude with a plea for prudency when interpreting static indicator-based quality indices. Six model species (three polychaetes, one amphipod and two bivalves) from the North Sea, Baltic Sea and the Mediterranean Sea region were selected. Our study demonstrated that there were no generic relationships between environment and biota and half of the studied species showed different responses in different seas. Consequently, the following points have to be carefully considered when applying static indicator-based quality indices: (1) species tolerances and preferences may change along environmental gradients and between different biogeographic regions, (2) as environment modifies species autecology, there is a need to adjust indicator species lists along major environmental gradients and (3) there is a risk of including sibling or cryptic species in calculating the index value of a species.

The use of benthic indicators in Europe: from the Water Framework Directive to the Marine Strategy Framework Directive.

The Water Framework Directive (WFD) and the Marine Strategy Framework Directive (MSFD) are the European umbrella regulations for water systems. It is a challenge for the scientific community to translate the principles of these directives into realistic and accurate approaches. The aim of this paper, conducted by the Benthos Ecology Working Group of ICES, is to describe how the principles have been translated, which were the challenges and best way forward. We have tackled the following principles: the ecosystem-based approach, the development of benthic indicators, the definition of 'pristine' or sustainable conditions, the detection of pressures and the development of monitoring programs. We concluded that testing and integrating the different approaches was facilitated during the WFD process, which led to further insights and improvements, which the MSFD can rely upon. Expert involvement in the entire implementation process proved to be of vital importance.

Status of biodiversity in the Baltic Sea.

The brackish Baltic Sea hosts species of various origins and environmental tolerances. These immigrated to the sea 10,000 to 15,000 years ago or have been introduced to the area over the relatively recent history of the system. The Baltic Sea has only one known endemic species. While information on some abiotic parameters extends back as long as five centuries and first quantitative snapshot data on biota (on exploited fish populations) originate generally from the same time, international coordination of research began in the early twentieth century. Continuous, annual Baltic Sea-wide long-term datasets on several organism groups (plankton, benthos, fish) are generally available since the mid-1950s. Based on a variety of available data sources (published papers, reports, grey literature, unpublished data), the Baltic Sea, incl. Kattegat, hosts altogether at least 6,065 species, including at least 1,700 phytoplankton, 442 phytobenthos, at least 1,199 zooplankton, at least 569 meiozoobenthos, 1,476 macrozoobenthos, at least 380 vertebrate parasites, about 200 fish, 3 seal, and 83 bird species. In general, but not in all organism groups, high sub-regional total species richness is associated with elevated salinity. Although in comparison with fully marine areas the Baltic Sea supports fewer species, several facets of the system's diversity remain underexplored to this day, such as micro-organisms, foraminiferans, meiobenthos and parasites. In the future, climate change and its interactions with multiple anthropogenic forcings are likely to have major impacts on the Baltic biodiversity.

An adjustment of benthic ecological quality assessment to effects of salinity.

In the last decade a politically inspired marine protection movement arose in the European Union. This movement leads to an holistic strategy. Merging the Water Framework Directive (WFD) and the Marine Strategy Directive (MSD) along the European coastline demands sophisticated ecological classification procedures. The 'Benthic Quality Index' (BQI) is one of several indices created in view of the WFD. We used the dynamic species reference system ES(50)(0.05) to test the capability of BQI to exclude primary environmental factors including the salinity gradient and depth (a proxy for the oxygen regime) from the ecological quality (EcoQ) assessment. A macrozoobenthos dataset of the southern Baltic Sea spreading over more than 20 years and over 100,000 km2 was used for the EcoQ assessment. Quality assurance rules were applied to the record set and an analytical dataset of 936 sampling events with 20,451 abundance records was used in the analysis. We show that the natural salinity gradient has a severe impact on the BQI based EcoQ. We adapted the calculation procedure to reduce the salinity effects to a minimum. According to the adaptation 503 sensitivity/tolerance values for 87 species were computed. These values were calculated within seven salinity ranges from 0 to >30 PSU and two depth zones. These values can be used as a reference for further investigation in the Baltic and other areas with similar environmental conditions.

Performance comparison of two biotic indices measuring the ecological status of water bodies in the Southern Baltic and Gulf of Lions.

Two biotic indices, ATZI Marine Biotic Index (AMBI) and Benthic Quality Index (BQI) have been recently introduced within the EC Water Framework Directive to assess the quality of marine habitats: both are based on sensitivity/tolerance classification and quantitative information on the composition of soft-bottom macrofauna. Their performance, especially with regard to sampling effort was assessed based on two data sets collected in Southern Baltic and one from the Gulf of Lions Mediterranean. AMBI was not affected by sampling effort but BQI was. Two modifications were proposed for BQI (i.e., BQI) (1) the removal of the scaling term (i.e., BQI(W)), and (2) the replacement of the scaling term by different scaling term (i.e., BQI(ES)). Both modified BQIs were largely independent of sampling effort. Variability was slightly lower for BQI(W) than for BQI(ES). BQI was highly correlated with BQI(W) and with BQI(ES) both in the Southern Baltic and in the Gulf of Lions. However, the proportions of stations, which were not attributed the same ecological quality status (EcoQ) when using BQI and its two modified forms were always high. Differences in ecological classification were mostly due to the scales used to infer EcoQ. Based on this study we recommend to use BQI(ES) in future studies because it apparently constitutes the best compromise in (1) being independent of sampling effort, (2) limiting the variability in computation in relation with sampling effort, (3) being correlated with BQI and corresponding EcoQ.

Benthic biodiversity indices versus salinity gradient in the southern Baltic Sea.

The need to assess the environmental status of marine and coastal waters according to the EU Water Framework Directive (WFD) encouraged the design of specific biotic indices to evaluate the response of benthic communities to human-induced changes in water quality. In the present study three of these indices, the traditional Shannon Wiener Index (H') and the more recently published AMBI (AZTI' Marine Biotic Index) and BQI (Benthic Quality Index), were tested along a salinity gradient in the southern Baltic Sea. The comparison of the three indices demonstrates that in the southern Baltic Sea the ecological quality (EcoQ) classification based on macrozoobenthic communities as indicator greatly depends on the biotic index chosen. We found a significant positive relation between species number, H', BQI and salinity resulting in EcoQ status of "Bad", "Poor" or "Moderate" in areas with a salinity value below 10 psu. The AMBI was less dependent on salinity but appear to partly overestimate the EcoQ status. Presently none of these biotic indices appear to be adjusted for application in a gradient system as given in the southern Baltic Sea. A potential approach describing how to overcome this limitation is discussed.