Seriatopora Diversity Preserved in Upper Mesophotic Coral Ecosystems in Southern Japan

Abstract

Coral reefs worldwide are facing increasing stress due to drastic changes in their environment. Mesophotic coral ecosystems (MCEs) have been considered as a potential refuge from several major stressors, such as warm-water bleaching events. However, their role as a subsequent source of larvae remains unclear for many species, particularly as genetic differentiation of corals over depth has frequently been observed. In 1998 and 2001, two severe bleaching events around Okinawa Island in Japan resulted in major changes to the shallow reefs, including the local "extinction" of species such as Seriatopora hystrix at Sesoko Island. However, recently this species was found to be present in abundance at mesophotic depths in the area, despite no clear signs of recovery being observed in the adjacent shallow waters. Here, we assessed the genetic diversity of Seriatopora from this deep population and provide a comparison with populations from shallow to mesophotic depths in other parts of the Ryukyu archipelago, to understand their depth specificity and their importance in genetic diversity conservation of affected shallow populations. High levels of genetic diversity were observed in both shallow and mesophotic Seriatopora populations for both the nuclear (internal transcribed spacer 2, ITS2) and the mitochondrial (hypervariable open reading frame, ORF) markers, with no clear partitioning of haplotypes over depth or across locations in the archipelago. Both ITS2 and ORF suggest the presence of potential cryptic species and the discrepancy between the markers could reflect hybridization or incomplete lineage sorting. Although associated endosymbionts (Symbiodinium spp.) all shared the same mitochondrial haplotype (cytochrome oxidase subunit 1, COI), the nuclear ribosomal ITS2 revealed slight potential habitat partitioning between the genotypes, with a small decrease of C59 Symbiodinium types below 10 m depth and a mirrored increase in C1/C78a-related types. The relative absence of depth-specific host lineages and the substantial overlap between shallow and deep Symbiodinium types indicate that Okinawan MCEs may act as a refuge preserving genotypic diversity of bleaching-sensitive coral such as Seriatopora, and on the long-term may have the potential to contribute to shallow-water recolonization of this species.

Genetic signatures through space, time and multiple disturbances in a ubiquitous brooding coral

“…Corals that inhabit variable thermal environments exhibit greater thermal tolerance than corals that have evolved in stable environments (Thomas et al., ), and these differences are often heritable and can occur either among inshore and offshore habitats (Kenkel & Matz, ), or at local scales due to habitat variability within the same reef (Schoepf, Stat, Falter, & McCulloch, ). Habitat also appears to influence the composition of the symbiotic microbiome living within the coral host (Bongaerts et al., ; Pantos et al., ; Sinniger, Prasetia, Yorifuji, Bongaerts, & Harii, ). In particular, microbes living in colonies from thermally variable or relatively warm environments may well confer heat tolerance (Howells et al., ; Ziegler, Seneca, Yum, Palumbi, & Voolstra, ).…”

To what extent do mesophotic coral ecosystems and shallow reefs share species of conservation interest? A systematic review

“…The refuge dynamics which may occur on MCEs must be underpinned by reproductively active source populations, rather than the sinks represented by outlier observations as hypothesised in deepsea ecosystems [86]. Though such outliers are unlikely to represent source populations for a deep reef refuge, they may none-the-less protect genetic diversity [17].…”

“…Protecting MCEs is often justified by the hypothesised existence of deep reef refuges [13] as shallow reefs continue to suffer damage [15]. In areas where there is a substantial degree of community overlap between shallow reefs and MCEs, species may persist locally on MCEs despite extirpation in the shallows [16,17]. If these deep populations are reproductively active [18] then shallow reefs may be able to recover through vertical connectivity [10,19].…”

Beyond the “Deep Reef Refuge” Hypothesis: A Conceptual Framework to Characterize Persistence at Depth

“…Nonetheless, there are definitely examples of panmixia over depth in species that are abundant at both shallow and mesophotic depths (Serrano et al 2014(Serrano et al , 2016Bongaerts et al 2017). While surviving populations in the mesophotic thermal refuge described for S. hystrix at Sesoko Island in Okinawa were found to be composed of lineages occurring elsewhere in the archipelago at shallow depths (Sinniger et al 2017), recruitment into the shallow may be limited due to a reduced reproductive window at depth , and reestablishment of a shallow-water populations at this location (> 15 years later) has not yet been reported.…”

“…Smith et al (2016a) described a thermal refuge at mesophotic depths in the U.S. Virgin Islands, where upper mesophotic coral communities escaped thermal stress during a shallow-water bleaching event. Another example represents the species-specific mesophotic thermal refuge described for Seriatopora hystrix in Okinawa, which was reported to be locally extinct on shallow reefs after the 1998 and 2001 bleaching events (Sinniger et al 2013(Sinniger et al , 2017. In terms of mesophotic storm refuges, there are a few studies from the Atlantic and Indo-Pacific Oceans documenting MCEs as protected from storms (e.g., Highsmith et al 1980;Harmelin-Vivien 1994;Robbart et al 2009).…”