Description: The transition from benthos to plankton requires multiple adaptations, yet so far it remains unclear how these are acquired in the course of the transition. To investigate this process, we analyzed the genetic diversity and distribution patterns of a group of foraminifera of the genus Bolivina with a tychopelagic mode of life (same species occurring both in benthos and plankton). We assembled a global sequence data set for this group from single-cell DNA extractions and occurrences in metabarcodes from pelagic environmental samples. The pelagic sequences all cluster within a single monophyletic clade within Bolivina. This clade harbors three distinct genetic lineages, which are associated with incipient morphological differentiation. All lineages occur in the plankton and benthos, but only one lineage exhibits no limit to offshore dispersal and has been shown to grow in the plankton. These observations indicate that the emergence of buoyancy regulation within the clade preceded the evolution of pelagic feeding and that the evolution of both traits was not channeled into a full transition into the plankton. We infer that in foraminifera, colonization of the planktonic niche may occur by sequential cooptation of independently acquired traits, with holoplanktonic species being recruited from tychopelagic ancestors

Description: Cruise M140 combined sampling of plankton, mineral dust and other particles in the water column with recovery of data and samples from long-term observational platforms (sediment traps and dust-collecting buoys). The aim of the cruise was to provide new observations to improve our understanding of the ecology of planktonic foraminifera as important carriers of paleoceanographic proxies and to investigate how mineral dust deposition and the production of marine snow and biogenic particle ballast vary in space and time and how they affect the marine biological pump. To this end, the cruise followed a transect in the central western Atlantic between oligotrophic waters of the subtropical gyre and the productive coastal waters off Mauretania affected by coastal upwelling. To characterise population dynamics, ecology and physiology of planktonic foraminifera, we obtained a series of fourteen vertically resolved plankton net profiles along the cruise track, together with profiles of physical and chemical properties of the ambient water masses. Live foraminifera extracted from these profiles were used to quantify photosynthetic activity of selected species and determine their photoadaptation. High-resolution spatial and temporal sampling of the upper 300 m over 24 hours was carried out at two locations (recovering 41 and 46 vertical profiles), allowing the characterisation of patchiness and daily vertical migration of planktonic foraminifera. Moorings with sediment traps monitoring the seasonal and short-term variability of particle fluxes and buoys monitoring atmospheric dust deposition in the region were successfully recovered in the central Atlantic (M3), south of Cabo Verde (M1) and off Mauretania (CB and CBi) and redeployed in the latter two regions to continue the monitoring. Short-term variability of sizes and types of sinking particles in the water column were characterised in each of the monitoring regions with drifting sediment traps and in the Cape Blanc region off Mauretania also with continuous vertical particle camera profile. All aims of the cruise have been met – the plankton sampling and particle characterization studies were carried out successfully and all moorings and buoys could be recovered and/or redeployed as planned.

Description: Diurnal vertical migration (DVM) is a widespread phenomenon in the upper ocean, but it remains unclear to what degree it also involves passively transported micro- and meso-zooplankton. These organisms are difficult to monitor by in situ sensing and observations from discrete samples are often inconclusive. Prime examples of such ambiguity are planktonic foraminifera, where contradictory evidence for DVM continues to cast doubt on the stability of species vertical habitats, which introduces uncertainties in geochemical proxy interpretation. To provide a robust answer, we carried out highly replicated randomised sampling with 41 vertically resolved plankton net hauls taken within 26 hours in a confined area of 400 km2 in the tropical North Atlantic, where DVM in larger plankton occurs. Manual enumeration of planktonic foraminifera cell density consistently reveals the highest total cell concentrations in the surface mixed layer (top 50 m) and analysis of cell density in seven individual species representing different shell sizes, life strategies and presumed depth habitats reveals consistent vertical habitats not changing over the 26 hours sampling period. These observations robustly reject the existence of DVM in planktonic foraminifera in a setting where DVM occurs in other organisms.

Description: Previous genetic studies of extant planktonic foraminifera have provided evidence that the traditional, strictly morphological definition of species in these organisms underestimates their biodiversity. Here, we report the first case where this pattern is reversed. The modern (sub)tropical species plexus Globigerinoides sacculifer is characterized by large morphological variability, which has led to the proliferation of taxonomic names attributed to morphological end-members within the plexus. In order to clarify the taxonomic status of its morphotypes and to investigate the genetic connectivity among its currently partly disjunct (sub)tropical populations, we carried out a global survey of two ribosomal RNA regions (SSU and ITS-1) in all recent morphotypes of the plexus collected throughout (sub)tropical surface waters of the global ocean. Unexpectedly, we find an extremely reduced genetic variation within the plexus and no correlation between genetic and morphological divergence, suggesting taxonomical overinterpretation. The genetic homogeneity within the morphospecies is unexpected, considering its partly disjunct range in the (sub)tropical Atlantic and Indo-Pacific and its old age (early Miocene). A sequence variant in the rapidly evolving ITS-1 region indicates the existence of an exclusively Atlantic haplotype, which suggests an episode of relatively recent (last glacial) isolation, followed by subsequent resumption of unidirectional gene flow from the Indo-Pacific into the Atlantic. This is the first example in planktonic foraminifera where the morphological variability in a morphospecies exceeds its rDNA genetic variability. Such evidence for inconsistent scaling of morphological and genetic diversity in planktonic foraminifera could complicate the interpretation of evolutionary patterns in their fossil record.

Description: Sedimentary specimens of the planktonic foraminifera Globorotalia inflata can provide much needed information on subsurface conditions of past oceans. However, interpretation of its geochemical signal is complicated by possible effects of cryptic diversity and encrustation. Here we address these issues using plankton tow and sediment samples from the western South Atlantic, where the two genotypes of G. inflata meet at the Brazil-Malvinas Confluence Zone. The δ18O and δ13C of encrusted specimens from both genotypes from a core within the confluence zone are indistinguishable. However, we do find a large influence of encrustation on δ18O and Mg/Ca. Whereas crust Mg/Ca ratios are at all locations lower than lamellar calcite, the crust effect on δ18O is less consistent in space. Plankton tows show that encrusted specimens occur at any depth and that even close to the surface crust Mg/Ca ratios are lower than in lamellar calcite. This is inconsistent with formation of the crust at lower temperature at greater depth. Instead we suggest that the difference between the crust and lamellar calcite Mg/Ca ratio is temperature-independent and due to the presence of high Mg/Ca bands only in the lamellar calcite. The variable crust effect on δ18O is more difficult to explain, but the higher incidence of crust free specimens in warmer waters and the observation that a crust effect is clearest in the confluence zone, hint at the possibility that the difference reflects advective mixing of specimens from warmer and colder areas, rather than vertical migration.

Description: The eastern Mediterranean is a hotspot of biological invasions. Numerous species of Indo-pacific origin have colonized the Mediterranean in recent times, including tropical symbiont-bearing foraminifera. Among these is the species Pararotalia calcariformata. Unlike other invasive foraminifera, this species has been discovered only two decades ago and is restricted to the eastern Mediterranean coast. Combining ecological, genetic and physiological observations, we attempt to explain the recent invasion of this species in the Mediterranean Sea. Using morphological and genetic data, we confirm the species attribution to P. calcariformata McCulloch 1977 and identify its symbionts as a consortium of diatom species dominated by Minutocellus polymorphus. We document photosynthetic activity of its endosymbionts using Pulse Amplitude Modulated Fluorometry and test the effects of elevated temperatures on growth rates of asexual offspring. The culturing of asexual offspring for 120 days shows a 30-day period of rapid growth followed by a period of slower growth. A subsequent 48-day temperature sensitivity experiment indicates a similar developmental pathway and high growth rate at 28°C, whereas an almost complete inhibition of growth was observed at 20°C and 35°C. This indicates that the offspring of this species may have lower tolerance to cold temperatures than what would be expected for species native to the Mediterranean. We expand this hypothesis by applying a Species Distribution Model (SDM) based on modern occurrences in the Mediterranean using three environmental variables: irradiance, turbidity and yearly minimum temperature. The model reproduces the observed restricted distribution and indicates that the range of the species will drastically expand westwards under future global change scenarios. We conclude that P. calcariformata established a population in the Levant because of the recent warming in the region. In line with observations from other groups of organisms, our results indicate that continued warming of the eastern Mediterranean will facilitate the invasion of more tropical marine taxa into the Mediterranean, disturbing local biodiversity and ecosystem structure.

Description: The use of planktonic foraminifera in paleoceanographic studies relies on the assumption that morphospecies represent biological species with ecological preferences that are stable through time and space. However, genetic surveys unveiled a considerable level of diversity in most morphospecies of planktonic foraminifera. This diversity is significant for paleoceanographic applications because cryptic species were shown to display distinct ecological preferences that could potentially help refine paleoceanographic proxies. Subtle morphological differences between cryptic species of planktonic foraminifera have been reported, but so far their applicability within paleoceanographic studies remains largely unexplored. Here we show how information on genetic diversity can be transferred to paleoceanography using Globorotalia inflata as a case study. The two cryptic species of G. inflata are separated by the Brazil-Malvinas Confluence (BMC), a major oceanographic feature in the South Atlantic. Based on this observation, we developed a morphological model of cryptic species detection in core top material. The application of the cryptic species detection model to Holocene samples implies latitudinal oscillations in the position of the confluence that are largely consistent with reconstructions obtained from stable isotope data. We show that the occurrence of cryptic species in G. inflata, can be detected in the fossil record and used to trace the migration of the BMC. Since a similar degree of morphological separation as in G. inflata has been reported from other species of planktonic foraminifera, the approach presented in this study can potentially yield a wealth of new paleoceanographical proxies.

Description: Invasive species allow an investigation of trait retention and adaptations after exposure to new habitats. Recent work on corals from the Gulf of Aqaba (GoA) shows that tolerance to high temperature persists thousands of years after invasion, without any apparent adaptive advantage. Here we test whether thermal tolerance retention also occurs in another symbiont-bearing calcifying organism. To this end, we investigate the thermal tolerance of the benthic foraminifera Amphistegina lobifera from the GoA (29° 30.14167 N 34° 55.085 E) and compare it to a recent "Lessepsian invader population" from the Eastern Mediterranean (EaM) (32° 37.386 N, 34°55.169 E). We first established that the studied populations are genetically homogenous but distinct from a population in Australia, and that they contain a similar consortium of diatom symbionts, confirming their recent common descent. Thereafter, we exposed specimens from GoA and EaM to elevated temperatures for three weeks and monitored survivorship, growth rates and photophysiology. Both populations exhibited a similar pattern of temperature tolerance. A consistent reduction of photosynthetic dark yields was observed at 34°C and reduced growth was observed at 32°C. The apparent tolerance to sustained exposure to high temperature cannot have a direct adaptive importance, as peak summer temperatures in both locations remain 〈32°C. Instead, it seems that in the studied foraminifera tolerance to high temperature is a conservative trait and the EaM population retained this trait since its recent invasion. Such pre-adaptation to higher temperatures confers A. lobifera a clear adaptive advantage in shallow and episodically high temperature environments in the Mediterranean under further warming.

Description: The transition from benthos to plankton requires multiple adaptations, yet so far it remains unclear how these are acquired in the course of the transition. To investigate this process, we analyzed the genetic diversity and distribution patterns of a group of foraminifera of the genus Bolivina with a tychopelagic mode of life (same species occurring both in benthos and plankton). We assembled a global sequence dataset for this group from single-cell DNA extractions and occurrences in metabarcodes from pelagic environmental samples. The pelagic sequences all cluster within a single monophyletic clade within Bolivina. This clade harbors three distinct genetic lineages, which are associated with incipient morphological differentiation. All lineages occur in plankton and benthos, but only one lineage shows no limit to offshore dispersal and has been shown to grow in the plankton. These observations indicate that the emergence of buoyancy regulation within the clade preceded the evolution of pelagic feeding and that the evolution of both traits was not channeled into a full transition into the plankton. We infer that in foraminifera, colonization of the planktonic niche may occur by sequential cooptation of independently acquired traits, with holoplanktonic species being recruited from tychopelagic ancestors.