skip to main content

Title: Ecophysiology of mesophotic reef‐building corals in Hawai‘i is influenced by symbiont–host associations, photoacclimatization, trophic plasticity, and adaptation

Mesophotic reef corals remain largely unexplored in terms of the genetic adaptations and physiological mechanisms to acquire, allocate, and use energy for survival and reproduction. In the Hawaiian Archipelago, theLeptoserisspecies complex form the most spatially extensive mesophotic coral ecosystem known and provide habitat for a unique community. To study how the ecophysiology ofLeptoserisspecies relates to symbiont–host specialization and understand the mechanisms responsible for coral energy acquisition in extreme low light environments, we examinedSymbiodinium(endosymbiotic dinoflagellate) photobiological characteristics and the lipids and isotopic signatures fromSymbiodiniumand coral hosts over a depth‐dependent light gradient (55–7μmol photons m−2s−1, 60–132 m). Clear performance differences demonstrate different photoadaptation and photoacclimatization across this genus. Our results also show that flexibility in photoacclimatization depends primarily onSymbiodiniumtype. Colonies harboringSymbiodiniumsp.COI‐2showed significant increases in photosynthetic pigment content with increasing depth, whereas colonies harboringSymbiodiniumspp.COI‐1andCOI‐3showed variability in pigment composition, yield measurements for photosystem II, as well as size and density ofSymbiodiniumcells. Despite remarkable differences in photosynthetic adaptive strategies, there were no significant differences among lipids ofLeptoserisspecies with depth. Finally, isotopic signatures of both host andSymbiodiniumchanged with depth, indicating that coral colonies acquired energy from different sources depending on depth. This study highlights the complexity in physiological adaptations within this symbiosis and the different strategies used by closely related mesophotic species to diversify energy acquisition and to successfully establish and compete in extreme light‐limited environments.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Limnology and Oceanography
Page Range / eLocation ID:
p. 1980-1995
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. In mesophotic coral ecosystems, reef-building corals and their photosynthetic symbionts can survive with less than 1% of surface irradiance. How depth-specialist corals rely upon autotrophically and heterotrophically derived energy sources across the mesophotic zone remains unclear. We analysed the stable carbon (δ13C) and nitrogen (δ15N) isotope values of aLeptoseriscommunity from the ‘Au‘au Channel, Maui, Hawai‘i (65–125 m) including four coral host species living symbiotically with three algal haplotypes. We characterized the isotope values of hosts and symbionts across species and depth to compare trophic strategies. Symbiontδ13C was consistently 0.5‰ higher than hostδ13C at all depths. Mean colony host and symbiontδ15N differed by up to 3.7‰ at shallow depths and converged at deeper depths. These results suggest that both heterotrophy and autotrophy remained integral to colony survival across depth. The increasing similarity between host and symbiontδ15N at deeper depths suggests that nitrogen is more efficiently shared between mesophotic coral hosts and their algal symbionts to sustain autotrophy. Isotopic trends across depth did not generally vary by host species or algal haplotype, suggesting that photosynthesis remains essential toLeptoserissurvival and growth despite low light availability in the mesophotic zone.

    more » « less
  2. null (Ed.)
    Energy sources of corals, ultimately sunlight and plankton availability, change dramatically from shallow to mesophotic (30–150 m) reefs. Depth-generalist corals, those that occupy both of these two distinct ecosystems, are adapted to cope with such extremely diverse conditions. In this study, we investigated the trophic strategy of the depth-generalist hermatypic coral Stylophora pistillata and the ability of mesophotic colonies to adapt to shallow reefs. We compared symbiont genera composition, photosynthetic traits and the holobiont trophic position and carbon sources, calculated from amino acids compound-specific stable isotope analysis (AA-CSIA), of shallow, mesophotic and translocated corals. This species harbors different Symbiodiniaceae genera at the two depths: Cladocopium goreaui (dominant in mesophotic colonies) and Symbiodinium microadriaticum (dominant in shallow colonies) with a limited change after transplantation. This allowed us to determine which traits stem from hosting different symbiont species compositions across the depth gradient. Calculation of holobiont trophic position based on amino acid δ 15 N revealed that heterotrophy represents the same portion of the total energy budget in both depths, in contrast to the dogma that predation is higher in corals growing in low light conditions. Photosynthesis is the major carbon source to corals growing at both depths, but the photosynthetic rate is higher in the shallow reef corals, implicating both higher energy consumption and higher predation rate in the shallow habitat. In the corals transplanted from deep to shallow reef, we observed extensive photo-acclimation by the Symbiodiniaceae cells, including substantial cellular morphological modifications, increased cellular chlorophyll a , lower antennae to photosystems ratios and carbon signature similar to the local shallow colonies. In contrast, non-photochemical quenching remains low and does not increase to cope with the high light regime of the shallow reef. Furthermore, host acclimation is much slower in these deep-to-shallow transplanted corals as evident from the lower trophic position and tissue density compared to the shallow-water corals, even after long-term transplantation (18 months). Our results suggest that while mesophotic reefs could serve as a potential refuge for shallow corals, the transition is complex, as even after a year and a half the acclimation is only partial. 
    more » « less
  3. Abstract

    The ecological distribution of coral species from shallow to mesophotic reefs is dependent on light, which varies drastically among local environments. Current definitions of mesophotic coral ecosystems primarily rely on a 30‐m recreational SCUBA boundary to define the upper limits of the community; however, this boundary does not consider local conditions and physiological adaptions of coral species. Using in situ benthic imagery and chlorophyll fluorescence measurements, we examined species distribution and community similarity, as well as photoacclimatization of two common depth‐generalist species (Montastraea cavernosaandPorites astreoides) across shallow to mesophotic reef zones at Little Cayman Island. Photoquadrat image analysis revealed a significant shift in coral species assemblages between 25 and 35 m, which was accompanied by a 30% drop in available surface light, suggesting light is a key driver of coral community composition. Patterns of photoacclimatization across depths differed significantly between the two coral species, with available surface light and the quantum yield of photochemistry in photosystem II found to be significant determinants of each species' abundance. These results provide valuable baseline data on coral community composition across a broad depth gradient in Little Cayman that can contribute to a growing body of evidence to set an upper boundary of mesophotic reefs based on light availability and photoacclimatization potential of depth‐generalist species.

    more » « less
  4. Abstract The morphological architecture of photosynthetic corals modulates the light capture and functioning of the coral-algal symbiosis on shallow-water corals. Since corals can thrive on mesophotic reefs under extreme light-limited conditions, we hypothesized that microskeletal coral features enhance light capture under low-light environments. Utilizing micro-computed tomography scanning, we conducted a novel comprehensive three-dimensional (3D) assessment of the small-scale skeleton morphology of the depth-generalist coral Stylophora pistillata collected from shallow (4–5 m) and mesophotic (45–50 m) depths. We detected a high phenotypic diversity between depths, resulting in two distinct morphotypes, with calyx diameter, theca height, and corallite marginal spacing contributing to most of the variation between depths. To determine whether such depth-specific morphotypes affect coral light capture and photosynthesis on the corallite scale, we developed 3D simulations of light propagation and photosynthesis. We found that microstructural features of corallites from mesophotic corals provide a greater ability to use solar energy under light-limited conditions; while corals associated with shallow morphotypes avoided excess light through self-shading skeletal architectures. The results from our study suggest that skeleton morphology plays a key role in coral photoadaptation to light-limited environments. 
    more » « less
  5. As the devastating impacts of global climate change and local anthropogenic stressors on shallow-water coral reefs are expected to rise, mesophotic coral ecosystems have increasingly been regarded as potential lifeboats for coral survival, providing a source of propagules to replenish shallower reefs. Yet, there is still limited knowledge of the capacity for coral larvae to adjust to light intensities that change with depth. This study elucidates the mechanisms underlying plasticity during early life stages of the coral Porites astreoides that enable survival across broad depth gradients. We examined physiological and morphological variations in larvae from shallow (8–10 m) and mesophotic (45 m) reefs in Bermuda, and evaluated differences in survival, settlement patterns and size among recruits depending on light conditions using a reciprocal ex situ transplantation experiment. Larvae released from mesophotic adults were found to have significantly lower respiration rates and were significantly larger than those derived from shallow adults, indicating higher content of energetic resources and suggesting a greater dispersal potential for mesophotic larvae compared to their shallow counterparts. Additionally, larvae released from mesophotic adults experienced higher settlement success and larger initial spat size compared to larvae from shallow adults, demonstrating a potential connection between parental origin, offspring quality, and recruitment success. Although both shallow and mesophotic larvae exhibited the capacity to survive and settle under reciprocal light conditions, all larvae had higher survival under mesophotic light conditions regardless of parental origin, suggesting that conditions experienced under low light may enable longer larval life, further extending the dispersal period. These results indicate that larvae from mesophotic Porites astreoides colonies are likely capable of reseeding shallow reefs in Bermuda, thereby supporting the Deep Reef Refugia Hypothesis. 
    more » « less