Effects of extreme temperatures and recovery potential of Gongolaria barbata from a coastal lagoon in the northern Adriatic Sea: An ex situ approach.

BACKGROUND AND AIMS: Globally, rising seawater temperatures contribute to the regression of marine macroalgal forests. Along the Istrian coastline (northern Adriatic), an isolated population of Gongolaria barbata persists in a coastal lagoon, representing one of the last marine macroalgal forests in the region. Our objective was to examine the impact of extreme temperatures on morphology and physiology of G. barbata, and test its potential for recovery after simulating marine heatwave (MHW) conditions. METHODS: We explored the occurrence of marine heatwaves in southern Istria, adjacent to the study area, as well as extreme temperatures inside the area itself. Subsequently, we performed a thermotolerance experiment, consisting of a stress and recovery phase where we exposed G. barbata thalli to four extreme (28 °C, 30 °C, 32 °C, 34 °C) and one favourable (18 °C) temperature. We then monitored morphological and physiological responses. KEY RESULTS: Our findings indicate a significant rise in frequency, duration, and intensity of MHWs over decades on the southern Istrian coast. Experimental results show that G. barbata demonstrates both morphological and physiological recovery potential after exposure to temperatures as high as 32 °C. However, exposure to 34 °C led to thallus decay, with limited regeneration ability. CONCLUSIONS: Our results show that G. barbata has a remarkable resilience to long term exposure to extreme temperatures up to 32 °C and suggests that short term exposure to temperatures beyond this, as currently recorded inside the lagoon, do not notably affect the physiology or morphology of local G. barbata. With more MHWs expected in the future, such an adapted population may represent an important donor suitable for future restoration activities along the Istrian coast. These results emphasize the resilience of this unique population, but also warns of the vulnerability of marine macroalgal forests to rising seawater temperatures under rapidly changing climate conditions.

First Restoration Experiment for Endemic Fucus virsoides on the Western Istrian Coast-Is It Feasible?

Fucus virsoides is an endemic species of the Mediterranean limited to the Adriatic Sea. In recent decades, it has undergone a severe regression, which is well documented in the northern Adriatic. To develop a tool for mitigating this problem, we tested the feasibility of F. virsoides restoration and designed a very simple yet effective method for ex situ cultivation and planting. We also tested the effect of positioning in the upper vs. lower intertidal on the growth of F. virsoides. After planting, the algae reached fertility in nine months, which was followed by a period of stagnation and reduction in size due to grazing and fouling. There were some differences in growth of the algae according to positioning in the intertidal at different measurement times, but that had little impact on the overall success of the restoration experiment. This represents, to our knowledge, the first successful F. virsoides ex situ cultivation and restoration attempt.

Impacts of environmental stress on resistance and resilience of algal-associated bacterial communities.

Algal-associated bacteria are fundamental to the ecological success of marine green macroalgae such as Caulerpa. The resistance and resilience of algal-associated microbiota to environmental stress can promote algal health and genetic adaptation to changing environments. The composition of bacterial communities has been shown to be unique to algal morphological niches. Therefore, the level of response to various environmental perturbations may in fact be different for each niche-specific community. Factorial in situ experiments were set up to investigate the effect of nutrient enrichment and temperature stress on the bacterial communities associated with Caulerpa cylindracea. Bacteria were characterized using the 16S rRNA gene, and the community compositions were compared between different parts of the algal thallus (endo-, epi-, and rhizomicrobiome). Resistance and resilience were calculated to further understand the changes of microbial composition in response to perturbations. The results of this study provide evidence that nutrient enrichment has a significant influence on the taxonomic and functional structure of the epimicrobiota, with a low community resistance index observed for both. Temperature and nutrient stress had a significant effect on the rhizomicrobiota taxonomic composition, exhibiting the lowest overall resistance to change. The functional performance of the rhizomicrobiota had low resilience to the combination of stressors, indicating potential additive effects. Interestingly, the endomicrobiota had the highest overall resistance, yet the lowest overall resilience to environmental stress. This further contributes to our understanding of algal microbiome dynamics in response to environmental changes.

Port Baseline Biological Surveys and seaweed bioinvasions in port areas: What's the matter in the Adriatic Sea?

One of the objectives of the BALMAS project was to conduct Port Baseline Biological Surveys of native and non-indigenous benthic flora in 12 Adriatic ports. Samples of macroalgae growing on vertical artificial substrates were collected in spring and autumn 2014 and/or 2015. A total number of 248 taxa, 152 Rhodophyta, 62 Chlorophyta, and 34 Ochrophyta, were identified. Of these, 13 were non-indigenous seaweeds, mainly filamentous macroalgae, that were probably introduced through hull fouling. Some of these taxa had already been described in the study areas, others were recorded for the first time, a few were no longer detected at sites where they had previously been recorded (e.g. Sargassum muticum). Some other NISS reported for the Adriatic Sea, were not collected at any sampling site (i.e. Caulerpa cylindracea, Codium fragile). Possible reasons for the absence of these species are discussed.

Harnessing positive species interactions as a tool against climate-driven loss of coastal biodiversity.

Habitat-forming species sustain biodiversity and ecosystem functioning in harsh environments through the amelioration of physical stress. Nonetheless, their role in shaping patterns of species distribution under future climate scenarios is generally overlooked. Focusing on coastal systems, we assess how habitat-forming species can influence the ability of stress-sensitive species to exhibit plastic responses, adapt to novel environmental conditions, or track suitable climates. Here, we argue that habitat-former populations could be managed as a nature-based solution against climate-driven loss of biodiversity. Drawing from different ecological and biological disciplines, we identify a series of actions to sustain the resilience of marine habitat-forming species to climate change, as well as their effectiveness and reliability in rescuing stress-sensitive species from increasingly adverse environmental conditions.

Linking disturbance and resistance to invasion via changes in biodiversity: a conceptual model and an experimental test on rocky reefs.

Biological invasions threaten biodiversity worldwide. Nonetheless, a unified theory linking disturbance and resistance to invasion through a mechanistic understanding of the changes caused to biodiversity is elusive. Building on different forms of the disturbance-biodiversity relationship and on the Biotic Resistance Hypothesis (BRH), we constructed conceptual models showing that, according to the main biodiversity mechanism generating invasion resistance (complementary vs. identity effects), disturbance can either promote or hinder invasion. Following the Intermediate Disturbance Hypothesis (IDH), moderate levels of disturbance (either frequency or intensity) are expected to enhance species richness. This will promote invasion resistance when complementarity is more important than species identity. Negative effects of severe disturbance on invasion resistance, due to reductions in species richness, can be either overcompensated or exacerbated by species identity effects, depending on the life-traits becoming dominant within the native species pool. Different invasion resistance scenarios are generated when the diversity-disturbance relationship is negative or positive monotonic. Predictions from these models were experimentally tested on rocky reefs. Macroalgal canopies differing in species richness (1 vs. 2 vs. 3) and identity, were exposed to either a moderate or a severe pulse disturbance. The effects of different canopy-forming species on the seaweed, Caulerpa cylindracea, varied from positive (Cystoseira crinita) to neutral (Cystoseira barbata) to negative (Cystoseira compressa). After 2 years, severely disturbed plots were monopolized by C. compressa and supported less C. cylindracea. Our study shows that the effects of disturbance on invasion depend upon its intensity, the main mechanism through which biodiversity generates invasion resistance and the life-traits selected within the native species pool. Disturbance can sustain invasion resistance when promoting the dominance of competitively subordinate species possessing traits that allow outperforming invaders.

The effects of an invasive seaweed on native communities vary along a gradient of land-based human impacts.

The difficulty in teasing apart the effects of biological invasions from those of other anthropogenic perturbations has hampered our understanding of the mechanisms underpinning the global biodiversity crisis. The recent elaboration of global-scale maps of cumulative human impacts provides a unique opportunity to assess how the impact of invaders varies among areas exposed to different anthropogenic activities. A recent meta-analysis has shown that the effects of invasive seaweeds on native biota tend to be more negative in relatively pristine than in human-impacted environments. Here, we tested this hypothesis through the experimental removal of the invasive green seaweed, Caulerpa cylindracea, from rocky reefs across the Mediterranean Sea. More specifically, we assessed which out of land-based and sea-based cumulative impact scores was a better predictor of the direction and magnitude of the effects of this seaweed on extant and recovering native assemblages. Approximately 15 months after the start of the experiment, the removal of C. cylindracea from extant assemblages enhanced the cover of canopy-forming macroalgae at relatively pristine sites. This did not, however, result in major changes in total cover or species richness of native assemblages. Preventing C. cylindracea re-invasion of cleared plots at pristine sites promoted the recovery of canopy-forming and encrusting macroalgae and hampered that of algal turfs, ultimately resulting in increased species richness. These effects weakened progressively with increasing levels of land-based human impacts and, indeed, shifted in sign at the upper end of the gradient investigated. Thus, at sites exposed to intense disturbance from land-based human activities, the removal of C. cylindracea fostered the cover of algal turfs and decreased that of encrusting algae, with no net effect on species richness. Our results suggests that competition from C. cylindracea is an important determinant of benthic assemblage diversity in pristine environments, but less so in species-poor assemblages found at sites exposed to intense disturbance from land-based human activities, where either adverse physical factors or lack of propagules may constrain the number of potential native colonizers. Implementing measures to reduce the establishment and spread of C. cylindracea in areas little impacted by land-based human activities should be considered a priority for preserving the biodiversity of Mediterranean shallow rocky reefs.

Long-term fluctuations in Cystoseira populations along the west Istrian Coast (Croatia) related to eutrophication patterns in the northern Adriatic Sea.

An exploration of historical data suggested that eutrophication patterns might drive long-term fluctuations in Cystoseira populations along the west Istrian Coast (northern Adriatic Sea, Croatia). The regimes of northern Italian rivers, which flow approximately 100km west of the study area, mainly modulate the eutrophication levels of the northern Adriatic Sea. A regression of Cystoseira populations from the 1970s through the 1990s corresponded to increased levels of eutrophication in the study area. During the late 1990s, the density of sea urchins, which are efficacious macroalgal predators, decreased, likely due to an intense formation of pelagic mucilage aggregates that resulted in mass mortality episodes of macrozoobenthic species. During the 2000-2013 period, an oligotrophication of the northern Adriatic formed the basis for the recovery of Cystoseira taxa, whose abundances from 2009 to 2013 were similar to those characterising the most flourishing Mediterranean Cystoseira assemblages.

Spreading patterns of the invasive Caulerpa cylindracea Sonder along the west Istrian Coast (northern Adriatic Sea, Croatia).

The northern Adriatic Sea represents the northernmost and thus the coldest biogeographic sector of the Mediterranean Sea. In 2004, the invasive green alga Caulerpa cylindracea was recorded for the first time in the northern Adriatic at a site of the west Istrian Coast. Until 2010, additional C. cylindracea mats have only formed up to 7 km northward from the first colonisation site. Subsequently, the alga was also recorded at sites widespread along the entire coast. Both the first 2004 colonisation event and the 2011-2014 colonisation of distant sites occurred during periods of winter seawater temperatures higher than 9 °C. In general, algal spreading was markedly slow. Approximately 10 years after the first record, C. cylindracea has affected less than 1% of the entire west Istrian coastline. The colonisation predominantly occurred in ports and urbanised bays (seaside resorts) suggesting that anthropogenic activities might enhance algal diffusion.

Toxin-producing Ostreopsis cf. ovata are likely to bloom undetected along coastal areas.

Mass appearances of the toxic dinoflagellate genus Ostreopsis are known to cause dangerous respiratory symptoms in humans exposed to aerosols. The outbreaks can appear in shallow marine waters of temperate regions around the globe. We followed a massive bloom event on a public beach on the northern Adriatic coast near Rovinj, Croatia. We identified the responsible species and the produced toxins as well as the dynamics of the event with respect to environmental conditions. Ostreopsis cf. ovata appeared in masses from September through October 2010 on a public beach near Rovinj, Croatia but stayed undetected by public health organizations. Respiratory symptoms were observed whenever humans were exposed to substrate samples containing large numbers of Ostreopsis cells. During the mass abundance of O. cf. ovata also exposure to the aerosols on the beach evoked respiratory symptoms in humans. Our measurements showed high cell abundances and high toxin contents with a stable relative contribution of putative Palytoxin and Ovatoxins a-e. Artificial beach structures proved to dramatically reduce settling of the observed Ostreopsis biofilm. Blooms like those reported herein have a high potential to happen undetected with a high potential of affecting the health of coastal human populations. Increased monitoring efforts are therefore required to understand the ecology and toxicology of those bloom events and reduce their negative impact on coastal populations.

Short term impact of planktonic mucilage aggregates on macrobenthos along the Istrian rocky coast (Northern Adriatic, Croatia).

During nearly every summer of the last 15 years, massive mucilage aggregations have formed in the water column of the northern Adriatic. The phenomenon also occurred during the summer of 2004, lasting approximately from the middle of June to the end of July. After approximately 20 days of mucilage impact (coverage of the rocky bottom from 40% to 90%), the effects on selected macrobenthic species were assessed at depths of 5-7m. The responses to the mucilage impact were species dependent. Smothering by mucilage caused partial necrosis of the sponge Verongia aerophoba: from 7% to 56% of the colony surface was deteriorated. In contrast, the impact was lethal for the mollusc Arca noae: from 5% to 45% of the molluscs died. Usually, no deleterious effects were ascertained on perennial parts of the thalli (axes) of macroalgae of the genus Cystoseira. However, primary branches showed signs of necrosis, and Cystoseira compressa was more sensitive compared to Cystoseira corniculata and Cystoseira barbata. Apparently, this does not profoundly affect Cystoseira populations, which have been in a phase of expansion along the shallow Istrian rocky coast over the last 15 years.

First record of Ostreopsis cfr. ovata on macroalgae in the Northern Adriatic Sea.

Ostreopsis ovata is an epiphytic potentially toxic dinoflagellate. It has a world-wide distribution, normally associated with other epiphytic or benthic dinoflagellates. In tropical seas O. ovata is often associated with the genera Gambierdiscus, Coolia and Prorocentrum, causing cinguatera fish poisoning. Recently, Ostreopsis spp. blooms in the Tyrrhenian and southern Adriatic Sea have been related to human health problems, such as breathing and skin irritation. Here we report the first record of Ostreopsis cfr. ovata in the Northern Adriatic Sea. O. cfr. ovata was isolated from macroalgae in two areas, the Gulf of Trieste (Italy) and close to Rovinj (Croatia). The microalga was identified by scanning electron microscopy and by fluorescence light microscopy. Size range and thecal pore structure were similar to those described for O. cfr. ovata in previous studies. Ostreopsis cfr. ovata was present on all the macroalgae collected, particularly browns and reds. The microalgal association on macroalgae was mostly composed of Ostreopsis sp., Coolia monotis and Coscinodiscus sp.