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

Abstract 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.


Introduction
The concern about the impacts of non-indigenous species (NIS) has grown steeply over the past half-century (David et al. 2017), and a large amount of evidence suggests that NIS can alter the structure of natural communities and the integrity of ecosystems causing substantial ecological, economic, and cultural losses, especially in case they become invasive (Invasive Alien Species, IAS hereafter; Anton et al. 2019, see also Thomsen 2020). The impact of IAS is mediated by biotic interactions with the native communities and changes in the ecosystem processes including nutrient dynamics, fluxes of energy, and material cycling (Gallardo et al. 2016, Corrales et al. 2020. The monitoring and assessment of the impact of IAS and the prioritisation of adequate management actions are crucial steps to mitigate and/or limit the potential adverse effects of those species that are more likely to represent a serious threat to native ecosystems (Dick et al. 2017, Cuthbert et al. 2019).
The Atlantic blue crab (Callinectes sapidus Rathbun, 1896) is considered one of the worst invasive species in the Mediterranean Sea owing to its impact on local biodiversity, fisheries, and aquaculture (Streftaris and Zenetos 2006). The Atlantic blue crab (hereafter blue crab) was first recorded in Europe at the start of the past century (Bouvier 1901) and 13 15 appeared in the Mediterranean Sea between 1947and 1949(Giordani Soika 1951, Serbetis 1959. Over the last decade, the blue crab has spread almost ubiquitously in the eastern and central Mediterranean Sea and in the Black Sea, and it is currently widening its distribution towards the western sectors of the basin (Mancinelli et al. 2017a, Mancinelli et al. 2021).
The blue crab is an opportunistic omnivore, feeding on a variety of food sources from plants and detritus, to molluscs, arthropods (including conspecifics), polychaetes, and fish (Belgrad and Griffen 2016). Similar to other IAS, such trophic plasticity represents a key adaptive feature explaining the establishment success of the blue crab in non-native ecosystems and its impact on invaded food webs (Mancinelli et al. 2017b). However, while the crucial role played by the blue crab in regulating the structure and functioning of native food webs is well recognised, the number of studies investigating the trophic role of this invader in non-native ecosystems is remarkably lower (Mancinelli et al. 2017b, but see Kampouris et al. 2019 for a counter-example). In native coastal ecosystems, the blue crab acts as a keystone species by regulating the carbon cycle and prey/predator abundance through both bottom-up and top-down interactions (Altieri et al. 2012, Pugesek et al. 2013). Thus, understanding how the trophic ecology of this taxon shapes benthic food webs in invaded ecosystems is crucial for an accurate assessment of its impact.
Stable isotope analysis of δ C and δ N has become an increasingly popular methodology in studies focusing on food web structure and functioning. Specifically, δ C can trace the flow of matter and nutrients from basal to higher trophic levels and δ N can clarify trophic interactions (Fry 2006). In addition, even though species-specific physiological or metabolic factors can influence δ N values (Tibbets et al. 2007;Doi et al. 2017), δ N is commonly used to infer the species trophic position within food webs (Post 2002). In fact, as the trophic level increases, the nitrogen enriches predictably in its heavier isotope N due to the preferential excretion of the lighter isotope N (Minagawa and Wada 1984;Post 2002). Noticeably, the assessment of the effects of non-indigenous species on native communities is one of the first applications of stable isotope analysis in invasion ecology (Mitchell et al. 1996). Mancinelli and Vizzini (2015)reviewed the advantages and limitations of the method for identifying and quantifying the ecological impact of invasive species, clearly emphasising how the estimation of invasive species trophic position, using stable isotopes, can be successfully used for assessing direct predatory impacts, as well as community-scale effects on the whole trophic structure. For the blue crab, recent evidence indicated substantial variability in its trophic level across closely-located coastal ecosystems and size-related shifts in individual trophic position within invaded food webs (Mancinelli et al. 2016, Mancinelli et al. 2017b. Ultimately, these studies demonstrate the utility of stable isotope analysis in detecting changes in food web structure after the invasion; an advanced understanding of such trophic interactions can, in turn, help to predict and quantify the impact of biological invasions on aquatic food webs (Jackson et al. 2012

General description
Purpose: This dataset collates available geo-referenced and individual-based isotopic values (δ C and δ N) of C. sapidus and its potential animal prey in Mediterranean waters. The isotopic values, included in the dataset, are expressed in delta notation (‰ deviation from atmospheric nitrogen and from Pee Dee Belemnite [PDB] limestone used as standards for N and C, respectively) and δ N or δ C = [(R /R ) -1] × 1000, where R = N/ N or C/ C. The analytical precision of measurements for all δ C and δ N values was 0.2‰ as calculated by the standard deviation of replicates of the internal standards. This dataset can be used for a variety of comparative analyses including the calculation of the trophic position of the crab and/or metrics and descriptors of its isotopic niche, and it was conceived as one of the input files for the Functional biogeography of invaders workflow of the LifeWatch ERIC Internal Joint Initiative. Specifically, the analytical workflow aims at identifying climatic predictors of the trophic position of two invasive crustaceans, i.e. the blue crab C. sapidus and the Louisiana crayfish Procambarus clarkii. For P. clarkii, the workflow runs on an aggregated dataset resolved at population scale, whereas for C. sapidus, two datasets can be used as input files to run the analyses: (i) an aggregated dataset at the population scale similar to the one built for P. clarkii and (ii) an individual-based dataset with isotopic values of single specimens as described in the present article. All datasets include isotopic information for potential prey to allow the estimation of the trophic position of the invasive species under analysis.

Project description
Title: LifeWatch ERIC Internal Joint Initiative -Functional biogeography of invaders: the case of two widely distributed omnivorous crustaceans (https://bit.ly/iji-crustaceans).

Personnel: Cristina Di Muri, Giorgio Mancinelli, Ilaria Rosati, Lucia Vaira
Study area description: Coastal and transitional areas of the Mediterranean Sea colonised by C. sapidus. The westernmost records are located in Spain, the northernmost in Croatia, the easternmost in Turkey, and the southernmost in Greece. The majority of records lie in Italy.

Design description:
The dataset contains geographical and temporal information on the sampling event including country, location, geographical coordinates, type of habitat, year, and month or season in which the sampling occurred. Biological features of the species included are also specified, such as the invasive or native nature of the species for each location and the prey-predator relationship. Such attributes, together with δ C and δ N values, can be used for downstream analyses including the calculation of the blue crab trophic position, which can be estimated using two different approaches. The first method estimates the trophic position using the following equation: This equation is a generalisation of the formula presented in Jepsen and Winemiller (2002), where δ N is the nitrogen isotopic value of the blue crab, Δ N is the trophic level fractionation of δ N, δ N and λ are the nitrogen isotopic value and the trophic level of the baseline species (e.g. for Phorcus turbinatus, λ = 2). Alternatively, the blue crab trophic position can be estimated using a Bayesian approach implemented in the R package tRophicPosition (Quezada-Romegialli et al. 2018, R Core Team 2021. In this case, the original δ C and δ N values can be back-estimated using mean values, standard deviations, and sample size for each location and species and assuming a normal distribution.

Sampling methods
Study extent: The literature search for compiling this dataset ended on 31 April 2021.

Sampling description:
The online platforms ISI Web of Science and Scopus were searched using multiple search criteria including the terms "Callinectes sapidus" and "stable isotopes" in conjunction with "non-indigenous", "alien", "invasive", "Mediterranean Sea", and "Black Sea". The results were integrated with those obtained by querying Google Scholar using the same search criteria, together with the corresponding terms in Spanish or Portuguese (e.g. "jaiba azul", "cangrejo azul", "siri azul") in order to access additional literature published in languages other than English. Google Scholar search results were saved using the freeware Publish or Perish ver. 7.27.2849 (Harzing 2007).

Quality control:
Only records with defined locations whose accuracy was checked using Google Earth were included in the dataset; geographic coordinates were converted to decimal degrees when not originally specified as such. The taxonomic check was performed using the World Register of Marine Species.
Step description: The blue crab preys preferentially on bivalves (Hines 2007); accordingly, this taxonomic group was chosen as a reference for the selection of baseline species included in the dataset. M. galloprovincialis was generally used in the dataset given the almost ubiquitous distribution in Mediterranean marine coastal waters. If not available, other bivalves and herbivorous gastropods occurring at the study sites were chosen. On only one occasion, the omnivorous polychaete (Alitta succinea) was used as the baseline species. The trophic level of prey species was assigned, based on their trophic habits as follows: bivalves' trophic position = 2 (filter feeders); gastropod Phorcus turbinatus trophic position = 2 (herbivore; Aslan and Polito 2021); polychaete A. succinea trophic position = 2.78 (omnivore; Jumars et al. 2015, Como et al. 2018. Both M. galloprovincialis and Arcuatula senhousia are filter feeders and their diets mainly rely on phytoplankton and suspended particulate matter (Inoue andYamamuro 2000, Ezgeta-Balić et al. 2014); hence, in agreement with the Sea Around Us database, we assumed for both taxa a trophic position = 2. However, it has been also repeatedly indicated that zooplankton can be included in the diet of M. galloprovincialis depending on local conditions, as well as on seasonal variations in resource availability  . Such variation could be due to individual-scale differences in feeding habits, ontogeny, and metabolism (Tibbets et al. 2007, Doi et al. 2017). The user is, therefore, free to calculate the trophic position of C. sapidus by adopting, for example, the grand mean of the δ N values or any other estimation of central tendency (e.g. mode or median). Alternatively, individual δ N values of baseline taxa can be selected by eliminating the outliers or by choosing only a subset of the specimens included (e.g. the lower quartile of the isotopic distribution).

Geographic coverage
Description: The dataset gathers isotopic values of different Mediterranean areas colonised by C. sapidus including seven study sites in Italy, two study sites in Greece, and one study site in Croatia, Spain, and Turkey ( Fig. 1  An individual-based dataset of carbon and nitrogen isotopic data of Callinectes ... trophicRole Statement specifying whether the species is a predator or a prey.

Usage licence
carbon-13 A value of the isotope of the chemical element carbon, expressed in permil (‰).

nitrogen-15
A value of the isotope of the chemical element nitrogen, expressed in permil (‰).
trophicLevel Any of the feeding levels through which the passage of energy through an ecosystem proceeds; examples are photosynthetic plants, herbivorous animals, and microorganisms of decay.