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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.

The persistence of coral reefs requires the survival of adult coral colonies and their continued sexual reproduction despite thermal stress. To assess the trophic pathway (i.e., autotrophy and/or heterotrophy) used to develop gametes following bleaching, we thermally stressedMontipora capitatafor one month at a time when corals in Hawai’i typically experience elevated seawater temperatures. After six and nine months of recovery, we pulse-chased non-bleached and previously bleached colonies using a dual-label design to compare the allocation of carbon and nitrogen at significant stages of gamete development. Dissolved inorganic carbon- (DI¹³C) and nitrogen- (DI¹⁵N) labelled seawater or¹³C- and¹⁵N-labelled rotifers were used to assess the autotrophic and heterotrophic pathways, respectively. At multiple time points for up to two years later, we collected adult coral fragments and isolated host tissue, Symbiodiniaceae cells, and developing eggs and captured gamete bundles to analyze their carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotopes. We found that the presence of Symbiodiniaceae was important for gametogenesis in both non-bleached and previously bleached colonies in two main ways. First, autotrophically-acquired carbon and nitrogen were both allocated to gametes during development, suggesting that recovery of photosynthesis after bleaching is critical for gametogenesis. Second, only heterotrophically-acquired nitrogen, not carbon, was incorporated into gametes and was readily recycled between host tissues and Symbiodiniaceae cells. This suggests that one of the purposes of heterotrophy following coral bleaching forM. capitatamay be to supplement the nitrogen pool, providing available nutrients for endosymbiotic algal growth. Allocation of carbon and nitrogen to eggs coincided with the period when vertical transmission of symbionts to gametes occurs, further supporting the important relationship between gametogenesis and availability of Symbiodiniaceae forM. capitata.

Warming ocean temperatures are severely compromising the health and resilience of coral reefs worldwide. Coral bleaching can affect coral physiology and the energy available for corals to reproduce. Mechanisms associated with reproductive allocation in corals are poorly understood, especially after a bleaching event occurs. Using isotopic labeling techniques, we traced the acquisition and allocation of carbon from adults to gametes by autotrophy and heterotrophy in previously bleached and non-bleachedMontipora capitataandPorites compressacorals. Experiments revealed that both species: (1) relied only on autotrophy to allocate carbon to gametes, while heterotrophy was less relied upon as a carbon source; (2) experienced a trade-off with less carbon available for adult tissues when provisioning gametes, especially when previously bleached; and (3) used different strategies for allocating carbon to gametes. Over time,M. capitataallocated 10% more carbon to gametes despite bleaching by limiting the allocation of carbon to adult tissues, with 50–80% less carbon allocated to bleached compared to non-bleached colonies. Over the same time period,P. compressamaintained carbon allocation to adult tissues, before allocating carbon to gametes. Our study highlights the importance of autotrophy for carbon allocation from adult corals to gametes, and species-specific differences in carbon allocation depending on bleaching susceptibility.

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.