Can mesophotic reefs replenish shallow reefs? Reduced coral reproductive performance casts a doubt

Mesophotic coral ecosystems (i.e., deep coral reefs at 30-120 m depth) appear to be thriving while many shallow reefs in the world are declining. Amid efforts to understand and manage their decline, it was suggested that mesophotic reefs might serve as natural refuges and a possible source of propagules for the shallow reefs. However, our knowledge of how reproductive performance of corals alters with depth is sparse. Here, we present a comprehensive study of the reproductive phenology, fecundity, and abundance of seven reef-building conspecific corals in shallow and mesophotic habitats. Significant differences were found in the synchrony and timing of gametogenesis and spawning between shallow and mesophotic coral populations. Thus, mesophotic populations exhibited delayed or protracted spawning events, which led to spawning of the mesophotic colonies in large proportions at times where the shallow ones had long been depleted of reproductive material. All species investigated demonstrated a substantial reduction in fecundity and/or oocyte sizes at mesophotic depths (40-60 m). Two species (Seriatopora hystrix and Galaxea fascicularis) displayed a reduction in both fecundity and oocyte size at mesophotic depths. Turbinaria reniformis had only reduced fecundity and Acropora squarrosa and Acropora valida only reduced oocyte size. In Montipora verrucosa, reduced fecundity was found during one annual reproductive season while, in the following year, only reduced oocyte size was found. In contrast, reduced oocyte size in mesophotic populations of Acropora squarrosa was consistent along three studied years. One species, Acropora pharaonis, was found to be infertile at mesophotic depths along two studied years. This indicates that reproductive performance decreases with depth; and that although some species are capable of reproducing at mesophotic depths, their contribution to the replenishment of shallow reefs may be inconsequential. Reduced reproductive performance with depth, combined with the possible narrower tolerance to environmental factors, further suggests that mesophotic corals may in fact be more vulnerable than previously conceived. Furthermore, we posit that the observed temporal segregation in reproduction could lead to assortative mating, and this, in turn, may facilitate adaptive divergence across depth.