Ocean acidification impairs seagrass performance under thermal stress in shallow and deep water.

Despite the effects of ocean acidification (OA) on seagrasses have been widely investigated, predictions of seagrass performance under future climates need to consider multiple environmental factors. Here, we performed a mesocosm study to assess the effects of OA on shallow and deep Posidonia oceanica plants. The experiment was run in 2021 and repeated in 2022, a year characterized by a prolonged warm water event, to test how the effects of OA on plants are modulated by thermal stress. The response of P. oceanica to experimental conditions was investigated at different levels of biological organization. Under average seawater temperature, there were no effects of OA in both shallow and deep plants, indicating that P. oceanica is not limited by current inorganic carbon concentration, regardless of light availability. In contrast, under thermal stress, exposure of plants to OA increased lipid peroxidation and decreased photosynthetic performance, with deep plants displaying higher levels of heat stress, as indicated by the over-expression of stress-related genes and the activation of antioxidant systems. In addition, warming reduced plant growth, regardless of seawater CO2 and light levels, suggesting that thermal stress may play a fundamental role in the future development of seagrass meadows. Our results suggest that OA may exacerbate the negative effects of future warming on seagrasses.

Marine heatwaves drive recurrent mass mortalities in the Mediterranean Sea.

Climate change is causing an increase in the frequency and intensity of marine heatwaves (MHWs) and mass mortality events (MMEs) of marine organisms are one of their main ecological impacts. Here, we show that during the 2015-2019 period, the Mediterranean Sea has experienced exceptional thermal conditions resulting in the onset of five consecutive years of widespread MMEs across the basin. These MMEs affected thousands of kilometers of coastline from the surface to 45 m, across a range of marine habitats and taxa (50 taxa across 8 phyla). Significant relationships were found between the incidence of MMEs and the heat exposure associated with MHWs observed both at the surface and across depths. Our findings reveal that the Mediterranean Sea is experiencing an acceleration of the ecological impacts of MHWs which poses an unprecedented threat to its ecosystems' health and functioning. Overall, we show that increasing the resolution of empirical observation is critical to enhancing our ability to more effectively understand and manage the consequences of climate change.

An integrated assessment of the Good Environmental Status of Mediterranean Marine Protected Areas.

Local, regional and global targets have been set to halt marine biodiversity loss. Europe has set its own policy targets to achieve Good Environmental Status (GES) of marine ecosystems by implementing the Marine Strategy Framework Directive (MSFD) across member states. We combined an extensive dataset across five Mediterranean ecoregions including 26 Marine Protected Areas (MPAs), their reference unprotected areas, and a no-trawl case study. Our aim was to assess if MPAs reach GES, if their effects are local or can be detected at ecoregion level or up to a Mediterranean scale, and which are the ecosystem components driving GES achievement. This was undertaken by using the analytical tool NEAT (Nested Environmental status Assessment Tool), which allows an integrated assessment of the status of marine systems. We adopted an ecosystem approach by integrating data from several ecosystem components: the seagrass Posidonia oceanica, macroalgae, sea urchins and fish. Thresholds to define the GES were set by dedicated workshops and literature review. In the Western Mediterranean, most MPAs are in good/high status, with P. oceanica and fish driving this result within MPAs. However, GES is achieved only at a local level, and the Mediterranean Sea, as a whole, results in a moderate environmental status. Macroalgal forests are overall in bad condition, confirming their status at risk. The results are significantly affected by the assumption that discrete observations over small spatial scales are representative of the total extension investigated. This calls for large-scale, dedicated assessments to realistically detect environmental status changes under different conditions. Understanding MPAs effectiveness in reaching GES is crucial to assess their role as sentinel observatories of marine systems. MPAs and trawling bans can locally contribute to the attainment of GES and to the fulfillment of the MSFD objectives. Building confidence in setting thresholds between GES and non-GES, investing in long-term monitoring, increasing the spatial extent of sampling areas, rethinking and broadening the scope of complementary tools of protection (e.g., Natura 2000 Sites), are indicated as solutions to ameliorate the status of the basin.

Native biodiversity collapse in the eastern Mediterranean.

Global warming causes the poleward shift of the trailing edges of marine ectotherm species distributions. In the semi-enclosed Mediterranean Sea, continental masses and oceanographic barriers do not allow natural connectivity with thermophilic species pools: as trailing edges retreat, a net diversity loss occurs. We quantify this loss on the Israeli shelf, among the warmest areas in the Mediterranean, by comparing current native molluscan richness with the historical one obtained from surficial death assemblages. We recorded only 12% and 5% of historically present native species on shallow subtidal soft and hard substrates, respectively. This is the largest climate-driven regional-scale diversity loss in the oceans documented to date. By contrast, assemblages in the intertidal, more tolerant to climatic extremes, and in the cooler mesophotic zone show approximately 50% of the historical native richness. Importantly, approximately 60% of the recorded shallow subtidal native species do not reach reproductive size, making the shallow shelf a demographic sink. We predict that, as climate warms, this native biodiversity collapse will intensify and expand geographically, counteracted only by Indo-Pacific species entering from the Suez Canal. These assemblages, shaped by climate warming and biological invasions, give rise to a 'novel ecosystem' whose restoration to historical baselines is not achievable.

Bright spots as climate-smart marine spatial planning tools for conservation and blue growth.

Marine spatial planning that addresses ocean climate-driven change ('climate-smart MSP') is a global aspiration to support economic growth, food security and ecosystem sustainability. Ocean climate change ('CC') modelling may become a key decision-support tool for MSP, but traditional modelling analysis and communication challenges prevent their broad uptake. We employed MSP-specific ocean climate modelling analyses to inform a real-life MSP process; addressing how nature conservation and fisheries could be adapted to CC. We found that the currently planned distribution of these activities may become unsustainable during the policy's implementation due to CC, leading to a shortfall in its sustainability and blue growth targets. Significant, climate-driven ecosystem-level shifts in ocean components underpinning designated sites and fishing activity were estimated, reflecting different magnitudes of shifts in benthic versus pelagic, and inshore versus offshore habitats. Supporting adaptation, we then identified: CC refugia (areas where the ecosystem remains within the boundaries of its present state); CC hotspots (where climate drives the ecosystem towards a new state, inconsistent with each sectors' present use distribution); and for the first time, identified bright spots (areas where oceanographic processes drive range expansion opportunities that may support sustainable growth in the medium term). We thus create the means to: identify where sector-relevant ecosystem change is attributable to CC; incorporate resilient delivery of conservation and sustainable ecosystem management aims into MSP; and to harness opportunities for blue growth where they exist. Capturing CC bright spots alongside refugia within protected areas may present important opportunities to meet sustainability targets while helping support the fishing sector in a changing climate. By capitalizing on the natural distribution of climate resilience within ocean ecosystems, such climate-adaptive spatial management strategies could be seen as nature-based solutions to limit the impact of CC on ocean ecosystems and dependent blue economy sectors, paving the way for climate-smart MSP.

A fast-moving target: achieving marine conservation goals under shifting climate and policies.

In the Anthropocene, marine ecosystems are rapidly shifting to new ecological states. Achieving effective conservation of marine biodiversity has become a fast-moving target because of both global climate change and continuous shifts in marine policies. How prepared are we to deal with this crisis? We examined EU Member States Programs of Measures designed for the implementation of EU marine environmental policies, as well as recent European Marine Spatial Plans, and discovered that climate change is rarely considered operationally. Further, our analysis revealed that monitoring programs in marine protected areas are often insufficient to clearly distinguish between impacts of local and global stressors. Finally, we suggest that while the novel global Blue Growth approach may jeopardize previous marine conservation efforts, it can also provide new conservation opportunities. Adaptive management is the way forward (e.g., preserving ecosystem functions in climate change hotspots, and identifying and targeting climate refugia areas for protection) using Marine Spatial Planning as a framework for action, especially given the push for Blue Growth.

Diverse effects of invasive ecosystem engineers on marine biodiversity and ecosystem functions: A global review and meta-analysis.

Invasive ecosystem engineers (IEE) are potentially one of the most influential types of biological invaders. They are expected to have extensive ecological impacts by altering the physical-chemical structure of ecosystems, thereby changing the rules of existence for a broad range of resident biota. To test the generality of this expectation, we used a global systematic review and meta-analysis to examine IEE effects on the abundance of individual species and communities, biodiversity (using several indices) and ecosystem functions, focusing on marine and estuarine environments. We found that IEE had a significant effect (positive and negative) in most studies testing impacts on individual species, but the overall (cumulative) effect size was small and negative. Many individual studies showed strong IEE effects on community abundance and diversity, but the direction of effects was variable, leading to statistically non-significant overall effects in most categories. In contrast, there was a strong overall effect on most ecosystem functions we examined. IEE negatively affected metabolic functions and primary production, but positively affected nutrient flux, sedimentation and decomposition. We use the results to develop a conceptual model by highlighting pathways whereby IEE impact communities and ecosystem functions, and identify several sources of research bias in the IEE-related invasion literature. Only a few of the studies simultaneously quantified IEE effects on community/diversity and ecosystem functions. Therefore, understanding how IEE may alter biodiversity-ecosystem function relationships should be a primary focus of future studies of invasion biology. Moreover, the clear effects of IEE on ecosystem functions detected in our study suggest that scientists and environmental managers ought to examine how the effects of IEE might be manifested in the services that marine ecosystems provide to humans.

Future warming and acidification effects on anti-fouling and anti-herbivory traits of the brown alga Fucus vesiculosus (Phaeophyceae).

Human-induced ocean warming and acidification have received increasing attention over the past decade and are considered to have substantial consequences for a broad range of marine species and their interactions. Understanding how these interactions shift in response to climate change is particularly important with regard to foundation species, such as the brown alga Fucus vesiculosus. This macroalga represents the dominant habitat former on coastal rocky substrata of the Baltic Sea, fulfilling functions essential for the entire benthic community. Its ability to withstand extensive fouling and herbivory regulates the associated community and ecosystem dynamics. This study tested the interactive effects of future warming, acidification, and seasonality on the interactions of a marine macroalga with potential foulers and consumers. F. vesiculosus rockweeds were exposed to different combinations of conditions predicted regionally for the year 2100 (+∆5°C, +∆700 µatm CO2 ) using multifactorial long-term experiments in novel outdoor benthic mesocosms ("Benthocosms") over 9-12-week periods in four seasons. Possible shifts in the macroalgal susceptibility to fouling and consumption were tested using consecutive bioassays. Algal susceptibility to fouling and grazing varied substantially among seasons and between treatments. In all seasons, warming predominantly affected anti-fouling and anti-herbivory interactions while acidification had a subtle nonsignificant influence. Interestingly, anti-microfouling activity was highest during winter under warming, while anti-macrofouling and anti-herbivory activities were highest in the summer under warming. These contrasting findings indicate that seasonal changes in anti-fouling and anti-herbivory traits may interact with ocean warming in altering F. vesiculosus community composition in the future.

Macroalgal blooms alter community structure and primary productivity in marine ecosystems.

Eutrophication, coupled with loss of herbivory due to habitat degradation and overharvesting, has increased the frequency and severity of macroalgal blooms worldwide. Macroalgal blooms interfere with human activities in coastal areas, and sometimes necessitate costly algal removal programmes. They also have many detrimental effects on marine and estuarine ecosystems, including induction of hypoxia, release of toxic hydrogen sulphide into the sediments and atmosphere, and the loss of ecologically and economically important species. However, macroalgal blooms can also increase habitat complexity, provide organisms with food and shelter, and reduce other problems associated with eutrophication. These contrasting effects make their overall ecological impacts unclear. We conducted a systematic review and meta-analysis to estimate the overall effects of macroalgal blooms on several key measures of ecosystem structure and functioning in marine ecosystems. We also evaluated some of the ecological and methodological factors that might explain the highly variable effects observed in different studies. Averaged across all studies, macroalgal blooms had negative effects on the abundance and species richness of marine organisms, but blooms by different algal taxa had different consequences, ranging from strong negative to strong positive effects. Blooms' effects on species richness also depended on the habitat where they occurred, with the strongest negative effects seen in sandy or muddy subtidal habitats and in the rocky intertidal. Invertebrate communities also appeared to be particularly sensitive to blooms, suffering reductions in their abundance, species richness, and diversity. The total net primary productivity, gross primary productivity, and respiration of benthic ecosystems were higher during macroalgal blooms, but blooms had negative effects on the productivity and respiration of other organisms. These results suggest that, in addition to their direct social and economic costs, macroalgal blooms have ecological effects that may alter their capacity to deliver important ecosystem services.

A dynamic subtropical coastal hotspot of benthic foraminifera in the Southeastern Mediterranean indicates early-stage tropicalization.

Due to ongoing ocean warming, subtropical environments are becoming accessible to tropical species. Among these environments are the vermetid reefs of the Southeastern Mediterranean (SEM). In the last decades, these valuable coastal habitats witnessed the proliferation of numerous alien species of tropical origin. Among the meiofauna thriving on these reefs are benthic foraminifera, single cell marine organisms that make a significant contribution to global carbonate production. It has been widely recognized that benthic foraminifera, among other invasive species, thrive in the macroalgal cover, and it has been suggested that their populations are becoming a significant new source of sediment substrate. Here, we report on the first systematic assessment of the population size of the benthic foraminifera, allowing a comparison with data from the native tropical habitat of these species. Our study is based on a seasonal sampling of benthic foraminifera from confined sampling areas at four sites along the vermetid reef platforms of the Israeli SEM coast. Our survey reveals a patchy distribution of each species with peak population densities exceeding 100,000 specimens per m2, making the SEM a hotspot of benthic foraminifera, with population densities comparable to tropical coral reef environments. The assemblages of the SEM hotspot are dominated by cosmopolitan foraminiferal taxa and tropical invaders from the Indo-Pacific (e.g., Amphistegina lobifera, Pararotalia calcariformata, soritids, and Hauerina diversa). In contrast to foraminiferal hotspots in the tropics, which are completely dominated by larger symbiont-bearing taxa, the SEM hotspot stands out due to high abundances of non-symbiont-bearing species Textularia agglutinans and small miliolids. An intriguing observation is the significant heterogeneity in composition and density of foraminiferal assemblages between the vermetid reefs' southern and northern areas (Israel), indicating that the productivity of the dominant species are also modulated by local yet unknown environmental factors.

Cross-basin and cross-taxa patterns of marine community tropicalization and deborealization in warming European seas.

Ocean warming and acidification, decreases in dissolved oxygen concentrations, and changes in primary production are causing an unprecedented global redistribution of marine life. The identification of underlying ecological processes underpinning marine species turnover, particularly the prevalence of increases of warm-water species or declines of cold-water species, has been recently debated in the context of ocean warming. Here, we track changes in the mean thermal affinity of marine communities across European seas by calculating the Community Temperature Index for 65 biodiversity time series collected over four decades and containing 1,817 species from different communities (zooplankton, coastal benthos, pelagic and demersal invertebrates and fish). We show that most communities and sites have clearly responded to ongoing ocean warming via abundance increases of warm-water species (tropicalization, 54%) and decreases of cold-water species (deborealization, 18%). Tropicalization dominated Atlantic sites compared to semi-enclosed basins such as the Mediterranean and Baltic Seas, probably due to physical barrier constraints to connectivity and species colonization. Semi-enclosed basins appeared to be particularly vulnerable to ocean warming, experiencing the fastest rates of warming and biodiversity loss through deborealization.

Invasive Fish and Sea Urchins Drive the Status of Canopy Forming Macroalgae in the Eastern Mediterranean.

Canopy-forming macroalgae, such as Cystoseira sensu lato, increase the three-dimensional complexity and spatial heterogeneity of rocky reefs, enhancing biodiversity and productivity in coastal areas. Extensive loss of canopy algae has been recorded in recent decades throughout the Mediterranean Sea due to various anthropogenic pressures. In this study, we assessed the biomass of fish assemblages, sea urchin density, and the vertical distribution of macroalgal communities in the Aegean and Levantine Seas. The herbivore fish biomass was significantly higher in the South Aegean and Levantine compared to the North Aegean. Very low sea urchin densities suggest local collapses in the South Aegean and the Levantine. In most sites in the South Aegean and the Levantine, the ecological status of macroalgal communities was low or very low at depths deeper than 2 m, with limited or no canopy algae. In many sites, canopy algae were restricted to a very narrow, shallow zone, where grazing pressure may be limited due to harsh hydrodynamic conditions. Using Generalized Linear Mixed Models, we demonstrated that the presence of canopy algae is negatively correlated with the biomass of the invasive Siganus spp. and sea urchins. The loss of Cystoseira s.l. forests is alarming, and urgent conservation actions are needed.

Parasitism enhances gastropod feeding on invasive and native algae while altering essential energy reserves for organismal homeostasis upon warming.

Marine bioinvasions are of increasing attention due to their potential of causing ecological and economic loss. The seaweed Gracilaria vermiculophylla has recently invaded the Baltic Sea, where, under certain conditions, it was found to outcompete the native alga Fucus vesiculosus. Parasites of grazers and temperature are among the potential factors which might indirectly modulate the interactions between these co-occurring algae through their single and combined effects on grazing rates. We tested the temperature and parasitism effects on the feeding of the gastropod Littorina littorea on F. vesiculosus vs. G. vermiculophylla. Uninfected and trematode-infected gastropods were exposed to 10, 16, 22, and 28 °C for 4 days while fed with either algae. Faeces production was determined as a proxy for grazing rate, and HSP70 expression, glycogen and lipid concentrations were used to assess the gastropod's biochemical condition. Gracilaria vermiculophylla was grazed more than F. vesiculosus. Trematode infection significantly enhanced faeces production, decreased glycogen concentrations, and increased lipid concentrations in the gastropod. Warming significantly affected glycogen and lipid concentrations, with glycogen peaking at 16 °C and lipids at 22 °C. Although not significant, warming and trematode infection increased HSP70 levels. Increased faeces production in infected snails and higher faeces production by L. littorea fed with G. vermiculophylla compared to those which fed on F. vesiculosus, suggest parasitism as an important indirect modulator of the interaction between these algae. The changes in the gastropod's biochemical condition indicate that thermal stress induced the mobilization of energy reserves, suggesting a possible onset of compensatory metabolism. Finally, glycogen decrease in infected snails compared to uninfected ones might make them more susceptible to thermal stress.

Superior growth traits of invaded (Caribbean) versus native (Red sea) populations of the seagrass Halophila stipulacea.

The seagrass Halophila stipulacea is native to the Red Sea. It invaded the Mediterranean over the past century and most of the Caribbean over the last two decades. Understanding the main drivers behind the successful invasiveness of H. stipulacea has become crucial. We performed a comprehensive study including field measurements, a mesocosm experiment, and a literature review to identify 'superior growth traits' that can potentially explain the success story of H. stipulacea. We assessed meadow characteristics and plant traits of three invasive H. stipulacea populations growing off the Island of Sint Eustatius (eastern Caribbean). We compared similar parameters between native (Eilat, northern Red Sea) and invasive (Caribbean) H. stipulacea plants in a common-garden mesocosm. Lastly, we compared our field measurements with published data. The newly arrived H. stipulacea plants from St. Eustatius were characterized by higher percent cover, higher below- and above-ground biomasses, more apical shoots, and faster leaf turnover rates than those measured in both native and older invaded habitats. These results were further confirmed by the mesocosm experiment where the invasive H. stipulacea plants grew faster and developed more apical shoots than the native plants. Results suggest that increased growth vigour is one of the main invasive traits that characterize successful invasive H. stipulacea populations in the Caribbean and potentially in other invaded areas. We encourage long-term monitoring of H. stipulacea in both native and invaded habitats to better understand the future spread of this species and its impacts on communities and their ecosystem functions and services. Supplementary Information: The online version contains supplementary material available at 10.1007/s10530-023-03045-z.

Heat sensitivity of first host and cercariae may restrict parasite transmission in a warming sea.

To predict global warming impacts on parasitism, we should describe the thermal tolerance of all players in host-parasite systems. Complex life-cycle parasites such as trematodes are of particular interest since they can drive complex ecological changes. This study evaluates the net response to temperature of the infective larval stage of Himasthla elongata, a parasite inhabiting the southwestern Baltic Sea. The thermal sensitivity of (i) the infected and uninfected first intermediate host (Littorina littorea) and (ii) the cercarial emergence, survival, self-propelling, encystment, and infection capacity to the second intermediate host (Mytilus edulis sensu lato) were examined. We found that infection by the trematode rendered the gastropod more susceptible to elevated temperatures representing warm summer events in the region. At 22 °C, cercarial emergence and infectivity were at their optimum while cercarial survival was shortened, narrowing the time window for successful mussel infection. Faster out-of-host encystment occurred at increasing temperatures. After correcting the cercarial emergence and infectivity for the temperature-specific gastropod survival, we found that warming induces net adverse effects on the trematode transmission to the bivalve host. The findings suggest that gastropod and cercariae mortality, as a tradeoff for the emergence and infectivity, will hamper the possibility for trematodes to flourish in a warming ocean.

An invasive herbivorous fish (Siganus rivulatus) influences both benthic and planktonic microbes through defecation and nutrient excretion.

Direct and indirect impacts by invasive animals on plants and other animals through predation and competition have been evidenced in many ecosystems. For instance, the rabbitfish Siganus rivulatus, originating from the Red Sea, is now the most abundant species in costal habitats of South-Eastern Mediterranean Sea where it overgrazes algae. However, little is known about its impacts on microbes through release of metabolic wastes and feces. We used a mesocosm experiment to test the effect of S. rivulatus on planktonic and benthic microbial communities. Excretion of dissolved nutrients by fish resulted in higher concentrations of dissolved inorganic nitrogen (NH4, NO2/NO3). This increase in availability of N was associated with higher N content in macroalgae, higher biomass of phytoplankton, higher abundance of bacterioplankton and shift in the structure of planktonic bacterial communities. The feces released mostly under the shelters where the fish rest at night, led to significant increases in diversity of sediment bacterial communities and shifts in their structure. The impact of S. rivulatus on planktonic microbes was related to the indirect bottom-up effect induced by excreted dissolved nutrients while its effect on benthic microbes was due to the direct release of both organic matter and microbes present in feces. Overall, this first evidence of the impacts of invasive species on planktonic and benthic microbes highlights that ongoing changes in fish biodiversity could have ecosystem-wide consequences.

Anthropogenic disruptions to longstanding patterns of trophic-size structure in vertebrates.

Diet and body mass are inextricably linked in vertebrates: while herbivores and carnivores have converged on much larger sizes, invertivores and omnivores are, on average, much smaller, leading to a roughly U-shaped relationship between body size and trophic guild. Although this U-shaped trophic-size structure is well documented in extant terrestrial mammals, whether this pattern manifests across diverse vertebrate clades and biomes is unknown. Moreover, emergence of the U-shape over geological time and future persistence are unknown. Here we compiled a comprehensive dataset of diet and body size spanning several vertebrate classes and show that the U-shaped pattern is taxonomically and biogeographically universal in modern vertebrate groups, except for marine mammals and seabirds. We further found that, for terrestrial mammals, this U-shape emerged by the Palaeocene and has thus persisted for at least 66 million years. Yet disruption of this fundamental trophic-size structure in mammals appears likely in the next century, based on projected extinctions. Actions to prevent declines in the largest animals will sustain the functioning of Earth's wild ecosystems and biomass energy distributions that have persisted through deep time.

Plastic and natural inorganic microparticles do not differ in their effects on adult mussels (Mytilidae) from different geographic regions.

Microplastics are ubiquitous in the marine environment and studies on their effects on benthic filter feeders at least partly revealed a negative influence. However, it is still unclear whether the effects of microplastics differ from those of natural suspended microparticles, which constitute a common stressor in many coastal environments. We present a series of experiments that compared the effects of six-week exposures of marine mussels to two types of natural particles (red clay and diatom shells) to two types of plastic particles (Polymethyl Methacrylate and Polyvinyl Chloride). Mussels of the family Mytilidae from temperate regions (Japan, Chile, Tasmania) through subtropical (Israel) to tropical environments (Cabo Verde) were exposed to concentrations of 1.5 mg/L, 15 mg/L and 150 mg/L of the respective microparticles. At the end of this period, we found significant effects of suspended particles on respiration rate, byssus production and condition index of the animals. There was no significant effect on clearance rate and survival. Surprisingly, we observed only small differences between the effects of the different types of particles, which suggests that the mussels were generally equally robust towards exposure to variable concentrations of suspended solids regardless of whether they were natural or plastic. We conclude, that microplastics and suspended solids elicit similar effects on the tested response variables, and that both types of microparticles mainly cause acute responses rather than more persistent carry-over effects.