Luigi Piazzi

Development of a new biotic index for ecological status assessment of Italian coastal waters based on coralligenous macroalgal assemblages

This paper presents a new biotic index (ESCA, Ecological Status of Coralligenous Assemblages), based on analyses of in situ records of coralligenous macroalgal assemblages in the Mediterranean Sea. The ESCA index was developed on the basis of previous impact evaluation studies carried out by traditional destructive methods. It was validated on an independent dataset collected during a 3-year study carried out at five localities in the north-western Mediterranean, and tested on a gradient of anthropogenic stressors. Assemblage descriptors selected as metrics of the ESCA index were: (a) presence/absence and abundance of sensitive taxa/groups (expressed as sensitivity level of assemblages, SL), (b) diversity of assemblages (expressed as α-diversity) and (c) heterogeneity of assemblages (expressed as β-diversity). The three metrics were combined to give a final value for the multimetric ecological index, Ecological Quality Ratio, calculated as the ratio between the measured values and the value obtained in the reference condition. The Ecological Quality Ratio values ranged from 0 to 1 and five ecological status classes were defined in accordance with the Water Framework Directive. The ESCA index could be used to define the ecological status of the studied sites, providing differences between assemblages similar to those shown by multivariate analyses. Moreover, ecological quality values were quite steady throughout the study period. The ESCA index may represent a useful tool for monitoring programmes in coastal waters, since it has been developed in compliance with the Water Framework Directive; it synthesizes complex information in a simple and reliable way; and its application is simple and cost-effective. However, further studies are necessary to complete index development and to properly evaluate its strengths and weaknesses on a larger scale.

The indirect role of nutrients in enhancing the invasion of Caulerpa racemosa var cylindracea

The effects of nutrients dynamics on biological invasions in marine habitats have not been fully investigated. The present study aimed to evaluate the role of nutrient pollution in determining the successful invasion of the introduced seaweed Caulerpa racemosa var. cylindracea in a Mediterranean subtidal rocky habitat. To this end, a manipulative field experiment was carried out by supplying the water column with nutrients for a one-year period. Afterwards C. racemosa was transplanted in both nutrient-enriched and control macroalgal assemblages. Results showed that the penetration and biomass of C. racemosa in the assemblages previously treated with nutrients were higher than in control ones, indicating that communities stressed by nutrient pollution are more vulnerable to invasion. The nutrient enrichment changed the structure of natural macroalgal assemblages, mainly by encouraging the growth of turf species. No significant effects were detected for the erect and prostrate layers and for the number of species, suggesting that the susceptibility of the community to invasion may depend more on the morpho-functional identity of macroalgae rather than on the diversity of assemblages. Changes in the availability of seawater nutrients may foster the spread of C. racemosa, both by enhancing its growth and eroding the natural resistance of macroalgal assemblages. Thus, the maintenance of good water quality may play an important role in containing both C. racemosa and other introduced seaweeds.

The two facets of species sensitivity: Stress and disturbance on coralligenous assemblages in space and time

Marine coastal ecosystems are affected by a vast array of human-induced disturbances and stresses, which are often capable of overwhelming the effects of natural changes. Despite the conceptual and practical difficulty in differentiating between disturbance and stress, which are often used interchangeably, the two terms bear different ecological meanings. Both are external agents, but the former causes mortality or physical damage (subtraction of biomass), whereas the latter causes physiological alteration (reduction in productivity). Sensitivity of marine organisms may thus have a dual connotation, being influenced in different ways by disturbance and by stress following major environmental change. Coralligenous assemblages, which shape unique biogenic formations in the Mediterranean Sea, are considered highly sensitive to change. In this paper, we propose a method to differentiate between disturbance and stress to assess the ecological status of the coralligenous assemblages. Disturbance sensitivity level (DSL) and stress sensitivity level (SSL) of the sessile organisms thriving in the coralligenous assemblages were combined into the integrated sensitivity level of coralligenous assemblages (ISLA) index. Changes in the coralligenous status were assessed in space, along a gradient of stress (human-induced pressures) at several sites of the western Mediterranean, and in time, from a long-term series (1961-2008) at Mesco Reef (Ligurian Sea) that encompasses a mass mortality event in the 1990s. The quality of the coralligenous assemblages was lower in highly urbanised sites than that in sites in both marine protected areas and areas with low levels of urbanisation; moreover, the quality of the assemblages at Mesco Reef decreased during the last 50years. Reduction in quality was mainly due to the increase in stress-tolerant and/or opportunist species (e.g. algal turfs, hydroids and encrusting sponges), the disappearance of the most sensitive macroalgae (e.g. Udoteaceae and erect Rhodophyta) and macro-invertebrates (e.g. Savalia savaglia, Alcyonium coralloides and Smittina cervicornis), and the appearance of invasive alien algal species. Although the specific indices of SSL or DSL well illustrated the changes in the spatial or temporal datasets, respectively, their integration in the ISLA index was more effective in measuring the change experienced by the coralligenous assemblages in both space and time.

Limpets compensate sea urchin decline and enhance the stability of rocky subtidal barrens

Understanding the mechanisms that regulate shifts among alternative ecosystems has become a priority for ecologists and environmental scientists. This study assessed the relative importance of different herbivorous invertebrates (urchins and limpets) in regulating transitions from barren to vegetated states on Mediterranean rocky reefs, under different levels of nutrient availability. Nutrient concentration and the herbivore assemblage were manipulated to test i) whether limpets can compensate for the decline or loss of sea urchin populations, thereby contributing to the persistence of barrens, ii) whether limpet effects vary according to nutrient availability and iii) whether limpets affect the structure of the algal assemblage. The complete removal of sea urchins was not sufficient to trigger the recovery of erect and turf-forming macroalgae if limpets were left at natural density, suggesting that these herbivores play an important role in the stability of the barren state. The effect of these mesograzers was particularly important under oligotrophic conditions. This suggests that limpets play an important role in sustaining the stability of the barren state. A more comprehensive assessment of top-down forces, implying the quantification of the relative effect of different herbivore guilds, is therefore necessary to estimate the strength of hysteresis and to identify critical thresholds at which shifts back to the vegetated state are initiated.

Nutrient exploitation and competition strategies of the invasive seaweed Caulerpa cylindracea

The aim of this study was to evaluate whether the success of invasive Caulerpa cylindracea (Caulerpa racemosa var. cylindracea) in Mediterranean habitats may be linked to particular nutritional requirements and/or nutrient accumulation/reallocation dynamics within the algal thallus. To this end, a manipulative field experiment was carried out transplanting C. cylindracea and supplying nutrients to subtidal rocky macroalgal assemblages. Morphological features of C. cylindracea were measured, while percentage cover and tissue nitrogen, carbon and phosphorus were determined for C. cylindracea and two co-occurring species (the introduced Laurencia chondrioides and native Flabellia petiolata) in nutrient-enriched and unenriched conditions. Growth of C. cylindracea was greater in the nutrient-enriched plots while no effect of nutrient enrichment was detected in co-occurring macroalgae. A particularly high requirement for nitrogen has been observed in C. cylindracea, but without severe N-limitation, while a general nutritional state of P-limitation was detected in both invasive and co-occurring macroalgae. The absence of inhibition in hypertrophic conditions and under high levels of ammonia together with a strong uptake and quick reallocation of nutrients within the coenocytic thallus probably represent the main advantages over the other co-occurring species which could explain part of the success of C. cylindracea in the Mediterranean Sea.

Immanent conditions determine imminent collapses: nutrient regimes define the resilience of macroalgal communities

Predicting where state-changing thresholds lie can be inherently complex in ecosystems characterized by nonlinear dynamics. Unpacking the mechanisms underlying these transitions can help considerably reduce this unpredictability. We used empirical observations, field and laboratory experiments, and mathematical models to examine how differences in nutrient regimes mediate the capacity of macrophyte communities to sustain sea urchin grazing. In relatively nutrient-rich conditions, macrophyte systems were more resilient to grazing, shifting to barrens beyond 1 800 g m−2 (urchin biomass), more than twice the threshold of nutrient-poor conditions. The mechanisms driving these differences are linked to how nutrients mediate urchin foraging and algal growth: controlled experiments showed that low-nutrient regimes trigger compensatory feeding and reduce plant growth, mechanisms supported by our consumer–resource model. These mechanisms act together to halve macrophyte community resilience. Our study demonstrates that by mediating the underlying drivers, inherent conditions can strongly influence the buffer capacity of nonlinear systems.

The Seagrass effect turned upside down changes the prospective of sea urchin survival and landscape implications

Habitat structure plays an important mediating role in predator-prey interactions. However the effects are strongly dependent on regional predator pools, which can drive predation risk in habitats with very similar structure in opposite directions. In the Mediterranean Sea predation on juvenile sea urchins is commonly known to be regulated by seagrass structure. In this study we test whether the possibility for juvenile Paracentrotus lividus to be predated changes in relation to the fragmentation of the seagrass Posidonia oceanica (four habitat classes: continuous, low-fragmentation, high-fragmentation and rocks), and to the spatial arrangement of such habitat classes at a landscape scale. Sea urchin predation risk was measured in a 20-day field experiment on tethered individuals placed in three square areas 35×35 m2 in size. Variability of both landscape and habitat structural attributes was assessed at the sampling grain 5×5 m2. Predation risk changed among landscapes, as it was lower where more ‘rocks’, and thus less seagrass, were present. The higher risk was found in the ‘continuous’ P. oceanica rather than in the low-fragmentation, high-fragmentation and rock habitats (p-values = 0.0149, 0.00008, and 0.0001, respectively). Therefore, the expectation that juvenile P. lividus survival would have been higher in the ‘continuous’ seagrass habitat, which would have served as shelter from high fish predation pressure, was not met. Predation risk changed across habitats due to different success between attack types: benthic attacks (mostly from whelks) were overall much more effective than those due to fish activity, the former type being associated with the ‘continuous’ seagrass habitat. Fish predation on juvenile sea urchins on rocks and ‘high-fragmentation’ habitat was less likely than benthic predation in the ‘continuous’ seagrass, with the low seagrass patch complexity increasing benthic activity. Future research should be aimed at investigating, derived from the complex indirect interactions among species, how top-down control in marine reserves can modify seagrass habitat effects.

Suitability of the ALien Biotic IndEX (ALEX) for assessing invasion of macroalgae across different Mediterranean habitats

The ALien Biotic IndEX (ALEX) has been recently proposed to evaluate biological invasions in soft-bottom macro-invertebrate assemblages. The present paper proposes the use of ALEX in sessile assemblages of Mediterranean hard bottom habitats and tests it along gradients of invasion. For five invasive macroalgae a variable number of case studies per each of four habitats were examined from the available data sets. For each case study samples were attributed to four levels of invasion depending on the abundance of the invading macroalgae. Results showed that the application of ALEX to sessile assemblages of hard bottoms allows to qualify the level of invasion along the considered gradients. Moreover, the decline of index values matched the impact of invasion on species number of the assemblages. Results also suggest that the concurrent use of ALEX and indices of benthic quality status can be a valuable tool to assess biopollution in hard bottom habitats.

Effects of non-native turf-forming Rhodophyta on mobile macro-invertebrate assemblages in the north-western Mediterranean Sea

Abstract The study compared mobile macro-invertebrate assemblages invaded by the two turf-forming invasive macroalgae Womersleyella setacea and Lophocladia lallemandii with non-invaded assemblages. The study was carried out at Pianosa Island, in the Tuscan Archipelago National Park, within the depth ranges where the two invasive species showed high abundance: 35 m depth for Womersleyella setacea and 10 m depth for Lophocladia lallemandii. Results showed significant differences between invaded sites and non-invaded ones for the two turf-forming Rhodophyta. Invaded assemblages showed a lower species richness and a reduction of decapods and molluscs and an increase of polychaetes compared with non-invaded ones. Amphipods showed a drastic reduction in abundance in sites invaded by W. setacea, while they appeared less influenced by the presence of L. lallemandii. Womersleyella setacea showed more severe effects than L. lallemandii, causing deep changes in the structure of assemblages and a reduction of beta diversity of the system.

An asymmetrical sampling design as a tool for sustainability assessment of human activities in coastal systems: a fish farming study case

ABSTRACT The proposed use of an asymmetrical sampling design to evaluate the sustainability of human activities in coastal systems was tested on an aquaculture impact assessment. Two small fish farms located in a protected area were studied, one sited on an unvegetated soft bottom and the other on a seagrass meadow. Biotic and abiotic variables at sites of fish farms were compared with appropriate reference sites located at two different distances from the cages (300 m and 1000 m) through an asymmetrical sampling design. All the considered descriptors significantly differed between the sites under the cages and the reference sites in both seagrass and unvegetated habitats; by contrast, no significant differences were detected between the reference sites located at the two different distances from the cages, suggesting a spatially limited impact of the farms. The asymmetrical sampling design was able not only to detect an impact on benthic assemblages, but also to evaluate the spatial extent of this impact. The approach proposed in this study can be considered suitable to evaluate the sustainability of aquaculture farms and other human activities in marine coastal areas.