Skeletal light-scattering accelerates bleaching response in reef-building corals

Abstract

BackgroundAt the forefront of ecosystems adversely affected by climate change, coral reefs are sensitive to anomalously high temperatures which disassociate (bleaching) photosynthetic symbionts (Symbiodinium) from coral hosts and cause increasingly frequent and severe mass mortality events. Susceptibility to bleaching and mortality is variable among corals, and is determined by unknown proportions of environmental history and the synergy of Symbiodinium- and coral-specific properties. Symbiodinium live within host tissues overlaying the coral skeleton, which increases light availability through multiple light-scattering, forming one of the most efficient biological collectors of solar radiation. Light-transport in the upper ~200 μm layer of corals skeletons (measured as ‘microscopic’ reduced-scattering coefficient, ), has been identified as a determinant of excess light increase during bleaching and is therefore a potential determinant of the differential rate and severity of bleaching response among coral species.ResultsHere we experimentally demonstrate (in ten coral species) that, under thermal stress alone or combined thermal and light stress, low- corals bleach at higher rate and severity than high- corals and the Symbiodinium associated with low- corals experience twice the decrease in photochemical efficiency. We further modelled the light absorbed by Symbiodinium due to skeletal-scattering and show that the estimated skeleton-dependent light absorbed by Symbiodinium (per unit of photosynthetic pigment) and the temporal rate of increase in absorbed light during bleaching are several fold higher in low- corals.ConclusionsWhile symbionts associated with low- corals receive less total light from the skeleton, they experience a higher rate of light increase once bleaching is initiated and absorbing bodies are lost; further precipitating the bleaching response. Because microscopic skeletal light-scattering is a robust predictor of light-dependent bleaching among the corals assessed here, this work establishes as one of the key determinants of differential bleaching response.Electronic supplementary materialThe online version of this article (doi:10.1186/s12898-016-0061-4) contains supplementary material, which is available to authorized users.

Physiological integration of coral colonies is correlated with bleaching resistance

“…For example, skeletal light scattering can increase light availability to in hospite Symbiodinium (Enríquez et al 2005, Stambler & Dubinsky 2005, Terán et al 2010 and is modulated by calcium carbonate microstructure (Marcelino et al 2013, Swain et al 2016b in concert with optical properties of coral tissues (Kühl et al 1995, Wangpraseurt et al 2012. Coloniality may be intertwined with the relationship between internal light enhancement and bleaching response as a contributing factor to observed species-specific differential bleaching resistance, or it may directly influence the internal light environment itself (En ríquez et al 2017) and thereby contribute to differ ential bleaching.…”

In vivo Microscale Measurements of Light and Photosynthesis during Coral Bleaching: Evidence for the Optical Feedback Loop?

“…At the cellular scale, coral bleaching involves enhanced thermal and radiative exposure of Symbiodinium cells, resulting in photodamage and the subsequent generation of reactive oxygen species (ROS) that induce the breakdown of the symbiosis (Lesser, 1996; Hoegh-Guldberg, 1999; Weis, 2008). The in vivo light and temperature exposure of Symbiodinium within the host tissue ultimately controls whether Symbiodinium undergoes photodamage, and it is thus important to resolve the optical and thermal microenvironment of coral hosts (Enriquez et al, 2005; Jimenez et al, 2008; Wangpraseurt et al, 2012; Swain et al, 2016). …”

“…Such irradiance enhancement is modulated by the unique optical properties of coral tissue and skeleton (Enriquez et al, 2005; Teran et al, 2010; Kahng et al, 2012; Marcelino et al, 2013; Wangpraseurt et al, 2016a) and can improve photosynthesis under low light conditions (Brodersen et al, 2014; Wangpraseurt et al, 2014a) or lead to light stress under high irradiance (Marcelino et al, 2013; Swain et al, 2016). The loss of Symbiodinium spp.…”

“…The loss of Symbiodinium spp. cells from corals under environmental stress has been hypothesized to further increase irradiance exposure in hospite due to decreased shading by photopigments and increased backscattered light from the coral skeleton (Enriquez et al, 2005; Teran et al, 2010; Swain et al, 2016). According to this so-called optical feedback hypothesis (Enriquez et al, 2005; Swain et al, 2016), skeleton backscattering can further stimulate symbiont loss inducing an accelerating cycle, where symbiont loss promotes light enhancement and vice versa.…”

Coral responses to temperature, irradiance and acidification stress: linking physiology to satellite remote sensing

“…Experiments on a taxonomically diverse group of other coral species show that those that don't experience a high increase in photon-pressure per symbiont with increasing temperature (like A. muricata: Figure 2.5a) experience reduced photophysiological dysfunction compared to those that do (like mounding Porites spp. : Figure 2.5b) (Swain et al 2016). In A. muricata, metabolic needs may instead have been the driving force of areal symbiont density changes and thermally induced bleaching may originate from a site of damage in A.…”