Deep reefs are not universal refuges: Reseeding potential varies among coral species

Bongaerts, Pim; Riginos, Cynthia; Brunner, Ramona; Englebert, Norbert; Smith, Struan R.; Høegh-Guldberg, Ove

doi:10.1126/sciadv.1602373

Cited by 208 publications

(285 citation statements)

References 81 publications

(136 reference statements)

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“…Similarly, Serrano et al (2014) found geographic differences in vertical connectivity due to local geophysical conditions. Species-specific differences in population connectivity with depth have also been reported in the Caribbean (Bongaerts et al, 2017).…”

Section: Mesophotic Reefsmentioning

confidence: 79%

The Future of Coral Reefs Subject to Rapid Climate Change: Lessons from Natural Extreme Environments

et al. 2018

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Global climate change and localized anthropogenic stressors are driving rapid declines in coral reef health. In vitro experiments have been fundamental in providing insight into how reef organisms will potentially respond to future climates. However, such experiments are inevitably limited in their ability to reproduce the complex interactions that govern reef systems. Studies examining coral communities that already persist under naturally-occurring extreme and marginal physicochemical conditions have therefore become increasingly popular to advance ecosystem scale predictions of future reef form and function, although no single site provides a perfect analog to future reefs. Here we review the current state of knowledge that exists on the distribution of corals in marginal and extreme environments, and geographic sites at the latitudinal extremes of reef growth, as well as a variety of shallow reef systems and reef-neighboring environments (including upwelling and CO 2 vent sites). We also conduct a synthesis of the abiotic data that have been collected at these systems, to provide the first collective assessment on the range of extreme conditions under which corals currently persist. We use the review and data synthesis to increase our understanding of the biological and ecological mechanisms that facilitate survival and success under sub-optimal physicochemical conditions. This comprehensive assessment can begin to: (i) highlight the extent of extreme abiotic scenarios under which corals can persist, (ii) explore whether there are commonalities in coral taxa able to persist in such extremes, (iii) provide evidence for key mechanisms required to support survival and/or persistence under sub-optimal environmental conditions, and (iv) evaluate the potential of current sub-optimal coral environments to act as potential refugia under changing environmental conditions. Such a collective approach is critical to better understand the future survival of corals in our changing environment. We finally outline priority areas for future research on extreme and marginal coral environments, and discuss the additional management options they may provide for corals through refuge or by providing genetic stocks of stress tolerant corals to support proactive management strategies.

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Section: Mesophotic Reefsmentioning

confidence: 79%

The Future of Coral Reefs Subject to Rapid Climate Change: Lessons from Natural Extreme Environments

et al. 2018

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“…Due to the symbiont natural rates of increase, corals steadily release Symbiodinium cells into the surrounding environment (Yamashita et al, 2011), suggesting that close to reefs, seawater should contain detectable quantities of DNA from both corals and Symbiodinium. Recently, whole genome sequences of an Acropora coral (Shinzato et al, 2011) and Symbiodinium (Shoguchi et al, 2013;Lin et al, 2015;Aranda et al, 2016) have been published, and nextgeneration sequencing (NGS) technologies have been used to investigate coral reef biodiversity (Shinzato et al, 2014b(Shinzato et al, , 2015Combosch and Vollmer, 2015;Bongaerts et al, 2017). In the genus Symbiodinium, each clade contains multiple genetic types, and identification has been performed using ribosomal, mitochondrial, plastid, and nuclear DNA markers (Rowan and Powers, 1991;Wilcox, 1998;Lajeunesse, 2001;Santos et al, 2002;Takabayashi et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Using Seawater to Document Coral-Zoothanthella Diversity: A New Approach to Coral Reef Monitoring Using Environmental DNA

et al. 2018

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Frequent, high-density coral monitoring is essential to understand coral reef ecosystems. For this purpose, we developed a novel method for simultaneous monitoring of Acropora corals and their symbiont, Symbiodinium, from environmental DNA (eDNA) in seawater using next generation sequencing technology (NGS). We performed a tank experiment with running seawater using 19 Acropora species. Complete mitochondrial genomes of all the Acropora species were assembled to create a database and major types of their Symbiodinium symbionts were identified. Then eDNA was isolated by filtering inlet and outlet seawater from the tanks. Acropora and Symbiodinium DNA were amplified by PCR and sequenced. We detected all of the tested Acropora types from eDNA samples. Proportions and numbers of DNA sequences were both positively correlated with masses of corals in the tanks. In this trial, we detected DNA sequences from as little as 0.04 kg of Acropora colony, suggesting that existence of at least one adult Acropora colony (∼30 cm diameter = 1 kg) per m 2 at depths <10 m could be detected using eDNA in the field. In addition, we detected major types of Symbiodinium within host corals from seawater, suggesting that it should be possible to detect major coral symbiont types if Acropora corals exist nearby, and possible free-living state Symbiodinium cells from eDNA in seawater. eDNA abundance of Symbiodinium types did not correlate well with frequencies of major Symbiodinium types in the corals, suggesting that quantification of Symbiodinium is difficult at this stage. Although this is the initial attempt to detect coral and Symbiodinium simultaneously from eDNA in seawater, this method may allow us to perform high-frequency, high-density coral reef monitoring of both corals and their symbionts in the near future.

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“…In the Atlantic, the brooding coral Porites astreoides also showed genetic patterns suggesting deep-shallow connectivity in several locations although in this case the symbionts exhibited depth-zonation in some cases (Serrano et al, 2016). Strong vertical connectivity was also detected in the Atlantic broadcasting species, Stephanocoenia intersepta, while another brooding coral, Agaricia fragilis, showed strong genetic structure with depth in the same region (Bongaerts et al, 2017).…”

Section: Discussionmentioning

confidence: 85%

“…This has sparked a recent interest and led to a definition of Mesophotic Coral Ecosystems (MCEs) as coral reef habitat occurring at depths greater than 30 m (Hinderstein et al, 2010). The role of MCEs as refuges against episodic disturbances, referred to as the Deep Reef Refuge Hypothesis (DRRH) (sensu Bongaerts et al, 2010aBongaerts et al, , 2017, has played a central part in the motivation of mesophotic studies (Slattery et al, 2011;Bridge et al, 2012;Smith et al, 2014). Based on the original hypothesis that deeper reefs could act as a thermal refuge (Glynn, 1996;Riegl and Piller, 2003), the DRRH was then extended to also include other disturbances (e.g., storms) and the subsequent potential of deep reef habitat to act as source of larvae for shallow reef areas post-disturbance (Bongaerts et al, 2010a).…”

Section: Introductionmentioning

confidence: 99%

“…Although, models of coral spawning and larval settlement suggest a strong potential for some upper mesophotic corals to act as a source of larvae for shallow environments (Holstein et al, 2016), initial genetic studies on both hosts and symbiotic algae, Symbiodinium, showed differences between coral populations at different depths as well as specific symbiont associations in mesophotic corals (Frade et al, 2008;Serrano et al, 2014;Pochon et al, 2015;Bongaerts et al, 2015a,b). A recent study demonstrated that the potential for vertical connectivity can differ greatly between species within a single reef location indicating that reseeding potential may be relevant for individual species rather than representing a broader ecosystem-wide phenomenon (Bongaerts et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

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Seriatopora Diversity Preserved in Upper Mesophotic Coral Ecosystems in Southern Japan

et al. 2017

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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.

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Deep reefs are not universal refuges: Reseeding potential varies among coral species

Abstract: Genome-wide assessment reveals opposing patterns of vertical connectivity in two depth-generalist coral species.

Cited by 208 publications

References 81 publications

The Future of Coral Reefs Subject to Rapid Climate Change: Lessons from Natural Extreme Environments

The Future of Coral Reefs Subject to Rapid Climate Change: Lessons from Natural Extreme Environments

Using Seawater to Document Coral-Zoothanthella Diversity: A New Approach to Coral Reef Monitoring Using Environmental DNA

Seriatopora Diversity Preserved in Upper Mesophotic Coral Ecosystems in Southern Japan

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