Night-Time Temperature Reprieves Enhance the Thermal Tolerance of a Symbiotic Cnidarian

Abstract

Responses of cnidarian-Symbiodiniaceae associations to warming are determined, in part, by high-frequency temperature variability. Yet, the role of such variability in determining specific maximum temperature thresholds of cnidarian holobionts (the ecological units comprised of cnidarian hosts and associated microorganisms, including Symbiodiniaceae) remains untested. Here we contrasted the thermal resilience (that is the ability to resist stress) of a model symbiotic cnidarian from the Red Sea (jellyfish of the genus Cassiopea) under stable and diel oscillating temperature conditions that provide night-time reprieves from daily maximum temperatures. Holobionts were subjected to two thermal trajectories; one that increased but plateaued at 2 • C below identified bleaching thresholds and another that increased incrementally until holobionts bleached. We used behavior, growth, photochemical efficiency, Symbiodiniaceae (symbiont) cell density, and total chlorophyll cell content to characterize thermal resilience and examined Symbiodiniaceae community composition responses at 1 and 13 days of exposure, and post-bleaching. Lower night-time temperatures, resulting in lower daily mean temperatures, allowed holobionts to withstand daily maximum temperatures close to their bleaching thresholds for two extra days than those under stable maximum temperature conditions. Lower night-time temperatures increased the bleaching threshold of the holobionts, whereby holobionts exposed to night-time thermal reprieves tolerated a more extreme daily mean temperature of 40.6 • C and reached a daily thermal maxima 4 • C higher than those under stable temperature conditions. However, post-bleaching observations indicate that night-time temperature reprieves did not prevent symbiont cell or pigment loss. Symbiodiniaceae communities were unaffected by lower night-time temperatures and no directional changes indicative of symbiont shuffling/ selection of thermally tolerant lineages were observed. We show that stable experimental treatments may fail to accurately identify maximum thermal thresholds of non-calcifying cnidarians and limit their relevance to in situ environments that are often characterized by high levels of temperature fluctuations.

Heat stress destabilizes symbiotic nutrient cycling in corals

“…Coupled with the effects of heat stress, NO 3 − may thus further destabilize symbiotic nutrient cycling in corals. Likewise, previous studies showed that symbiotic cnidarians from areas with strong diurnal temperature variations are more thermotolerant than their counterparts in areas of low temperature variability (41,71,72). Here we found that heat stress stimulates both respiration as well as photosynthesis rates.…”

“…Consequently, the observed depletion of host energy reserves during heat stress is likely more pronounced at night in the absence of photosynthesis. As diurnal temperature variability commonly involves a cooling at night and warming during the day ( 72 ), this implies that strong diurnal temperature variations will reduce the effects of heat stress on the energy budget of the host compared to areas with similar mean temperature but lower diurnal variability. Hence, high diurnal temperature variations may stabilize symbiotic nutrient cycling during heat stress.…”

How do we overcome abrupt degradation of marine ecosystems and meet the challenge of heat waves and climate extremes?

“…For example, regions of higher mixing and temporal thermal respite have be found to result in lower mortality in benthic invertebrates and habitat‐forming organisms (Baird et al, ; Frade et al, ; Green et al, ; Richards et al, ; Roberts et al, ). These examples support the assertion that regions characterized by high thermal variance, and those with short‐term respite during extremes, have greater capacity to withstand extreme conditions (Ainsworth et al, ; Castillo, Ries, Weiss, & Lima, ; Klein et al, ; Morikawa & Palumbi, ; Page et al, ).…”

The Internal Microenvironment of the Symbiotic Jellyfish Cassiopea sp. From the Red Sea

“…At the end of the experiment, the oral arms (in their entirety) were cut into smaller sections and stored at −20 • C for chlorophyll a content, total protein, and Symbiodiniaceae density analyses (LaJeunesse et al, 2018) following a protocol adapted from Klein et al (2016Klein et al ( , 2019. Marginal appendages and vesicles were included in the analyses.…”