Progress in Oceanography 210 (2023) 102930 Contents lists available at ScienceDirect Progress in Oceanography journal homepage: www.elsevier.com/locate/pocean Shelled pteropod abundance and distribution across the Mediterranean Sea during spring Roberta Johnson a, *, Clara Manno b, Patrizia Ziveri a, c a Institute of Environmental Science and Technology (ICTA), Universitat Autònoma de Barcelona, Barcelona, Spain b The British Antarctic Survey, Natural Environment Research Council, Cambridge, United Kingdom c Catalan Institution for Research and Advanced Studies (ICREA), Barcelona, Spain A R T I C L E I N F O A B S T R A C T Keywords: Thecosome pteropods are a dominant group of calcifying pelagic molluscs and an important component of the Pteropod food web. In this study, we characterise spring pteropod distribution throughout the Mediterranean Sea, an Mediterranean Sea understudied region for this common group of marine calcifying organisms. This semi-enclosed sea is rapidly Ocean acidification changing under climatic and anthropogenic forcings. The presence of surface water biogeochemical gradients Ocean warming Plankton from the Atlantic Ocean/Gibraltar Strait to the Eastern Mediterranean Sea allowed us to investigate pteropod Foraminifera distribution and their ecological preferences. In the ultra-oligotrophic Eastern Mediterranean Sea, we found the Aragonite mean upper 200 m pteropod standing stock of 2.13 ind. m− 3 was approximately 5x greater than the Western Heliconoides inflatus basin (mean 0.42 ind. m− 3). Where standing stocks were high, pteropods appeared largely in the same family Ecology grouping belonging to Limacinidae. Temperature, O2 concentration, salinity, and aragonite saturation (Ωar) explain 96 % of the observed variations in the community structure at the time of sampling, suggesting that pteropods might show a preference for environmental conditions with a lower energetic physiological demand. We also document that pteropods and planktonic foraminifera have an opposite geographical distribution in the Mediterranean Sea. Our findings indicate that in specific pelagic ultra-oligotrophic conditions, such as the Eastern Mediterranean Sea, different feeding strategies could play an important role in regulating calcifying zooplankton distribution. 1. Introduction state (Caldeira and Wickett, 2003; Gattuso et al., 2015). Calcifying zooplankton, such as pteropods and foraminifera, are sensitive to The Mediterranean region is undergoing rapid changes as a result of changes in seawater carbonate chemistry as they biomineralise their climatic and non-climatic forcings (Cramer et al., 2018; MedECC, 2020) CaCO3 exoskeleton (Bednaršek et al., 2019, 2016; Davis et al., 2017; and is experiencing warming at a rate that exceeds global trends, with Kuroyanagi et al., 2021). Pteropods in particular are known for their atmospheric temperatures rising as much as 20 % faster than the global sensitivity to ocean acidification (e.g. Bednaršek et al., 2019; Bednaršek average (Lazzari et al., 2013; Lionello and Scarascia, 2018). Sea surface et al., 2016; Comeau et al., 2012a; Lischka et al., 2011; Maas et al., 2017; pH is projected to decrease in line with the global average (approxi­ Manno et al., 2012), mainly due to their aragonite shell, which is a more mately 0.3 to 0.4 units by 2100) (Flecha et al., 2015; Geri et al., 2014; soluble form of calcium carbonate compared to other mineral forms such Kapsenberg et al., 2017), or to exceed the global rate of decline (Hassoun as calcite (Mucci et al., 1989). As there are notorious difficulties asso­ et al., 2022; Gemayel et al., 2015). Within this scenario, it is essential to ciated with maintaining pteropods in captivity through a full life cycle improve our knowledge of how Mediterranean marine ecosystems might (Howes et al., 2014; Thabet et al., 2015), field observations are funda­ respond to ocean conditions under climate change and ocean mental to improve the current knowledge on their vulnerability to acidification. climate change and to provide key data on their ecological preferences. Ocean acidification is a direct consequence of the surface ocean Thecosome pteropods are shelled holoplanktic molluscs found in all uptake of carbon dioxide from the atmosphere, resulting in a reduction major world oceans (Lalli and Gilmer, 1989; Peijnenburg et al., 2020). of seawater pH, carbonate ion concentrations, and carbonate saturation These pelagic snails are passive feeders, utilising large mucous webs to * Corresponding author. E-mail address: roberta.johnson@uab.cat (R. Johnson). https://doi.org/10.1016/j.pocean.2022.102930 Received 2 August 2022; Accepted 22 November 2022 Available online 28 November 2022 0079-6611/© 2022 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/). R. Johnson et al. Progress in Oceanography 210 (2023) 102930 Fig. 1. Location map of sampled stations are indicated by dots. The numbers represent the station codes. Research cruise Leg 1: stations 1 to 13, Leg 2: stations 14 to 22. The colour scale corresponds to the satellite-derived surface chlorophyll a concentration (in µg/l), retrieved from MODIS Aqua (L2) (NASA OB.DAAC, 2018), closest day to the start of each new sector, as indicated by each date. Stations: 1 – Atlantic; 2 – Strait of Gibraltar; 3 – Alboran Sea; 5 – Southern Alguero-Balear; 6 – Strait of Sardinia; 7a – Strait of Sicily; 9 – Ionian Sea; 10 – Southern Crete; 11 – Eastern basin; 12 – Nile Delta; 13 – Lebanon; 14 – Antikythera Strait; 15 – Eastern Ionian Sea; 16 – Otronto Strait; 17 – Adriatic Sea; “16–18” – Between Otronto Strait and Central Ionian; 19 – Tyrrhenian Sea; 20 – Northern Alguero-Balear; 21 - Central Alguero-Balear; 22 – Catalano-Balear (Ocean Data View - odv.awi.de; Schlitzer, 2021). Coloured points at each station correspond to different biogeo­ chemical regions (Reygondeau et al., 2017). collect food particles (Lalli and Gilmer, 1989). Pteropods play an (Lessa et al., 2020) and feed on bacteria, phytoplankton, and small important role in both the trophic system and biogeochemical cycling zooplankton using their many, thin pseudopodia which extend out from (Bednaršek et al., 2012b; Buitenhuis et al., 2019; Manno et al., 2010, apertures in their test (Anderson et al., 1979). Investigating the rela­ 2019), linking phytoplankton and larger pelagic predators, such as tionship between pteropods and foraminifera is important as the fore­ carnivorous zooplankton, cephalopods (Fabry, 1989; Lalli and Gilmer, casted change in carbonate chemistry, due to increasing surface ocean 1989), fish (Armstrong et al., 2008; Sturdevant et al., 2012), marine uptake of atmospheric CO2 and ocean acidification, has been shown to birds (Karnovsky et al., 2008) as well as other gymnosomes (Seibel and trigger ecosystem shifts due to altered competition between calcareous Dierssen, 2003). species (Kroeker et al., 2013). The direct comparison of these two major Pteropods make up 1–6.6 % of the total zooplankton community in groups of calcifying zooplankton allows us to improve our understand­ the Mediterranean Sea (Fernández de Puelles et al., 2007; Granata et al., ing of their ecological niches and their sensitivities to environmental 2020; Mazzocchi et al., 2011), yet there are few studies within this re­ change. gion that focus solely on detailed pteropod community distribution (e.g. Howes, 2015; Manno et al., 2019) and those that do are limited to 2. Materials and methods restricted geographical and/or coastal regions. Further, many published studies addressing the entire zooplankton community (Batistić et al., Samples were collected from the Mediterranean Sea during the 2004; Fernández de Puelles et al., 2007; Mazzocchi et al., 2011), or those MedSeA research cruise on R/V Angeles Alvariño from May 2nd to June that include both pteropods and other non-calcifying taxa (Andersen 3rd, 2013 (Fig. 1; Ziveri and Grelaud, 2015). The sampling covered the et al., 1998; Tarling et al., 2001), focus on the direct comparison of few majority of the Mediterranean Sea sub-basins (Fig. 1) and was part of the target pteropod species only, and do not include seawater carbonate European project “Mediterranean Sea Acidification in a changing chemistry data. The thesis manuscript of Rampal (1975) was the first climate - MedSeA”. The main aim of the research cruise was to charac­ study investigating pteropod distribution and ecology across the Medi­ terise the Mediterranean Sea biogeochemistry at the basin scale, focus­ terranean Sea, combining samples collected with different methods and sing on the marine CaCO3 system, and to investigate target calcifying within different seasons and regions. More recently, Bednaršek et al., organisms due to their known vulnerability to increasing CO2 conditions 2012b; Buitenhuis et al., 2013, and Buitenhuis et al. (2019) estimated (Busch et al., 2014; Fox et al., 2020; Goyet et al., 2015; Kroeker et al., the global distribution of pteropods and their importance as CaCO3 2013; Ziveri and Grelaud, 2015). producers by merging a large number of existing and diverse datasets collected globally, as well as in several Mediterranean regions (Bed­ naršek et al., 2012b). To our knowledge, there is no published peer 2.1. Study region reviewed study on pteropod abundance and distribution across the whole Mediterranean basin, covering relatively large biogeochemical The Mediterranean Sea has distinct biogeochemical regions (Rey­ gradients and using a consistent sampling and processing methodology. gondeau et al., 2017), with the sill system of the Strait of Sicily con­ We explore shelled pteropod ecological preferences by investigating necting the Eastern and Western sub-basins (Rohling et al., 2009). It’s their distribution across the Mediterranean Sea at a large spatial scale, anti-estuarine circulation is characterised by surface Atlantic waters spanning the east–west environmental gradient from the Atlantic sur­ entering the Western basin through the Strait of Gibraltar, and by a net face water influx in the Gibraltar Strait, to the Levantine basin in the evaporation, that results in eastward increases in sea surface tempera­ Eastern Mediterranean Sea, and to the North Western Mediterranean Sea ture, salinity, and alkalinity (Fedele et al., 2022; Rohling et al., 2009; during the spring season. We also compare our results with a previous Schneider et al., 2007). In general, the Western basin has higher con­ study by Mallo et al. (2017) which presented the distribution of planktic centrations and production of surface phosphate and nitrate compared foraminifera collected during the same research cruise and in the same to the Eastern basin. The Eastern basin is characterised by ultra- sampling nets as the pteropods of this study. Planktic foraminifera are oligotrophic surface water conditions, including phosphorus limitation calcifying single-celled protists with a calcite shell, and together with (Krom et al., 1991) and deep chlorophyll maxima. The Atlantic- shelled pteropods, constitute the main marine calcifying zooplankton Gibraltar region connects the Mediterranean Sea with the Atlantic groups. They generally reside in the upper 100 m of the water column Ocean through the Strait of Gibraltar (Fig. 1), which is comprised of cooler, less saline waters and relatively higher levels of chlorophyll a 2 R. Johnson et al. Progress in Oceanography 210 (2023) 102930 Table 1 An overview of published pteropod studies in the Mediterranean Sea. Region of Min-max conc. of x conc. (ind. Period of Sampling Water Most Net/mesh Reference Collection pteropods community m¡2 or m3) sampling depth (m) column abundant size (ind. m¡2 or m¡3) depth (m) species/taxa Ligurian and Ind. m¡2 Ind. m¡2 April 1994 Various Various Cavolina BIONESS Andersen Tyrrhenian Seas Study focuses on Day: 0–350 700–2700 inflexa 1 m2 mouth et al., 1998 (NW C. inflexa, C. pyramidata Cavolina inflexa: 0–450 500 μm mesh Mediterranean) and S. subula). 4.0 ± 3.1 0–550 Clio pyramidata: 0–700 Min-max not provided 2.1 ± 2.6 Oblique Styliola subula: haul 0.3 ± 0.8 Night: Cavolina inflexa: 1.7 ± 2.7 Clio pyrimidata: 1.6 ± 0.9 Styliola subula: 0.4 ± 1.5 Southern Adriatic Ind. m¡2 Not provided April 1993 0–50 1242 Heliconoides Nansen Batistić et al., Min: 1 September 50–100 inflatus opening- 2004 Max: 2412 (0–50 m) November 100–200 closing net February 200–300 113 cm June 1994 300–400 diameter 400–600 380 cm length 600–1000 250 μm mesh Vertical haul Balearic Sea Ind. m¡3 Ind. m¡3 1994–2003 75 Various Creseis acicula Bongo-20 Fernández de Only monthly × 5.9 (all year Oblique 78–200 Plankton net Puelles et al., provided. round) haul 100 μm and 2007 Min: 4 ± 6 120 μm Max: 11 ± 6 meshes Ligurian Sea Not provided Ind. m¡2 April-May 0–60 Various Heliconoides BIONESS Granata et al., Day: 2013 60–100 1400–1639 inflatus multinet 2020 C. inflexa: 41.2 100–600 1 m2 mouth C. pyramidata: 9 600–1300 230 μm mesh H. inflatus: 340 Oblique Night: haul C. inflexa: 31.5 C. pyramidata: 1.4 H. inflatus: 9.6 NW Ligurian Sea Ind. m¡3 Ind. m¡3 1967–2003 0–75 ~80 Creseidae Juday Howes et al. Creseidae: ~630 Creseidae: 15.7 (all year Vertical Bogorov net (2015) Cavoliniidae: Cavoliniidae: round) haul 330 μm mesh ~790Limacinidae 13.8 50 (incl. H. inflatus): max Limacinidae: 5.5 cmdiameter 60.8 Tyrrhenian Sea Ind. m¡3 Ind. m¡3 August 2015 Various Various Creseis acicula Bongo-40 (Manno et al., Min: 0.00 C. acicula: 1.48 0–65 to (73–185) 200 μm mesh 2019) Max: 4.02 C. conica: 1.11 0–170 H. inflatus: 1.03 L. trochiformis: 0.64 L. bulimoides: 0.33 Eastern Ind. m¡3 Not provided October - 0–50 Various: N/A WP-3 net Mazzocchi Mediterranean Sicilian Channel: Max. November 50–100 449–4359 113 cm et al., 1997 120 ind. m− 3 1991 100–200 diameter 200–300 200 μm mesh Vertical haul Ligurian Sea Ind. m¡3 Not provided September 0–25 Not provided Cavolina MOCNESS Tarling et al., Study focuses solely on 1997 25–50 inflexa 1 m2 mouth 2001 Cavolina inflexa 50–75 300 μm and Max: x 1.64 (0–200 m) 75–100 2000 μm 100–125 meshes 125–150 150–200 Oblique haul 3 R. Johnson et al. Progress in Oceanography 210 (2023) 102930 due to the influx of water from the Atlantic and Alboran gyre dynamics (Oguz et al., 2014). The northwest Mediterranean region combines the Central and Northern Alguero-Balear basin and Tyrrhenian Sea, and is comprised of warmer and more saline modified Atlantic surface waters compared to the Atlantic-Gibraltar region. The southwest Mediterra­ nean, made up of the Southern Alguero-Balear basin and the shallow Strait of Sicily, is comprised of modified Atlantic surface water moving eastward along the weakening Algerian current (Rohling et al., 2009), resulting in a lower chlorophyll a content than other regions in the Western basin, as well as warmer and more saline waters. The Ionian- Adriatic waters in the Eastern Mediterranean basin are 3–4 ◦ C warmer here than the southwest Mediterranean and are distinctly ultra- oligotrophic. The eastern Mediterranean regions, including the Levan­ tine and Cretan basins, remain ultra-oligotrophic throughout, with wa­ ters gradually increasing in temperature and salinity moving further east. The Adriatic Sea stands apart and is characterized by cooler surface waters than the southern Mediterranean Sea and has a higher chloro­ phyll a content. It is connected to the eastern Mediterranean through the Strait of Otranto into the Ionian Sea. 2.2. Hydrological and chemical collection analyses Temperature, salinity, oxygen and fluorescence (proxy for phyto­ plankton biomass and therefore food availability) for the upper 200 m of the plankton tow stations were obtained from the corresponding conductivity-temperature-depth (CTD) stations using an ITS-90 and an oxygen sensor SBE 43. The overall accuracy for temperature was ± 0.001 ◦ C and ± 0.0003 for salinity. Oxygen concentrations were measured using Winkler iodometric titration (Hansen, 1999) with a Mettler-Toledo with a Platinum ring redox electrode, with an overall Fig. 2. Pteropod standing stocks from stations 1–22 from the western to the accuracy of ± 1.5 µmol kg-1. Samples for phosphate (PO4) and nitrate eastern Mediterranean Sea. Stations are organized according to their respective (NO3) were filtered using a Whatman glass fibre filter (0.7 µm) after biogeochemical region: Atlantic Gibraltar; North-western Mediterranean; South-western Mediterranean; Ionian-Aegean; Adriatic; Levantine-Cretan. collection, then stored at − 20 ◦ C. The final nutrient concentrations were obtained using a Bran + Luebbe3 AutoAnalyzer (detection limits were 0.01 and 0.02 μM for PO4 and NO3 respectively; see Grasshoff and Using the dataset in Bednaršek et al. (2012b), we calculated that our Kremling, 1999; D’Amario et al., 2017 for a detailed methodology of the sampling allows us to characterise approximately 93 % of the total nutrient analysis). Methods for the analysis of water chemistry (based on pteropod abundance (Supplementary Table 1 and Supplementary collected samples for total alkalinity and dissolved inorganic carbon) Fig. 1). However, a small number of species with deeper distribution have been described in Goyet et al. (2015) and Gemayel et al. (2015). might be underestimated in this study and this limitation is considered Ocean chemistry data were input into the software CO2sys v2.1 (van (see below). Heuven et al., 2009) for carbonate system calculation of pHTotal, The plankton towing was performed while the vessel was moving at aragonite saturation (Ωar) and [CO2– approximately 1 nautical knot. A flow meter attached to the ring of the 3 ] using dissolved inorganic carbon (DIC) and total alkalinity (TA) and applying the equilibrium constants of net was used to determine the volume filtered through the net. Please Mehrbach et al. (1973) refitted by Dickson and Millero (1987). Satellite- refer to Appendix Table 1 for information pertaining to the date, time, derived surface chlorophyll a concentration during the sampling period location, environmental parameters and water volume per plankton was obtained from Moderate Resolution Imaging Spectroradiometer sample. From these samples, pteropod standing stocks were determined (MODIS) Aqua L2. We used these data to illustrate the Mediterranean- for each station. Plankton samples were preserved on board in a 4 % wide surface distribution of primary production (NASA OB.DAAC, formaldehyde solution that was buffered with hexamethylenetetramine 2018; Fig. 1). at pH 8.2 and were stored in 500 ml polycarbonate bottles at 4 ◦ C in the dark. The pH of all samples was measured at the beginning, middle, and 2.3. Pteropod sample collection and analyses end of the storing period to ensure that the state of the pteropod shells were not affected by the preservation technique. The samples were Oblique plankton tow sampling for this pteropod study was con­ processed within one month of collection. Pteropod standing stocks ducted using BONGO nets (mesh size 150 μm, 40 cm diameter), inte­ were determined for each station and species were identified and grating the upper 200 m water depth. The net mesh size in this study counted using a Leica z16 APO binocular light microscope. Standing targets the majority of the pteropod community in the upper 200 m of stocks were calculated as absolute abundance (ind. m− 3) and integrated the water column (Bednaršek et al., 2012b), including different life abundance 0–200 m (ind. m2; Table A2). Here, findings are reported as stages (Howes et al., 2014) and therefore allowed for the quantification ind. m− 3 (unless for the purpose of comparison with other studies). We of most of the pteropod community standing stock. Based on a study identified four target families (Limacinidae, Heliconoididae [both in the investigating the global distribution of pteropods, which utilised a very limacinid super family Limacinoidea], Cavoliniidae and Cresidae) and large dataset (25939 data points) that included 41 scientific studies seven species (Heliconoides inflatus, Limacina trochiformis, Limacina (Bednaršek et al., 2012a), it was found that most of the species live in the bulimoides, Cavolina inflexa, Creseis acicula, Creseis conica and Styliola photic zone. In the Mediterranean Sea specifically, Bednaršek et al. subula). The online plankton portal (https://www.planktonportal.org) (2012b) showed that pteropod abundance from depths deeper than 200 was used to aid in the identification of pteropods to species level. m is one order of magnitude lower (mean 0.07 ± 0.89 ind. m− 3) Limacina bulimoides, L. trochiformis, C. acicula and C. conica are compared to the upper 200 m community (mean 0.98 ± 2.77 ind. m− 3). classified as surface and subsurface species (Rampal, 1975). Heliconoides 4 R. Johnson et al. Progress in Oceanography 210 (2023) 102930 inflatus and S. subula can be found at depths larger than 200 m and are 0.02 ind. m− 3 was at the Catalan-Balearic Station (station 22) off the classified as mesopelagic by Rampal (1975), however recent studies coast of Spain (Supplementary Table 2, Fig. 2). A long-term zooplankton show that H. inflatus primarily occurs in the upper water column study reported average pteropod abundances of 5.9 ind. m− 3 in the (Batistić et al., 2004; Granata et al., 2020; Juranek et al., 2003; Schiebel Balearic Sea, however this was for a coastal site with a relatively shallow et al., 2002) while S. subula is more abundant below 150 m (Andersen water depth of 78 – 200 m (Fernández de Puelles et al., 2007; Table 1). et al., 1998). Cavolina inflexa is classified by Rampal (1975) as a Coastal systems are complex and highly dynamic, and likely not repre­ bathypelagic species with a distribution extending below 1000 m, and sentative of the open sea where the samples from this study were this preference for deeper water has been corroborated by more recent collected. A low standing stock was also recorded in the Strait of Sicily studies in the Ligurian Sea (Granata et al., 2020; Sardou et al., 1996; (0.11 ind. m2), however a very high density (120 ind. m− 3) has been Tarling et al., 2001). Due to the strong diel and seasonal variations in the previously noted (Mazzocchi et al., 1997). In terms of biogeochemical depth distribution habitat of some species (Andersen et al., 1998; regions (as identified by Reygondeau et al., 2017, Fig. 1), the Ionian- Rampal, 1975; Tarling et al., 2001), we do not incorporate S. subula and Aegean region had the highest average abundance in the Eastern basin C. inflexa into our statistical analyses of species distribution to discuss (3.05 ind. m− 3; SD = 1.98 ind. m− 3), followed by the Adriatic Sea (2.74 their ecological preferences. This conservative methodological approach ind. m− 3; SD = 3.49 ind. m− 3), which also has the greatest variance is to prevent any artefact related to species depth preferences versus between stations, and then the Levantine-Cretan basins (0.90 ind. m− 3; sampling depth. SD = 0.83 ind. m− 3). A large range in abundance has previously been noted in the Adriatic Sea (Batistić et al., 2004; Table 1). 2.4. Statistical methods The Western basin had consistently lower standing stocks when compared to the Eastern basin, with an average of 0.63 ind. m− 3 (SD = Heliconoides inflatus, L. trochiformis, L. bulimoides, C. acicula and 0.49 ind. m− 3) in the Atlantic-Gibraltar region, 0.25 ind. m− 3 (SD = 0.19 C. conica were investigated in relation to the environmental conditions ind. m− 3) in the south western Mediterranean, and 0.51 ind. m− 3 (SD = at the time of sampling. All environmental parameters used in the an­ 0.47 ind. m− 3) in the north western Mediterranean (Fig. 2). Similar alyses were averaged from 5 to 200 m. A parsimonious Canonical Cor­ average abundances were recorded in the Tyrrhenian Sea (C. acicula – respondence Analysis (CCA) was used to explore the species 1.48 ind. m− 3; C. conica – 1.11 ind. m− 3; H. inflatus – 1.03 ind. m− 3; environmental preferences using the standing stock data. It should be L. trochiformis – 0.64 ind. m− 3; L. bulimoides – 0.33 ind. m− 3), albeit in noted that due to the high collinearity among several environmental shallower waters (73 – 185 m; Manno et al., 2019; Table 1). variables (Supplementary Fig. 2), the variability of the coefficients could The super family Limacinoidea made up 76.4 % of the total pteropod be overestimated (Alves et al., 2017). However, to prevent bias to in­ abundance. Limacinidae was the most abundant family (47.0 %), which dividual parameters, we have included all parameters in the statistical dominated the eastern part of the Mediterranean Sea, followed by Hel­ analysis to widen our power of explanation and to provide as much in­ iconoididae (29.4 %), Creseidae (15.4 %) and then Cavoliniidae (6.8 %). formation as possible about the relationship of species with all the Specimens within the target families that were unidentifiable to species measured environmental variables. level made up 1.4 % of the total abundance. A previous study based on To investigate species groupings across all stations, a K-means cluster pteropod distribution is the seminal work of Rampal (1975) who per­ analysis was conducted until all species significantly contributed to the formed a comparative analysis of abundances within the different cluster formation (ANOVA; < p = 0.5; standing stock values stand­ Mediterranean sectors. Unfortunately, the heterogeneity of the pre­ ardised between − 3 to 3; 10 iterations). The CCA and correlation matrix sented studies (no standardized sampling strategy; samples collected were analysed using R version 3.6.0 (R Core Team, 2020) and the K- using different methods) limited the quantitative approach of this work means cluster analysis was performed using IBM SPSS v23. To run the and the results are not presented in terms of pteropod concentration. environmental parsimonious CCA, the functions cca and ordistep from Howes et al. (2015) is the only study investigating pteropod abundance the “vegan” package were used for the CCA and the permutation test, in the Mediterranean Sea from a time-series over a long-term scale respectively (Oksanen et al., 2019). (1957–2003). This study is solely focused in a shallow water coastal site of the Ligurian Sea (water depth approximately 80 m), and contrary to 3. Results and discussion our results, Limacinidae was the least abundant family, which the au­ thors attributed to a sampling bias. In our study, H. inflatus was the most 3.1. Mediterranean Sea pteropod distribution abundant species in the Mediterranean Sea (29.4 %) and recorded at all stations, followed by L. bulimoides (23.8 %) and L. trochiformis (23.2 %). In our Mediterranean basin-wide study, we found the mean standing H. inflatus has previously been reported as the most common species in stock was 1.27 ± 1.62 (SD) ind. m− 3 (Supplementary Table 2) which specific regions in the Mediterranean Sea (Batistić et al., 2004 – was approximately-five times greater in the Eastern basin (2.13 ind. Southern Adriatic Sea; Granata et al., 2020 - Ligurian Sea). Species m− 3; SD = 0.4 ind. m− 3) compared to the Western basin (0.42 ind. m− 3; belonging to the super family Limacinodea, included H. inflatus, SD = 2.0 ind. m− 3). Mean pteropod standing stocks are comparable to L. bulimoides and L. trochiformis, and followed a similar distribution reported records in studies investigating pteropod communities in pattern with high standing stocks in the Ionian Sea (station 9) and the different Mediterranean Sea regions (e.g. Ligurian Sea, Balearic Sea, Antikythera Strait (station 14) and the Otranto Strait (station 16), while Adriatic Sea, Tyrrhenian Sea; Batistić et al., 2004; Fernández de Puelles there were lower standing stocks in the southwest Mediterranean. et al., 2007; Howes et al., 2015, Fernández de Puelles et al., 2007; C. inflexa (6.8 %), C. acicula (7.7 %) and C. conica (6.8 %) all presented Manno et al., 2019; Table 1). However, all the previous investigations the highest standing stocks in the Eastern Ionian Sea (station 15), while mentioned here (Table 1) differed in sampling methodology (including S. subula (0.63 %) was most abundant at the easternmost station of the different net sizes and sampling depths), in sampling seasons and in Levantine basin (Station 13 Supplementary Table 2). Howes et al. oceanographic settings (mainly from coastal systems rather than open (2015), indicated that the dominant species in each family sea), making a direct comparison between the studies and regions were C. acicula and H. inflatus (previously Limacina inflata), corrobo­ difficult. rating our overall findings. The highest standing stock was recorded in the Otranto Straight A global study showed that pteropod biomass generally peak in the (station 16) toward the southern end of the Adriatic Sea with 5.21 ind. spring in both hemispheres (Bednaršek et al., 2012b), suggesting that m− 3/1041.04 ind. m2 (Supplementary Table 2, Fig. 2). High pteropod total pteropod community abundances reported here may be at their abundances have previously been reported in the Adriatic Sea (2412 ind. peak. This seasonal pattern has also been reported from a long-term m2 0–50 m; Batistić et al., 2004; Table 1). The lowest standing stock of (1994 – 2003) zooplankton time-series study in the Balearic Sea, 5 R. Johnson et al. Progress in Oceanography 210 (2023) 102930 Fig. 3. The results of a K-means cluster based on species standing stocks split the 20 stations within the Mediterranean into 3 clusters. A Cluster dis­ tribution according to the sampling stations, each cluster is characterized by a colour. In this figure, we can see more homogenous communities in the Western Mediterranean and more heterogeneity in the Eastern Mediterranean. Blue circles = cluster 1; orange circles = cluster 2; yellow circles = cluster 3. B Column graph indicating the relative contribution of each species to each cluster. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) where pteropod abundance was highest during late spring (Fernández communities in the Western Mediterranean Sea were more homogenous, de Puelles et al., 2007). In addition, in a coastal region of the Ligurian while there was more variability in community groupings in the Eastern Sea, a distinct Mediterranean biogeochemical region (Reygondeau et al., Mediterranean Sea. Cluster analysis on species standing stocks (Fig. 3) 2017), Howes et al. (2015) observed a species-specific seasonal pattern, shows that cluster 1 makes up the entirety of the Western basin and the with blooms for Limacinid pteropods in both the spring and early central Levantine basin, with overall lower species standing stocks. autumn, while Cresidae bloomed during summer and winter, suggesting Cluster 2 is comprised of only 2 stations (stations 13 and 15) and that different species groups could experience different peaks dominated by family Cresidae. The dominant taxa in cluster 3 belong to throughout the year. In contrast, an inter-comparison of long-term the super family Limacinodea, and is mainly found in the Ionian Sea zooplankton studies in the Mediterranean Sea shows that peaks in (stations 9, 14 and 16). abundance during spring may not be uniform across the region, and that A recent study investigating pteropod trophic dynamics in the overall, late summer to autumn experience the highest annual maxima Southern Ocean suggested that the niche partitioning for groups of (Berline et al., 2012; Skjoldal et al., 2013). Pteropod biomass also ex­ species (between thecosomes and gymnosomes) was likely associated periences seasonal oscillations corresponding to their various life- with anatomical differences, particularly those used for feeding (Wel­ history stages, therefore further Mediterranean-wide investigations drick et al., 2019). The super family Limacinodea (H. inflatus and over different seasons would be important in determining temporal Limacina species) and the super family Cavoliniidae (Creseis species) are differences in pteropod abundance and distribution. evolutionarily and anatomically distinct (Burridge et al., 2017a). Limacinodea are characterised by a coiled shell and Cavoliniidae are characterised by a bilaterally symmetrical conical shell. While these taxa 3.2. Species groupings in the Mediterranean have similar feeding structures, their anatomical differences may lead to one group being more successful or favouring a particular environment We found that mean pteropod standing stocks were not only greater over another, which may in part explain some of the taxonomic clus­ in the Eastern Mediterranean, but this basin also presented high vari­ tering that we see in the Eastern Mediterranean Sea. While we did not ability in pteropod distribution between, and within, the distinct investigate what specific taxonomic differences have led to the clus­ biogeochemical regions. The pteropod populations, when abundant, tering in this study, taxonomic clustering was also observed in the were generally made up of family groups. The Western basin was typi­ Atlantic Ocean between uncoiled and coiled pteropods (Burridge et al., fied by low standing stocks of both the super family Limacinoidea and 2017b). family Cresidae, as was the central Levantine basin in the easternmost Mediterranean Sea (stations 10–12). High numbers of the super family Limacinoidea were associated with lower standing stocks of Cresidae 3.3. Environmental drivers of pteropod distribution (Fig. 3). Where Cresidae was more abundant however, H. inflatus was also present in higher numbers (Fig. 3). Notably, the pteropod The CCA that includes all variables explains 90.8 % (CCA1 – 67.6 %; 6 R. Johnson et al. Progress in Oceanography 210 (2023) 102930 Fig. 4. Triplot of the CCA indicating the relationship between pteropod species (as indicated by species name only) in the Mediterranean Sea and the envi­ ronmental variables. The first CCA (black) shows that NO3 (NO3), PO4 (PO4), fluorescence (Fluores), tem­ perature, salinity, pH, O2 (O2), and Ωar (Aragonite) are affecting 90.8 % (CCA1 – 67.6 %; CCA2 – 23.2 %) of the structure of the observed community at the time of sampling (adj. r2 = 0.32, F = 1.99, p = <0.06). The red text and asterisks indicate the results of parsimonious CCA showing the relationship be­ tween pteropod species in the Mediterranean and the significant environmental variables. Temperature, O2, salinity and Ωar are significantly affecting 96.0 % (CCA1 – 73.6 %; CCA2 – 22.4 %) of the structure of the observed community at the time of sampling (adj. r2 = 0.51, F = 4.14, p = <0.001). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) CCA2 – 23.2 %) of the observed community structure at the time of pteropods (Ωar < 1 - Bednaršek et al., 2019). The pteropod shell is made sampling. CCA1 exhibits positive loadings for O2, pH, salinity and Ωar, of aragonite and therefore changes in Ωar might modulate the net and negative loadings for fluorescence, PO4 and NO3 (Fig. 4). CCA2 calcification process (Bednaršek et al., 2014; Mekkes et al., 2021). exhibits positive loadings for O2 and negative loadings for temperature Further, pteropod distribution is predicted to decline as a result of the (Fig. 4). Temperature, O2, salinity and Ωar are significantly affecting projected global decrease in Ωar (Comeau et al., 2012b). A study in the 96.0 % (CCA1 – 73.6 %; CCA2 – 22.4 %) of the structure of the observed Mediterranean Sea at CO2 vents in the Gulf of Naples investigated community at the time of sampling (adj. r2 = 0.51, F = 4.14, p = <0.001; pteropod abundance along an Ωar gradient (1.9–2.7; Manno et al., 2019) Fig. 4). and found a positive correlation between pteropod abundance and Ωar in The CCA indicates that in the Mediterranean Sea, the distribution of oversaturated conditions, similar to our study. Howes et al. (2017; the super family Limacinodea is predominately driven by specific Ligurian Sea) showed that shells of S. subula were thicker and shells of environmental parameters. In particular, H. inflatus is mainly linked to C. inflexa were denser under higher Ωar conditions when comparing temperature, and L. trochiformis and L. bulimoides more strongly to O2 samples collected from 1910 (Ωar – 3.97) to 2012 (Ωar – 3.4). Similarly, a (Fig. 4). C. acicula is not driven by any significant parameter, but is 50 year long-term Australian study (tropical waters) revealed a signifi­ negatively associated with salinity, Ωar, and O2. Creseis conica does not cant decrease in shell thickness of C. acicula and Diacavolinia longirostris, exhibit a clear pattern, which may be because the standing stock of this coinciding with a decrease in 0.4 Ωar in waters greater than 3.0 Ωar species is too low to statistically identify any solid relationship with the (averaged over 7 sites; Roger et al. 2011). An experiment using over­ environmental parameters. The inverse distribution of family Creseidae, saturated aragonite conditions showed that with a reduction of Ωar and the super family Limacinodea, as indicated by the cluster analysis (control − 2.8; reduced − 2.1 Ωar), H. inflatus calcification rate (Fig. 3), is reflected in the opposite relationship these groups have with decreased, and metabolic rate increased (Moya et al., 2016). Overall, the environmental variables in the Mediterranean Sea (Fig. 4). these studies suggest a high level of sensitivity to carbonate saturation The results indicate that temperature is one of the main factors for pteropods, and even in oversaturated conditions such as the Medi­ modulating shelled pteropod distribution in the Mediterranean Sea, as terranean Sea, variability in Ωar (2.68 – 3.61 here) can generate physi­ observed in previous studies (Beaugrand et al., 2012, North Atlantic; ological stress. While pH, another key parameter of the carbonate Howes et al., 2015, Ligurian Sea; Kacprzak et al., 2017, Barents Sea; system that was not significant here, has also been shown to induce a Thibodeau et al., 2019, Southern Ocean). Indeed, a positive correlation response in pteropods to reduced pH conditions (from pH 8.1 – 7.9 T; between pteropod respiration rates and temperature have been Moya et al., 2016). Increased gene expression involved in acid-base observed in eastern tropical North Pacific, Arctic, and Antarctic ptero­ regulation in pteropods demonstrates that this is an important mecha­ pods under experimental conditions (Comeau et al., 2010; Maas et al., nism for many physiological processes, including calcification (Moya 2012a; Thibodeau et al., 2020). For instance, in the Mediterranean, sea et al., 2016), and shows that impacts on internal pH homeostasis can be surface temperatures (SST) vary by about 10 ◦ C over the course of a year, costly. Due to the collinearity of carbonate chemistry parameters, with winter-summer averages of 12–21 ◦ C and 18–28 ◦ C in the North­ including both pH and Ωar, it is difficult to disentangle their individual west and Southwest Mediterranean, respectively. Therefore, the tem­ effects on pteropod physiology. Nevertheless, pteropods in the Medi­ perature variability of this springtime study is by comparison relatively terranean Sea may show an ecological preference for areas (i.e., the small (14.08 – 18.18 ◦ C) and are temperatures that will likely be expe­ Eastern Mediterranean Sea) with relatively high pH and Ωar, where they rienced at some point over the course of the year for all pteropod pop­ will likely devote less energy to maintaining physiological processes. ulations (Rohling et al., 2009). Given the ongoing rapid warming of the We observed a positive correlation between O2 concentration and Mediterranean Sea, further studies should address the potential impacts L. bulimoides and L. trochiformis distribution. Oxygen is an important of sustained warming on pteropod distribution in this region. driver of pteropod biology and ecology (Bednaršek et al., 2016). The We found that pteropod standing stocks are positively related to Ωar, Mediterranean is in general a well oxygenated sea (Powley et al., 2016), even in waters above critical values of aragonite saturation state for and the O2 measurements collected in this study are within the normal 7 R. Johnson et al. Progress in Oceanography 210 (2023) 102930 Fig. 5. Box plot comparing the abundance distribu­ tion of pteropods (blue) and foraminifera (orange) (ind. m− 3) between the east and west of the Medi­ terranean Sea. Pteropods and foraminifera are inversely distributed within the two major sub-basins of the Mediterranean Sea. The results of the General­ ized Linear Mixed Model indicate that there are sig­ nificant differences between the abundance of both taxa (chisq = 29.27, p < 0.05) including between the Eastern and Western Mediterranean basins (chisq = 5.57, p < 0.05), and also in their interaction (chisq = 4.97, p < 0.05). Note that the scale of foraminiferal abundance is distinctly lower than pteropod abun­ dance. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) range for pteropods (191–233 µmol O2 kg− 1 – well above hypoxic con­ majority of shelled pteropods have a unique feeding behaviour involving ditions for pteropods characterised as < 20 µmol O2 kg− 1 in Manno the production of a large mucous web that is suspended in the water et al., 2017). However, different pteropod species have different O2 column, which passively entraps organic particles and motile organisms, requirements (Maas et al., 2012a), and the positive correlation between enabling them to filter water at high rates (Conley et al., 2018). This L. bulimoides and L. trochiformis, both shallow water species, could feeding method may allow them to overcome low food conditions due to reflect higher oxygen requirements for these limacinid species, and their ability to capture and filter through relatively large amounts of therefore an ecological preference for areas with higher O2 concentra­ organic matter (Hamner et al., 1975). tion compared to other species, such as Clio pyramidata and Creseis vir­ Other factors outside of those measured in this study may affect gula (Maas et al., 2012b), which may be better adapted to experience pteropod community composition. For instance, lateral advection is one lower O2 levels during their vertical migration. of the major physical forcings experienced by marine life and plankton. The results indicate that salinity significantly affected pteropod In the Mediterranean Sea, however, the large-scale surface circulation in distribution in the Mediterranean Sea. Only relatively low salinities the Mediterranean has been described as sub-basin-scale, with meso­ (<33 PSU) have been shown to negatively impact pteropod abundance scale gyres interconnected and bounded by currents and jets (Millot and (Pasternak et al., 2020) and the range of salinity in this study (36.2 – Taupier-Letage, 2012; Rohling et al., 2009). The general circulation flow 39.1 PSU) is within the normal range for most pteropods. For C. acicula can impact coastal regions and heavily influence local current dynamics. however, their preferred salinity is between 28 and 33 ppt based on Mediterranean shelf areas are relatively small and are separated from physiological responses such as oxygen consumption and calcification deeper regions by steep continental shelf breaks. While lateral advection rate (Han et al., 2022), and here this species does exhibit a negative may play a role in pteropod distribution, it is more likely that the coastal relationship with salinity. However, a study investigating the impacts of pteropod populations in the Mediterranean Sea are influenced by coastal ocean acidification and sea water freshening on Limacina retroversa currents and local dynamics rather than the deeper, ocean-like stations found that mortality significantly increased only with a combined of this study. We also investigated the effect of day/night on pteropod decrease in pH and salinity, and it was suggested that high salinities may standing stocks (ANOVA – day/night fixed factor; IBM SPSS v23) and be energetically favourable to pteropods as they are benefited by found there was no significant effect of day/night on total and individual increased buoyancy (Manno et al., 2012). species abundances (Supplementary Table 2). Given that these species Fluorescence (as indicative of food availability) was not a significant primarily occur in the upper water column (above 200 m depth), we parameter affecting pteropod distribution in this study. Fluorescence suggest that the time of day did not play a major role in pteropod species has a weak and slightly negative relationship with the super family distribution here. Limacinodea (76.4 % of total pteropod abundance), which is unexpected as pteropod distribution has been previously correlated with high pro­ 3.4. Pteropod and foraminiferal interaction ductivity (Bednaršek et al., 2012b; Burridge et al., 2017b; Fig. 4). There is an east–west gradient of oligotrophy in the Mediterranean Sea that Planktic foraminiferal standing stocks and distribution data pre­ does not have much seasonal variability (Pasqueron de Fommervault sented in Mallo et al. (2017) were compared to the pteropod data from et al., 2015) and in our study, pteropod abundance was higher in the this study. Pteropod samples from this study and foraminiferal samples ultra-oligotrophic eastern Mediterranean, which accounts for the weak from Mallo et al. (2017) came from the same plankton tow samples and negative correlation to fluorescence. An intercomparison of long-term stations, and were preserved using the same methodology. For a more studies in the Mediterranean also showed an overall negative correla­ detailed description of the foraminiferal collection, preservation and tion between abundance and chlorophyll a (Berline et al., 2012). taxonomic identification methods, please refer to Mallo et al. (2017). To However, the quality of food (in terms of energy), rather than quantity, compare the standing stocks of pteropods and foraminifera within spe­ might be an important factor driving distribution, and further analysis of cific regions of the Mediterranean Sea, we used a generalized linear gut contents would be required to investigate this aspect. Further, the mixed model (GLMM) with a gamma distribution. As the magnitude of 8 R. Johnson et al. Progress in Oceanography 210 (2023) 102930 the count data is very different between pteropods and foraminifera Location and environmental parameters for each station of the cruise. All the parameters are averaged from 5 to 200 m depth. The table includes: Station code, Station name, day (day/month/year), location time (LT), latitude (Lat.), longitude (Long.), bottom depth (m), volume (m3), temperature (Temp. ◦ C), salinity (PSU), fluorescence (Fluor.), pH, aragonite saturation (Ωar), nitrate (NO3), phosphate (PO4), and oxygen (O2). Ωar is a (almost one order of magnitude), it was transformed to logarithmic scale 226.03 191.05 214.19 224.38 212.38 216.91 227.67 211.61 224.16 225.32 222.81 229.53 228.12 229.39 231.22 216.01 212.45 208.91 233.14 210.47 to make standing stocks from both groups comparable. For this analysis, (µmol kg¡1) the Mediterranean Sea was split into two main sub-basins: “Western” O2 stations (1, 2, 3, 5, 6, 7, 19, 20, 21, 22) and “Eastern” stations (11, 12, (µmol 13, 14, 15, 16, 17, 16–18). The GLMM was conducted with R version 0.13 0.22 0.13 0.05 0.15 0.06 0.02 0.03 0.02 0.03 0.03 0.03 0.04 0.05 0.03 0.06 0.07 0.20 0.04 0.17 PO4 L-1) 3.6.0 (R Core Team, 2020) using functions “glm” in the glmmTMB package (Brooks et al., 2017). (µmol The results from the GLMM, comparing the standing stocks of 1.92 4.18 2.08 1.22 2.30 1.35 0.41 1.03 0.58 0.50 0.40 0.37 1.08 1.70 0.90 1.97 1.60 4.01 0.81 3.55 NO3 L-1) pteropods and foraminifera between the two basins (Eastern and Western basins), indicates that there are significant differences between the abundance of both taxa (chisq = 29.27, p < 0.05) between the (µmol kg¡1) Eastern and Western Mediterranean basins (chisq = 5.57, p < 0.05), and 2.70 2.68 2.87 2.97 2.96 3.07 3.44 3.43 3.61 3.56 3.53 3.57 3.40 3.22 3.50 3.40 3.21 3.24 3.03 3.23 Ωar also in their interaction (chisq = 4.97, p < 0.05). These results indicate that an inverse relationship between taxa distribution and the Medi­ 8.06 8.06 8.09 8.10 8.08 8.09 8.12 8.11 8.12 8.11 8.11 8.13 8.12 8.10 8.13 8.11 8.12 8.14 8.11 8.13 pH terranean Sea sub-basins is present (Fig. 5). Pteropod abundance is distinctly greater in the Eastern Mediterranean Sea than in the Western Fluor. (µg Mediterranean Sea. Foraminifera showed a contrasting abundance dis­ tribution (Fig. 5) with higher abundances in the Western Mediterranean 0.36 0.11 0.45 0.18 0.19 0.23 0.13 0.12 0.10 0.15 0.16 0.12 0.15 0.20 0.16 0.14 0.18 0.36 0.17 0.25 L1) Sea than in the Eastern Mediterranean Sea. There have been only a handful of studies that investigate the rela­ tionship between pteropod and foraminiferal distribution. In the West­ Salinity ern Arabian Sea (January – September 1993), the ratio between 36.19 37.20 36.97 37.89 38.13 38.09 38.75 39.04 38.85 39.06 38.96 39.06 39.05 38.81 38.82 38.88 38.29 38.39 37.88 38.39 PSU pteropod and foraminifera abundance shifted throughout the year, indicating an opposing temporal distribution (Mohan et al., 2006). A multi-decadal study at two sites off the coast of Southern California and Temp. Central California showed no relationship between foraminifera or 16.39 14.68 15.43 14.60 14.60 15.40 16.64 16.70 17.73 18.18 17.80 16.90 16.52 15.14 16.34 16.15 15.05 14.08 14.51 14.62 (OC) pteropod abundances (Ohman et al., 2009). In the Gulf Stream, Sargasso Sea and the Gulf of Mexico, pteropod and foraminifera distribution followed a similar pattern, with abundance decreasing closer to oligo­ Volume trophic conditions (Casey et al., 1979). In Schiebel et al. (2001), fora­ 1016 1403 (m3) 537 459 423 447 425 320 372 364 397 334 391 385 440 426 391 356 392 339 miniferal and pteropod abundance in the North Atlantic was positively correlated with chlorophyll-a. In the Arctic Ocean, there was no clear trend between foraminifera and pteropod abundances along a longitu­ Bottom depth dinal transect (Zamelczyk et al., 2021). The results of these studies indicate that the environmental factors that impact pteropod and fora­ 1337 2844 2237 3775 1845 2865 1648 2043 2897 3069 3165 2561 2834 2275 (m) 557 557 469 619 808 970 miniferal abundance and distribution might be distinct. In the Mediterranean Sea, Mallo et al. (2017) found that foraminif­ eral distribution is not strongly linked to carbonate saturation levels as Longitude observed for pteropod distribution in this study (see section 3.3), but − 6◦ 64′ − 5◦ 56′ − 4◦ 19′ 13◦ 19′ 18◦ 29′ 24◦ 27′ 28◦ 00′ 32◦ 00′ 33◦ 23′ 23◦ 42′ 20◦ 81′ 18◦ 84′ 17◦ 25′ 18◦ 52′ 12◦ 52′ 5◦ 55′ 8◦ 69′ 5◦ 67′ 5◦ 95′ 3◦ 32′ instead links more to trophic complexity. Mallo et al. (2017) found that foraminifera distribution was strongly dependent on food availability, and suggested that the lower forami­ Latitude 36◦ 03′ 35◦ 95′ 36◦ 12′ 38◦ 52′ 38◦ 27′ 37◦ 04′ 35◦ 11′ 33◦ 81′ 33◦ 50′ 33◦ 21′ 34◦ 22′ 35◦ 70′ 36◦ 40′ 40◦ 23′ 41◦ 84′ 37◦ 71′ 39◦ 83′ 41◦ 32′ 40◦ 07′ 40◦ 95′ niferal abundance in the Eastern Mediterranean Sea (ultra-oligotrophic sector) results from reduced reproduction due to limiting resources. Planktic foraminifera have lifespans on the scale of weeks to months, and their production is often seasonal, thus peaks and troughs in fora­ 00:03 12:47 20:55 10:44 20:34 00:20 11:31 14:40 13:01 03:14 16:15 21:25 23:49 21:09 09:30 12:30 20:00 10:30 13:55 Time 6:06 (LT) miniferal abundance are often in line with peaks and troughs in phytoplankton biomass (Hernández-Almeida et al., 2011), their main food source. In contrast to foraminifera, pteropod feeding behaviour Day (dd/mm/ 5/11/2013 5/12/2013 5/14/2013 5/15/2013 5/17/2013 5/17/2013 5/21/2013 5/21/2013 5/24/2013 5/23/2013 5/25/2013 5/27/2013 5/29/2013 5/30/2013 5/31/2013 allows them to capture large amounts of organic matter (see prg.3.3) 5/2/2013 5/3/2013 5/4/2013 5/8/2013 5/9/2013 and they are also able to actively swim (Hamner et al., 1975; Lalli and yyyy) Gilmer, 1989) and potentially search for more favourable food condi­ tions. These different feeding strategies indicate that foraminifera are more reliant on sustenance in their immediate surroundings, whereas Station 16–18 pteropods may not be as restricted. Holocene downcore samples from 10 11 12 13 14 15 16 17 19 20 21 22 7a 1 2 3 5 6 9 the North Aegean Sea also indicated that pteropod and foraminifera distribution did not respond similarly to changes in productivity (Gia­ Between Otranto Strait and mali et al., 2021). Further, results from incubation experiments show Northern Alguero-Balear Southern Alguero-Balear that the survival of pteropods does not appear to be affected when Central Alguero-Balear calculated parameter. experiencing prolonged starvation (i.e. Busch et al., 2014; Lischka et al., Eastern Ionian Sea Antikythera Strait Strait of Sardinia Central Ionian 2011). Catalano-Balear Tyrrhenian Sea Southern Crete Strait of Sicily Station name Otranto Strait Eastern Basin Our results show a relationship between pteropod distribution and Adriatic Sea Alboran Sea Ionian Sea Nile Delta Gibraltar several environmental parameters, however it is difficult to determine if Table A1 Lebanon Atlantic there is a single main driver or a combination of drivers. Overall, we suggest that the Eastern Mediterranean basin is more energetically 9 R. Johnson et al. Table A2 Absolute (ind. m− 3), integrated abundance 0–200 m (ind. m2), and relative abundance (%) of pteropods collected from BONGO nets. Western stations are 1-7a, 19–22 and Eastern stations are 9-‘16-18′ . Absolute abundance (individuals m− 3) Station name Station H. inflata L. trochiformis L. bulimoides Limacinidae sp. C. inflexa Cavoliniidae sp. C. acicula C. conica S. subula Creseidae sp. Total Atlantic 1 0.049 0.010 0.038 0.002 0.022 0.000 0.037 0.049 0.010 0.002 0.219 Gibraltar 2 0.196 0.019 0.119 0.006 0.047 0.002 0.065 0.039 0.007 0.002 0.501 Alboran Sea 3 0.523 0.003 0.249 0.008 0.007 0.001 0.154 0.200 0.019 0.011 1.176 S. central W. Med. 5 0.031 0.007 0.026 0.002 0.020 0.002 0.052 0.305 0.015 0.004 0.464 Str. of Sardinia 6 0.026 0.000 0.092 0.007 0.000 0.000 0.007 0.028 0.002 0.002 0.165 Str. of Sicily 7a 0.018 0.056 0.013 0.002 0.022 0.002 0.000 0.000 0.000 0.000 0.114 S. of Ionian Sea 9 1.278 0.475 1.584 0.099 0.056 0.000 0.061 0.054 0.005 0.002 3.614 Off S. Crete 10 0.550 0.394 0.034 0.025 0.019 0.000 0.034 0.013 0.003 0.003 1.075 Eastern Basin 11 0.153 0.027 0.046 0.000 0.005 0.000 0.011 0.003 0.000 0.003 0.247 Off Nile delta 12 0.093 0.038 0.069 0.003 0.025 0.000 0.025 0.014 0.003 0.003 0.272 Off Lebanon 13 0.987 0.063 0.020 0.013 0.018 0.000 0.645 0.191 0.063 0.010 2.010 Antikythera Str. 14 1.677 1.428 1.162 0.042 0.009 0.000 0.072 0.057 0.000 0.000 4.446 E. Ionian Sea 15 0.488 0.327 0.504 0.041 1.440 0.000 0.552 0.601 0.036 0.013 4.003 Otranto Str. 16 0.818 2.353 1.894 0.002 0.016 0.000 0.036 0.034 0.000 0.000 0.270 Adriatic Sea 17 0.066 0.070 0.132 0.052 0.000 0.003 0.000 0.000 0.000 0.000 5.205 N. Ionian Sea 16–18 0.049 0.040 0.019 0.002 0.005 0.000 0.002 0.005 0.002 0.000 0.124 Tyrrhenian Sea 19 0.340 0.445 0.023 0.000 0.018 0.000 0.090 0.064 0.008 0.003 0.990 N-central W. Med. 20 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 Central W. Med. 21 0.120 0.138 0.041 0.000 0.000 0.000 0.102 0.077 0.000 0.003 0.480 Catalano-Balear 22 0.018 0.015 0.000 0.000 0.015 0.000 0.012 0.000 0.000 0.000 0.059 Avg. Western Stations 1-7a, 19–22 0.132 0.069 0.060 0.003 0.015 0.001 0.052 0.076 0.006 0.003 0.417 Avg. Eastern Stations 9-’16-18′ 0.616 0.522 0.546 0.028 0.159 0.000 0.144 0.097 0.011 0.003 2.127 Avg. All Stations 1–22 0.374 0.295 0.303 0.015 0.087 0.000 0.098 0.087 0.009 0.003 1.272 Integrated abundance 0–200 m (individuals m2) 10 Station H. inflata L. trochiformis L. bulimoides Limacinidae sp. C. inflexa Cavoliniidae sp. C. acicula C. conica S. subula Creseidae sp. Total Atlantic 1 9.843 1.969 7.677 0.394 4.331 0.000 7.480 9.843 1.969 0.394 43.898 Gibraltar 2 39.106 3.724 23.836 1.117 9.311 0.372 13.035 7.821 1.490 0.372 100.186 Alboran Sea 3 104.633 0.570 49.893 1.568 1.426 0.143 30.791 40.057 3.849 2.281 235.210 S. central W. Med. 5 6.100 1.307 5.229 0.436 3.922 0.436 10.458 61.002 3.050 0.871 92.810 Str. of Sardinia 6 5.201 0.000 18.440 1.418 0.000 0.000 1.418 5.674 0.473 0.473 33.097 Str. of Sicily 7a 3.579 11.186 2.685 0.447 4.474 0.447 0.000 0.000 0.000 0.000 22.819 S. of Ionian Sea 9 255.529 95.059 316.706 19.765 11.294 0.000 12.235 10.824 0.941 0.471 722.824 Off S. Crete 10 110.000 78.750 6.875 5.000 3.750 0.000 6.875 2.500 0.625 0.625 215.000 Eastern Basin 11 30.645 5.376 9.140 0.000 1.075 0.000 2.151 0.538 0.000 0.538 49.462 Off Nile delta 12 18.681 7.692 13.736 0.549 4.945 0.000 4.945 2.747 0.549 0.549 54.396 Off Lebanon 13 197.481 12.594 4.030 2.519 3.526 0.000 128.967 38.287 12.594 2.015 402.015 Antikythera Str. 14 335.329 285.629 232.335 8.383 1.796 0.000 14.371 11.377 0.000 0.000 889.222 E. Ionian Sea 15 97.698 65.473 100.767 8.184 287.980 0.000 110.486 120.205 7.161 2.558 800.512 Otranto Str. 16 163.636 470.649 378.701 10.390 3.117 0.519 7.273 6.753 0.000 0.000 1041.039 Adriatic Sea 17 13.182 14.091 26.364 0.455 0.000 0.000 0.000 0.000 0.000 0.000 54.091 N. Ionian Sea 16–18 9.859 7.981 3.756 0.469 0.939 0.000 0.469 0.939 0.469 0.000 24.883 Progress in Oceanography 210 (2023) 102930 Tyrrhenian Sea 19 68.031 89.003 4.604 0.000 3.581 0.000 17.903 12.788 1.535 0.512 197.954 N-central W. Med. 20 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 Central W. Med. 21 23.980 27.551 8.163 0.000 0.000 0.000 20.408 15.306 0.000 0.510 95.918 Catalano-Balear 22 3.540 2.950 0.000 0.000 2.950 0.000 2.360 0.000 0.000 0.000 11.799 Western Stations 1-7a, 19–22 26.401 13.826 12.053 0.538 2.999 0.140 10.385 15.249 1.236 0.541 83.369 Eastern Stations 9-’16-18′ 123.204 104.330 109.241 5.571 31.842 0.052 28.777 19.417 2.234 0.676 425.344 All Stations 1–22 74.803 59.078 60.647 3.055 17.421 0.096 19.581 17.333 1.735 0.608 254.357 Relative abundance (%) Station H. inflata L. trochiformis L. bulimoides Limacinidae sp. C. inflexa Cavoliniidae sp. C. acicula C. conica S. subula Creseidae sp. Total Atlantic 1 22.4 4.5 17.5 0.9 9.9 0.0 17.0 22.4 4.5 0.9 0.9 Gibraltar 2 39.0 3.7 23.8 1.1 9.3 0.4 13.0 7.8 1.5 0.4 2.0 Alboran Sea 3 44.5 0.2 21.2 0.7 0.6 0.1 13.1 17.0 1.6 1.0 4.6 (continued on next page) R. Johnson et al. Progress in Oceanography 210 (2023) 102930 Table A3 Absolute (10 ind. m− 3) and relative abundance (%) of foraminifera (all species) Total collected from BONGO nets. Western stations are 1-7a, 19–22 and Eastern sta­ 16.4 14.2 17.5 15.7 20.5 83.6 100 1.1 0.5 3.9 0.0 1.9 0.2 1.8 0.7 0.4 4.2 1.0 1.1 7.9 tions are 9-‘16-18′ . For data regarding individual species of foraminifera, please refer to Mallo et al. (2017). Creseidae sp. Station name Station Total Relative abundance abundance (%) (10 ind. m− 3) 0.0 0.0 0.3 0.0 0.5 0.6 0.9 1.4 0.0 0.1 0.3 1.1 1.0 0.5 0.0 0.3 0.0 0.2 0.2 Atlantic 1 0.985 3.476 0 Gibraltar 2 5.120 18.070 Alboran Sea 3 4.141 14.614 S. subula S. central W. Med. 5 1.460 5.153 Str. of Sardinia 6 0.709 2.502 1.9 0.8 0.0 0.0 1.5 3.3 1.4 0.0 0.1 0.3 0.0 1.0 3.1 0.0 0.9 0.0 0.0 0.5 0.7 Str. of Sicily 7a 1.006 3.550 0 S. of Ionian Sea 9 0.683 2.410 Off S. Crete 10 3.003 10.598 C. conica Eastern Basin 11 0.753 2.657 Off Nile delta 12 0.439 1.549 16.0 18.3 15.0 65.7 17.1 6.5 0.0 0.0 1.5 1.2 1.1 5.1 9.5 1.3 0.6 0.0 3.8 4.6 6.8 Off Lebanon 13 1.689 5.961 0 Antikythera Str. 14 0.898 3.169 E. Ionian Sea 15 0.307 1.083 C. acicula Otranto Str. 16 1.482 5.230 Adriatic Sea 17 0.114 0.402 21.3 12.5 32.1 13.8 11.3 N. Ionian Sea 16–18 0.258 0.911 1.9 9.0 0.0 4.3 0.0 1.7 3.2 4.3 9.1 1.6 0.7 0.0 6.8 7.7 20 Tyrrhenian Sea 19 3.607 12.730 N-central W. Med. 20 0.365 1.288 Central W. Med. 21 0.638 2.252 Cavoliniidae sp. Catalano-Balear 22 0.678 2.393 Avg. Western 1-7a, 1.871 66.028 Stations 19–22 Avg. Eastern Stations 9-’16-18′ 0.963 33.972 0.0 0.0 0.0 0.0 0.2 0.5 0.0 2.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 Avg. All Stations 1–22 1.417 100.000 0 C. inflexa favourable for pteropods due to more favourable environmental condi­ tions (i.e., low energetic physiological demand due to higher Ωar), and 36.0 19.6 0.3 0.0 3.8 1.8 0.0 0.0 3.6 4.2 0.0 1.6 1.7 2.2 9.1 0.9 0.2 7.5 6.8 25 that pteropods may be able to adapt better to the low food availability than foraminifera, which could be due to a combination of both their feeding behaviour, a greater capability to actively move along the water Limacinidae sp. column, and their ability to withstand starvation. 4. Conclusions 0.0 0.6 0.9 1.0 1.0 0.8 1.9 0.0 0.0 0.5 4.3 2.0 2.7 2.3 0.0 1.0 0.6 1.3 1.2 0 Our results provide new insights into pteropod distribution during L. bulimoides spring across diverse biogeochemical regions of the Mediterranean Sea, with particular focus on the two largest Mediterranean basins (Western and Eastern). Spring pteropod standing stocks in the Eastern, and largely 14.5 48.7 15.1 55.7 11.8 43.8 18.5 25.3 26.1 12.6 36.4 25.7 23.8 2.3 0.0 8.5 5.6 3.2 1.0 ultra-oligotrophic sector of the Mediterranean Sea, were 5x greater than 0 in the Western basin. The natural environmental longitudinal gradient across the Mediterranean Sea influences pteropod distribution, and they L. trochiformis may be exhibiting a preference for environments with a lower energy demand, such as regions with higher aragonite saturation levels. During the sampling period, foraminifera and pteropods were inversely 45.0 28.7 16.6 49.0 13.2 36.6 10.9 14.1 32.1 45.2 26.1 32.1 24.5 23.2 0.0 3.1 8.2 1.4 0.0 25 distributed in the Mediterranean, with greater foraminiferal abundance in the Western Mediterranean Sea, a region of greater nutrients and H. inflata surface food availability. We speculate that feeding behaviour, alongside swimming capability, may be factors promoting the observed inverse 31.7 15.7 24.4 39.6 34.4 25.0 15.7 15.7 35.4 51.2 62.0 34.3 49.1 37.7 12.2 29.0 29.4 0.0 6.6 30 distribution. While our findings provide only a snapshot during the spring season, the paucity of pteropod studies in the Mediterranean Sea makes this work important in providing ecological data on pteropod 1-7a, 19–22 Absolute abundance (individuals m− 3) distribution across this entire region. Future studies covering other 9-’16-18′ Station 16–18 seasons, depths, and additional sites would further help to characterise 1–22 20 21 22 10 11 12 13 14 15 16 17 19 7a the pteropod distribution across the Mediterranean Sea over large 5 6 9 temporal scales as a function of environmental forcings, with implica­ tions for their global ecological preferences, life cycle, and impacts on Table A2 (continued ) S. central W. Med. ocean biogeochemistry. N-central W. Med. Western Stations Central W. Med. Eastern Stations Antikythera Str. Catalano-Balear S. of Ionian Sea Tyrrhenian Sea Str. of Sardinia Station name Off Nile delta Eastern Basin N. Ionian Sea E. Ionian Sea Off Lebanon Str. of Sicily Adriatic Sea Otranto Str. Off S. Crete All Stations Declaration of Competing Interest The authors declare that they have no known competing financial 11 R. Johnson et al. Progress in Oceanography 210 (2023) 102930 interests or personal relationships that could have appeared to influence Berline, L., Siokou-Frangou, I., Marasović, I., Vidjak, O., Fernández de Puelles, M.L., Mazzocchi, M.G., Assimakopoulou, G., Zervoudaki, S., Fonda-Umani, S., the work reported in this paper. Conversi, A., Garcia-Comas, C., Ibanez, F., Gasparini, S., Stemmann, L., Gorsky, G., 2012. Intercomparison of six Mediterranean zooplankton time series. Prog. Data availability Oceanogr. 97–100, 76–91. https://doi.org/10.1016/j.pocean.2011.11.011. 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