Abstract
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.
Highlights
Among extant species or whether these species will be able to draw on these adaptations as present climatic change proceeds extremely rapidly[24]
To constrain the temperature range to which the natural populations at the two studied sites are exposed even during short, extreme heat spells, we deployed in-situ loggers in Hadera and in Nachsholim recording temperature every 15 minutes between February 2013 and January 2014 (Fig. 1). We found that both locations show similar seasonal cycles, but temperatures above 33 °C never occurred in the natural habitat (Nachsholim), whilst maximum daily average temperatures of 36.2 °C up to 37 °C were recorded inside the heat-plume (Fig. 1)
Fv:Fm maximum quantum yield, Y(II) effective quantum yield measured at experimental light intensity, data plotted are shown as boxplots, each graph has N = 29–33 independent data points, which are given as means per well, each well contained N = 5–6 specimens, see Table S1 for statistical analysis
Summary
Among extant species or whether these species will be able to draw on these adaptations as present climatic change proceeds extremely rapidly[24]. We take advantage of the recent discovery of the occurrence of symbiont-bearing foraminifera at a thermally polluted site (Hadera) on the Mediterranean coast of Israel, where cooling water discharge from a power plant raises local sea surface temperatures by on average 6 °C above the baseline[25]. We use this artificial “window” into a warmer ocean to investigate the thermal tolerance of the benthic foraminifera Pararotalia calcariformata. We recorded sea-water temperatures at both sites throughout one year and monitored the foraminiferal population in-situ. Demonstrating the representativeness of our laboratory conditions, the first two experiments included populations of Amphistegina lobifera from the same locality, a genus which is known to bleach at 32 °C in other locations worldwide[15,26,27]
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