“Hidden invaders” conquer the Sicily Channel and knock on the door of the Western Mediterranean sea

Estuarine, Coastal and Shelf Science 225 (2019) 106234

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“Hidden invaders” conquer the Sicily Channel and knock on the door of the Western Mediterranean sea

T

Roberta Guastellaa, Agnese Marchinia, Antonio Carusob, Claudia Cosentinob, Julian Evansc, Anna E. Weinmannd, Martin R. Langerd, Nicoletta Mancina,∗ a

Department of Earth and Environment Sciences, University of Pavia, Via Ferrata 1, 27100, Pavia, Italy Dipartimento di Scienze della Terra e del Mare, Università di Palermo, Via Archirafi 22, 90123, Palermo, Italy c Department of Biology, University of Malta, Msida, MSD2080, Malta d Institut für Geowissenschaften, Paläontologie, Rheinische Friedrich-Wilhelms Universität Bonn, Nussallee 8, 53115, Bonn, Germany b

A R T I C LE I N FO

A B S T R A C T

Keywords: Benthic foraminifera Amphistegina lobifera Non-indigenous species Central mediterranean Distribution models

This study updates the current distribution, range expansion and establishment status of the non-indigenous species Amphistegina lobifera Larsen, 1976 and other foraminifera that are cryptogenic in the Sicily Channel. Prior to this study, amphisteginids were reported from the Levantine Basin, the Central Mediterranean (Tunisia, Malta, Pelagian islands) and the southern Adriatic Sea. Here, we provide new records documenting a north-western expansion in the Central Mediterranean. In summer-autumn 2017 and spring-summer 2018, we collected algae and sediment samples from shallow coastal habitats along the shores of the Maltese archipelago, southern and north-western Sicily, Pantelleria and the Aegadian islands. Analysis of the foraminiferal assemblages showed that A. lobifera is effectively established around Malta and in southern/south-eastern Sicily, and has reached the oceanographic boundary between the Central and Western Mediterranean. Our results also show that the thermotolerant A. lobifera is at an advanced stage of invasion in the Sicily Channel, probably favoured by a recent rise in Mediterranean sea surface temperatures. New species distribution models are provided for the years 2040–2050 and 2090–2100, indicating that the predicted warming trend will facilitate north-westward migration of Mediterranean amphisteginids along the coast of northern Africa into the Alboran Sea, and deep into the Adriatic Sea.

1. Introduction The dispersal of marine non-indigenous species (NIS) by human activities is redefining the biogeography of the oceans and is one aspect of global change (Occhipinti-Ambrogi, 2007). NIS are considered a major threat to global marine biodiversity and ecosystem functioning, impairing the associated ecosystem services (Katsanevakis and Crocetta, 2014; Servello et al., 2019). In order to understand the role of NIS in structuring and affecting marine communities, accurate information on their temporal occurrence, abundance, geographic distribution, and effect on native communities is required (Ojaveer et al., 2014). However many NIS, particularly those belonging to small-sized taxa such as protists, are largely overlooked and undetected, and the lag time between their introduction into a new area and their first record may span from years to centuries (Carlton, 2009). Moreover, little is

known about their impact on native communities and habitats. These data gaps impair our ability to understand and quantify marine invasions, assess the impact on native communities, and forecast the spread of NIS and their potential harm. Consequently, policy decisions related to the management of marine bio-invasions could be either delayed or designed based on inadequate data. In the Mediterranean Sea, “hidden invaders” include several unicellular taxa, such as benthic foraminifera (fora-NIS). A few species from this group, widespread in the Red Sea and the Indo-Pacific region, have entered the Mediterranean Sea via the Suez Canal and are now abundant along the coasts of Israel, Turkey and Greece (Hyams et al., 2002; Meriç et al., 2008; Triantaphyllou et al., 2009; Çinar et al., 2011; Langer et al., 2012; Schmidt et al., 2015). Most of them have a calcite test that persists after their death forming biogenic sands. Although foraminifera are considered “harmless as sand particles” (Langer and

∗

Corresponding author. E-mail addresses: [email protected] (R. Guastella), [email protected] (A. Marchini), [email protected] (A. Caruso), [email protected] (C. Cosentino), [email protected] (J. Evans), [email protected] (A.E. Weinmann), [email protected] (M.R. Langer), [email protected] (N. Mancin). https://doi.org/10.1016/j.ecss.2019.05.016 Received 3 December 2018; Received in revised form 6 May 2019; Accepted 24 May 2019 Available online 30 May 2019 0272-7714/ © 2019 Elsevier Ltd. All rights reserved.

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genetic analyses, is Pararotalia calcariformata McCulloch, 1977 (Meriç et al., 2013; Schmidt et al., 2015). Finally, a number of additional Indo-Pacific foraminiferal species have also been reported from the Mediterranean Sea, e.g.: Amphisorus hemprichii Ehrenberg, 1839, Coscinospira arietina (Batsch, 1791), Coscinospira hemprichii Ehrenberg, 1839, Cymbaloporetta squammosa d’Orbigny, 1839, Heterostegina depressa d’Orbigny, 1826, Pseudolachlanella slitella Langer, 1992, Sorites orbiculus (Forskål, 1775), and Sorites variabilis Lacroix, 1941 (Meriç et al., 2008, 2013; Merkado et al., 2012; Caruso and Cosentino, 2014 and references therein; Schmidt et al., 2015; Ounifi-Ben Amor et al., 2016). However, the available knowledge is insufficient to clearly assess their current status – either as introduced or native species – in the Central Mediterranean, and it is more prudent to consider them as cryptogenic species (Marchini et al., 2015). The Sicily Channel, located centrally in the Mediterranean Sea, is a natural biogeographical corridor for foraminifera originating from the Red Sea, and represents the oceanographic boundary between the colder western and warmer eastern Mediterranean basins (Azzurro et al., 2014; Di Lorenzo et al., 2017 and references therein). It is therefore the ideal region to assess if thermophilic fora-NIS are able to breach this boundary. Particularly, the invasive A. lobifera is purposed to live and spread only in warm water conditions, delimited by the 14 °C winter isotherm (Hallock, 1999; Langer and Hottinger, 2000; Triantaphyllou et al., 2012). The recent findings in Malta, Albania, the Pelagian Islands and Tunisia (Yokes et al., 2007; Caruso and Cosentino, 2014; Langer and Mouanga, 2016; El Kateb et al., 2018) suggest a continuous range extension towards the Central and Western Mediterranean Sea. This study provides a suite of new occurrence records and an updated overview of the current distribution and establishment status of A. lobifera in the Sicily Channel. The new records were used to create species distribution models (SDM) to assess the potential distribution of A. lobifera in the Central and Western Mediterranean Sea under current and future climate conditions. The study also provides new information on the current distribution of other Indo-Pacific foraminiferal species, here considered as cryptogenic, in the Sicily Channel.

Bell, 1995; Kosnik et al., 2015), hyperabundances of NIS foraminiferal tests have been reported to contribute significantly to the carbonate budget of sediments, triggering changes in community structures and locally replacing rocky substrata with carbonate sands (Yokes and Meriç, 2009; Abu Tair and Langer, 2010; Langer et al., 2012; Caruso and Cosentino, 2014; Langer and Mouanga, 2016; Ounifi-Ben Amor et al., 2016). Moreover, the massive increase of fora-NIS populations is also changing ecosystem functioning, negatively affecting native foraminiferal assemblages and causing biodiversity loss (Triantaphyllou et al., 2009; Langer et al., 2012; Mouanga and Langer, 2014). The most widespread and successful fora-NIS belong to the large algal symbiont-bearing genus Amphistegina, represented by two species: A. lobifera Larsen, 1976 and A. lessonii d’Orbigny in Guerin-Meneville, 1832. Amphistegina lobifera abounds at tropical and subtropical latitudes in the Indo-Pacific region, on firm and vegetated substrates and more rarely on sandy bottoms, at depth < 20 m, preferentially with mid to high light conditions and in high energy environments (Langer and Hottinger, 2000; Triantaphyllou et al., 2012 and references therein). In the last decades, this species has become particularly abundant in the Eastern Mediterranean, where its populations reach extremely high densities (e.g. Langer et al., 2012). Amphistegina lobifera has recently extended its range reaching the Maltese and Pelagian islands in the Central Mediterranean (Yokes et al., 2007; Caruso and Cosentino, 2014) and Albania in the southern Adriatic Sea (Langer and Mouanga, 2016). The origin of A. lobifera populations in the Mediterranean Sea has been treated with uncertainty in the literature, where the species is reported as either non-indigenous or as a cryptogenic species in inventories (e.g. see Koukousioura et al., 2010; Zenetos et al., 2008, 2018 and references therein). The uncertainty arises from reports of the presence of the genus Amphistegina in fossil Mediterranean records, starting from the Miocene but mainly during Pliocene-early Pleistocene time, until about 2.1 Ma, when warm conditions still persisted before the abrupt climatic deterioration at 1.8 Ma that drove amphisteginids to extinction (Di Bella et al., 2005). One possibility is that Mediterranean populations of Amphistegina spp. represent Tethyan relicts that somehow survived the late Miocene Messinian Salinity Crisis (MSC; Manzi et al., 2005; Pérez-Asensio et al., 2012; Roveri et al., 2014), but this is unlikely since the MSC caused a massive and abrupt extinction of most marine organisms, including benthic foraminifera (Kennett et al., 1977; Wright, 1979; Kouwenhoven et al., 2006; Rouchy et al., 2007). The subsequent recolonization in the early Pliocene (since about 5.3 Ma) was exclusively by taxa from the Atlantic Ocean via the Gibraltar strait (e.g. Langer and Schmidt-Sinns, 2006; Hayward et al., 2009 and references therein). This is the most likely origin of Amphistegina lessonii, Amphistegina gibbosa d’Orbigny, 1839, Amphistegina lessonii var. bowdenensis Palmer, 1945 and Amphistegina targioni Meneghini, 1881, all species that occurred and characterized Mediterranean shallow-water deposits of Pliocene-early Pleistocene age (Amphisteginarich beds; Di Bella et al., 2005). Instead, the present occurrence of the Indo-Pacific A. lobifera in the Mediterranean can most reasonably be explained by a Lessepsian immigration from the Red Sea. Meriç et al. (2016) have recently suggested that Mediterranean A. lobifera may have originated from ancient introductions during the Pleistocene through some natural waterway connecting the Indo-Pacific to the Eastern Mediterranean. However, geological data from that region suggest otherwise, because a possible connection between the two basins persisted only until the Gelasian (Popov et al., 2006). In addition, rDNA analyses performed on extant A. lobifera specimens from both the Mediterranean and the Red Sea (Schmidt et al., 2016) have shown that the two populations are genetically clustered together and distinct from Australian populations. This suggests that the population of A. lobifera currently spreading in the Mediterranean cannot represent the survival of an independent lineage of Plio-Pleistocene or Tethyan relicts, but results from a recent introduction of Red Sea specimens. Another foraminifer of Indo-Pacific origin reported from the Eastern Mediterranean Sea, with valid non-indigenous status confirmed by

2. Oceanographic setting The modern surface circulation of the Sicily Channel is characterized by currents of the Modified Atlantic Water (MAW), originating from the Atlantic Ocean surface water that enters the Mediterranean basin via the Strait of Gibraltar. This current flows eastward along the coasts of Morocco and Algeria, reaching the northern coast of Tunisia and the northwestern coast of Sicily (Fig. 1). From there, the MAW divides into two branches moving in different directions: the first one flows along the northern Sicilian coast into the Tyrrhenian Sea, the other one flows southeastward into the Sicily Channel to reach the Levantine basin in the Eastern Mediterranean (Drago et al., 2010; Di Lorenzo et al., 2017). The meandering flow of the latter branch within the Sicily Channel forms two wide counterclockwise vortices located, respectively, east of Pantelleria island around Adventure Bank (Adventure Bank Vortex – ABV), and off Capo Passero (Ionian Shelf break Vortex – ISV) at the southernmost tip of Sicily (Fig. 1). In the Alboran Sea, the MAW is characterized by an average salinity of 37.5 PSU (Practical Salinity Unit); in the Levantine basin, due to a higher evaporation rate, the MAW significantly increases its salinity (38.73–38.78 PSU) hence becoming denser (Drago et al., 2010); this in turn causes its sinking to depths of 200–600 m as Levantine Intermediate Water (LIW). The LIW flows westward, below the MAW and in the opposite direction, moving back through the Sicily Channel and reaching again the Atlantic Ocean via the Strait of Gibraltar. The spreading pattern of organisms with planktonic life cycle stages, benthic foraminiferal propagules and/or shallow-water specimens passively transported by floating rafts is likely to be affected by this 2

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climate conditions, medium to high values of habitat suitability for A. lobifera (Weinmann et al., 2013a). A total of 56 different sites were sampled during summer-autumn 2017 and spring-summer 2018, in the framework of various surveys conducted independently by several co-authors of this paper. Since A. lobifera is known to live on both sediments and algae (Hallock, 1999; Langer and Hottinger, 2000; Hohenegger, 2011), both types of substratum were sampled. Sediment samples (98) were collected at different depths, from the shoreline to depths of ∼20 m, depending on the local context of the sampling site. Samples were taken from the uppermost part of the sea-bottom (about 2 cm of sediment) using a diveroperated corer or a small Van Veen grab; when possible, 2–3 replicate samples were collected for each locality. Algal samples (51) were all hand-collected at shallow depths (less than 6 m). Details on sampling localities, including geographical coordinates, type of habitat, number of replicates, depth and other information are synthesized in Table S1 (available as online supplementary data). Moreover, this study includes unpublished results from surveys conducted by one of the co-authors in 2015 and 2016 along the southeastern Sicilian coast (sites 34–39, Table S1 supplementary data), which allowed us to assess possible changes in A. lobifera relative abundance in the same area over a temporal range of 3 years.

Fig. 1. Scheme of the surface circulation in the Sicily Channel (redrawn after Drago et al., 2010) together with the location of the five sampling areas; A) Maltese islands, B) Southern Sicily; C) Pantelleria island, D) Favignana island, E) Northwestern Sicily. The sites previously studied by Yokes et al. (2007) and Caruso and Cosentino (2014) are also indicated.

3.2. Sampling processing and foraminiferal analyses After collection, algal and sediment samples were immediately stored in polyethylene bottles and treated with buffered Rose Bengal dye (∼ 2 g of Rose Bengal in 1 l of ethanol) for at least 14 days, in order to distinguish living (stained) from dead (unstained) foraminiferal specimens. The staining protocol was not applied for the samples from Pantelleria island, collected in summer 2017, and from southeastern and northwestern Sicily collected respectively in summer 2015 and spring 2018 (Table S1, supplementary data). For foraminiferal analyses, samples were prepared following the standard procedures suggested by the FOraminiferal BIo-MOnitoring group (FOBIMO; Schönfeld et al., 2012). Sediment samples were ovendried at 40 °C, weighed (ca. 50 g) and washed over two overlapped sieves (meshes of 150 and 63 μm). The washed residues were ovendried again at 40 °C, separated in discrete aliquots using a precision micro-splitter and finally analysed under a stereomicroscope. In representative splits of the > 150 μm fraction, about 300 specimens were counted (both stained and unstained), in order to obtain census counts of the most common species of shallow-water benthic foraminifera. We also inspected the smaller fraction (63–150 μm) of each sample for small-sized species. Algal samples were prepared following Wilson (1998). Algae were oven-dried at 40 °C until they crumbled and then passed through a 63 μm mesh size sieve. The > 63 μm residue was analysed at the stereomicroscope through the counting of about 300 stained and unstained specimens when possible, otherwise the whole residue was counted. The largest algal remains were also examined for evidence of permanently attached foraminiferal individuals. All fora-NIS specimens were stored in micro-slides and some of them were photographed using a Canon S50 camera connected to a stereomicroscope. Relative abundances of A. lobifera and of the other cryptogenic foraminifera were calculated as a percentage of the total benthic foraminiferal census counts. Taxonomical attributions, at the species level whenever possible, follow Loeblich and Tappan (1987), Cimerman and Langer (1991), Hottinger et al. (1993) and Milker and Schmiedl (2012), and the World Register of Marine Species (WoRMS; www.marinespecies.org) for updated nomenclature.

general circulation scheme (Alve and Goldstein, 2003, 2010; Weinmann and Goldstein, 2017; Finger, 2018). However, several discontinuities or “oceanographic fronts” that could act as barriers to gene flow among populations have been identified in the Mediterranean Sea (Pascual et al., 2017), whereas mechanisms other than passive propagule dispersal have also been proposed for benthic foraminiferal spreading (Guy-Haim et al., 2017). The Sea Surface Temperature (SST) in the Mediterranean Sea is heavily affected by both the cold and humid air masses coming from the Atlantic Ocean and northern Europe, and the hot and arid air masses coming from sub-Saharan Africa. The Mediterranean SST varies between 8 °C during the winter season in the upper Adriatic and 30 °C during the summer in the Levantine Sea, with average values of about 14.5 °C and 26 °C in winter and summer, respectively (Pastor et al., 2017). In the Sicily Channel, the SST follows the main pattern of the surface current flow (NW–SE main direction); in fact, a gradient of increasing temperature is present between the northern and southern portion of the channel. The SST varies between about 24 °C (in the north) and 28 °C (in the south) in summer and between 15 °C (in the north) and 18 °C (in the south) in winter. During the winter season SST does not drop below 14 °C anywhere in the channel (Sorgente et al., 2003), allowing survival of thermophilic species such as A. lobifera (Zmiri et al., 1974; Langer and Hottinger, 2000). The 14 °C isotherm is located above the northern Sicilian coasts, which may reasonably represent the northernmost limit of the potential distribution of this species and of other thermophilic fora-NIS.

3. Materials and methods 3.1. Study areas and sampling strategy Sampling was carried out at four areas in the Sicily Channel (Fig. 1A–D) and one area in the Western Mediterranean (Fig. 1E): Maltese islands (A), southeastern coast of Sicily (B), Pantelleria island (C), Favignana island (D), and northwestern coast of Sicily (E). Amphistegina lobifera was recorded from the Maltese islands in 2006 (Yokes et al., 2007), but had not been previously reported from the other study areas. However, all the selected localities display, under the current

3.3. Species distribution models For the SDMs the new occurrence records of Amphistegina lobifera 3

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(2005), which has also been used in previous foraminiferal models (Langer et al., 2013; Schmidt et al., 2015).

from around Sicily were processed together with existing records previously published in Langer et al. (2012), Weinmann et al. (2013a), Mouanga and Langer (2014) and Langer and Mouanga (2016), and a few additional findings from other Central Mediterranean locations (Table S2, supplementary data). The final dataset includes a total of 126 records from the Eastern and the Central Mediterranean, the Adriatic and the Tyrrhenian Seas. Environmental data were obtained from the BIO-Oracle database (http://www.bio-oracle.org/), which consists of oceanographic variables obtained through remotely sensed and in situ measured datasets (Tyberghein et al., 2012; Assis et al., 2018). Each grid-cell has a resolution of 5 arc min or 9 × 9 km. BIO-Oracle also provides future datasets that are based on Representative Concentration Pathway (RCP) scenarios described within the Fifth Assessment Report of the IPCC (Collins et al., 2013). The RCP 4.5 scenario, which assumes that global emissions will peak in the mid 21st century and decline afterwards, was used for our model. This translates to a warming range of 0.9–2.0 °C between 2046 and 2065, and of 1.1–2.6 °C between 2081 and 2100 (Collins et al., 2013). As limiting constraints, the annual minimum temperature (accounting for the known temperature limit of A. lobifera) and the mean primary productivity (accounting for potentially unsuitable areas with high eutrophication) were applied. This allowed us to 1) model potentially suitable areas for modern specimens of A. lobifera in the Mediterranean Sea, and 2) project future distribution ranges. The future SDM projections include scenarios for 2040–2050 and 2090–2100 and are based on predicted environmental change (Tyberghein et al., 2012; Assis et al., 2018). Maxent 3.4.1 (Phillips et al., 2006) was utilized to model the potential distribution and to project it onto future environmental conditions. The program uses a grid-based machine-learning algorithm following the principles of maximum entropy (Jaynes, 1957). During the modelling process, Maxent starts with a uniform distribution and successively fits it to the data (occurrence records and environmental variables). By iteratively permuting and varying the input variables and features thereof, Maxent repeatedly tests the predictive capability and improves the model. This is measured in the log likelihood or “model gain”, which displays the increasing distance from the uniform distribution (Elith et al., 2011). For a detailed overview on the operating mode of Maxent, the interpretation of its output and its application in ecological studies, see Elith et al. (2011). A total of 10,000 random background points were automatically selected by Maxent within the range of A. lobifera in the Central and Eastern Mediterranean Sea, the Tyrrhenian Sea as well as the Red Sea. Maxent then predicts the relative suitability of the habitat, which is interpreted as the potential distribution of the modelled taxon. The logistic output format with suitability values ranging from 0 (unsuitable) to 1 (optimal) was used (Phillips and Dudík, 2008). In this case, the probability of presence at sites with “typical” conditions is set to 0.5 by default (Elith et al., 2011). A multivariate environmental similarity surface (MESS) analysis was performed, but did not highlight an extrapolation of probability values within the target area, suggesting high confidence for model predictions. The modelling process was performed with 50 replicates and the average predictions across all replicates were used for further processing. Maxent allows for model testing by calculating the Area Under the Curve (AUC), referring to the Receiver Operation Characteristic (ROC) curve (Phillips et al., 2006). It evaluates the ability of the model to distinguish presence from background points. To compute AUC scores, the set of occurrence records were randomly split into training (70%) and test subsets (30%), which were used for model calibration and testing of the predictive performance, respectively. Being non-parametric, this method is recommended for ecological applications (see Langer et al., 2012, 2013). The continuous probability surfaces of the SDMs were subsequently converted into presence/absence maps using the “Equal training sensitivity and specificity logistic threshold” as recommended by Liu et al.

4. Results About 90 native benthic foraminiferal species were recognised: the most common taxa are represented in both algal and sediment samples by the shallow-water genera Peneroplis, Elphidium, Rosalina, Lobatula, Cibicides, Ammonia, Planorbulina and the miliolid genera Quinqueloculina and Triloculina. In algal samples, the epiphytic species (i.e. Lobatula lobatula, Peneroplis pertusus, Rosalina bradyi, Planorbulina mediterranensis and Quinqueloculina disparilis) usually dominate in the assemblages, also showing a higher number of stained tests (Tables S3–S7, supplementary data). In sediment samples, on the contrary, stained tests are less abundant and usually represented by both epiphytic and epifaunal or shallow infaunal taxa (i.e. Elphidium crispum, Elphidium macellum, Ammonia inflata, Ammonia parkinsoniana, Textularia pala and Uvigerina mediterranea); some tests of dead specimens from the shallowest sediment samples are abraded. Noteworthy is the co-occurrence of modern benthic foraminifera with reworked fossil benthic and planktic foraminifera (i.e., Anomalinoides helicinus, Heterolepa bellincionii, Stilostomella monilis, Uvigerina striatissima, nodosariids and the planktic genera Globigerinoides and Globigerina) in sediment samples from the Maltese sites. In most samples, fossil taxa, deriving from the erosion of Miocene strata (from about 25 to about 6 Ma in age) are particularly abundant, well preserved, and often difficult to distinguish from modern dead benthic foraminifera. In these samples, the census count was limited to Rose Bengal stained specimens or dead specimens that were clearly of modern origin. Amphistegina lobifera occurs in most of the sediment samples from the Maltese islands and living specimens of this species were found for the first time in algal and sediment samples from south-eastern Sicily, Pantelleria and Favignana islands (Fig. 2). Other cryptogenic foraminiferal species, namely Amphistegina lessonii, Amphisorus hemprichii, Coscinospira arietina, Coscinospira hemprichii and Sorites orbiculus, were also recorded (Fig. 2; Tables S3–S7, supplementary data). 4.1. Maltese islands Stained specimens of A. lobifera occur in samples from most of the studied localities (Fig. 3, Table S3 supplementary data); the species is absent in only three of the Maltese sites (14-Għadira Bay, 21-Għajn Tuffieħa Bay and 22-Golden Bay; Table S3, supplementary data). Its abundance ranges from 1% to 98%, reaching the highest abundances (> 70%) in the northern part of Malta and between the islands of Comino and Gozo (localities 3, 5, 11, 12, 13, 26, 27, 28 and 31; Fig. 3, Table S3 supplementary data). Amphistegina lobifera is particularly abundant in samples consisting of coarse-grained coralline limestone particles; lowest abundances are recorded in fine-grained substrata (Tables S1 and S3 supplementary data). In all the samples analysed, A. lobifera is usually present with largesized specimens and higher abundances than the congeneric A. lessonii (a cryptogenic species), whose highest abundances (3%–8%) are mostly observed in the northern part of Malta (localities 2, 15, 16, and 19; Table S3 supplementary data). The other cryptogenic species (A. hemprichii, C. arietina, C. hemprichii, S. orbiculus) show similar abundances, from 2% to 8%, and a homogeneous distribution (Fig. 3, Table S3 supplementary data). 4.2. Southern Sicily A total of 18 sites were analysed from 2015 to 2017. In particular, in summer 2015 three sites were sampled (34–36; Table S4 supplementary data), one of which (35-Vendicari) had also been previously studied in summer 2012 by Caruso and Cosentino (2014). In summer 2016 three 4

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Fig. 2. Photomicrographs of Rose Bengal stained and unstained non-indigenous benthic foraminifera recorded in the Sicily Channel. 1-Rose Bengal stained specimen of Amphistegina lobifera; a) umbilical view, b) dorsal view (site 12-Malta). 2- Rose Bengal stained specimen of A. lobifera showing the typical chamber sutures strongly lobulated in both umbilical (a) and dorsal (b) views (site 11Malta). 3- Rose Bengal stained specimen of A. lobifera showing the typical chamber sutures strongly lobulated in both umbilical (a) and dorsal (b) views (site 36-Southern Sicily); 4- Rose Bengal stained specimen of A. lobifera; a) umbilical view, b) profile, c) dorsal view (site 40Southern Sicily); 5- unstained specimen of A. lobifera showing a brownish colour of the last chambers characteristic of the living animal; a) umbilical view, b) dorsal view (site 53-Pantelleria); 6 - Rose Bengal stained specimen of A. lobifera: a) umbilical view, b) profile, c) dorsal view (site 5-Favignana) 7 - Rose Bengal stained specimen of A. lessonii showing a planoconvex test characterized by falciform chamber sutures well visible on the dorsal side: a) umbilical view, b) dorsal view (site 5-Favignana); 8unstained specimen of A. lessonii characterized by a smallsized planoconvex test and typical chamber sutures forming long falciform arcs on the dorsal side, a) umbilical view, b) dorsal view (site 7-Malta); 9- Rose Bengal stained specimen of A. lessonii showing a planoconvex test characterized by falciform chamber sutures well visible on the dorsal side, a) umbilical view, b) dorsal view (site 36-Southern Sicily); 10- unstained small-sized specimen of A. lessonii showing a brownish colour of the last chambers characteristic of live specimens; a) umbilical view, b) dorsal view (site 54-Pantelleria); 11- unstained specimen of Coscinospira arietina (site 11-Malta); 12- Rose Bengal stained specimen of Sorites orbiculus (site 36Southern Sicily). Scale bars are 500 μm. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

orbiculus, A. hemprichii and C. arietina) were recorded, but only at a few localities and usually with very low abundances (< 1%; Fig. 4 and Table S4, supplementary data).

other sites were sampled (37–39; Table S4 supplementary data) and in autumn 2017 twelve sites (40–51; Table S4 supplementary data) were sampled. Two of these last sites (43-Capo Passero and 48-Punta Secca) were also analysed during the previous surveys, respectively in summer 2016 and 2015, allowing temporal comparison. Amphistegina lobifera was not found in 2015 in Vendicari, whereas at the same locality (site 35; Fig. 4) very rare specimens (< 1%) of A. lessonii had been documented in 2012 (Caruso and Cosentino, 2014). Instead, A. lobifera was first recorded in 2016 from one of the three sites studied (38-Island of currents; Fig. 4, Table S4 supplementary data), with relatively low abundance (10–12% on algae and < 1% in sediment). One year later, in 2017, stained specimens (both juveniles and adults) of A. lobifera were recorded at seven of the 12 study sites in algal and sediment samples (sites 41, 42, 43, 44, 45, 46 and 48; Fig. 4, Table S4 supplementary data) with relative abundance varying from 1% to 50%. The highest abundances (35%–50%) were recorded in the southernmost portion of the area, around site 38 (Fig. 4) where the species was found for the first time in 2016; lower abundances were recorded at sites located westward or northward of this region. Amphistegina lobifera and A. lessonii often co-occur in the samples, but the latter always exhibits lower abundances (1%–4%), as well as smaller test sizes. In addition, three other symbiont-bearing taxa (S.

4.3. Pantelleria and Favignana islands and northern Sicily In Pantelleria island, A. lobifera was recorded at all 4 study sites (Table S1, supplementary data), with abundances ranging from 2% to 82%; the highest values (39%–82%) being in the southern and eastern portion of the island (sites 53 and 54; Fig. 5A, Table S5 supplementary data). Although the collected samples were not treated with Rose Bengal, live specimens are easily recognised by the characteristic greenish to brownish colour of cytoplasm and the extrusion of pseudopods (Fig. 2, image 5). Small-sized tests of A. lessonii co-occur with A. lobifera in this area, in both algal and sediment samples, but with low abundances not exceeding 7% (Table S5, supplementary data). Furthermore, C. arietina and S. orbiculus occur with relative abundance of around 1% (Table S5 supplementary data), whereas A. hemprichii and C. hemprichii were not found. In Favignana island, stained specimens of A. lobifera were found for the first time in summer 2018 on algal samples (abundances of 2%–3%) at 2 sites (sites 58-Lido Burrone and 59-Cala del Passo; Fig. 5B, Table S6 5

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Fig. 3. Relative abundances of Amphistegina lobifera and cryptogenic foraminifera (stained and unstained specimens) recorded from the Maltese islands. The geographic coordinates and other details of each site are reported in Table S1 (available online as supplementary data).

The projection onto the RCP4.5 scenario suggests that the overall habitat suitability for A. lobifera in the Mediterranean Sea will increase in 2040–2050 (Fig. 6b). This includes potential range expansions into the western area of the Mediterranean along the coast of northern Africa into the Alboran and Balearic Sea, along the Tyrrhenian coast in Italy, and deep into the Adriatic Sea, following a continuous northwestward dispersal. For the years 2090–2100 (Fig. 6c), the model predicts that habitat suitability will slightly increase westward, into the Alboran Sea and along the Tyrrhenian and Adriatic coasts of Italy (suitability values > 8). Favourable conditions are also predicted for the coasts of northern Albania, Montenegro and Croatia.

supplementary data) at very shallow depths (1–4 m); A. lobifera is absent in sediment samples from the same localities. Amphistegina lessonii and S. orbiculus only occur at one site (59-Cala del Passo), with very low abundances (< 1% and around 2% respectively; Fig. 5B). No amphisteginids were found in north-western Sicily (60-Santa Mangherita and 61-San Vito; Fig. 5C), whereas A. hemprichii and S. orbiculus occur at the two study sites with abundances of about 15% (Fig. 5C, Table S7 supplementary data). Amphisteginids and A. hemprichii are also not yet known from the Aeolian Islands (NE-Sicily, in the Tyrrhenian sea) but S. orbiculus was found to be abundant as an epiphyte on seagrass leaves and algae (Langer, 1988, 1993). 4.4. New distribution models

5. Discussion Based on a previously established occurrence database and the new records presented in this study (Table S2, supplementary data), a new species distribution model for A. lobifera in the Mediterranean Sea was computed. Good AUC values for our model (AUCtraining: 0.7978 and AUCtest: 0.7825 based on 88 training and 37 test records) were obtained. Annual minimum temperature contributed with 64.1% to the model performance. The resulting SDM (Fig. 6a) depicts the highest habitat suitability along the coastal areas of the Levantine Sea as well as the eastern and western Aegean Sea. Medium suitability values that still represent “typical” habitat conditions for A. lobifera can be found along the western coast of Greece, the coast of Albania as well as northern Tunisia. Within the Sicily Channel, habitat suitability is lower and further decreases westward. On the other hand, suitability values > 0.5 can be found along the coast of southern Croatia, western Italy, southern France, eastern and southern Spain, Morocco and Algeria.

5.1. Spatial and temporal patterns and possible spreading vectors Within the Sicily Channel, the non-indigenous species Amphistegina lobifera was first recorded in southern Tunisia in 1979 (Blanc-Vernet et al., 1979), in the Pelagian islands in 2005 (Caruso and Cosentino, 2014), in Malta in 2006 (Yokes et al., 2007) and more recently around Djerba (Tunisia) in 2014 (El Kateb et al., 2018). Our data (Figs. 3–5, Table S1 supplementary data) document the presence of A. lobifera in three new areas: in the south-eastern corner of Sicily along the coast between Catania and Ragusa, and in Pantelleria and Favignana islands. The cryptogenic species Amphistegina lessonii co-occurs with A. lobifera in all the studied sites but with lower abundances (Figs. 3–5, Table S1 supplementary data). This can be explained by the shallow sampling depths used in the present work (down to 23 m, but mostly < 10 m) given that A. lessonii prefers deeper habitats (Mateu-Vicens et al., 6

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Fig. 4. Relative abundances of Amphistegina lobifera and cryptogenic foraminifera (stained and unstained specimens) recorded from Southern Sicily. The geographic coordinates and other sampling details of each site are reported in Table S1 (available online as supplementary data). A) Quantitative data from the sampling surveys performed in 2015; B) Quantitative data from the sampling survey performed in 2016; C) Quantitative data from the sampling survey performed in 2017. A marked increase in the relative abundance and an extension of the geographic distribution of the invasive species A. lobifera is evident when comparing the 2016 and 2017 results.

2009). In south-eastern Sicily A. lessonii was first recorded in 2012 (Caruso and Cosentino, 2014): the present findings from the Maltese archipelago, Pantelleria and Favignana are new records for this species within the Sicily Channel. At present, the occurrence of A. lobifera around Pantelleria and Favignana represents the westernmost limit of its distribution range in the Mediterranean. The colonization process is particularly evident along the coasts of south-eastern Sicily, where within one year, A. lobifera has markedly increased its abundance (from 12% in 2016 to about 50% of the total benthic foraminiferal assemblage in 2017) and colonised a coastal area over 150 km long (Fig. 4). The very high abundance observed around Pantelleria suggests that the species had arrived much earlier than the present (first) record. The new records from Favignana in north-western Sicily indicate an average expansion rate of ∼13.2 km per year (since the opening of the Suez Canal in 1869). This is slightly higher than previous estimates for Mediterranean amphisteginids (Langer et al., 2013) but concordant with expansion rates of other Lessepsian migrants in the Mediterranean Sea (Hiddink et al., 2012). Recently observed range shifts from Malta (Yokes et al., 2007) to the Pelagian Islands (Caruso and Cosentino, 2014) and along the coast of Sicily to Favignana suggest that range expansion rates have increased over the last two decades (∼20 km year−1). A particularly steep warming trend has been recorded in the Mediterranean Sea over the same period (Pastor et al., 2017), suggesting that the northwestern spreading of thermophilic amphisteginids is tracking contemporary climate change.

The present results allow us to hypothesize three different stages of colonization for A. lobifera within the Sicily Channel (Fig. 7): an “early stage” of colonization, where A. lobifera sporadically and rarely occurred (abundance < 20%) at the study sites; a “medium stage” of colonization, where the species was present only at some of the study sites with abundances varying between 20% and 50%; and an “advanced stage”, where A. lobifera was found at most of the study sites with very high abundances (> 50%). In most of the studied sites around Malta and Pantelleria, benthic foraminiferal assemblages are strongly dominated by A. lobifera with abundances that often exceed 80% and a consequent reduction in the relative abundance of native benthic species of foraminifera (Tables S3 and S5, supplementary data). Amphistegina lobifera was already considered as established in Maltese waters based on the records by Yokes et al. (2007), who reported it from four separate localities, but the present work shows that it occurs in very high abundances along virtually all the coasts of the Maltese archipelago and also at Pantelleria. The cryptogenic foraminifera (A. lessonii, A. hemprichii, C. arietina, C. hemprichii and S. orbiculus) are also widespread in the Sicily Channel, where they occur in most of the study sites but always with very low abundances (usually < 5%). This suggests that they lack the adaptive ability of A. lobifera in the colonization of new regions, thus achieving lower invasion success. However these observations are preliminary and further studies are needed to elucidate the role of A. lobifera, A. lessonii and other cryptogenic species in structuring the benthic foraminiferal community. 7

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Fig. 5. Relative abundances of Amphistegina lobifera and cryptogenic foraminifera (stained and unstained specimens) recorded from Pantelleria (A) and Favignana (B) islands, and from Northern Sicily (C). The geographic coordinates and other details of each site are reported in Table S1 (available online as supplementary data). Note that none of the studied samples from Northern Sicily yields Amphistegina lobifera.

Suez Canal to the Eastern Mediterranean Sea (Schmidt et al., 2016). These results suggest that the Mediterranean populations of A. lobifera are well adapted to high temperature and solar irradiation (see also Prazeres et al., 2017; Weinmann and Langer, 2017; Morard et al., 2018). Based on our data, we may also speculate about possible dispersal mechanisms for A. lobifera within the Sicily Channel. Its present distribution and abundance pattern (Fig. 7) indicates that the invasion is proceeding northward, ultimately reaching the southern shores of Sicily at Capo Passero (where A. lobifera was first found in 2016; Table S4 supplementary data), probably favoured by existing surface currents that are directed from the Pelagian and Maltese islands towards Sicily (Ionian Shelf break Vortex; Fig. 1). In addition, A. lobifera has been observed to live epiphytically attached to algal thalli or seagrass leaves and passive transport via floating algae, floating rafts or marine litter (e.g. Finger, 2018) may facilitate its spread over large distances (Saidova, 1961; Katsanevakis and Crocetta, 2014). Other potential dispersal vectors may be involved in this successful case of invasion, such as ichthyochory, as recently proposed by Guy-Haim et al. (2017) who observed living specimens of A. lobifera in fecal pellets of herbivorous rabbitfish.

In the Sicily Channel nothing is known about the actual impact of the A. lobifera invasion on indigenous communities, or on how this small-sized invader may modify habitats altering sedimentation rates with negative effects for sessile organisms such as encrusting macroalgae (Balata et al., 2007, and references therein). Furthermore, in situ observations, meta-analyses and, more recently, epigenetic studies across habitats and taxa have suggested that invasion success is related to the ability of a species to adapt to a wide range of environmental conditions (i.e., phenotypic plasticity; Daehler, 2003; Karatayev et al., 2009; Davidson et al., 2011; Ardura et al., 2017; Cardeccia et al., 2018). Amphistegina lobifera is known to thrive at tropical and subtropical latitudes in the Indo-Pacific region, preferentially at depth < 20 m under mid to high light conditions (Langer and Hottinger, 2000; Triantaphyllou et al., 2012 and references therein). In situ observations performed at the Maldives on Amphistegina populations have documented bleaching of specimens when temperature exceeds 30 °C and solar irradiation is too intense (Spezzaferri et al., 2018), hence causing photodamage in the symbionts. Amphistegina lobifera, in fact, seeks protection beneath algal thalli or reef rubble when light is too strong (Beavington-Penney and Racey, 2004). In some of our sites from southern Sicily, however, we found abundant living specimens of A. lobifera attached to algae, sampled at very shallow depths, from 50 cm to only 5 cm (Fig. 4, sites 42, 44, 45 and 46; Table S4 supplementary data), where radiation can be particularly intense and the SST reach values that exceed 30 °C. A high thermal tolerance of A. lobifera has also been observed in populations introduced via the

5.2. Present and future ranges: implications from SDM for Amphistegina in the Mediterranean Sea The distribution model computed for present-day Amphistegina 8

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Fig. 7. Current geographic distribution and invasion success of Amphistegina lobifera in the Sicily Channel. Note how the invasion of A. lobifera seems to proceed northwards, probably favoured by the surface current circulation of the Modified Atlantic Water (MAW).

with our model predictions. The new records of A. lobifera from the Sicily Channel (this paper), Tunisia (El Kateb et al., 2018), and the southern Adriatic Sea (Langer and Mouanga, 2016) lead to a refinement of the lower temperature tolerances of this species, which survives and thrives close to its current distribution limit. They also provide evidence for a renewed expansion of the range front into the Tyrrhenian Sea and along the coastline of northern Africa (Tunisia). Minimum winter SST has previously been invoked to be among the main agents controlling the latitudinal distribution of amphisteginids (Zmiri et al., 1974; Betzler et al., 1997; Langer and Hottinger, 2000). Rapidly rising sea surface temperatures and the extension of climate belts are likely to alter the range of numerous species (Tittensor et al., 2010). One of the most severely affected areas in the world is the Mediterranean Sea, where range shifts are fuelled in response to temperature increases (Bianchi and Morri, 1994; Lejeusne et al., 2010). In the Western Mediterranean, shallow-water temperature has increased between 0.8 and 4.0 °C over the last 30 years (Prieur, 2002; VargasYanez et al., 2008; Coma et al., 2009). In the Eastern Mediterranean, surface waters have warmed by 1.0 °C over the last 20 years (Theocharis, 2008). The observed range extension of thermophilic amphisteginids thus strongly suggests that the northwestern spread is tracking contemporary SST increase. The decreasing habitat suitability within the Strait of Sicily (Fig. 6a) matches well with the observations from our study area (Fig. 7), showing decreasing numbers of A. lobifera from Malta in the southeast to Favignana in the northwest. The present-day model also predicts suitable habitats along the coast of northern Africa (Algeria, Morocco) and the Alboran Sea. This suggests that besides minimum winter surface temperature, other factors (e.g. dispersal capacity, eutrophication; Weinmann et al., 2013b) restrict the current range of A. lobifera mainly to the Eastern and Central Mediterranean. With ongoing ocean warming, as suggested by the RCP4.5 scenario, it can be expected that A. lobifera has a high potential to colonize wide areas in the Adriatic, Central and Western Mediterranean Sea. As shown by the present study, the establishment of this “hidden invader” may take place within a short time range (see also Langer and Mouanga, 2016 for Albania). Our new SDMs thus highlight potential areas that might be subject to rapid invasions and predict future range expansions of amphisteginids in the

Fig. 6. Species distribution models for A. lobifera under current (6a) and future climates (6b for 2040–2050; 6c for 2090–2100) as projected by Maxent. White triangles represent occurrence records for the computation of the species models (see also Supplementary data, Table S2). Coloured areas highlight habitat suitability, increasing from unsuitable (no colour) to typical (green) and highly suitable (orange). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

lobifera traces current occurrence records of the species very well (Fig. 6a), especially in the Eastern and Central Mediterranean. This includes the shallow coastlines of the Nile Delta, the Levantine Basin (Egypt, Gaza, Israel, Lebanon, Syria, and Cyprus) and coastal areas and islands of the Aegean Sea (Turkey, Greece). Along the coast of northern Africa, A. lobifera has been reported from Egypt, Libya and Tunisia (El Kateb et al., 2018). Additional occurrence records of amphisteginids from Malta (Yokes et al., 2007), Corfu (Zenetos et al., 2010), the Pelagian islands (Caruso and Cosentino, 2014) and the Adriatic Sea (Langer and Mouanga, 2016) show that these fora-NIS have been rapidly spreading northwestward towards the Tyrrhenian and into the Adriatic Sea and provide strong support for range extensions predicted by species distribution models (Langer et al., 2012; Weinmann et al., 2013a, b). Recent reports of A. lessonii from around 500 m water depth from the Ligurian Sea are enigmatic (Di Bella et al., 2019) but in line 9

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Mediterranean Sea.

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6. Final remarks The Mediterranean Sea is a hotspot of global warming where SSTs have increased at a faster rate compared to the global oceans. The warming trend affects biogeographic distributions and is likely to trigger major changes in ecosystem functioning. This study documents that the current range extension of Amphistegina lobifera is tracking contemporary sea-surface temperature increase and isotherm shifts recorded in the Mediterranean Sea (Coll et al., 2010; Lejeusne et al., 2010; Bianchi et al., 2013). Scenarios obtained from species distribution models predict increases in habitat suitability and an ongoing range expansion towards the western Mediterranean and the northern Adriatic Sea. The proliferation and extreme abundances of amphisteginid invaders may locally affect native assemblages of benthic foraminifera whose resilience remains to be determined. Up to a few years ago, the colonization of the Western Mediterranean basin by thermophilic species of Red-Sea origin, such as A. lobifera, was unlikely since the low temperatures (especially during the winter) acted as an oceanographic barrier to dispersal. Our recent findings and the current distribution patterns of A. lobifera within the Sicily Channel demonstrate a rapid spreading of this species towards the Western Mediterranean. Acknowledgements The authors thank J. Pignatti and an anonymous reviewer for helpful comments and suggestions that improved the manuscript. This work is part of a PhD project of the University of Pavia (R. G.) financially supported by FRG-2016 and FFABR funds (to N. M. and A. M., University of Pavia) and by R1D14-PLHA2010_MARGINE (to A. C., University of Palermo). J. E. received financial support from the University of Malta's Research Fund. Collection and study of the material by M. L. and A. W. was supported by the German Science Foundation - Deutsche Forschungsgemeinschaft (DFG; LA 884/10–1). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.ecss.2019.05.016. References Abu Tair, N., Langer, M.R., 2010. Foraminiferal invasions: the effect of Lessepsian migration on the diversity and composition of benthic foraminferal assemblages around Cyprus (Mediterranean Sea). In: FORAMS 2010- International Symposium on Foraminifera, Abstracts with Program. University of Bonn, Bayleydruck GmbH Bonn, pp. 42. Alve, E., Goldstein, S.T., 2003. Propagule transport as a key method of dispersal in benthic foraminifera (Protista). Limnol. Oceanogr. 48 (6), 2163–2170. Alve, E., Goldstein, S.T., 2010. Dispersal, survival and delayed growth of benthic foraminiferal propagules. J. Sea Res. 63 (1), 36–51. Ardura, A., Zaiko, A., Morán, P., Planes, S., Garcia-Vazquez, E., 2017. Epigenetic signatures of invasive status in populations of marine invertebrates. Sci. Rep. 7, 42193. Assis, J., Tyberghein, L., Bosh, S., Verbruggen, H., Serrão, E.A., De Clerck, O., 2018. BioORACLE v2.0: extending marine data layers for bioclimatic modelling. Glob. Ecol. Biogeogr. 27, 277–284. Azzurro, E., Ben Souissi, J., Boughedir, W., Castriota, L., Deidun, A., Falautano, M., Ghaen, R., Zammit-Mangion, M., Andaloro, F., 2014. The Sicily Strait: a transitional observatory for monitoring the advance of non-indigenous species. Biol. Mar. Mediterr. 21 (1), 105–106. Balata, D., Piazzi, L., Benedetti-Cecchi, L., 2007. Sediment disturbance and loss of beta diversity on subtidal rocky reefs. Ecology 88 (10), 2455–2461. Beavington-Penney, S.J., Racey, A., 2004. Ecology of extant nummulitids and other larger benthic foraminifera: applications in palaeoenvironmental analysis. Earth Sci. Rev. 67, 219–265. Betzler, C., Brachert, T.C., Nebelsick, J., 1997. The Warm Temperate Carbonate Province – A Review of the Facies, Zonations, and Delimitations, vol. 201. Courier Forsch.-Inst. Senckenberg, pp. 83–99. Bianchi, C.N., Morri, C., 1994. Southern species in the Ligurian Sea (northern Mediterranean): new records and a review. Boll. dei Musei degli Ist. Biol. dell Univ.

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