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

Abstract

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.

Geochemical signatures of benthic foraminiferal shells from a heat‐polluted shallow marine environment provide field evidence for growth and calcification under extreme warmth

“…For this reason, we included additional cultured specimens of P. calcariformata that precipitated new chambers under 20°C from the material of Schmidt et al. ().…”

“…It recently invaded the eastern Mediterranean from the Red Sea and is now common from Israel to southern Turkey. It was recognized as heat tolerant relatively to other species in both field studies and laboratory experiments (Arieli et al., ; Schmidt et al., , ; Titelboim et al., ). Lachlanella sp.…”

“…Unlike the well documented effect of elevated temperatures on corals that is expected to cause bleaching and even host mortality, less is known about how other marine symbioses, including foraminifera with algal endosymbionts, will respond to future warming (Doo, Fujita, Byrne, & Uthicke, 2014). Previous studies have shown that resistance to elevated temperatures greatly varied between symbiont-bearing foraminifera species indicating considerable differences in their thermal tolerance (Schmidt, Heinz, Kucera, & Uthicke, 2011;Schmidt et al, 2015;Titelboim et al, 2016;Uthicke, Vogel, Doyle, Schmidt, & Humphrey, 2012). So far, most data on thermal tolerance of foraminifera have been obtained by laboratory experiments.…”

“…This was most prominent among cultured specimens of P. calcariformata that either did not show any growth or added only one new chamber throughout the entire experiment. For this reason, we included additional cultured specimens of P. calcariformata that precipitated new chambers under 20°C from the material ofSchmidt et al (2015).…”

Evolutionary significance of the microbial assemblages of large benthic Foraminifera

“…However, molecular studies demonstrate that this diversity is likely to have been underestimated by morphological studies (Holzmann, Berney, & Hohenegger, ; Prazeres et al, ). Molecular studies of diatom symbionts in LBF also suggest a strong, species‐specific host–symbiont relationship (Holzmann et al, ; Schmidt et al, , ; Barnes, ; Prazeres et al, ). Diatom‐bearing species also have associations with other groups of algae such as the green microalga Chlorella (Lee, ), and possibly with rhodophytes, usually at very low relative densities (Prazeres et al, ).…”