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

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.

In Situ Observations of Foraminiferal Bleaching in the Maldives, Indian Ocean

“…Hallock et al (1995) demonstrated that onset of bleaching in Amphistegina consistently preceded maximum temperatures (see also Mendez-Ferrer et al, 2018). The response to acute photo-inhibition occurs within hours to days and to chronic stress over several days to a few weeks (Hallock et al, 1995(Hallock et al, , 2006aStuhr et al, 2017). These responses can be detected cytologically before visible loss of symbionts becomes evident .…”

“…The only parameter assessed at the sampling sites that appears problematic is temperature (means range between 28.8-31.7 • C), with only two of the means reported in Table 2 falling below 30 • C, and several exceeding 30.5 • C. Schmidt et al (2011) have shown that temperature effects are species-specific, and that a temperature above 31 • C has a negative effect on Amphistegina. Several authors have demonstrated that temperatures exceeding 30 • C significantly decrease photosynthetic activity in the diatom symbionts of LBF (Sinutok et al, 2011;Uthicke et al, 2012;Schmidt et al, 2016a, b;Stuhr et al, 2017).…”

“…Temperature can also induce bleaching in foraminifers (Talge & Hallock, 2003;Schmidt et al, 2011;Stuhr et al, 2017). Schmidt et al (2011) observed that a 2-3 • C increase in temperature can produce rapid bleaching in several diatom-bearing benthic foraminiferal species, including Amphistegina, which hosts naked diatom cells lacking silica frustules (e.g., Lee & Anderson, 1991;Talge & Hallock, 2003).…”

Recurring Episodes of Thermal Stress Shift the Balance From a Dominant Host-Specialist to a Background Host-Generalist Zooxanthella in the Threatened Pillar Coral, Dendrogyra cylindrus

“…It has been proposed that colonies exposed to moderate thermal stress are better conditioned to dealing with episodes of severe thermal stress (Oliver and Palumbi, 2011;Ainsworth et al, 2016). Thermal profiles showing a prebleaching spike in water temperatures, followed by a recovery period of cooler temperatures, prior to a hyperthermal event, reduced the severity of bleaching.…”

Challenges in using CellTracker Green on foraminifers that host algal endosymbionts

“…Hallock (2000) summarized the potential and benefits of using reef-dwelling larger benthic foraminifers (LBF) as indicators of water quality conducive to coral-reef accretion. Experimental approaches have included studies of growth rates (Hallock, Forward & Hansen, 1986), photosynthetic activity (e.g., Talge & Hallock, 2003; Méndez-Ferrer, Hallock & Jones, 2018), prevalence of morphological anomalies (e.g., Prazeres, Uthicke & Pandolfi, 2016), symbiont loss (e.g., Hallock et al, 1995), and, most recently, proteomics (e.g., Prazeres et al, 2011; Stuhr et al, 2018) and antioxidant capacity (i.e., Prazeres, Uthicke & Pandolfi, 2016; Stuhr et al, 2017). …”