Reef calcifiers are adapted to episodic heat stress but vulnerable to sustained warming.

Marleen Stuhr,Michal Kucera,Pamela Hallock,Vera Rieder,Claire E Reymond,Hildegard Westphal,Jörg Rahnenführer,Fabrizio Frontalini

doi:10.1371/journal.pone.0179753

Abstract

Shallow marine ecosystems naturally experience fluctuating physicochemical conditions across spatial and temporal scales. Widespread coral-bleaching events, induced by prolonged heat stress, highlight the importance of how the duration and frequency of thermal stress influence the adaptive physiology of photosymbiotic calcifiers. Large benthic foraminifera harboring algal endosymbionts are major tropical carbonate producers and bioindicators of ecosystem health. Like corals, they are sensitive to thermal stress and bleach at temperatures temporarily occurring in their natural habitat and projected to happen more frequently. However, their thermal tolerance has been studied so far only by chronic exposure, so how they respond under more realistic episodic heat-event scenarios remains unknown. Here, we determined the physiological responses of Amphistegina gibbosa, an abundant western Atlantic foraminifera, to four different treatments––control, single, episodic, and chronic exposure to the same thermal stress (32°C)––in controlled laboratory cultures. Exposure to chronic thermal stress reduced motility and growth, while antioxidant capacity was elevated, and photosymbiont variables (coloration, oxygen-production rates, chlorophyll a concentration) indicated extensive bleaching. In contrast, single- and episodic-stress treatments were associated with higher motility and growth, while photosymbiont variables remained stable. The effects of single and episodic heat events were similar, except for the presumable occurrence of reproduction, which seemed to be suppressed by both episodic and chronic stress. The otherwise different responses between treatments with thermal fluctuations and chronic stress indicate adaptation to thermal peaks, but not to chronic exposure expected to ensue when baseline temperatures are elevated by climate change. This firstly implies that marine habitats with a history of fluctuating thermal stress potentially support resilient physiological mechanisms among photosymbiotic organisms. Secondly, there seem to be temporal constraints related to heat events among coral reef environments and reinforces the importance of temporal fluctuations in stress exposure in global-change studies and projections.

Highlights

The health and the geographical distribution of coral reefs are rapidly declining with ever increasing local and global pressures [1]
As in the photosymbiont-specific variables, the holobiont response appeared to be similar for the single- and episodic-stress treatments (Table 2, Fig 4C–4E). The response of these treatments was comparable to the control, except for motility, which was significantly higher in the single- and episodic-stress treatments, and the antioxidant capacity against peroxyl radicals (ACAP), which showed different temporal trends
Because empty shells were associated with treatments where photosymbiont and holobiont variables indicated optimum growth, and because the experiment was conducted at the time of year when these populations normally reproduce [33], the presence of empty shells in this study is interpreted as being caused by reproduction

Summary

Introduction

The health and the geographical distribution of coral reefs are rapidly declining with ever increasing local and global pressures [1]. The LBF Amphistegina spp. is a circumglobal, warm-water, calcifying eukaryote inhabiting oligotrophic coral-reef and shallow-shelf environments and hosting diatom photosymbionts [9]. Facilitated by their algal symbionts, LBF are vital constituents of coral-reef ecosystems [10] and important marine calcifiers, responsible for the global production of approximately 0.1 Gt/year of carbonate sediments [11]. Due to their physiological sensitivity, LBF are commonly used as bioindicators for past and present environmental conditions such as water quality and coral reef health [12, 13]. This is a vital aspect of adaptive physiology, because episodic stress followed by a phase of recovery, represents a realistic scenario for predicting the consequences of present and future global warming [18]

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