Mangrove lagoons of the Great Barrier Reef support coral populations persisting under extreme environmental conditions

By E. Camp, J. Edmondson, A. Doheny, J. Rumney, Amanda J. Grima, Alfredo R. Huete, David John Suggett. Marine Ecology Progress Series, 2019

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Global degradation of coral reefs has increased the urgency of identifying stress-tolerant coral populations, to enhance understanding of the bio logy driving stress tolerance, as well as identifying stocks of stress-hardened populations to aid reef rehabilitation. Surprisingly, scientists are continually discovering that naturally extreme environments house established coral populations adapted to grow within extreme abiotic conditions comparable to seawater conditions predicted over the coming century. Such environments include inshore mangrove lagoons that carry previously unrecognised ecosystem service value for corals, spanning from refuge to stress preconditioning. However, the existence of such hot-spots of resilience on the Great Barrier Reef (GBR) remains entirely unknown. Here we describe, for the first time, 2 extreme GBR mangrove lagoons (Woody Isles and Howick Island), exposing taxonomically diverse coral communities (34 species, 7 growth morphologies) to regular extreme low pH (<7.6), low oxygen (<1 mg l−1) and highly variable temperature range (>7°C) conditions. Coral cover was typically low (<5%), but highly patchy and included established colonies (>0.5 m diameter), with net photosynthesis and calcification rates of 2 dominant coral species (Acropora millepora, Porites lutea) reduced (20− 30%), and respiration enhanced (11−35%), in the mangrove lagoon relative to adjacent reefs. Further analysis revealed that physiological plasticity (photosynthetic ‘strategy’) and flexibility of Symbiodiniaceae taxa associations appear crucial in supporting coral capacity to thrive from reef to lagoon. Prevalence of corals within these extreme conditions on the GBR (and elsewhere) increasingly challenge our understanding of coral resilience to stressors, and highlight the need to study unfavourable coral environments to better resolve mechanisms of stress tolerance. OPEN ACCESS © The authors 2019. Open Access under Creative Commons by Attribution Licence. Use, distribution and reproduction are un restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com Acropora millepora colony thriving under extreme low pH, low oxygen and highly variable temperatures of a Great Barrier Reef mangrove lagoon. Photo: Emma Camp Mar Ecol Prog Ser 625: 1–14, 2019 declines in coral reproductive capacity (Hughes et al. 2019) and reef accretion (McMahon et al. 2019), compromising the potential resilience of the reef to the anticipated increase in frequency and intensity of bleaching events (Oliver et al. 2018). While environmental filtering of thermally tolerant corals surviving after bleaching events will naturally select for some thermally resilient taxa, reductions in coral species that have traits supporting key ecological functions, e.g. reductions in species contributing to habitat provision and rapid reef accretion (Hughes et al. 2018), creates a need to identify and study potential hotspots of coral resilience where these species will be supported. Such hot-spots of resilience include both coral refugia (locations maintaining favourable conditions being lost elsewhere, sensu Keppel & WardellJohnson 2012; e.g. the northern Red Sea, Osman et al. 2018) and habitats housing intrinsically resilient coral populations (reviewed by Camp et al. 2018a). To date, studies of coral refugia environments documented on the GBR have focussed on environments that dampen the effects of heat stress; for example, microrefugia operating over small scales appeared to enable stress-sensitive Acropora coral populations to persist through the 2016−2017 marine heatwaves (Hoogenboom et al. 2017). Bleaching models have also predicted that the southern end of the GBR may act as a temporary coral refugium (van Hooidonk et al. 2013). However, with current rates of ocean warming (IPCC 2014), and the increased frequency of marine heatwaves (Oliver et al. 2018), it remains unclear how long this geographic thermal refuge may operate. Deep reefs of the GBR were also documented to provide transient refuge to corals during the 2016− 2017 bleaching event (Frade et al. 2018). Although incidence of coral bleaching was lower at deep reef sites (40 m), the cold water associated with the refugia resulted from seasonal oceanographic processes, temporally constraining the refuge capacity (Frade et al. 2018). These findings are consistent with other global upwelling refugia sites, where such temporal refuge restrictions operate (e.g. Chollett et al. 2010). In contrast, more temporally stable refugia on the GBR are inshore, turbid reefs. Inshore reefs of the GBR attenuate solar irradiance that otherwise can exacerbate thermal stress, resulting in reduced bleaching severity and sustained coral cover post-bleaching (Morgan et al. 2017). While refugia will contribute to aiding some coral populations through periods of stress, their temporal and spatial restrictions, combined with the fact that most refugia only offset a single stressor (reviewed by Camp et al. 2018b), means that there is arguably a more time-critical need to identify and study naturally resilient coral populations in order to (1) understand which coral species can best survive multiple stressors, (2) identify the key mechanisms that support coral survival and (3) reveal any associated biological and ecological costs to corals with enhanced stress tolerance. Such knowledge can aid decisions that currently need to be made regarding which species should be targeted for restoration and adaptive management options (e.g. the GBR; Suggett et al. 2019), while highlighting potential risks associated with bio diversity and reef services. Studies from natural extreme reef environments, such as carbon dioxide vents (e.g. Fabricius et al. 2011, Enochs et al. 2015), back reef tide pools on Ofu Island (Smith et al. 2007, Oliver & Palumbi 2009, 2011a) and mangrove lagoons (Camp et al. 2016a, 2017) have revealed that phenotypic plasticity, particularly in traits related to energy acquisition, are important in supporting coral survival (Camp et al. 2018b). For example, under naturally acidified waters, corals continue to calcify through increased photosynthesis rates to meet the required energy demands (Strahl et al. 2015). Changes in dominant algal symbiont (e.g. Oliver & Palumbi 2011b) and increased photosynthetic efficiency per cell of Symbiodiniaceae (Camp et al. 2016b) have also been shown to facilitate coral survival in naturally variable in-shore reef habitats. In mangrove lagoons, corals also ap pear to enhance respiration rates, indicative of in creased heterotrophy, which may offset losses to photosynthetic capacity and therefore facilitate their survival (Camp et al. 2017). Mangrove lagoons are of particular interest because they consistently expose resident coral populations to low pH, low oxygen and warmer waters relative to adjacent reefs (Seychelles, Indonesia, Camp et al. 2016a; New Caledonia, Camp et al. 2017), i.e. the primary trio of stressors predicted to impact coral reefs under climate change (IPCC 2014, Camp et al. 2018b). For example, in New Caledonia, corals in the Bouraké mangrove lagoon were regularly exposed to pH below 7.4, oxygen below 2 mg l−1, and temperature 2°C higher than the adjacent reef (Camp et al. 2017). Whether mangrove lagoons of the GBR have similarly extreme abiotic conditions and house abundant and/or diverse coral communities remains entirely unknown. Furthermore, if these locations exist, whether resident coral populations employ plasticity in energy acquisition modes and conform with observations reported from other extreme inshore coral habitats is also unknown. Here we surveyed 250 km of the northern GBR, visiting lagoons located on 5 off-shore islands. From this exploration, we identified for the first time 2 man2 Camp et al.: GBR corals thriving in extreme lagoons grove lagoons with relatively extreme environmental conditions (low pH, low oxygen and highly varying temperature), coupled to significant coral cover and/or diversity. Targeted studies of resident corals at one of these locations (Woody Isles) were then used to test our hypotheses that the mangrove corals relative to adjacent reef corals would (1) have enhanced respiration rates relative to net photosynthesis, (2) house different dominant Symbiodiniaceae taxa, and consequently (3) use different photosynthetic ‘strategies’ to survive the extreme physicochemical conditions. Through this work, we demonstrate that physiological plasticity (photosynthetic ‘strategy’) combined with unique symbiont diversity supports coral survival in the GBR mangrove lagoons, but that reductions in calcification rates are an associated survival trade-off. These findings contribute to the growing body of evidence that these traits are important for coral survival under suboptimal environmental conditions that are analogous to those predicted under climate change (Camp et al. 2018b). 2. MATERIALS AND METHODS Five islands (Woody Isles, Two Isles, Hope Isles, Nymph Isles and Howick Island) adjacent to coral reefs on the GBR were investigated in June 2017 for prevalence of coral communities and associated abiotic conditions (Table 1). These sites were selected based on local knowledge (J. Rumney pers. obs.) and prior knowledge of mangrove lagoon geomorphologies likely to house extreme coral communities (Camp et al. 2016a, 2017). Sites were initially examined via satellite imagery (Google EarthTM) for key features (e.g. distance from a coral reef, presence of channels in the mangroves, their orientation to wind direction and image optical signatures characteristic of corals). Upon exploration, we found that 2 of these sites, Woody Isles (16.388° S, 145.566° E) and Howick Island (14.497° S, 144.972° E), housed corals living within the mangrove lagoons (Fig. S1 in the Supplement at www. int-res. com/ articles/ suppl/ m625 p001 _ supp .pdf). Both sites had no visible significant freshwater catchme

Subfields: Ecology, Global and Planetary Change, Oceanography

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