New observations on test architecture and construction of Jullienella foetida Schlumberger, 1890, the largest shallow-water agglutinated foraminifer in modern oceans.

We present new observations on Jullienella foetida Schlumberger, 1890, a giant agglutinated foraminifer with a leaf- or fan-like test reaching a maximum dimension of 14 cm, that is common on some parts of the west African continental shelf. The test wall comprises a smooth, outer veneer of small (<10 µm) mineral grains that overlies the much thicker inner layer, which has a porous structure and is composed of grains measuring several hundreds of microns in size. Micro-CT scans suggest that much of the test interior is filled with cytoplasm, while X-ray micrographs reveal an elaborate system of radiating internal partitions that probably serve to channel cytoplasmic flow and strengthen the test. Jullienella foetida resembles some xenophyophores (giant deep-sea foraminifera) in terms of test size and morphology, but lacks their distinctive internal organization; the similarities are therefore likely to be convergent. Based on micro-CT scan data, we calculated an individual cytoplasmic biomass of 3.65 mg wet weight for one specimen. When combined with literature records of seafloor coverage, this yielded an estimate of >7.0 g wet weight m-2 for the seafloor biomass of J. foetida in areas where it is particularly abundant. The relatively restricted distribution of this species off the north-west African coast at depths above 100 m is probably related to the elevated, upwelling-related surface productivity along this margin, which provides enough food to sustain this high biomass. This remarkable species appears to play an important, perhaps keystone, role in benthic ecosystems where it is abundant, providing the only common hard substrate on which sessile organisms can settle.

Effects of sampling site, season, and substrate on foraminiferal assemblages grown from propagule banks from lagoon sediments of Corfu Island (Greece, Ionian Sea).

Foraminiferal propagule banks occur in fine sediment fractions that contain small individuals of benthic foraminifera. These sediments include locally sourced juveniles and propagules, as well as allochthonous propagules that have dispersed from surrounding areas. Such propagules can remain viable even under unfavorable local conditions. When exposed to more favorable conditions, they may grow to adult stages. Accordingly, during environmental changes, propagule banks have the potential to function as species pools and allow quick assemblage reactions. The propagule method was designed to study responses of foraminiferal assemblages by exposing propagule banks to controlled conditions in the laboratory, an approach that is applicable to a variety of ecological questions. Therefore it is important to understand the nature and dynamics of propagule banks, including local and seasonal influences. To obtain insights into the composition of local propagule banks, we studied experimentally grown assemblages from two shallow-water lagoons on Corfu Island in western Greece, and compared the results with in situ assemblages. We sampled in spring and autumn of 2017 and experimental treatments included the use of different substrates in our experiments to account for potential effects on assemblage compositions. Results revealed that sediments from each lagoon contained a distinct propagule bank. We found abundant allochthonous taxa among specimens grown in all experimental treatments, indicating dispersal of propagules, and possibly also juveniles, from adjacent regions into both lagoons. The time of sampling had a significant effect on experimental assemblages, indicating that the composition of propagule banks can vary throughout the year. However, no significant differences were found in assemblages grown in different substrata, suggesting a stronger influence of water variables (e.g., temperature or salinity) on assemblage compositions. Moreover, the experimental set-ups favored small, fast-growing, sediment-dwelling species tolerant of relatively high organic content. Our findings highlight the potential of propagule banks as species pools and will help to refine and improve future applications of the method.

Recent Invasion of the Symbiont-Bearing Foraminifera Pararotalia into the Eastern Mediterranean Facilitated by the Ongoing Warming Trend.

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 was 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.

Heading for new shores: projecting marine distribution ranges of selected larger foraminifera.

The distribution of modern symbiont-bearing larger foraminifera is confined to tropical and subtropical shallow water marine habitats and a narrow range of environmental variables (e.g. temperature). Most of today's taxa are restricted to tropical and subtropical regions (between 30°N and 30°S) and their minimum temperature limits are governed by the 14 to 20°C isotherms. However, during times of extensive global warming (e.g., the Eocene and Miocene), larger foraminifera have been found as far north as 50°N (North America and Central Europe) as well as towards 47°S in New Zealand. During the last century, sea surface temperatures have been rising significantly. This trend is expected to continue and climate change scenarios for 2050 suggest a further increase by 1 to 3°C. We applied Species Distribution Models to assess potential distribution range changes of three taxa of larger foraminifera under current and future climate. The studied foraminifera include Archaias angulatus, Calcarina spp., and Amphistegina spp., and represent taxa with regional, superregional and global distribution patterns. Under present environmental conditions, Amphistegina spp. shows the largest potential distribution, apparently due to its temperature tolerance. Both Archaias angulatus and Calcarina spp. display potential distributions that cover currently uninhabited regions. Under climate conditions expected for the year 2050, all taxa should display latitudinal range expansions between 1 to 2.5 degrees both north- and southward. The modeled range projections suggest that some larger foraminifera may colonize biogeographic regions that so far seemed unsuitable. Archaias angulatus and Calcarina spp. also show an increase in habitat suitability within their native occurrence ranges, suggesting that their tolerance for maximum temperatures has yet not been fully exploited and that they benefit from ocean warming. Our findings suggest an increased role of larger foraminifera as carbonate producers and reef framework builders in future oceans.

Climate-driven range extension of Amphistegina (protista, foraminiferida): models of current and predicted future ranges.

Species-range expansions are a predicted and realized consequence of global climate change. Climate warming and the poleward widening of the tropical belt have induced range shifts in a variety of marine and terrestrial species. Range expansions may have broad implications on native biota and ecosystem functioning as shifting species may perturb recipient communities. Larger symbiont-bearing foraminifera constitute ubiquitous and prominent components of shallow water ecosystems, and range shifts of these important protists are likely to trigger changes in ecosystem functioning. We have used historical and newly acquired occurrence records to compute current range shifts of Amphistegina spp., a larger symbiont-bearing foraminifera, along the eastern coastline of Africa and compare them to analogous range shifts currently observed in the Mediterranean Sea. The study provides new evidence that amphisteginid foraminifera are rapidly progressing southwestward, closely approaching Port Edward (South Africa) at 31°S. To project future species distributions, we applied a species distribution model (SDM) based on ecological niche constraints of current distribution ranges. Our model indicates that further warming is likely to cause a continued range extension, and predicts dispersal along nearly the entire southeastern coast of Africa. The average rates of amphisteginid range shift were computed between 8 and 2.7 km year(-1), and are projected to lead to a total southward range expansion of 267 km, or 2.4° latitude, in the year 2100. Our results corroborate findings from the fossil record that some larger symbiont-bearing foraminifera cope well with rising water temperatures and are beneficiaries of global climate change.