Hay, K.B.

The composition, ecology and environmental conditions of mesophotic coral ecosystems near the lower limits of their bathymetric distributions remain poorly understood. Here we provide the first in-depth assessment of a lower mesophotic coral community (60–100 m) in the Southern Caribbean through visual submersible surveys, genotyping of coral host-endosymbiont assemblages, temperature monitoring and a growth experiment. The lower mesophotic zone harbored a specialized coral community consisting of predominantly Agaricia grahamae, Agaricia undata and a “deep-water” lineage of Madracis pharensis, with large colonies of these species observed close to their lower distribution limit of ~90 m depth. All three species associated with “deep-specialist” photosynthetic endosymbionts (Symbiodinium). Fragments of A. grahamae exhibited growth rates at 60 m similar to those observed for shallow Agaricia colonies (~2–3 cm yr −1), but showed bleaching and (partial) mortality when transplanted to 100 m. We propose that the strong reduction of temperature over depth (Δ5°C from 40 to 100 m depth) may play an important contributing role in determining lower depth limits of mesophotic coral communities in this region. Rather than a marginal extension of the reef slope, the lower mesophotic represents a specialized community, and as such warrants specific consideration from science and management. 

Bathymetric distributions of photosynthetic marine invertebrate species are relatively well studied, however the importance of symbiont zonation (i.e. hosting of distinct algal endosymbiont communities over depth) in determining these depth distributions still remains unclear. Here, we assess the prevalence of symbiont zonation in tropical scleractinian corals by genotyping the Symbiodinium of the 25 most common species over a large depth range (down to 60 m) on a Caribbean reef. Symbiont depth zonation was found to be common on a reef-wide scale (11 out of 25 coral species), and a dominant feature in species with the widest depth distributions. With regards to reproductive strategy, symbiont zonation was more common in broadcasting species, which also exhibited a higher level of polymorphism in the symbiont zonation (i.e. number of different Symbiodinium profiles involved). Species with symbiont zonation exhibited significantly broader depth distributions than those without, highlighting the role of symbiont zonation in shaping the vertical distributions of the coral host. Overall, the results demonstrate that coral reefs can consist of highly structured communities over depth when considering both the coral host and their obligate photosymbionts, which probably has strong implications for the extent of connectivity between shallow and mesophotic habitats. 

Abstract

Background: Scleractinian corals and their algal endosymbionts (genus Symbiodinium) exhibit distinct bathymetric distributions on coral reefs. Yet, few studies have assessed the evolutionary context of these ecological distributions by exploring the genetic diversity of closely related coral species and their associated Symbiodinium over large depth ranges. Here we assess the distribution and genetic diversity of five agariciid coral species (Agaricia humilis, A. agaricites, A. lamarcki, A. grahamae, and Helioseris cucullata) and their algal endosymbionts (Symbiodinium) across a large depth gradient (2-60 m) covering shallow to mesophotic depths on a Caribbean reef.

Results: The five agariciid species exhibited distinct depth distributions, and dominant Symbiodinium associations were found to be species-specific, with each of the agariciid species harbouring a distinct ITS2-DGGE profile (except for a shared profile between A. lamarcki and A. grahamae). Only A. lamarcki harboured different Symbiodinium types across its depth distribution (i.e. exhibited symbiont zonation). Phylogenetic analysis (atp6) of the coral hosts demonstrated a division of the Agaricia genus into two major lineages that correspond to their bathymetric distribution (“shallow”: A. humilis / A. agaricites and “deep”: A. lamarcki / A. grahamae), highlighting the role of depth-related factors in the diversification of these congeneric agariciid species. The divergence between “shallow” and “deep” host species was reflected in the relatedness of the associated Symbiodinium (with A. lamarcki and A. grahamae sharing an identical Symbiodinium profile, and A. humilis and A. agaricites harbouring a related ITS2 sequence in their Symbiodinium profiles), corroborating the notion that brooding corals and their Symbiodinium are engaged in coevolutionary processes.

Conclusions: Our findings support the hypothesis that the depth-related environmental gradient on reefs has played an important role in the diversification of the genus Agaricia and their associated Symbiodinium, resulting in a genetic segregation between coral host-symbiont communities at shallow and mesophotic depths.