**5. Discussion**

## *5.1. Ecological and Oceanographic Context of the Planktonic Foraminiferal Biogeographic Distribution in Adriatic and Ionian Basins*

Changes in oceanographic parameters could lead to a geographic offset among modern planktonic associations that may lead to differential abundance patterns and/or shell mass variability towards the optimum growth conditions, modifying the size spectrum of the entire population [20,21,24,49,89,107]. Therefore, the assessment of the dominant environmental parameters controlling the planktonic foraminiferal communities within the Mediterranean Sea, such as SST, SSS, and PP [8,28,89,108,109], along with their correlation with the ecological characteristics of the identified species are crucial for explaining the offsets mentioned above.

Although the Adriatic and the Ionian sub-basins are quite similar from the faunistic point of view, some differences seem to exist regarding the abundance of the most significant species. Both sub-basins are dominated by *G. bulloides* and *G. ruber* (w), which exhibit an antagonistic faunal pattern. The maximum abundance peaks of *G. ruber* (s.s. and s.l.) are coincident with minimum relative peaks of *G. bulloides* in the Ionian basin, while the opposite trend is recorded for the Adriatic Sea (Figure 3), indicating the partly replacement between these species in the planktonic fauna. The high percentages of the opportunistic species *G. bulloides* are controlled by phyto- and zoo-plankton blooms [22] mainly attributed to the fertilizing effect to the Po River discharge waters and additional local eastern Italian freshwater inputs in the south Adriatic Sea. On the contrary, relative abundance of this species gradually decreases within the Ionian Sea, where the plume waters lose their characteristic features when mixed with other south-eastern Mediterranean surface waters. *Globigerinoides ruber* is evenly abundant by showing a continuous presence throughout the study transect, due to its ability to withstand large fluctuations in temperature and salinity of the water column [22,110]. Its slightly higher contribution (including both morphotypes) in the Ionian basin (Figure 3) could be attributed to more favorable (compared to those of the Adriatic Sea) conditions for its flourishment in the more oligotrophic water column. We highlight that such growth optimum conditions based on depth habitat preference and environmental parameters would certainly help to explain the observed regionally variable abundance patterns of the analyzed morphotypes.

The observed dominance of the normal morphotype in central Mediterranean subbasins possibly is due to its depth and ecological characteristics. *G. ruber* s.s. has a very constant depth habitat (top 30–50 m; [99,111,112]) and prefers a temperature- and salinitystratified environment [113], which in the study area is attained by the halocline due to riverine inputs and/or the seasonal thermocline due to surface warming during late spring to early fall. The less abundant *G. ruber* s.l. reaches its highest percentages in sample GeoB 10,718 south of the strait of Otranto and at sites H02, H03, and H-05 in the central-eastern part of the Ionian basin, where recurrent or transient small-scale cyclonic and anticyclonic gyres are formed and enhance the primary productivity (eastern Ionian bloom of D'Ortenzio, et al. [114]), which primarily controls its distribution [21,100]. The intermittent nature of these localized blooms (known as "intermittently blooming areas" of D'Ortenzio and Ribera d'Alcalà [115]) due to their pronounced interannual variability in the spatial shape and timing [114], in combination with the seasonal control of primary

production trapped at the subsurface Deep Chlorophyll Maximum (DCM) layer [116], which is estimated to be at times even more important than surface production in such oligotrophic setting [117], could be considered the most plausible explanations for their slight record in the satellite-sensed Chl-a data in the study area [114,115]. Moreover, satellite data provide no information on subsurface production, which is known to be important in the eastern part of the Mediterranean and does not always match the timing of surface Chl-a peaks [118] (Figure 4).

**Figure 4.** (**A**) Chlorophyll-a (Chl-a), (**B**) sea surface temperature (SST), and (**C**) sea surface salinity (SSS) distribution map for the study area.

However, the additional factors of heterogeneous bathymetry and distance from the coast could not be omitted as they have a large influence on the distributional abundance pattern of this morphotype, as have already been indicated for the Adriatic [85] and the Aegean Sea [21]. Given the above factors, the observed distributional pattern of *G. ruber* s.l. could be correlated with a relevant trend to deeper habitats at these sites. As the nutrient content decreases offshore [77,119], this regime causes unfavorable conditions for this species, reflected by even more reduced percentages of the most productivity-sensitive morphotype Elongate (belonging to *G. ruber* s.l.). Consequently, the representatives of *G. ruber* s.l. are adapted to a different depth habitat, possibly beneath the halocline or deeper in the mixed layer to avoid the highly stratified and oligotrophic surface waters.

Besides the two abundant aforementioned species, most of the species that live in the central Mediterranean are surface/sub-surface symbiont bearing species (e.g., *G. ruber rosea, G. rubescens, O. universa, G. siphonifera, T. trilobus*) each one displaying percentages up to ~10%, while important components in some places are also the productivity- and stratification-related indicators, such as *N. pachyderma, G. inflata, T. quinqueloba,* and *G. glutinata* [1,120]. The significant cumulative percentage (up to 30%) of symbiont-bearing species seems to reflect the ability of this group to cope with the oligotrophy of the study area. Particularly, *G. ruber rosea* and *G. rubescens* thrive in a warmer and overall, more oligotrophic and stratified water column [28,103,121], and *T. trilobus* dwells in warm, oligotrophic to mesotrophic waters but prefers less salty superficial waters [95,122]. *Orbulina universa* is usually abundant in (sub)tropical to temperate waters and tolerates a wide range of salinity and temperature [47,95]. Its increased percentages in the Adriatic and Ionian sites could be interpreted as an increase in depth and possibly the extent of the thermocline. In only some locations (e.g., samples H-11, GeoB 10729), these species are replaced by asymbionts (e.g., *T. quinqueloba, G. bulloides*) and some deeper dwellers, mostly by *N. pachyderma* and *G. inflata*, that are associated with deep winter mixing and generally more productive environments [22,95,123]. The relatively low percentages of *G. inflata* and its general displacement from the Ionian to the Adriatic basin could be explained by the fact that this species is less frequent or absent in warmer, stratified, and nutrient-depleted regions of the Mediterranean than in more productive areas (e.g., western Mediterranean; [22,109]). The same applies to *T. quinqueloba*, which maintains a residual presence in the study area, since its ecological preferences are mostly linked to cold and very productive surface waters [103,124]. The cosmopolitan species *G. glutinata* comprises significant percentages up to ~10% of the assemblage composition since it is able to survive both in oligotrophic and mesotrophic environments [125] due to its dual behavior related to diet requirements, being thus very sensitive to changes in productivity [42,126], while it is not dependent on temperature, salinity or depth [1]. Its presence in the Mediterranean Sea has been attributed to the spring bloom, triggered by the increased nutrients at the end of the winter mixing and increased solar irradiation [22,127].

#### *5.2. On the Environmental Component on the Latitudinal Size Variability*

The average maximum diameter (282 µm) of the central Mediterranean (excluding the Tyrrhenian Sea) assemblages is comparable with that of the eastern Mediterranean (279 µm; [24]), but slightly lower than that reported for subtropical assemblages on a global scale (309 µm; [37]). The ~8% offset in planktonic size could be considered reliable due to the more oligotrophic nature of higher water density in the marginal Mediterranean Sea compared to the global open ocean. Although tolerance limits of modern foraminifera are not completely defined, the progressive increase in test size is initially believed to be related to ecological optimum conditions [37,128–130]. Nevertheless, we note that the majority (apart from Schmidt et al. [37] who analyzed 69 Holocene samples worldwide) of the studies supports the optimum-size hypothesis focused on sediment samples collected within a single oceanic basin [31,131–135], reflecting a limited part of the biogeographical range of each species.

Most shell-mass-related studies have shown that the planktonic foraminiferal shell size increase with seawater temperature (e.g., [38]). In the case of the central Mediterranean basin, the increase in sea surface temperature from the Adriatic to the southernmost Ionian sites (Figure 4) could partly explain the average 11% increase observed in most of the species. However, this trend does not exist for the most dominant species, since both *G. bulloides* and *G. ruber* (w; s.s. and s.l.) present larger tests at higher latitudes. The decreasing trend with latitude of these two species is quite similar to that (~10% decrease towards the Levantine basin) reported by Zarkogiannis et al. [24] for the eastern sector of the Mediterranean Sea, indicating the latitudinal influence on these species within the entire Mediterranean Sea. This finding is also supplemented by the recent observations of Mallo et al. [81] showing a W-E difference in size of the same species (more extreme in *G. ruber* than *G. bulloides*, as similarly observed in our N-S transect), with the western basin hosting the largest individuals, while the gradual decrease in shell size occurs in the Tyrrhenian, eastern Ionian and finally in Levantine basin. Both latitudinal and longitudinal trends clearly reveal that the most abundant and paleoceanographically significant species for the Mediterranean Sea are possibly driven by environmental forces, beyond the SST, in terms of the specific hydrographic dynamics of each sub-basin within the Mediterranean Sea. Our findings are consistent with the observations of Rillo et al. [136] highlighting that SST does not always explain shell size variations, and further show that contrasting results can be obtained when analyzing intra-specific size patterns, even in a narrower geographical range as that one adopted here. Furthermore, given the species-specific size variability presented for the first time here, this study could be considered as a pioneer since it fills the gap characterized by the lack of studies testing the intraspecific consistency of the optimum-size hypothesis.

Nutrient availability can mediate the temperature-size relationships observed in the plankton communities and has been shown to affect planktonic foraminifera size [136,137]. More explicitly, enhanced food availability in the water column facilitates faster cell growth and larger final shell size [138,139]. On a global scale, surface primary productivity is strongly correlated with plankton size. Below the value of 150 g C m−<sup>2</sup> yr−<sup>1</sup> there is a positive relationship, while above this threshold the cell size decreases with increasing primary productivity [37]. Within the low-productivity ecosystem of the Mediterranean Sea (<150 g C m−<sup>2</sup> yr−<sup>1</sup> ; [140]) it would be expected shell size to be increased with productivity. According to the current and the already known from the literature's Mediterranean dataset, the above size-productivity relationship is evident for several species, mostly the symbiont-barren taxa, and is more pronounced in a longitudinal way. For instance, *O. universa* presents larger size fractions in the eutrophic upwelling areas from the Atlantic to the Strait of Sicily [89], relatively intermediate-sized shells in mesotrophic-to-oligotrophic Adriatic and Ionian basins (this study) and lowermost sizes into the ultra-oligotrophic eastern Mediterranean basin [24]. Into the general oligotrophic Adriatic and Ionian settings, *G. ruber* and other photosymbiotic species seem to have an advantage due to their symbionts which they use as an ecological strategy to survive in nutrient-limited environments [141]. The relatively stable shell sizes reported between Adriatic and Ionian domains of the most abundant species *G. ruber* s.s. (229 vs. 223 µm; Table 2) and *G. bulloides* (227 vs. 217 µm; Table 2) clearly support this concept. Moreover, the fact that these species were developed almost equally in size, presenting size structure values around roughly 220 µm, indicates that they possibly reach the optimum environmental conditions for the study area. The less abundant species (e.g., *G. ruber* s.l., *G. ruber rosea*, and *G. rubescens*), which are usually influenced by the competition with more abundant co-occurring species, present significant size variability and thereby reach their highest shell sizes in sub-optimal conditions. The comparison between the average intraspecific shell sizes for the central and the eastern basins (Table 3) points toward which species reaches the optimum or sub-optimum conditions and in which basin exactly within the Mediterranean setting. We nonetheless note that an additional N-S transect in the western Mediterranean, where the

eutrophic species dominate, is needed to complete full geographic coverage of the shell differentiation into the entire Mediterranean Sea.

**Table 3.** Average population size of the identified planktonic foraminifera species within the Central Mediterranean (this study) and comparison with the Eastern Mediterranean basin [24]. The number of sampling locations that each species was encountered is also shown together with the total number of specimens counted. nd: not determined.

