A dynamic subtropical coastal hotspot of benthic foraminifera in the Southeastern Mediterranean indicates early-stage tropicalization.

Due to ongoing ocean warming, subtropical environments are becoming accessible to tropical species. Among these environments are the vermetid reefs of the Southeastern Mediterranean (SEM). In the last decades, these valuable coastal habitats witnessed the proliferation of numerous alien species of tropical origin. Among the meiofauna thriving on these reefs are benthic foraminifera, single cell marine organisms that make a significant contribution to global carbonate production. It has been widely recognized that benthic foraminifera, among other invasive species, thrive in the macroalgal cover, and it has been suggested that their populations are becoming a significant new source of sediment substrate. Here, we report on the first systematic assessment of the population size of the benthic foraminifera, allowing a comparison with data from the native tropical habitat of these species. Our study is based on a seasonal sampling of benthic foraminifera from confined sampling areas at four sites along the vermetid reef platforms of the Israeli SEM coast. Our survey reveals a patchy distribution of each species with peak population densities exceeding 100,000 specimens per m2, making the SEM a hotspot of benthic foraminifera, with population densities comparable to tropical coral reef environments. The assemblages of the SEM hotspot are dominated by cosmopolitan foraminiferal taxa and tropical invaders from the Indo-Pacific (e.g., Amphistegina lobifera, Pararotalia calcariformata, soritids, and Hauerina diversa). In contrast to foraminiferal hotspots in the tropics, which are completely dominated by larger symbiont-bearing taxa, the SEM hotspot stands out due to high abundances of non-symbiont-bearing species Textularia agglutinans and small miliolids. An intriguing observation is the significant heterogeneity in composition and density of foraminiferal assemblages between the vermetid reefs' southern and northern areas (Israel), indicating that the productivity of the dominant species are also modulated by local yet unknown environmental factors.

ForCenS-LGM: a dataset of planktonic foraminifera species assemblage composition for the Last Glacial Maximum.

Species assemblage composition of marine microfossils offers the possibility to investigate ecological and climatological change on time scales inaccessible using conventional observations. Planktonic foraminifera - calcareous zooplankton - have an excellent fossil record and are used extensively in palaeoecology and palaeoceanography. During the Last Glacial Maximum (LGM; 19,000 - 23,000 years ago), the climate was in a radically different state. This period is therefore a key target to investigate climate and biodiversity under different conditions than today. Studying LGM climate and ecosystems indeed has a long history, yet the most recent global synthesis of planktonic foraminifera assemblage composition is now nearly two decades old. Here we present the ForCenS-LGM dataset with 2,365 species assemblage samples collected using standardised methods and with harmonised taxonomy. The data originate from marine sediments from 664 sites and present a more than 50% increase in coverage compared to previous work. The taxonomy is compatible with the most recent global core top dataset, enabling direct investigation of temporal changes in foraminifera biogeography and facilitating seawater temperature reconstructions.

The global genetic diversity of planktonic foraminifera reveals the structure of cryptic speciation in plankton.

The nature and extent of diversity in the plankton has fascinated scientists for over a century. Initially, the discovery of many new species in the remarkably uniform and unstructured pelagic environment appeared to challenge the concept of ecological niches. Later, it became obvious that only a fraction of plankton diversity had been formally described, because plankton assemblages are dominated by understudied eukaryotic lineages with small size that lack clearly distinguishable morphological features. The high diversity of the plankton has been confirmed by comprehensive metabarcoding surveys, but interpretation of the underlying molecular taxonomies is hindered by insufficient integration of genetic diversity with morphological taxonomy and ecological observations. Here we use planktonic foraminifera as a study model and reveal the full extent of their genetic diversity and investigate geographical and ecological patterns in their distribution. To this end, we assembled a global data set of ~7600 ribosomal DNA sequences obtained from morphologically characterised individual foraminifera, established a robust molecular taxonomic framework for the observed diversity, and used it to query a global metabarcoding data set covering ~1700 samples with ~2.48 billion reads. This allowed us to extract and assign 1 million reads, enabling characterisation of the structure of the genetic diversity of the group across ~1100 oceanic stations worldwide. Our sampling revealed the existence of, at most, 94 distinct molecular operational taxonomic units (MOTUs) at a level of divergence indicative of biological species. The genetic diversity only doubles the number of formally described species identified by morphological features. Furthermore, we observed that the allocation of genetic diversity to morphospecies is uneven. Only 16 morphospecies disguise evolutionarily significant genetic diversity, and the proportion of morphospecies that show genetic diversity increases poleward. Finally, we observe that MOTUs have a narrower geographic distribution than morphospecies and that in some cases the MOTUs belonging to the same morphospecies (cryptic species) have different environmental preferences. Overall, our analysis reveals that even in the light of global genetic sampling, planktonic foraminifera diversity is modest and finite. However, the extent and structure of the cryptic diversity reveals that genetic diversification is decoupled from morphological diversification, hinting at different mechanisms acting at different levels of divergence.

Continuous reproduction of planktonic foraminifera in laboratory culture.

Planktonic foraminifera were long considered obligate sexual outbreeders but recent observations have shown that nonspinose species can reproduce by multiple fission. The frequency of multiple fission appears low but the survival rate of the offspring is high and specimens approaching fission can be distinguished. We made use of this observation and established a culturing protocol aimed at enhancing the detection and frequency of fission. Using this protocol, we selectively cultured specimens of Neogloboquadrina pachyderma and raised the frequency of reproduction by fission in culture from 3% in randomly selected specimens to almost 60%. By feeding the resulting offspring different strains of live diatoms, we obtained a thriving offspring population and during the subsequent 6 months of culturing, we observed two more successive generations produced by fission. This provides evidence that in nonspinose species of planktonic foraminifera, reproduction by multiple fission is likely clonal and corresponds to the schizont phase known from benthic foraminifera. We subsequently tested if a similar culturing strategy could be applied to Globigerinita glutinata, representing a different clade of planktonic foraminifera, and we were indeed able to obtain offspring via multiple fission in this species. This work opens new avenues for laboratory-based experimental work with planktonic foraminifera.