The Eastern Mediterranean is experiencing a large-scale invasion of alien tropical species from the Red Sea. This "Lessepsian invasion" began with the opening of the Suez Canal and is promoted by the ...ongoing oceanic warming. The environmental differences between the Red Sea and the Mediterranean act as a buffer allowing the invasion of certain species. This provides an opportunity to study the differences in temperature sensitivity between two sibling species of the cosmopolitian foraminifera Amphistegina. Both species are very common in the Red Sea. Whilest, only one is a successful invader and the other is absent in the Eastern Mediterranean. Here we show that the two species are different in their temperature sensitivity, which explains their selective invasion into the Mediterranean. These differences demonstrate that in respect to climate change resilient marine species can be distinguished by their ability to compensate for temperature changes by adjusting their physiological performance and by having tolerance to a wider temperature range. Moreover, we demonstrate that selective filtering mechanisms during invasion can prefer species that are more resilient to colder rather than expected warmer temperatures.
Among the most successful Lessepsian invaders is the symbiont-bearing benthic foraminifera Amphistegina lobifera. In its newly conquered habitat, this prolific calcifier and ecosystem engineer is ...exposed to environmental conditions that exceed the range of its native habitat. To disentangle which processes facilitated the invasion success of A. lobifera into the Mediterranean Sea we analyzed a ~ 1400 bp sequence fragment covering the SSU and ITS gene markers to compare the populations from its native regions and along the invasion gradient. The genetic variability was studied at four levels: intra-genomic, population, regional and geographical. We observed that the invasion is not associated with genetic differentiation, but the invasive populations show a distinct suppression of intra-genomic variability among the multiple copies of the rRNA gene. A reduced genetic diversity compared to the Indopacific is observed already in the Red Sea populations and their high dispersal potential into the Mediterranean appears consistent with a bridgehead effect resulting from the postglacial expansion from the Indian Ocean into the Red Sea. We conclude that the genetic structure of the invasive populations reflects two processes: high dispersal ability of the Red Sea source population pre-adapted to Mediterranean conditions and a likely suppression of sexual reproduction in the invader. This discovery provides a new perspective on the cost of invasion in marine protists: The success of the invasive A. lobifera in the Mediterranean Sea comes at the cost of abandonment of sexual reproduction.
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.
Coralline algae form complex habitats which are biodiversity hotspots. Experimental studies suggest that climate change will decrease coralline algal structural integrity. These experiments, however, ...lack information on local morphological variability and how much structural change would be needed to threaten habitat formation. Here, using finite element modelling, we assess variability in cellular structure and chemical composition of the carbonate skeleton of four coralline algal species from Britain in contemporary and historical specimens collected over the last 130 years. Cellular and mineral properties are highly variable within species, between sites and through time, with structurally weaker cells in the southern species and contemporary material compared to northern taxa and historical material. Yet, temporal differences in strength were smaller than spatial differences. Our work supports long term experiments which show the adaptation potential of this group. Our results suggest that future anthropogenic climate change may lead to loss of habitat complexity in the south and expansion of structurally weaker southern species into northern sites.
The genus
Operculina
, a large symbiont-bearing benthic foraminifer, is characterized by high morphological variability showing thick involute to intermediate semi-involute to flat evolute tests. ...Different morphotypes are either considered as ecophenotypes or distinct species. In order to test the hypothesis of ecophenotypes versus different species, a single cell high throughput sequencing approach was applied to assess the interspecific diversity of
Operculina
. This results in two groups of ribotypes, one corresponding to
Operculina ammonoides
/
Operculina discoidalis
, the other containing
Operculina complanata
/
Operculina elegans
. These groups can also be separated morphologically. Therefore,
O. complanata
and
O. elegans
represent a single species and the latter can be regarded as a junior synonym of
O. complanata. Operculina ammonoides
and
O. discoidalis
also form a single species, which makes the latter a junior synonym of
O. ammonoides
. Because generic differences in
Operculina
species are manifested in morphology and molecular genetics, the genus
Neoassilina
with the designated species
Neoassilina ammonoides
is installed. Additional analysis of ribosomal SSU rDNA data of eight recent nummulitid genera confirms the obtained high troughput sequencing results and further shows that
Palaeonummulites venosus
builds a clade with
O. complanata
that branches at the base of other Nummulitidae containing
Planostegina
,
Planoperculina
,
Cycloclypeus
,
Heterostegina
,
Operculinella
and
Neoassilina
.
Global warming permits range expansions of tropical marine species into mid‐latitude habitats, where they are, however, faced with cold winter temperatures. Therefore, tolerance to cold temperatures ...may be the key adaptation controlling zonal range expansion in tropical marine species.
Here we investigated the molecular and physiological response to cold and heat stress in a tropical symbiont‐bearing foraminifera that has successfully invaded the Eastern Mediterranean.
Our physiological measurements indicate thermal tolerance of the diatom symbionts but a decrease in growth for the foraminifera host under both cold and warm stress.
The combined (‘holobiont’) transcriptome revealed an asymmetric response in short‐term gene expression under cold versus warm stress. Cold stress induced major reorganization of metabolic processes, including regulation of genes involved in photosynthesis. Analyses limited to genes that are inferred to belong to the symbionts confirm that the observed pattern is due to changes in the regulation of photosynthesis‐related genes and not due to changes in the abundance of the symbionts.
In contrast to cold stress, far fewer genes change expression under heat stress and those that do are primarily related to movement and cytoskeleton. This implies that under cold stress, cellular resources are allocated to the maintenance of photosynthesis, and the key to zonal range shifts of tropical species could be the cold tolerance of the symbiosis.
A free Plain Language Summary can be found within the Supporting Information of this article
A free Plain Language Summary can be found within the Supporting Information of this article.
Shallow marine calcifiers play an important role as marine ecosystem engineers and in the global carbon cycle. Understanding their response to warming is essential to evaluate the fate of marine ...ecosystems under global change scenarios. A rare opportunity to test the effect of warming acting on natural ecosystems is by investigation of heat‐polluted areas. Here, we study growth and calcification in benthic foraminifera that inhabit a thermally polluted coastal area in Israel, where they are exposed to elevated temperatures reaching up to ~42°C in summer. Live specimens of two known heat‐tolerant species Lachlanella sp. 1 and Pararotalia calcariformata were collected over a period of 1 year from two stations, representing thermally polluted and undisturbed (control) shallow hard bottom habitats. Single‐chamber element ratios of these specimens were obtained using laser ablation, and the Mg/Ca of the most recently grown final chambers were used to calculate their calcification temperatures. Our results provide the first direct field evidence that these foraminifera species not only persist at extreme warm temperatures but continue to calcify and grow. Species‐specific Mg/Ca thermometry indicates that P. calcariformata precipitate their shells at temperatures as high as 40°C and Lachlanella sp. 1 at least up to 36°C, but both species show a threshold for calcification at cold temperatures: calcification in P. calcariformata only occurred above 22°C and in Lachlanella sp. 1 above 15°C. Our observations from the heat‐polluted area indicate that under future warming scenarios, calcification in heat‐tolerant foraminifera species will not be inhibited during summer, but instead the temperature window for their calcification will be expanded throughout much of the year. The observed inhibition of calcification at low temperatures indicates that the role of heat‐tolerant foraminifera in carbonate production will most likely increase in future decades.
Understanding the response to warming of shallow marine calcifiers is essential to evaluate the fate of marine ecosystems under global warming scenarios. So far, most data on thermal tolerance of marine calcifiers have been obtained by laboratory experiments. A rare opportunity to test the effect of warming acting on ecosystems is by investigation of heat‐polluted coastal areas. Here, we study growth and calcification in benthic foraminifera that inhabit a thermally polluted coastal area, where they are exposed to elevated temperatures reaching up to ~42°C in summer. Our observations from the heat‐polluted area indicate that under future warming scenarios, calcification in heat‐tolerant foraminifera species will not be inhibited during summer, and the temperature window for their calcification will be expanded throughout much of the year. The observed inhibition of calcification at low temperatures indicates that the role of heat‐tolerant foraminifera in carbonate production will most likely increase in future decades.
•Foraminifera incorporate Zn and Pb in their calcite shells proportionate to seawater.•No species-specific or temperature effect on metal incorporation is observed.•Heavy metal concentrations can be ...measured by laser-ablation of individual chambers.•Such single-chamber analyses could record short-term pollution events.
The establishment of sustainable coastal industries requires better temporal and spatial monitoring of heavy metal (HM) pollutants, even at low concentrations and during pulse-release events, before their accumulation becomes hazardous for local ecosystems or for the use of seawater in desalination (for drinking water). Foraminifera, unicellular marine organism, build their shells by sequential addition of chambers made of calcite, which contains impurities reflecting the composition of the growth medium. Therefore, the chemical composition of each chamber reflects HM in the ambient water at the time of calcification. To test the applicability of single-chamber analyses of foraminifera shells as a tool for HM monitoring in seawater, we conducted culturing experiments to calibrate the relationship of zinc and lead in foraminiferal shells and the ambient seawater. Two species of the cosmopolitan genus Amphistegina were cultured under a range of concentrations of both metals and two temperatures. We show that concentrations of zinc and lead in shells increase linearly with metal concentration in seawater with no difference between species and no effect of temperature. Our experiments further show that the concentrations in seawater can be directly inferred from concentrations in the shells at least up to the levels representing chronic pollution for both metals (68 ug/L for Zn and 8 ug/L for Pb). Combined with their high abundances in all marine environments and good preservation of their shells in sediments, our results demonstrate that foraminifera represent a powerful natural recording system offering high spatial and temporal resolution, allowing the establishment of historical baselines and detection of confined or short-term events of HM release, which could escape traditional monitoring methods.
One of the challenges in monitoring the marine coastal environments is quantifying the magnitude and duration of pollution events. This study introduces a new concept of defining heavy metal (HM) ...baseline assessment levels (BALs) in coastal environments using foraminiferal shells. We demonstrated the potential of this approach by examining a nature reserve along the Mediterranean coast of Israel. Our previous investigation of this site in 2013–2014 using foraminiferal single-chamber LA-ICPMS created a large dataset consisting of HM measurements of two species, Lachlanella and Pararotalia calcariformata. This database was used to establish the BAL of Zn, Cu and Pb, associated with anthropogenic sources. In February 2021, a significant tar pollution event affected the entire Mediterranean coast of Israel, derived from an offshore oil spill. This event provided a unique opportunity to test the applicability of the foraminiferal BAL by comparing it to whole-shell ICPMS measurements of the two species collected in winter and summer 2021. Results reveal a significant increase (2–34-fold) in the three HMs between 2013–2014 and 2021, with Pb/Ca displaying the most prominent increase in both species. This suggests a possible linkage between the oil spill event and the significantly elevated metal/Ca ratios in 2021.
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.
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