Light gradients and optical microniches in coral tissues

Abstract

Light quantity and quality are among the most important factors determining the physiology and stress response of zooxanthellate corals. Yet, almost nothing is known about the light field that Symbiodinium experiences within their coral host, and the basic optical properties of coral tissue are unknown. We used scalar irradiance microprobes to characterize vertical and lateral light gradients within and across tissues of several coral species. Our results revealed the presence of steep light gradients with photosynthetically available radiation decreasing by about one order of magnitude from the tissue surface to the coral skeleton. Surface scalar irradiance was consistently higher over polyp tissue than over coenosarc tissue in faviid corals. Coral bleaching increased surface scalar irradiance by ~150% (between 500 and 700 nm) relative to a healthy coral. Photosynthesis peaked around 300 μm within the tissue, which corresponded to a zone exhibiting strongest depletion of scalar irradiance. Deeper coral tissue layers, e.g., ~1000 μm into aboral polyp tissues, harbor optical microniches, where only ~10% of the incident irradiance remains. We conclude that the optical microenvironment of corals exhibits strong lateral and vertical gradients of scalar irradiance, which are affected by both tissue and skeleton optical properties. Our results imply that zooxanthellae populations inhabit a strongly heterogeneous light environment and highlight the presence of different optical microniches in corals; an important finding for understanding the photobiology, stress response, as well as the phenotypic and genotypic plasticity of coral symbionts.

Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change

“…These particular clade B and D symbionts outperform one another in less-and more-bleached tissues, respectively (as indicated by photochemical efficiency; figures 2 and 4), which may be owing to the different microenvironments characterizing coral tissues that have been bleached to varying degrees. Healthy (or mildly bleached) tissues with higher symbiont abundances may have lower light levels owing to symbiont self-shading [44,45] and fewer nutrients owing to resource competition [46,47], which may allow clade B to outperform clade D. By contrast, higher light and nutrient levels in more severely bleached tissues (with fewer symbionts) may favour clade D. Warmer temperatures further boost the performance advantage of stress-tolerant D symbionts during recovery (figure 4). In this way, variable coral tissue microenvironments post-bleaching, mediated by the remnant symbiont population size and external conditions, define the niche space in which differential performance of symbiont types drives variable trajectories of mixed communities repopulating their hosts.…”

Light microenvironment and single-cell gradients of carbon fixation in tissues of symbiont-bearing corals

“…We thus consider it likely that excess irradiance triggering photoinhibition in oral tissues is unlikely to cause photoinhibition of Symbiodinium in aboral polyp tissues. The internal light field is species specific and in some thintissued, branching corals such as Pocillopora damicornis, intra-tissue light attenuation is not very pronounced (Wangpraseurt et al, 2012;Szabó et al, 2014). The ability to harbour Symbiodinium cells in low-light niches might be an important resilience factor for thick-tissued corals, such as massive faviids, during and after coral bleaching.…”

“…These first experiments were performed under sub-saturating irradiance of~80 μmol photons per m 2 per s. Earlier studies showed that the local scalar irradiance in upper vs deeper tissue layers relates to the incident photon irradiance in a linear fashion such that at stressful incident irradiance levels of, for example, 2000 μmol photons per m 2 per s, light levels in the lowermost polyp tissue layers are~200 μmol photons per m 2 per s (Wangpraseurt et al, 2012), still representing optimal conditions for photosynthesis. We thus consider it likely that excess irradiance triggering photoinhibition in oral tissues is unlikely to cause photoinhibition of Symbiodinium in aboral polyp tissues.…”

“…Recent studies on the optical properties of corals have shown that light is also a highly stratified resource at the level of individual coral polyps and tissue layers . Steep light gradients exist within the polyp tissues of some corals and light can attenuate by more than an order of magnitude within tissues, that is, comparable to the attenuation that can occur in open oceanic waters between the surface and 425 m of water depth (Kirk, 1994;Wangpraseurt et al, 2012). In this study, we investigated whether such light gradients within coral tissues are correlated with a stratification of Symbiodinium physiology in hospite.…”

“…To ensure incubations at irradiance levels where photosynthesis and irradiance correlated linearly, that is, on the linearly increasing part of the P vs I curve, all experiments were performed at~80 μmol photons per m 2 per s (12/12 h cycle). Microsensor measurements of scalar irradiance (tip size~60 μm; Lassen et al, 1992) and O 2 concentration (OX-50, tip size 50 μm, Unisense A/S, Aarhus, Denmark) were performed within the polyp and coenosarc tissues of corals as described previously (Figures 1a and b; Wangpraseurt et al, 2012). After microsensor measurements, corals were incubated with 13 C-bicarbonate (Supplementary Text S1).…”