Heterotrophy in marine animal forests in an era of climate change.

Marine animal forests (MAFs) are benthic ecosystems characterised by biogenic three-dimensional structures formed by suspension feeders such as corals, gorgonians, sponges and bivalves. They comprise highly diversified communities among the most productive in the world's oceans. However, MAFs are in decline due to global and local stressors that threaten the survival and growth of their foundational species and associated biodiversity. Innovative and scalable interventions are needed to address the degradation of MAFs and increase their resilience under global change. Surprisingly, few studies have considered trophic interactions and heterotrophic feeding of MAF suspension feeders as an integral component of MAF conservation. Yet, trophic interactions are important for nutrient cycling, energy flow within the food web, biodiversity, carbon sequestration, and MAF stability. This comprehensive review describes trophic interactions at all levels of ecological organisation in tropical, temperate, and cold-water MAFs. It examines the strengths and weaknesses of available tools for estimating the heterotrophic capacities of the foundational species in MAFs. It then discusses the threats that climate change poses to heterotrophic processes. Finally, it presents strategies for improving trophic interactions and heterotrophy, which can help to maintain the health and resilience of MAFs.

Isotopic Overlap of Invasive and Native Consumers in the Food Web of Lake Trasimeno (Central Italy).

An advanced characterization of the trophic niche of non-indigenous species (NIS) may provide useful information on their ecological impact on invaded communities. Here, we used carbon and nitrogen stable isotopes to estimate pairwise niche overlaps between non-indigenous and native consumers in the winter food web of Lake Trasimeno (central Italy). Overall, a relatively low pairwise overlap of isotopic niches was observed between NIS and native species. The only exception was the Louisiana crayfish Procambarus clarkii, which showed a relatively high and diffuse overlap with other native invertebrates. Our findings highlighted a high niche divergence between non-indigenous and native species in Lake Trasimeno, suggesting a potentially low degree of interspecific competition that may facilitate coexistence and, in turn, limit the strength of impacts. The divergent results obtained for the Louisiana crayfish indicate that additional control measures for this invasive species are needed to mitigate its impact on the Lake Trasimeno system.

The trophic niche of subterranean populations of Speleomantes italicus.

The determination of a species trophic niche can clarify its functional role within a food web and how prey resources are used in relation with the spatial and temporal variability of environmental conditions. This information may result particularly useful for the implementation of conservation plans of endangered species having a cryptic behaviour or living in places difficult to be surveyed. Here we present the first long-term study on the trophic niche of the Italian cave salamander Speleomantes italicus, a strictly protected facultative cave species that seasonally exploits surface environments (e.g., forested areas) as well as both natural and artificial subterranean environments. We analysed the diet variation of six populations of S. italicus inhabiting natural caves, surveyed 24 times in a full year. During the surveys, all sampled individuals were subjected to stomach flushing and the ingested prey were identified and enumerated; furthermore, salamanders' body condition was also evaluated. The results of the analyses provided the first comprehensive, year-round assessment of the diet for a Speleomantes species. Remarkable divergences in terms of trophic niche and body condition were observed between the studied populations. We found a discrepancy in the foraging activity of the populations located in different areas; specifically, the individuals that experienced sub-optimal microclimatic conditions poorly performed in foraging. Furthermore, we found temporal and spatial variability in the body condition of individuals. Our study highlighted a remarkably high spatial and temporal divergence in the trophic habits of conspecific populations, a feature that may represent one of the major factors promoting the variability of multiple population traits.

Severe, rapid and widespread impacts of an Atlantic blue crab invasion.

The Atlantic blue crab (Callinectes sapidus) has rapidly invaded coastal environments in the western Mediterranean, but there is no consistent assessment of its impacts yet. We use interviews and long-term data series in the Ebro Delta (NE Spain) to: i) characterise the evolution of the blue crab invasion; and ii) identify its impacts. The blue crab was first recorded in 2012, but its expansion started around 2016, with an exponential increase in abundance between 2017 and 2018. Aquatic communities have tended to be dominated by the blue crab, coinciding with the steep and consistent declines of several species, including threatened and commercially exploited ones. Blue crab impacts seem to be exerted even at low abundances, arguably hindering the recovery of declining species. The blue crab is becoming a keystone species in invaded systems and efforts should be made to understand its many-folds impacts in order to prevent or mitigate them.

Occurrence of the protozoan parasites Toxoplasma gondii and Cyclospora cayetanensis in the invasive Atlantic blue crab Callinectes sapidus from the Lesina Lagoon (SE Italy).

The occurrence of the protozoan parasites Toxoplasma gondii and Cyclospora cayetanensis was molecularly investigated in the hemolymph, gills, stomach, hepatopancreas and gonads of the eleven invasive Atlantic blue crab Callinectes sapidus from the Lesina Lagoon (Mediterranean Sea). Out of 11 blue crabs, 6 (54.5%) and 4 (36.4%) were found positive to T. gondii and C. cayetanenis, respectively; parasites were found only in the six females analysed, while the remaining five males resulted negative. Moreover, out of 55 tissues samples, 7 (12.7%) and 8 (14.5%) were positive to T. gondii and C. cayetanensis, respectively with hemolymph and gills being the most infected tissues. This is the first report of the presence of protozoan pathogens in wild crab species collected from a Mediterranean lagoon. The present results may provide a baseline reference on microbial infection in the species for invaded Mediterranean waters, and on the potential health risks related with its consumption if eaten raw.

An individual-based dataset of carbon and nitrogen isotopic data of Callinectessapidus in invaded Mediterranean waters.

BACKGROUND: The characterisation of functional traits of non-indigenous and invasive species is crucial to assess their impact within invaded habitats. Successful biological invasions are often facilitated by the generalist diet of the invaders which can modify their trophic position and adapt to new ecosystems determining changes in their structure and functioning. Invasive crustaceans are an illustrative example of such mechanisms since their trophic habits can determine important ecological impacts on aquatic food webs. The Atlantic blue crab Callinectessapidus is currently established and considered invasive in the Mediterranean Sea where it has been recorded for the first time between 1947 and 1949. In the last decade, the blue crab colonised most of the eastern and central Mediterranean Sea and the Black Sea and it is currently widening its distribution towards the western region of the basin. NEW INFORMATION: Stable isotope analysis is increasingly used to investigate the trophic habits of invasive marine species. Here, we collated individual measures of the blue crab δ13C and δ15N values and of its potential invertebrate prey into a geo-referenced dataset. The dataset includes 360 records with 236 isotopic values of the blue crab and 224 isotopic data of potential prey collected from five countries and 12 locations between 2014 and 2019. This dataset allows the estimation of the trophic position of the blue crab within a variety of invaded ecosystems, as well as advanced quantitative comparisons of the main features of its isotopic niche.

Phylogeography of the Atlantic Blue Crab Callinectes sapidus (Brachyura: Portunidae) in the Americas versus the Mediterranean Sea: Determining Origins and Genetic Connectivity of a Large-Scale Invasion.

The American blue crab Callinectes sapidus is a particularly successful invader in estuarine ecosystems worldwide. Despite increasing awareness of its potential harm, the invasion history and underlying genetic diversity of this species within the Mediterranean Sea remain unknown. This study constitutes the first large-scale approach to study phylogeographic patterns of C. sapidus in Europe, facilitated by the first comparison of all currently available COI sequence data. For this investigation, 71 individuals of C. sapidus were newly analyzed and the entire COI gene was sequenced and used for a comparative phylogeographic analyses. For the first time, two separately used adjacent regions of this gene were combined in a single dataset. This allowed emphasizing the prevalence of three geographically defined lineages within the native range: (1) eastern North America, including the Gulf of Mexico, (2) the Caribbean, and (3) Brazil. New data from the Mediterranean reveal that non-native populations of C. sapidus are characterized by a conspicuously low genetic diversity (except for Turkey, where stocking took place), and that there is surprisingly low connectivity among established populations. The occurrence of strong genetic bottlenecks suggests few founder individuals. This confirms that, even under a scenario of restricted large-scale gene flow, a very limited number of invasive individuals is sufficient for a massive impact.

Individual and population-scale carbon and nitrogen isotopic values of Procambarusclarkii in invaded freshwater ecosystems.

Background: Freshwater ecosystems are amongst the most threatened habitats on Earth; nevertheless, they support about 9.5% of the known global biodiversity while covering less than 1% of the globe's surface. A number of anthropogenic pressures are impacting species diversity in inland waters and, amongst them, the spread of invasive alien species is considered one of the main drivers of biodiversity loss and homogenisation in freshwater habitats.Crayfish species are widely distributed freshwater invaders and, while alien species introductions occur mostly accidentally, alien crayfish are often released deliberately into new areas for commercial purposes. After their initial introduction, crayfish species can rapidly establish and reach high-density populations as a result of their adaptive functional traits, such as their generalist diet.The Louisiana crayfish Procambarusclarkii (Girard, 1852) is globally considered one of the worst invaders and its impact on recipient freshwater communities can vary from predation and competition with native species, to modification of food webs and habitat structure and introduction of pathogens. Native to the south United States and north Mexico, P.clarkii has been introduced in Europe, Asia and Africa, determining negative ecological and economic impacts in the majority of invaded habitats where it became dominant within the receiving benthic food webs. Due to its flexible feeding strategy, P.clarkii exerts adverse effects at different trophic levels, ultimately affecting the structure and dynamics of invaded food webs. It is, therefore, paramount to evaluate the ecological consequences of P.clarkii invasion and to quantify its impact in a spatially explicit context. New information: In the past decades, the analysis of stable isotopes of carbon, nitrogen and other elements has become a popular methodology in food web ecology. Notably, stable isotope analysis has emerged as a primary tool for addressing applied issues in biodiversity conservation and management, such as the assessment of the trophic ecology of non-indigenous species in invaded habitats. Here, we built two geo-referenced datasets, resolved respectively at the population and individual scale, by collating information on δ13C and δ15N values of P.clarkii within invaded inland waters. The population-scale dataset consists of 160 carbon and nitrogen isotopic values of the Louisiana crayfish and its potential prey, including living and non-living primary producers and benthic invertebrates. The dataset resolved at individual scale consists of 1,168 isotopic records of P.clarkii. The isotopic values included within the two datasets were gathered from 10 countries located in Europe, Asia, Africa and North America, for a total of 41 studies published between 2005 and 2021. To the best of the authors' knowledge, this effort represents the first attempt to collate in standardised datasets the sparse isotopic information of P.clarkii available in literature. The datasets lend themselves to being used for providing a spatially explicit resolution of the trophic ecology of P.clarkii and to address a variety of ecological questions concerning its ecological impact on recipient aquatic food webs.

A global occurrence database of the Atlantic blue crab Callinectes sapidus.

The Atlantic blue crab Callinectes sapidus is a portunid native to the western Atlantic, from New England to Uruguay. The species was introduced in Europe in 1901 where it has become invasive; additionally, a significant northward expansion has been emphasized in its native range. Here we present a harmonized global compilation of C. sapidus occurrences from native and non-native distribution ranges derived from online databases (GBIF, BISON, OBIS, and iNaturalist) as well as from unpublished and published sources. The dataset consists of 40,388 geo-referenced occurrences, 39,824 from native and 564 from non-native ranges, recorded in 53 countries. The implementation of quality controls imposed a severe reduction, in particular from online databases, of the records selected for inclusion in the dataset. In addition, a technical validation procedure was used to flag entries showing identical coordinates but different year of record, in-land occurrences and those located close to the coast. Similarly, a flagging system identified entries outside the known distribution of the species, or associated with unsuccessful introductions.

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.

Interspecific and interpopulation variation in individual diet specialization: Do environmental factors have a role?

Individual diet specialization (IS) has important community- and population-level implications and its ecological drivers are actively investigated. Here, to test the hypothesis that local environmental conditions may influence IS in wild populations, we analyzed the stomach contents of 395 individuals from eight populations of five allopatric species of European cave salamanders (genus Hydromantes). We assessed whether their degree of individual diet specialization (1) scaled positively with the respective niche widths, in agreement with Van Valen's niche variation hypothesis (NVH), and (2) could be predicted by satellite-derived climatic and vegetation characteristics of the sites where the populations live. Consistent with the NVH, the degree of individual diet specialization increased with the populations' total niche width. Furthermore, two variables describing local nonarboreal vegetation cover and habitat heterogeneity successfully predicted the variation in individual specialization across the eight populations. Climatic factors had a generally low predictive power, with individual specialization in low- and high-elevation populations showing contrasting patterns of co-variation with air temperature in the warmest quarter of the year. However, independently from elevation, specialization peaked under conditions of high nonarboreal vegetation cover and high precipitation regimes. We discussed the results against two mutually nonexclusive scenarios hypothesizing different mechanisms linking environmental factors to salamanders' trophic strategy at an individual and population level. We concluded that satellite-derived climatic and vegetation variables to date generally adopted to model Grinnellian niches might also be useful in predicting spatial variations in dietary habits of populations, that is, their Eltonian niches.

Marine litter in stomach content of small pelagic fishes from the Adriatic Sea: sardines (Sardina pilchardus) and anchovies (Engraulis encrasicolus).

Marine litter impacts oceans and affects marine organisms, representing a potential threat for natural stocks of pelagic fish species located at the first levels of the marine food webs. In 2013-2014, on a seasonal basis, marine litter and microplastics in stomach contents from Sardinia pilchardus and Engraulis encrasicolus were evaluated. Selected species are plankitivores of great ecological and commercial importance in the Adriatic Sea. Collected data were correlated to possible factors able to affect ingested levels as well as species, season of sampling, biometry and sex of animals. Almost all tested samples (80 organisms for each species) contained marine litter (over 90% of samples from both species) and also microplastics; while any meso- or macroplastics were recorded. On average, recorded items were as follows: 4.63 (S. plichardus) and 1.25 (E. encrasicolus) per individual. Sardines evidenced a higher number of microplastics characterised by a smaller size than those recorded in anchovies. For sardines, sex, Gastro Somatic Index and sampling season showed negligible effects on the number of ingested litter; conversely, anchovies showed differences related with both sex of animals and dominant colour of ingested materials with prevalence for black and blue colours.

Baseline assessment of heavy metals content and trophic position of the invasive blue swimming crab Portunus segnis (Forskål, 1775) in the Gulf of Gabès (Tunisia).

This study provides a baseline assessment of cadmium, copper, iron, manganese, lead, and zinc concentrations in muscles, gills, and exoskeleton of the Lessepsian blue swimming crab Portunus segnis captured in the Gulf of Gabès (Southern Mediterranean Sea, Tunisia) in November 2015. Furthermore, the species' trophic position is estimated using CN stable isotope analysis. The exoskeleton showed the lowest metal contents; in soft tissues, the essential Cu, Fe, and Zn and the non-essential Cd, Mn, and Pb showed the highest and lowest concentrations, respectively. The crab was characterized by a trophic position of 3.32, confirming its carnivorous trophic habits. Compared with literature data on invertebrate and fish species from the same area, Cd and Pb resulted remarkably low in the crab's soft tissues, while a food web-scale dilution effect was indicated. The need of a comprehensive assessment of the ecological impact of Portunus segnis in invaded Mediterranean waters is discussed.

What shapes the trophic niche of European plethodontid salamanders?

The trophic niche is a life trait that identifies the consumer's position in a local food web. Several factors, such as ontogeny, competitive ability and resource availability contribute in shaping species trophic niches. To date, information on the diet of European Hydromantes salamanders are only available for a limited number of species, no dietary studies have involved more than one species of the genus at a time, and there are limited evidences on how multiple factors interact in determining diet variation. In this study we examined the diet of multiple populations of six out of the eight European cave salamanders, providing the first data on the diet for five of them. In addition, we assessed whether these closely related generalist species show similar diet and, for each species, we tested whether season, age class or sex influence the number and the type of prey consumed. Stomach condition (empty/full) and the number of prey consumed were strongly related to seasonality and to the activity level of individuals. Empty stomachs were more frequent in autumn, in individuals far from cave entrance and in juveniles. Diet composition was significantly different among species. Hydromantes imperialis and H. supramontis were the most generalist species; H. flavus and H. sarrabusensis fed mostly on Hymenoptera and Coleoptera Staphylinidae, while H. genei and H. ambrosii mostly consumed Arachnida and Endopterygota larvae. Furthermore, we detected seasonal shifts of diet in the majority of the species examined. Conversely, within each species, we did not find diet differences between females, males and juveniles. Although being assumed to have very similar dietary habits, here Hydromantes species were shown to be characterized by a high divergence in diet composition and in the stomach condition of individuals.

Beyond the mean: A comparison of trace- and macroelement correlation profiles of two lacustrine populations of the crayfish Procambarus clarkii.

In invertebrate biomonitors of chemical pollution, emphasis has been generally given to mean accumulation patterns and how they reflect varying environmental levels of contamination. Intra-population variability, and how it relates with individual phenotypic traits, has received less attention. Here, a set of analytes including trace elements (B, Ba, Cd, Cr, Cu, Fe, Li, Mn, Ni, Pb, Sr, V, and Zn), macroelements (C, Ca, K, Mg, N, Na), and carbon and nitrogen stable isotopes (δ13C and δ15N) was measured in two populations of the crayfish Procambarus clarkii from Lake Trasimeno and Lake Bolsena (Central Italy). The influence of location, sex, body size, and condition factor was assessed; in addition, the analyte correlation profiles of the two populations were compared to verify their congruence. In general, significant inter-lake differences were observed in the concentration of both trace- and macroelements in crayfish tissues, generally mirroring the local chemistry of water and of benthic non-living matrices (sediment and plant detritus). Crayfish CN isotopic signatures excluded the occurrence of inter-lake variations in their omnivorous trophic habits. Correlation profiles varied considerably between the two populations in the nature and strength of bivariate relationships. However, Mantel tests and procrustean analyses indicated a general, significant congruence; C, N, and, to a lesser extent K, Li, Ni, Pb, and δ13C showed the highest procrustean residuals, suggesting that their associations with other analytes may be partially influenced by inter-population differences in growing phases. Our study indicates that the local geochemistry of the lacustrine environment influences the elemental fingerprint of Procambarus clarkii; the considerable inter-individual variability in the concentration of analytes, however, does not significantly reflect on their association, thus corroborating its effectiveness as an indicator species.

The Atlantic blue crab Callinectes sapidus in southern European coastal waters: Distribution, impact and prospective invasion management strategies.

The native distribution of the blue crab Callinectes sapidus in the western Atlantic extends from Nova Scotia to Argentina. Introduced to Europe at the beginning of the 20th century, it is currently recorded almost ubiquitously in the Mediterranean and in the Black Sea. An overview of the occurrence, abundance, and ecological impact of the species in southern European waters is provided; additionally, we present a pragmatic assessment of its management scenarios, explicitly considering the dual nature of C. sapidus as both an invasive species and a fishery resource. We emphasise that the ongoing expansion of C. sapidus in the region may represent a stimulating challenge for the identification and implementation of future strategies in the management of invasive crustaceans. The impact of the invader could be converted into an enhancement of the services delivered by southern European coastal ecosystems, while mitigation costs could be transformed into profits for local populations.

Comparative analysis of the proximate and elemental composition of the blue crab Callinectes sapidus, the warty crab Eriphia verrucosa, and the edible crab Cancer pagurus.

The proximate composition and element contents of claw muscle tissue of Atlantic blue crabs (Callinectes sapidus) were compared with the native warty crab (Eriphia verrucosa) and the commercially edible crab (Cancer pagurus). The scope of the analysis was to profile the chemical characteristics and nutritive value of the three crab species. Elemental fingerprints showed significant inter-specific differences, whereas non-significant variations in the moisture and ash contents were observed. In the blue crab, protein content was significantly lower than in the other two species, while its carbon content resulted lower than that characterizing only the warty crab. Among micro-elements, Ba, Cr, Cu, Li, Mn, Ni, and Pb showed extremely low concentrations and negligible among-species differences. Significant inter-specific differences were observed for Na, Sr, V, Ba, Cd and Zn; in particular, cadmium and zinc were characterized in the blue crab by concentrations significantly lower than in the other two species. The analysis of the available literature on the three species indicated a general lack of comparable information on their elemental composition. The need to implement extended elemental fingerprinting techniques for shellfish quality assessment is discussed, in view of other complementary profiling methods such as NMR-based metabolomics.

(1)H NMR metabolomic profiling of the blue crab (Callinectes sapidus) from the Adriatic Sea (SE Italy): A comparison with warty crab (Eriphia verrucosa), and edible crab (Cancer pagurus).

The metabolomic profile of blue crab (Callinectes sapidus) captured in the Acquatina lagoon (SE Italy) was compared to an autochthonous (Eriphia verrucosa) and to a commercial crab species (Cancer pagurus). Both lipid and aqueous extracts of raw claw muscle were analyzed by (1)H NMR spectroscopy and MVA (multivariate data analysis). Aqueous extracts were characterized by a higher inter-specific discriminating power compared to lipid fractions. Specifically, higher levels of glutamate, alanine and glycine characterized the aqueous extract of C. sapidus, while homarine, lactate, betaine and taurine characterized E. verrucosa and C. pagurus. On the other hand, only the signals of monounsaturated fatty acids distinguished the lipid profiles of the three crab species. These results support the commercial exploitation and the integration of the blue crab in human diet of European countries as an healthy and valuable seafood.

Colonization of ephemeral detrital patches by vagile macroinvertebrates in a brackish lake: a body size-related process?

The mechanisms regulating the build-up of invertebrate assemblages on ephemeral detritus patches are still poorly understood. Here, the daily colonization of decaying reed leaves by vagile macroinvertebrates was monitored in an brackish lake in Italy. The highly variable abundance patterns of dominant taxa were analysed by spectral and geostatistical techniques to test for nonrandomness and to further determine whether they were related to body size. Comparisons between two contrasting sites allowed an assessment of the generality of our observations. At both sites, the macroinvertebrate assemblage was dominated by three detritivorous taxa, i.e. the isopod Lekanesphaera monodi, the amphipod Microdeutopus gryllotalpa and the polychaete Neanthes caudata. Overall, their abundance patterns were characterised by short-term fluctuations of a nonrandom, autocorrelated nature. In addition, a significant covariation was observed between the average body mass of each taxon and the complexity of the respective abundance pattern, expressed by the fractal dimension D. The covariation was observed at both study sites, notwithstanding the diverging outcomes of bivariate pattern comparisons for similar-sized taxa. Our findings indicate that the size of macroinvertebrates is strongly related to the short-term dynamics of their abundance patterns on reed detritus, suggesting that the interaction between vagile consumers and ephemeral resource patches might be influenced by individual energetics. The implications of size-related constraints for the coexistence of species on decaying detrital patches are discussed.