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Marine coastal zones are highly productive, and dominated by engineer species (e.g. macrophytes, molluscs, corals) that modify the chemistry of their surrounding seawater via their metabolism, causing substantial fluctuations in oxygen, dissolved inorganic carbon, pH, and nutrients. The magnitude of these biologically driven chemical fluctuations is regulated by hydrodynamics, can exceed values predicted for the future open ocean, and creates chemical patchiness in subtidal areas at various spatial (µm to meters) and temporal (minutes to months) scales. Although the role of hydrodynamics is well explored for planktonic communities, its influence as a crucial driver of benthic organism and community functioning is poorly addressed, particularly in the context of ocean global change. Hydrodynamics can directly modulate organismal physiological activity or indirectly influence an organism's performance by modifying its habitat. This review addresses recent developments in (i) the influence of hydrodynamics on the biological activity of engineer species, (ii) the description of chemical habitats resulting from the interaction between hydrodynamics and biological activity, (iii) the role of these chemical habitat as refugia against ocean acidification and deoxygenation, and (iv) how species living in such chemical habitats may respond to ocean global change. Recommendations are provided to integrate the effect of hydrodynamics and environmental fluctuations in future research, to better predict the responses of coastal benthic ecosystems to ongoing ocean global change.
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Ecosistema , Agua de Mar , Hidrodinámica , Concentración de Iones de Hidrógeno , Océanos y Mares , Agua de Mar/químicaRESUMEN
Ocean warming impacts the fitness of marine ectothermic species, leading to poleward range shifts, re-shuffling of communities, and changes in ecosystem services. While the detrimental effects of summer heat waves have been widely studied, little is known about the impacts of winter warming on marine species in temperate regions. Many species benefit from low winter temperature-induced reductions in metabolism, as these permit conservation of energy reserves that are needed to support reproduction in spring. Here, we used a unique outdoor mesocosm system to expose a coastal predator-prey system, the sea star Asterias and the blue mussel Mytilus, to different winter warming scenarios under near-natural conditions. We found that the body condition of mussels decreased in a linear fashion with increasing temperature. Sea star growth also decreased with increasing temperature, which was a function of unaltered predation rates and decreased mussel body condition. Asterias relative digestive gland mass strongly declined over the studied temperature interval (ca twofold). This could have severe implications for reproductive capacity in the following spring, as digestive glands provide reserve compounds to maturing gonads. Thus, both predator and prey suffered from a mismatch of energy acquisition versus consumption in warmer winter scenarios, with pronounced consequences for food web energy transfer in future oceans.
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Bivalvos/fisiología , Cambio Climático , Conducta Predatoria/fisiología , Agua de Mar/química , Estrellas de Mar/fisiología , Animales , Ecosistema , Cadena Alimentaria , Océanos y Mares , Estaciones del Año , Inanición , TemperaturaRESUMEN
Reef-building corals live in highly hydrodynamic environments, where water flow largely controls the complex chemical microenvironments surrounding them-the concentration boundary layer (CBL). The CBL may be key to alleviate ocean acidification (OA) effects on coral colonies by partially isolating them. However, OA effects on coral CBL remain poorly understood, particularly under different flow velocities. Here, we investigated these effects on the reef-building corals Acropora cytherea, Pocillopora verrucosa, and Porites cylindrica. We preconditioned corals to a control (pH 8.0) and OA (pH 7.8) treatment for four months and tested how low flow (2 cm s-1) and moderate flow (6 cm s-1) affected O2 and H+ CBL traits (thickness, surface concentrations, and flux) inside a unidirectional-flow chamber. We found that CBL traits differed between species and flow velocities. Under OA, traits remained generally stable across flows, except surface pH. In all species, the H+ CBL was thin and led to lower surface pH. Still, low flow thickened H+ CBLs and increased light elevation of surface pH. In general, our findings reveal a weak to null OA modulation of the CBL. Moreover, the OA-buffering capacity by the H+ CBL may be limited in coral species, though low flow could enhance CBL sheltering.
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Antozoos , Océanos y Mares , Oxígeno , Agua de Mar , Antozoos/fisiología , Antozoos/metabolismo , Animales , Concentración de Iones de Hidrógeno , Oxígeno/metabolismo , Oxígeno/química , Agua de Mar/química , Arrecifes de Coral , Movimientos del Agua , Acidificación de los OcéanosRESUMEN
There is growing evidence that reef-building corals can acclimate to novel and challenging thermal conditions. However, potential trade-offs that accompany acclimation remain largely unexplored. We investigated physiological trade-offs in colonies of a globally abundant coral species (Pocillopora acuta) that were acclimated ex situ to an elevated temperature of 31 °C (i.e., 1 °C above their bleaching threshold) for six years. By comparing them to conspecifics maintained at a cooler temperature, we found that the energy storage of corals was prioritized over skeletal growth at the elevated temperature. This was associated with the formation of higher density skeletons, lower calcification rates and consequently lower skeletal extension rates, which entails ramifications for future reef-building processes, structural complexity and reef community composition. Furthermore, symbionts were physiologically compromised at 31 °C and had overall lower energy reserves, likely due to increased exploitation by their host, resulting in an overall lower stress resilience of the holobiont. Our study shows how biological trade-offs of thermal acclimation unfold, helping to refine our picture of future coral reef trajectories. Importantly, our observations in this six-year study do not align with observations of short-term studies, where elevated temperatures were often associated with the depletion of energy reserves, highlighting the importance of studying acclimation of organisms at relevant biological scales.
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Aclimatación , Antozoos , Arrecifes de Coral , Antozoos/fisiología , Animales , Aclimatación/fisiología , TemperaturaRESUMEN
The relationship between energy reserves of cold-water corals (CWCs) and their physiological performance remains largely unknown. In addition, it is poorly understood how the energy allocation to different metabolic processes might change with projected decreasing food supply to the deep sea in the future. This study explores the temporal and spatial variations of total energy reserves (proteins, carbohydrates and lipids) of the CWC Desmophyllum dianthus and their correlation with its calcification rate. We took advantage of distinct horizontal and vertical physico-chemical gradients in Comau Fjord (Chile) and examined the changes in energy reserves over one year in an in situ reciprocal transplantation experiment (20 m vs. 300 m and fjord head vs. mouth). Total energy reserves correlated positively with calcification rates. The fast-growing deep corals had higher and less variable energy reserves, while the slower-growing shallow corals showed pronounced seasonal changes in energy reserves. Novel deep corals (transplanted from shallow) were able to quickly increase both their calcification rates and energy reserves to similar levels as native deep corals. Our study shows the importance of energy reserves in sustaining CWC growth in spite of aragonite undersaturated conditions (deep corals) in the present, and potentially also future ocean.
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Antozoos , Animales , Antozoos/fisiología , Estuarios , Calcificación Fisiológica/fisiología , Agua , Carbonato de Calcio , Arrecifes de CoralRESUMEN
Pocillopora damicornis (Linnaeus, 1758), a species complex, consists of several genetic lineages, some of which likely represent reproductively isolated species, including the species Pocillopora acuta Lamarck, 1816. Pocillopora acuta can exhibit similar morphological characteristics as P. damicornis, thus making it difficult to identify species-level taxonomic units. To determine whether the P. damicornis-like colonies on the reefs in the Andaman Sea (previously often identified as P. damicornis) consist of different species, we sampled individual colonies at five sites along a 50 km coastal stretch at Phuket Island and four island sites towards Krabi Province, Thailand. We sequenced 210 coral samples for the mitochondrial open reading frame and identified six distinct haplotypes, all belonging to P. acuta according to the literature. Recently, P. acuta was observed to efficiently recolonize heat-damaged reefs in Thailand as well as globally, making it a potentially important coral species in future reefs. Specifically in the light of global change, this study underscores the importance of high-resolution molecular species recognition, since taxonomic units are important factors for population genetic studies, and the latter are crucial for management and conservation efforts.
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BACKGROUND: The widespread Indo-Pacific coral species Pocillopora acuta Lamarck, 1816 displays varying levels of asexual versus sexual reproduction, with strong repercussions on genetic diversity, connectivity and genetic structuring within and among populations. For many geographic regions, baseline information on genetic diversity is still lacking, particularly in the Andaman Sea. The region suffered a massive heat-induced bleaching event in 2010 with high coral cover loss of branching coral species such as P. acuta. A subsequent bleaching in 2016, however, revealed a mild bleaching response in pocilloporids compared to other coral taxa in the region, suggesting that rare, heat tolerant genotypes had been selected by the 2010 bleaching event. In order to test whether this potential 'evolutionary rescue' event has led to a low genetic diversity, we conducted a population genetic survey covering a total of nine different P. acuta populations (336 individuals) along a 50 km coastal stretch around Phuket Island, Thailand. We used six microsatellite markers to assess genotypic diversity and to determine the prevalent mode of reproduction (i.e. sexual or asexual recruitment). RESULTS: In contrast to other Indian Ocean P. acuta populations, the majority of corals in this study adopted a sexual reproduction mode (75% across all populations). At the same time, substantial regional gene flow was observed around Phuket Island with strong genetic differentiation as indicated by three genetic clusters that were separated by only a few kilometers. Patterns of isolation by distance over 0.7 - 40 km suggest small-scale genetic barriers, such as changing currents throughout each monsoonal season, potentially contributing to locally restricted dispersal of P. acuta larvae. CONCLUSIONS: The occurrence of distinct genetic clusters within short coastal stretches suggests that the 2010 bleaching event has not led to extreme genetic impoverishment. While more in-depth genomic analyses are necessary to investigate changes in genetic diversity following extreme bleaching events, our results will help guide conservation efforts to maintain genetic diversity of a coral species that likely will be dominant in future, warmer Andaman Sea reefs.
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Antozoos , Animales , Antozoos/genética , Tailandia , Flujo Genético , Evolución Biológica , Ácido Hipocloroso , Genética de PoblaciónRESUMEN
Cold-water corals (CWCs) are considered vulnerable to environmental changes. However, previous studies have focused on adult CWCs and mainly investigated the short-term effects of single stressors. So far, the effects of environmental changes on different CWC life stages are unknown, both for single and multiple stressors and over long time periods. Therefore, we conducted a six-month aquarium experiment with three life stages of Caryophyllia huinayensis to study their physiological response (survival, somatic growth, calcification and respiration) to the interactive effects of aragonite saturation (0.8 and 2.5), temperature (11 and 15 °C) and food availability (8 and 87 µg C L-1). The response clearly differed between life stages and measured traits. Elevated temperature and reduced feeding had the greatest effects, pushing the corals to their physiological limits. Highest mortality was observed in adult corals, while calcification rates decreased the most in juveniles. We observed a three-month delay in response, presumably because energy reserves declined, suggesting that short-term experiments overestimate coral resilience. Elevated summer temperatures and reduced food supply are likely to have the greatest impact on live CWCs in the future, leading to reduced coral growth and population shifts due to delayed juvenile maturation and high adult mortality.
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Antozoos , Animales , Antozoos/fisiología , Agua de Mar , Concentración de Iones de Hidrógeno , Acidificación de los Océanos , Agua , Arrecifes de CoralRESUMEN
Coral calcification is a complex biologically controlled process of hard skeleton formation, and it is influenced by environmental conditions. The chemical composition of coral skeletons responds to calcification conditions and can be used to gain insights into both the control asserted by the organism and the environment. Boron and its isotopic composition have been of particular interest because of links to carbon chemistry and pH. In this study, we acquired high-resolution boron images (concentration and isotopes) in a skeleton sample of the azooxanthellate cold-water coral Lophelia pertusa. We observed high boron variability at a small spatial scale related to skeletal structure. This implies differences in calcification control during different stages of skeleton formation. Our data point to bicarbonate active transport as a critical pathway during early skeletal growth, and the variable activity rates explain the majority of the observed boron systematic.
RESUMEN
The stratified Chilean Comau Fjord sustains a dense population of the cold-water coral (CWC) Desmophyllum dianthus in aragonite supersaturated shallow and aragonite undersaturated deep water. This provides a rare opportunity to evaluate CWC fitness trade-offs in response to physico-chemical drivers and their variability. Here, we combined year-long reciprocal transplantation experiments along natural oceanographic gradients with an in situ assessment of CWC fitness. Following transplantation, corals acclimated fast to the novel environment with no discernible difference between native and novel (i.e. cross-transplanted) corals, demonstrating high phenotypic plasticity. Surprisingly, corals exposed to lowest aragonite saturation (Ωarag < 1) and temperature (T < 12.0 °C), but stable environmental conditions, at the deep station grew fastest and expressed the fittest phenotype. We found an inverse relationship between CWC fitness and environmental variability and propose to consider the high frequency fluctuations of abiotic and biotic factors to better predict the future of CWCs in a changing ocean.
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Antozoos , Dianthus , Adaptación Fisiológica , Animales , Antozoos/fisiología , Carbonato de Calcio , Estuarios , AguaRESUMEN
BACKGROUND: Microbiome manipulation could enhance heat tolerance and help corals survive the pressures of ocean warming. We conducted coral microbiome transplantation (CMT) experiments using the reef-building corals, Pocillopora and Porites, and investigated whether this technique can benefit coral heat resistance while modifying the bacterial microbiome. Initially, heat-tolerant donors were identified in the wild. We then used fresh homogenates made from coral donor tissues to inoculate conspecific, heat-susceptible recipients and documented their bleaching responses and microbiomes by 16S rRNA gene metabarcoding. RESULTS: Recipients of both coral species bleached at lower rates compared to the control group when exposed to short-term heat stress (34 °C). One hundred twelve (Pocillopora sp.) and sixteen (Porites sp.) donor-specific bacterial species were identified in the microbiomes of recipients indicating transmission of bacteria. The amplicon sequence variants of the majority of these transmitted bacteria belonged to known, putatively symbiotic bacterial taxa of corals and were linked to the observed beneficial effect on the coral stress response. Microbiome dynamics in our experiments support the notion that microbiome community evenness and dominance of one or few bacterial species, rather than host-species identity, were drivers for microbiome stability in a holobiont context. CONCLUSIONS: Our results suggest that coral recipients likely favor the uptake of putative bacterial symbionts, recommending to include these taxonomic groups in future coral probiotics screening efforts. Our study suggests a scenario where these donor-specific bacterial symbionts might have been more efficient in supporting the recipients to resist heat stress compared to the native symbionts present in the control group. These findings urgently call for further experimental investigation of the mechanisms of action underlying the beneficial effect of CMT and for field-based long-term studies testing the persistence of the effect. Video abstract.
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Antozoos , Microbiota , Termotolerancia , Animales , Arrecifes de Coral , ARN Ribosómico 16S/genética , SimbiosisRESUMEN
The Andaman Sea and other macrotidal semi-enclosed tropical seas feature large amplitude internal waves (LAIW). Although LAIW induce strong fluctuations i.e. of temperature, pH, and nutrients, their influence on reef development is so far unknown. A better-known source of disturbance is the monsoon affecting corals due to turbulent mixing and sedimentation. Because in the Andaman Sea both, LAIW and monsoon, act from the same westerly direction their relative contribution to reef development is difficult to discern. Here, we explore the framework development in a number of offshore island locations subjected to differential LAIW- and SW-monsoon impact to address this open question. Cumulative negative temperature anomalies - a proxy for LAIW impact - explained a higher percentage of the variability in coral reef framework height, than sedimentation rates which resulted mainly from the monsoon. Temperature anomalies and sediment grain size provided the best correlation with framework height suggesting that so far neglected subsurface processes (LAIW) play a significant role in shaping coral reefs.