Danna Titelboim

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.

Extremely heat tolerant photo-symbiosis in a shallow marine benthic foraminifera

Bleaching, the loss of algal symbionts, occurs in marine photosymbiotic organisms at water temperatures minimally exceeding average summer SST (sea surface temperatures). Pre-adaptation allows organisms to persist under warmer conditions, providing the tolerance can be carried to new habitats. Here we provide evidence for the existence of such adaptation in the benthic foraminifera Pararotalia calcariformata. This species occurs at a thermally polluted site in the Mediterranean, where water temperatures reach a maxima daily average of 36 °C during the summer. To test whether this occurrence represents a widespread adaptation, we conducted manipulative experiments exposing this species from an unpolluted site to elevated temperatures (20–42 °C). It was kept in co-culture with the more thermally sensitive foraminifera Amphistegina lobifera in two experiments (20–36 °C). Reduced photosynthetic activity in A. lobifera occurred at 32 °C whereas photochemical stress in P. calcariformata was first observed during exposure to 36 °C. Pararotalia calcariformata survived all treatment conditions and grew under 36 °C. The photosymbiosis in P. calcariformata is unusually thermally tolerant. These observations imply that marine eukaryote-eukaryote photosymbiosis can respond to elevated temperatures by drawing on a pool of naturally occurring pre-adaptations. It also provides a perspective on the massive occurrence of symbiont-bearing foraminifera in the early Cenozoic hothouse climate.

Selective responses of benthic foraminifera to thermal pollution

Persistent thermohaline pollution at a site along the northern coast of Israel, due to power and desalination plants, is used as a natural laboratory to evaluate the effects of rising temperature and salinity levels on benthic foraminifera living in shallow hard-bottom habitats. Biomonitoring of the disturbed area and a control station shows that elevated temperature is a more significant stressor compared to salinity, thus causing a decrease in abundance and richness. Critical temperature thresholds were observed at 30 and 35°C, the latter representing the most thermally tolerant species in the studied area Pararotalia calcariformata, which is the only symbiont-bearing species observed within the core of the heated area. Common species of the shallow hard-bottom habitats including several Lessepsian invaders are almost absent in the most exposed site indicating that excess warming will likely impede the survival of these species that currently benefit from the ongoing warming of the Eastern Mediterranean.

Molecular Phylogeny and Ecology of Textularia agglutinans d'Orbigny from the Mediterranean Coast of Israel: A Case of a Successful New Incumbent.

Textularia agglutinans d’Orbigny is a non-symbiont bearing and comparatively large benthic foraminiferal species with a widespread distribution across all oceans. In recent years, its populations have considerably expanded along the Israeli Mediterranean coast of the eastern Levantine basin. Despite its exceptionally widespread occurrence, no molecular data have yet been obtained. This study provides the first ribosomal DNA sequences of T. agglutinans complemented with morphological and ecological characterization, which are based on material collected during environmental monitoring of the hard bottom habitats along the Israeli Mediterranean coast, and from the Gulf of Elat (northern Red Sea). Our phylogenetic analyses reveal that all specimens from both provinces belong to the same genetic population, regardless their morphological variability. These results indicate that modern population of T. agglutinans found on the Mediterranean coast of Israel is probably Lessepsian. Our study also reveals that T. agglutinans has an epiphytic life mode, which probably enabled its successful colonization of the hard bottom habitats, at the Mediterranean coast of Israel, which consist of a diverse community of macroalgae. Our study further indicates that the species does not tolerate high SST (> 35°C), which will probably prevent its future expansion in the easternmost Mediterranean in light of the expected rise in temperatures.

Foraminiferal single chamber analyses of heavy metals as a tool for monitoring permanent and short term anthropogenic footprints

In order to establish environmentally sustainable industries there is a need for high-resolution temporal and spatial monitoring of heavy metal pollutants even at low concentrations before they become hazardous for local ecosystems. Here we present single chamber records of Cu, Zn and Pb in shells of two benthic foraminifera species with different shell types from two shallow coastal stations in Israel: An area adjacent to an electrical power plant and desalination factory (Hadera) and an industrially free nature reserve (Nachsholim). Records of both foraminifera species show elevated metal concentrations in Hadera clearly identifying the footprint of the local industrial facilities. Moreover, short-term events of elevated Cu and Pb concentrations were detected by single chamber analyses. This study demonstrates the potential of using heavy metals anomalies in foraminiferal single chambers as a tool for detecting the industrial footprint of coastal facilities as well as short term events of elevated heavy metals.