Exploring the impact of temporal resolution on detecting shifts in the invasive species niche: Insights from Lessepsian fishes.

In this study, we estimate the niche overlap between native and invaded ranges of 36 Lessepsian fish, focusing on how this estimate might vary in relation to the temporal resolution of sea surface temperature and salinity, which are the main niche axes determining their distribution. Specifically, we wanted to address the following questions: (i) Does the choice of temporal averaging method of variables influence the estimation of niche overlap for individual variables? (ii) Does this temporal resolution effect persist when conducting bivariate niche estimations? Niches overlap was estimated by calculating two indices and these analyses were repeated at two temporal resolutions, matching observations to the classic 'multidecadal' average of environmental conditions and to the corresponding annual average of records. Results are compared with verify whether differences can be detected in the magnitude of niche commonality measured at annual or multidecadal temporal resolution. The findings show that the temporal resolution of the data significantly influences estimates of overlap in the thermal niche. Specifically, our analysis indicates a considerable disparity between native and invasive niche regions for most species, particularly when evaluated over multidecadal periods compared with matching occurrence data to the annual mean values of years the occurrence was observed, that is matching occurrence data to a common average of 'present' conditions or to the annual mean values of years of observation. In particular, the largest overlaps between native and invaded niches occur along the salinity axis, regardless of temporal resolution. When considering both temperature and salinity together, the results remain unaffected by the temporal resolution of the environmental data. Almost 30% of the species show a different niche in their introduced range, and for the other species, the overlap between native and invaded ranges was reduced with respect to the univariate analyses.

Spatio-temporal dynamics of exotic fish species in the Mediterranean Sea: Over a century of invasion reconstructed.

With over a thousand of introduced species, the Mediterranean is the most heavily invaded marine region in the world. Yet, the spatio-temporal dynamics of this bioinvasion has never been analysed. Examination of a comprehensive dataset of 4015 georeferenced observations, extracted from the scientific literature, allowed (i) reconstructing the invasion and the introduction and post-introduction dynamics of exotic fish species, (ii) calculating introduction and spread rates, and (iii) investigating the time correlates since introduction. Our analysis encompasses 188 fish species that entered the Mediterranean from 1896 to 2020, including 25 Atlantic species that naturally expanded their range through the Strait of Gibraltar. Cumulative occurrences, reported in 264 distribution maps, documented the progressive expansion of the most represented species and the spatio-temporal patterns associated with three introduction routes: the Suez Canal (CAN); other human-mediated vectors (HM) and the Strait of Gibraltar (NRE). The arrival rate of the species introduced through all three routes increased steeply after 1990, without a sign of saturation. Data analysis highlighted some temporal and geographical patterns, such as the effect and eventual weakening of the biogeographical barriers represented by the Strait of Sicily and the North Aegean Sea and the asymmetrical distribution of occurrences along the northern and southern Mediterranean coasts. Finally, there was an exponential increase in the secondary spread rates of CAN and NRE immigrants, as the more recent introductions achieved the fastest geographical expansions. Our findings provide a detailed and spatially explicit summary of a massive invasion that has changed the history of the Mediterranean biota and represent a remarkable example of rapid biotic homogenization in the global ocean.

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.

Climate change, biological invasions, and the shifting distribution of Mediterranean fishes: A large-scale survey based on local ecological knowledge.

Climate change and biological invasions are rapidly reshuffling species distribution, restructuring the biological communities of many ecosystems worldwide. Tracking these transformations in the marine environment is crucial, but our understanding of climate change effects and invasive species dynamics is often hampered by the practical challenge of surveying large geographical areas. Here, we focus on the Mediterranean Sea, a hot spot for climate change and biological invasions to investigate recent spatiotemporal changes in fish abundances and distribution. To this end, we accessed the local ecological knowledge (LEK) of small-scale and recreational fishers, reconstructing the dynamics of fish perceived as "new" or increasing in different fishing areas. Over 500 fishers across 95 locations and nine different countries were interviewed, and semiquantitative information on yearly changes in species abundance was collected. Overall, 75 species were mentioned by the respondents, mostly warm-adapted species of both native and exotic origin. Respondents belonging to the same biogeographic sectors described coherent spatial and temporal patterns, and gradients along latitudinal and longitudinal axes were revealed. This information provides a more complete understanding of the shifting distribution of Mediterranean fishes and it also demonstrates that adequately structured LEK methodology might be applied successfully beyond the local scale, across national borders and jurisdictions. Acknowledging this potential through macroregional coordination could pave the way for future large-scale aggregations of individual observations, increasing our potential for integrated monitoring and conservation planning at the regional or even global level. This might help local communities to better understand, manage, and adapt to the ongoing biotic transformations driven by climate change and biological invaders.

Genomic signatures of rapid adaptive evolution in the bluespotted cornetfish, a Mediterranean Lessepsian invader.

Biological invasions are increasingly creating ecological and economical problems both on land and in aquatic environments. For over a century, the Mediterranean Sea has steadily been invaded by Indian Ocean/Red Sea species (called Lessepsian invaders) via the Suez Canal, with a current estimate of ~450 species. The bluespotted cornetfish, Fistularia commersonii, considered a 'Lessepsian sprinter', entered the Mediterranean in 2000 and by 2007 had spread through the entire basin from Israel to Spain. The situation is unique and interesting both because of its unprecedented rapidity and by the fact that it took this species c. 130 years to immigrate into the Mediterranean. Using genome scans, with restriction site-associated DNA (RAD) sequencing, we evaluated neutral and selected genomic regions for Mediterranean vs. Red Sea cornetfish individuals. We found that few fixed neutral changes were detectable among populations. However, almost half of the genes associated with the 47 outlier loci (potentially under selection) were related to disease resistance and osmoregulation. Due to the short time elapsed from the beginning of the invasion to our sampling, we interpret these changes as signatures of rapid adaptation that may be explained by several mechanisms including preadaptation and strong local selection. Such genomic regions are therefore good candidates to further study their role in invasion success.

Niche shift can impair the ability to predict invasion risk in the marine realm: an illustration using Mediterranean fish invaders.

Climatic niche conservatism, the tendency of species-climate associations to remain unchanged across space and time, is pivotal for forecasting the spread of invasive species and biodiversity changes. Indeed, it represents one of the key assumptions underlying species distribution models (SDMs), the main tool currently available for predicting range shifts of species. However, to date, no comprehensive assessment of niche conservatism is available for the marine realm. We use the invasion by Indo-Pacific tropical fishes into the Mediterranean Sea, the world's most invaded marine basin, to examine the conservatism of the climatic niche. We show that tropical invaders may spread far beyond their native niches and that SDMs do not predict their new distributions better than null models. Our results suggest that SDMs may underestimate the potential spread of invasive species and call for prudence in employing these models in order to forecast species invasion and their response to environmental change.

External morphology explains the success of biological invasions.

Biological invasions have become major players in the current biodiversity crisis, but realistic tools to predict which species will establish successful populations are still unavailable. Here we present a novel approach that requires only a morphometric characterisation of the species. Using fish invasions of the Mediterranean, we show that the abundance of non-indigenous fishes correlates with the location and relative size of occupied morphological space within the receiving pool of species. Those invaders that established abundant populations tended to be added outside or at the margins of the receiving morphospace, whereas non-indigenous species morphologically similar to resident ones failed to develop large populations or even to establish themselves, probably because the available ecological niches were already occupied. Accepting that morphology is a proxy for a species' ecological position in a community, our findings are consistent with ideas advanced since Darwin's naturalisation hypothesis and provide a new warning signal to identify invaders and to recognise vulnerable communities.

Invasion genomics of lionfish in the Mediterranean Sea.

The rate of biological invasions is steadily increasing, with major ecological and economic impacts accounting for billions of dollars in damage as a result. One spectacular example is the western Atlantic invasion by lionfishes. In the Mediterranean Sea, invasions from the Red Sea via the Suez Canal (termed Lessepsian invasions) comprise more than 100 fish species, including a recent invasion by lionfish. In light of the devastating effects of lionfish in the Caribbean Sea, understanding the dynamics of Mediterranean lionfish invasion is crucial. The Lessepsian lionfish invasion started in 2012, and rapidly spread to the central Mediterranean. Here, we used thousands of RAD seq genomic markers to study the population dynamics of this invasion. While we did not find a reduction in genetic diversity between source (Red Sea) and invasive (Mediterranean) populations (i.e., bottleneck effects), we found evidence of population structure within the invasive range in the Mediterranean Sea. We found that loci that are potentially under selection may play an important role in invasion success (in particular, genes involved in osmoregulation and fin spine sizes). Genomic approaches proved powerful in examining the ecological and evolutionary patterns of successful invaders and may be used as tools to understand and potentially mitigate future invasions.

Conservation physiology of marine fishes: advancing the predictive capacity of models.

At the end of May, 17 scientists involved in an EU COST Action on Conservation Physiology of Marine Fishes met in Oristano, Sardinia, to discuss how physiology can be better used in modelling tools to aid in management of marine ecosystems. Current modelling approaches incorporate physiology to different extents, ranging from no explicit consideration to detailed physiological mechanisms, and across scales from a single fish to global fishery resources. Biologists from different sub-disciplines are collaborating to rise to the challenge of projecting future changes in distribution and productivity, assessing risks for local populations, or predicting and mitigating the spread of invasive species.

ORMEF: a Mediterranean database of exotic fish records.

The Mediterranean Sea is recognized today as the World's most invaded marine region, but observations of species occurrences remain scattered in the scientific literature and scarcely accessible. Here we introduce the ORMEF database: a first comprehensive and robust compilation of exotic fish observations recorded over more than a century in the Mediterranean. ORMEF consists today of 4015 geo-referenced occurrences from 20 Mediterranean Countries, extracted from 670 scientific published papers. We collated information on 188 fish taxa that are thus divided: 106 species entered through the Suez Canal; 25 species introduced by shipping, mariculture, aquarium release or by means of other human activities; 57 Atlantic species, whose arrival in the Mediterranean has been attributed to the unassisted immigration through the strait of Gibraltar. Each observation included in the ORMEF database was submitted to a severe quality control and checked for geographical and taxonomic biases. ORMEF is a new authoritative reference for Mediterranean bio-invasion research and a living archive to inform management strategies and policymakers in a period of rapid environmental transformation.

Habitat suitability, niche unfilling and the potential spread of Pterois miles in the Mediterranean Sea.

The common lionfish Pterois miles has rapidly spread across the eastern Mediterranean Sea. We compiled occurrence data from both native and invaded range under the framework of Species Distribution Modelling (SDM). Through a construction of an environmental suitability model and estimation of spread rates we investigated the lionfish climate niche in both its native and invaded domains, this latter represented by the Mediterranean region. Model projections allowed to identify suitable areas for lionfish establishment in the Mediterranean. Spread analysis suggested that a further geographical expansion in this basin could be completed within the next years. Our results did not provide evidence for niche expansion but highlighted a high degree of niche unfilling thus prospecting a likely spread of Mediterranean lionfish invasion beyond the predictions of current SDMs. These findings provide novel inputs to forecast the future geographical evolution of the lionfish in the Mediterranean Sea and asses the related risk of invasion.

Using online questionnaires to assess marine bio-invasions: A demonstration with recreational fishers and the Atlantic blue crab Callinectes sapidus (Rathbun, 1986) along three Mediterranean countries.

Marine bioinvasions require integrating monitoring tools with other complementary strategies. In this study, we collected information about the invasive alien crab Callinectes sapidus in Italy, Croatia and Montenegro, by means of online questionnaires administered to recreational fishers (n = 797). Our records matched the current distribution of the species: C. sapidus resulted far more common in the Adriatic/Ionian than in the Tyrrhenian/Ligurian sector. Most respondents rated the species as 'occasional' or 'rare'. Moreover, the more C. sapidus was considered to be abundant, the more fishers tended to perceive it as a negative disturbance over fisheries and the environment. Our findings suggest that C. sapidus is more common than previously thought in most of the study area, and it could have reached the levels of a true invasions in the south-eastern Adriatic Sea. This experience demonstrates that online questionnaires can be appropriate tools to effectively engage stakeholders in alien species monitoring.

Annual rhythms of temporal niche partitioning in the Sparidae family are correlated to different environmental variables.

The seasonal timing of recurring biological processes is essential for organisms living in temperate regions. While ample knowledge of these processes exists for terrestrial environments, seasonal timing in the marine environment is relatively understudied. Here, we characterized the annual rhythm of habitat use in six fish species belonging to the Sparidae family, highlighting the main environmental variables that correlate to such rhythms. The study was conducted at a coastal artificial reef through a cabled observatory system, which allowed gathering underwater time-lapse images every 30 minutes consecutively over 3 years. Rhythms of fish counts had a significant annual periodicity in four out of the six studied species. Species-specific temporal patterns were found, demonstrating a clear annual temporal niche partitioning within the studied family. Temperature was the most important environmental variable correlated with fish counts in the proximity of the artificial reef, while daily photoperiod and salinity were not important. In a scenario of human-induced rapid environmental change, tracking phenological shifts may provide key indications about the effects of climate change at both species and ecosystem level. Our study reinforces the efficacy of underwater cabled video-observatories as a reliable tool for long-term monitoring of phenological events.

Management priorities for marine invasive species.

Managing invasive alien species is particularly challenging in the ocean mainly because marine ecosystems are highly connected across broad spatial scales. Eradication of marine invasive species has only been achieved when species were detected early, and management responded rapidly. Generalized approaches, transferable across marine regions, for prioritizing actions to control invasive populations are currently lacking. Here, expert knowledge was elicited to prioritize 11 management actions for controlling 12 model species, distinguished by differences in dispersion capacity, distribution in the area to be managed, and taxonomic identity. Each action was assessed using five criteria (effectiveness, feasibility, acceptability, impacts on native communities, and cost), which were combined in an 'applicability' metric. Raising public awareness and encouraging the commercial use of invasive species were highly prioritized, whereas biological control actions were considered the least applicable. Our findings can guide rapid decision-making on prioritizing management options for the control of invasive species especially at early stages of invasion, when reducing managers' response time is critical.

Tracking Fish Abundance by Underwater Image Recognition.

Marine cabled video-observatories allow the non-destructive sampling of species at frequencies and durations that have never been attained before. Nevertheless, the lack of appropriate methods to automatically process video imagery limits this technology for the purposes of ecosystem monitoring. Automation is a prerequisite to deal with the huge quantities of video footage captured by cameras, which can then transform these devices into true autonomous sensors. In this study, we have developed a novel methodology that is based on genetic programming for content-based image analysis. Our aim was to capture the temporal dynamics of fish abundance. We processed more than 20,000 images that were acquired in a challenging real-world coastal scenario at the OBSEA-EMSO testing-site. The images were collected at 30-min. frequency, continuously for two years, over day and night. The highly variable environmental conditions allowed us to test the effectiveness of our approach under changing light radiation, water turbidity, background confusion, and bio-fouling growth on the camera housing. The automated recognition results were highly correlated with the manual counts and they were highly reliable when used to track fish variations at different hourly, daily, and monthly time scales. In addition, our methodology could be easily transferred to other cabled video-observatories.

Warming-related shifts in the distribution of two competing coastal wrasses.

Warming induces organisms to adapt or to move to track thermal optima, driving novel interspecific interactions or altering pre-existing ones. We investigated how rising temperatures can affect the distribution of two antagonist Mediterranean wrasses: the 'warm-water' Thalassoma pavo and the 'cool-water' Coris julis. Using field surveys and an extensive database of depth-related patterns of distribution of wrasses across 346 sites, last-decade and projected patterns of distribution for the middle (2040-2059) and the end of century (2080-2099) were analysed by a multivariate model-based framework. Results show that T. pavo dominates shallow waters at warmest locations, where C. julis locates deeper. The northernmost shallow locations are dominated by C. julis where T. pavo abundance is low. Projections suggest that the W-Mediterranean will become more suitable for T. pavo whilst large sectors of the E-Mediterranean will be unsuitable for C. julis, progressively restricting its distribution range. These shifts might result in fish communities' re-arrangement and novel functional responses throughout the food-web.

Predicting future thermal habitat suitability of competing native and invasive fish species: from metabolic scope to oceanographic modelling.

Global increase in sea temperatures has been suggested to facilitate the incoming and spread of tropical invaders. The increasing success of these species may be related to their higher physiological performance compared with indigenous ones. Here, we determined the effect of temperature on the aerobic metabolic scope (MS) of two herbivorous fish species that occupy a similar ecological niche in the Mediterranean Sea: the native salema (Sarpa salpa) and the invasive marbled spinefoot (Siganus rivulatus). Our results demonstrate a large difference in the optimal temperature for aerobic scope between the salema (21.8°C) and the marbled spinefoot (29.1°C), highlighting the importance of temperature in determining the energy availability and, potentially, the distribution patterns of the two species. A modelling approach based on a present-day projection and a future scenario for oceanographic conditions was used to make predictions about the thermal habitat suitability (THS, an index based on the relationship between MS and temperature) of the two species, both at the basin level (the whole Mediterranean Sea) and at the regional level (the Sicilian Channel, a key area for the inflow of invasive species from the Eastern to the Western Mediterranean Sea). For the present-day projection, our basin-scale model shows higher THS of the marbled spinefoot than the salema in the Eastern compared with the Western Mediterranean Sea. However, by 2050, the THS of the marbled spinefoot is predicted to increase throughout the whole Mediterranean Sea, causing its westward expansion. Nevertheless, the regional-scale model suggests that the future thermal conditions of Western Sicily will remain relatively unsuitable for the invasive species and could act as a barrier for its spread westward. We suggest that metabolic scope can be used as a tool to evaluate the potential invasiveness of alien species and the resilience to global warming of native species.

Tracking signals of change in Mediterranean fish diversity based on local ecological knowledge.

One of the expected effects of global change is increased variability in the abundance and distribution of living organisms, but information at the appropriate temporal and geographical scales is often lacking to observe these patterns. Here we use local knowledge as an alternative information source to study some emerging changes in Mediterranean fish diversity. A pilot study of thirty-two fishermen was conducted in 2009 from four Mediterranean locations along a south-north gradient. Semi-quantitative survey information on changes in species abundance was recorded by year and suggests that 59 fish species belonging to 35 families have experienced changes in their abundance. We distinguished species that increased from species that decreased or fluctuated. Multivariate analysis revealed significant differences between these three groups of species, as well as significant variation between the study locations. A trend for thermophilic taxa to increase was recorded at all the study locations. The Carangidae and the Sphyraenidae families typically were found to increase over time, while Scombridae and Clupeidae were generally identified as decreasing and Fistularidae and Scaridae appeared to fluctuate in abundance. Our initial findings strongly suggest the northward expansion of termophilic species whose occurrence in the northern Mediterranean has only been noted previously by occasional records in the scientific literature.

Sewage pollution impact on Mediterranean rocky-reef fish assemblages.

The effects of sewage outfalls on subtidal fish assemblages were studied along the NW coasts of Malta (Sicily channel, Mediterranean Sea) by means of underwater visual census. The presence of two spatially distinct outfalls discharging untreated wastewaters allowed to use a balanced symmetrical after control/impact (ACI) design that consisted of two putatively impacted locations and two controls, with four sites nested in each location. Surveys were performed in 2006 at two random dates. The study highlighted significant changes at both assemblage and individual species levels. Fish assemblages structures were different between controls and sewages, where total abundance of fish were higher. The responses of individual species to sewage pollution were mostly related to an anomalous increase of two small opportunistic species i.e. Gobius bucchichii and Parablennius rouxi and to a decrease of species of the genus Symphodus, particularly S. roissali and S. ocellatus. Moreover in correspondence of the outfalls, significant changes of the fish size distribution were detected for several species. These results support the use of fish assemblages as biological indicators for marine coastal waters and demonstrated the possibility to obtain sharp signals of environmental impact from some individual fish species.

Genetic bottlenecks and successful biological invasions: the case of a recent Lessepsian migrant.

Our current understanding of the mechanisms that lead to successful biological invasions is limited. Although adaptations play a central role in biological invasions, genetic studies have so far failed to produce a unified theory. The bluespotted cornetfish, a recent Red Sea invader in the Mediterranean Sea via the Suez Canal, provides an ideal case study for research in the mechanisms of invasive genetics. In this study, we show that the invading bluespotted cornetfish underwent a severe population bottleneck that reduced the genetic diversity of this immigrant to only two mitochondrial haplotypes. Although loss of genetic diversity is considered detrimental to the need to adapt to new environments, bluespotted cornetfish experienced an unprecedented success and rapid spread across the Mediterranean.