Designing a blueprint for coral reef survival

Kleypas, Joan A.; Allemand, Denis; Anthony, Ken; Baker, Andrew C.; Beck, Michael W.; Hale, Lynne Zeitlin; Hilmi, Nathalie; Høegh-Guldberg, Ove; Hughes, Terry P.; Kaufman, Les; Kayanne, Hajime; Magnan, Alexandre; McLeod, Elizabeth; Mumby, Peter J.; Palumbi, Stephen R.; Richmond, Robert H.; Rinkevich, Baruch; Steneck, Robert S.; Voolstra, Christian R.; Wachenfeld, David; Gattuso, Jean Pierre

doi:10.1016/j.biocon.2021.109107

Cited by 98 publications

(85 citation statements)

References 24 publications

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“…As warming oceans continue to trigger mass bleaching and mortality of reef-building corals around the world, the fate of reef ecosystems is now tightly linked to the heat tolerance of surviving corals. While immediate reduction of emissions and mitigation of warming is of primary importance to ensure coral reef persistence, biological interventions using naturally heat-tolerant corals may also be necessary to maximize resilience in challenging future environments [1][2][3].…”

Section: Introductionmentioning

confidence: 99%

Census of heat tolerance among Florida's threatened staghorn corals finds resilient individuals throughout existing nursery populations

et al. 2021

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The rapid loss of reef-building corals owing to ocean warming is driving the development of interventions such as coral propagation and restoration, selective breeding and assisted gene flow. Many of these interventions target naturally heat-tolerant individuals to boost climate resilience, but the challenges of quickly and reliably quantifying heat tolerance and identifying thermotolerant individuals have hampered implementation. Here, we used coral bleaching automated stress systems to perform rapid, standardized heat tolerance assays on 229 colonies of Acropora cervicornis across six coral nurseries spanning Florida's Coral Reef, USA. Analysis of heat stress dose–response curves for each colony revealed a broad range in thermal tolerance among individuals (approx. 2.5°C range in F v /F m ED50), with highly reproducible rankings across independent tests ( r = 0.76). Most phenotypic variation occurred within nurseries rather than between them, pointing to a potentially dominant role of fixed genetic effects in setting thermal tolerance and widespread distribution of tolerant individuals throughout the population. The identification of tolerant individuals provides immediately actionable information to optimize nursery and restoration programmes for Florida's threatened staghorn corals. This work further provides a blueprint for future efforts to identify and source thermally tolerant corals for conservation interventions worldwide.

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Section: Introductionmentioning

confidence: 99%

Census of heat tolerance among Florida's threatened staghorn corals finds resilient individuals throughout existing nursery populations

et al. 2021

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“…They also form barriers along coastlines which protect lagoons and mangrove habitats, both of which are crucial for vulnerable life-stages of a broad range of commercial and non-commercial species (Coker et al, 2014;McCook et al, 2009). Furthermore, life for tens of millions of people depends on reef ecosystems for protein and other services (Kleypas et al, 2021;Veron et al, 2009).…”

Section: Reef Ecosystem and Threatsmentioning

confidence: 99%

“…The frequency and scale of mass coral bleaching events have escalated since the early 1980s (Baker et al, 2008;Glynn, 1993;Hoegh-Guldberg et al, 2007;Hughes et al, 2018) due to rapid increases in the atmospheric carbon dioxide concentration, which is leading to global warming and ocean acidification; this is threatening the survival of coral reefs beyond the end of the current century (Hoegh-Guldberg et al, 2007;Kleypas et al, 2021). More importantly, the consequences of coral reef destruction are not just limited to socioeconomic losses through impacts on fisheries, tourism and other ecosystem services, but likely also involve the extinction of a large part of the Earth's total biodiversity to a degree that has never happened before in human history (Veron et al, 2009).…”

Section: Reef Ecosystem and Threatsmentioning

confidence: 99%

“…The cnidarian-dinoflagellate association is another symbiotic interaction which plays a key ecological role, in this case the functioning of coral reef ecosystems (Muscatine and Porter, 1977;. This symbiotic association forms one of the most biologically diverse and productive ecosystems on the planet (Hoegh-Guldberg et al, 2007), which provides human communities with benefits such as food, income, recreation, coastal protection and cultural settings (Hoegh-Guldberg et al, 2017;Kleypas et al, 2021).…”

Section: Chapter 1 General Introduction Symbiosismentioning

confidence: 99%

“…Coral reefs are among the most diverse and productive tropical ecosystems. Hermatypic corals are fundamental to these ecosystems and provide a broad range of ecological services, such as providing habitat for other reef organisms (Hoegh-Guldberg, 1999; Kleypas et al, 2021). The success of corals is dependent on their obligatory endosymbiotic relationship with photosynthetic dinoflagellate algae from the family Symbiodiniaceae (Veron et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

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The Impact of Symbiont Diversity on Cellular Integration and Function in the Cnidarian-Dinoflagellate Symbiosis

Mashini¹

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Coral reef ecosystems are one the most important tropical ecosystems, providing a wide variety of ecological services. Reef-building corals form a symbiosis with phototrophic dinoflagellates of the family Symbiodiniaceae, however elevated temperatures disrupt this relationship in a process known as coral bleaching and worldwide bleaching events are increasing in frequency and intensity due to climate change. There is considerable interest in whether corals might adapt to warming conditions by changing their symbionts to a more thermally-tolerant type. The potential to respond is related to capacity for cellular integration between the partners, which underlies the specificity of the host-symbiont relationship. The aim of this thesis was to elucidate the cellular processes associated with hosting native vs. non-native symbionts in the model symbiotic cnidarian Exaiptasia pallida (commonly referred to as ‘Aiptasia’), to assess the potential for establishing a novel partnership. A multidisciplinary approach, including proteomics and quantitative immunocytochemistry, was used, with a particular focus on processes involved in inter-partner nutritional exchange. In Chapter 2, a new method for characterising the proteome of Symbiodiniaceae is described. This method was used to compare the molecular and metabolic pathways underlying a successful symbiosis. Specifically, the proteome of Breviolum minutum, the native symbiont of Aiptasia, was compared when in culture (i.e., free-living) vs. in symbiosis, under a range of nutritional regimes (i.e., N-deplete or N-enriched in culture; starved or well-fed anemones in symbiosis). These various treatments induced distinct proteomes in B. minutum, especially related to immunosuppression to avoid host cell phagosome maturation, metabolic integration, and increased oxidative stress in the symbiotic state. Moreover, the different nutritional regimes impacted the B. minutum proteome, with evidence for increased efficiency nutrient uptake and assimilation under more nutrient-limited conditions. Chapter 3 further characterised the proteome of B. minutum during the process of host colonization, and then compared this to the proteome of a non-native symbiont, the putatively opportunistic but thermally tolerant Durusdinium trenchii, when in symbiosis with Aiptasia. During host colonization over a fourteen-week period, the proteome of B. minutum showed changes related to photosynthesis and chloroplast maintenance as the symbiont density increased, until it eventually reached its peak. Conversely, the proteome of the non-native D. trenchii exhibited a lower abundance of photosynthetic proteins in the fully-established symbiosis, but an upregulation of parasite-like immunosuppression mechanisms, consistent with the view of this species of Symbiodiniaceae being opportunistic. Lastly, in Chapter 4, host nutrient transporters were localized and quantified in Aiptasia, colonized with either the native B. minutum or the non-native D. trenchii and Symbiodinium microadriaticum. Specific immunofluorescent antibodies were designed for four different host transporters of interest: ammonium transporter 1 (AMT1); V-type proton ATPase (VHA); facilitated glucose transporter member 8 (GLUT8); and aquaporin-3 (AQP3, a sugar transporter). Tissue sections were then analysed by confocal microscopy. Hosts harbouring the non-native symbionts showed different transporter localization patterns to those harbouring the native B. minutum, suggesting a lesser degree of host-symbiont integration and disrupted nutritional flux with the non-native symbionts, with S. microadriaticum-colonized anemones being particularly distinct. This thesis therefore adds further weight to the view that the cellular integration necessary to establish a functional symbiosis, with efficient inter-partner nutritional exchange, is not necessarily replicated with non-native symbiont species, which in some cases may persist even when symbiosis function is compromised. Ultimately, this will likely reduce the likelihood that corals might adapt to climate change by changing their symbiont population. On a more positive note, however, this thesis provides new insights into the fundamental cellular mechanisms that underlie a successful cnidarian-dinoflagellate symbiosis and contribute to observable patterns of host-symbiont specificity. Such information is essential if we are to develop the tools necessary for saving the world’s coral reefs, for example through gene-editing and the engineering of more thermally tolerant coral-dinoflagellate partnerships.

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A tale of two reef systems: Local conditions, disturbances, coral life histories, and the climate catastrophe

Gilmour

Cook

Ryan

et al. 2022

Ecological Applications

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Coral reefs have evolved over millennia to survive disturbances. Yet, in just a few decades chronic local pressures and the climate catastrophe have accelerated so quickly that most coral reefs are now threatened. Rising ocean temperatures and recurrent bleaching pose the biggest threat, affecting even remote and well-managed reefs on global scales. We illustrate how coral bleaching is altering reefs by contrasting the dynamics of adjacent reef systems over more than two decades. Both reef systems sit near the edge of northwest Australia's continental shelf, have escaped chronic local pressures and are regularly affected by tropical storms and cyclones. The Scott reef system has experienced multiple bleaching events, including mass bleaching in 1998 and 2016, from which it is unlikely to fully recover. The Rowley Shoals has maintained a high cover and diversity of corals and has not yet been impacted by mass bleaching. We show how the dynamics of both reef systems were driven by a combination of local environment, exposure to disturbances and coral life history traits, and consider future shifts in community structure with ongoing climate change. We then demonstrate how applying knowledge of community dynamics at local scales can aid management strategies to slow the degradation of coral reefs until carbon emissions and other human impacts are properly managed.

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Designing a blueprint for coral reef survival

Cited by 98 publications

References 24 publications

Census of heat tolerance among Florida's threatened staghorn corals finds resilient individuals throughout existing nursery populations

Census of heat tolerance among Florida's threatened staghorn corals finds resilient individuals throughout existing nursery populations

The Impact of Symbiont Diversity on Cellular Integration and Function in the Cnidarian-Dinoflagellate Symbiosis

A tale of two reef systems: Local conditions, disturbances, coral life histories, and the climate catastrophe

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