The Bouraké semi-enclosed lagoon (New Caledonia) – a natural laboratory to study the lifelong adaptation of a coral reef ecosystem to extreme environmental conditions

Abstract

Abstract. According to current experimental evidence, coral reefs could disappear within the century if CO2 emissions remain unabated. However, recent discoveries of diverse and high cover reefs that already live under extreme conditions suggest that some corals might thrive well under hot, high-pCO2, and deoxygenated seawater. Volcanic CO2 vents, semi-enclosed lagoons, and mangrove estuaries are unique study sites where one or more ecologically relevant parameters for life in the oceans are close to or even worse than currently projected for the year 2100. Although they do not perfectly mimic future conditions, these natural laboratories offer unique opportunities to explore the mechanisms that reef species could use to keep pace with climate change. To achieve this, it is essential to characterize their environment as a whole and accurately consider all possible environmental factors that may differ from what is expected in the future, possibly altering the ecosystem response. This study focuses on the semi-enclosed lagoon of Bouraké (New Caledonia, southwest Pacific Ocean) where a healthy reef ecosystem thrives in warm, acidified, and deoxygenated water. We used a multi-scale approach to characterize the main physical-chemical parameters and mapped the benthic community composition (i.e., corals, sponges, and macroalgae). The data revealed that most physical and chemical parameters are regulated by the tide, strongly fluctuate three to four times a day, and are entirely predictable. The seawater pH and dissolved oxygen decrease during falling tide and reach extreme low values at low tide (7.2 pHT and 1.9 mg O2 L−1 at Bouraké vs. 7.9 pHT and 5.5 mg O2 L−1 at reference reefs). Dissolved oxygen, temperature, and pH fluctuate according to the tide by up to 4.91 mg O2 L−1, 6.50 ∘C, and 0.69 pHT units on a single day. Furthermore, the concentration of most of the chemical parameters was 1 to 5 times higher at the Bouraké lagoon, particularly for organic and inorganic carbon and nitrogen but also for some nutrients, notably silicates. Surprisingly, despite extreme environmental conditions and altered seawater chemical composition measured at Bouraké, our results reveal a diverse and high cover community of macroalgae, sponges, and corals accounting for 28, 11, and 66 species, respectively. Both environmental variability and nutrient imbalance might contribute to their survival under such extreme environmental conditions. We describe the natural dynamics of the Bouraké ecosystem and its relevance as a natural laboratory to investigate the benthic organism's adaptive responses to multiple extreme environmental conditions.

Novel coexisting mangrove-coral habitats: Extensive coral communities located deep within mangrove canopies of Panama, a global classification system and predicted distributions

“…All presently reported CMC habitats in the literature occur at a shallow depth and are microtidal (≤2 m) [ 36 , 44 , 47 , 48 , 61 , 62 ]. We therefore narrowed down the potential CMC habitat by areas with a tidal amplitude of ≤2 m, since a greater tidal amplitude would lead to prolonged air exposure of corals in this area.…”

Metabolomic signatures of corals thriving across extreme reef habitats reveal strategies of heat stress tolerance

“…Coral populations that can cope with, or recover from, increasingly frequent and intense stress events are critical to the persistence of tropical reefs, and recent efforts to predict the future structure and functioning of reefs have logically focussed on resolving the nature of coral tolerance to acute heating events [5][6][7][8][9][10]. One approach has been to examine coral populations that have adapted to present day extreme environments; for example, warm lagoons [11,12], intertidal pools [13,14] and thermally extreme seas [15,16]. Profiling coral biology from these so-called 'natural laboratories' has shown how numerous factors contribute to high heat tolerance, including rapid modifications in gene expression related to extracellular matrix formation and oxidative stress [17,18], heat-shock protein upregulation [19], but also rapid recovery to a pre-disturbance baseline level of these differentially expressed genes [20].…”

“…Corals thriving in mangrove lagoons adjacent to tropical reefs are characterized by particularly extreme environmental conditions. Waters within reef-neighbouring mangrove lagoon habitats can reach 33°C (Woody Isles, Great Barrier Reef) in summer [24], which is well above the tolerance threshold for many reef corals [3], but also experience extensive diel acidification ( pH range 7.2-8.2) and deoxygenation (oxygen range 0.6-7.33 mg l −1 ) [11,25]. Despite these relatively extreme lagoonal conditions, coral populations can thrive through associations with different microbial communities, including both micro-algal endosymbionts (family: Symbiodiniaceae) and bacteria [24,26,27], and exhibit very different metabolic properties compared to the reef corals [12,25,27].…”

Rapid Shifts in Bacterial Communities and Homogeneity of Symbiodiniaceae in Colonies of Pocillopora acuta Transplanted Between Reef and Mangrove Environments

“…Extreme systems recently identified as ideal sites for studying coral resilience to complex stressor regimes are reef adjacent mangrove lagoons ( Camp et al, 2018 ), which can be inhabited by species of reef-building corals commonly found on nearby reefs ( Macintyre et al, 2000 ; Rogers, 2009 , 2017 ; Camp et al, 2017 , 2019 ; Lord et al, 2020 ). Mangroves can reduce thermal stress by shading corals, but these shallow environments also expose corals to hotter, more acidic and deoxygenated conditions ( Rogers and Herlan, 2012 ; Camp et al, 2017 ; Rogers, 2017 ; Maggioni et al, 2021 ). Compared to adjacent reefs, where pH levels fluctuate between 8.1 and 8.2, mangrove lagoons can exhibit consistently low pH (below 7.8), with daily drops to below 7.3 ( Camp et al, 2017 , 2019 ).…”