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Patterns and implications of spatial covariation in herbivore functions on resilience of coral reefsAbstract Persistent shifts to undesired ecological states, such as shifts from coral to macroalgae, are becoming more common. This highlights the need to understand processes that can help restore affected ecosystems. Herbivory on coral reefs is widely recognized as a key interaction that can keep macroalgae from outcompeting coral. Most attention has been on the role ‘grazing’ herbivores play in preventing the establishment of macroalgae, while less research has focused on the role of ‘browsers’ in extirpating macroalgae. Here we explored patterns, environmental correlates and state shift consequences of spatial co-variation in grazing and browsing functions of herbivorous fishes. Grazing and browsing rates were not highly correlated across 20 lagoon sites in Moorea, French Polynesia, but did cluster into 3 (of 4) combinations of high and low consumption rates (no site had low grazing but high browsing). Consumption rates were not correlated with grazer or browser fish biomass, but both were predicted by specific environmental variables. Experiments revealed that reversibility of a macroalgal state shift was strongly related to spatial variation in browsing intensity. Our findings provide insights and simple diagnostic tools regarding heterogeneity in top-down forcing that influences the vulnerability to and reversibility of shifts to macroalgae on coral reefs.more » « less
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ABSTRACT MotivationHere, we make available a second version of the BioTIME database, which compiles records of abundance estimates for species in sample events of ecological assemblages through time. The updated version expands version 1.0 of the database by doubling the number of studies and includes substantial additional curation to the taxonomic accuracy of the records, as well as the metadata. Moreover, we now provide an R package (BioTIMEr) to facilitate use of the database. Main Types of Variables IncludedThe database is composed of one main data table containing the abundance records and 11 metadata tables. The data are organised in a hierarchy of scales where 11,989,233 records are nested in 1,603,067 sample events, from 553,253 sampling locations, which are nested in 708 studies. A study is defined as a sampling methodology applied to an assemblage for a minimum of 2 years. Spatial Location and GrainSampling locations in BioTIME are distributed across the planet, including marine, terrestrial and freshwater realms. Spatial grain size and extent vary across studies depending on sampling methodology. We recommend gridding of sampling locations into areas of consistent size. Time Period and GrainThe earliest time series in BioTIME start in 1874, and the most recent records are from 2023. Temporal grain and duration vary across studies. We recommend doing sample‐level rarefaction to ensure consistent sampling effort through time before calculating any diversity metric. Major Taxa and Level of MeasurementThe database includes any eukaryotic taxa, with a combined total of 56,400 taxa. Software Formatcsv and. SQL.more » « less
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Rodil, Ivan (Ed.)Abstract Understanding the mechanisms underlying nutrient (nitrogen and phosphorus) and carbon cycling in reefs is critical for effective management. Research on reef nutrient and carbon cycling needs to account for (i) the contributions of multiple organisms, (ii) abiotic and biotic drivers, and (iii) a social-ecological perspective. In this paper, we review the mechanisms underlying nutrient and carbon cycling in reef social-ecological systems and analyse them using causal loop analysis. We identify direct and indirect pathways and feedback loops through nutrient and carbon cycles that shape the dominant benthic state of reefs: coral, algal, and sponge-dominated states. We find that two of three anthropogenic impact scenarios (size-selective fishing and land use change) have primarily negative consequences for coral and macroalgae via the nutrient and carbon cycles. A third scenario (runoff) has fewer negative impacts on sponges compared to other benthos. In all scenarios, frequent positive feedback loops (size-selective fishing: 7 of 12 loops; runoff: 6 of 9 loops; land use change: 8 of 11 loops) lead to system destabilization; however, the presence of multiple loops introduces avenues whereby reefs may retain coral dominance despite anthropogenic pressures. Context-specific information on the relative strength of loops will be necessary to predict future reef state.more » « less
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ABSTRACT Spatial processes, particularly scale‐dependent feedbacks, may play important and underappreciated roles in the dynamics of bistable ecosystems. For example, self‐organised spatial patterns can allow for stable coexistence of alternative states outside regions of bistability, a phenomenon known as a Busse balloon. We used partial differential equations to explore the potential for such dynamics in coral reefs, focusing on how herbivore behaviour and mobility affect the stability of coral‐ and macroalgal‐dominated states. Herbivore attraction to coral resulted in a Busse balloon that enhanced macroalgal resilience, with patterns persisting in regions of parameter space where nonspatial models predict uniform coral dominance. Thus, our work suggests herbivore association with coral (e.g., for shelter) can prevent reefs from reaching a fully coral‐dominated state. More broadly, this study illustrates how consumer space use can prevent ecosystems from undergoing wholesale state transitions, highlighting the importance of explicitly accounting for space when studying bistable systems.more » « less
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ABSTRACT Dissolved organic matter (DOM) comprises diverse compounds with variable bioavailability across aquatic ecosystems. The sources and quantities of DOM can influence microbial growth and community structure with effects on biogeochemical processes. To investigate the chemodiversity of labile DOM in tropical reef waters, we tracked microbial utilisation of over 3000 untargeted mass spectrometry ion features exuded from two coral and three algal species. Roughly half of these features clustered into over 500 biologically labile spectral subnetworks annotated to diverse structural superclasses, including benzenoids, lipids, organic acids, heterocyclics and phenylpropanoids, comprising on average one‐third of the ion richness and abundance within each chemical class. Distinct subsets of these labile compounds were exuded by algae and corals during the day and night, driving differential microbial growth and substrate utilisation. This study expands the chemical diversity of labile marine DOM with implications for carbon cycling in coastal environments.more » « less
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Abstract Coral reefs are in global decline with coral diseases playing a significant role. This is especially true for Acroporid corals that represent ~25% of all Pacific coral species and generate much of the topographic complexity supporting reef biodiversity. Coral diseases are commonly sediment-associated and could be exacerbated by overharvest of sea cucumber detritivores that clean reef sediments and may suppress microbial pathogens as they feed. Here we show, via field manipulations in both French Polynesia and Palmyra Atoll, that historically overharvested sea cucumbers strongly suppress disease among corals in contact with benthic sediments. Sea cucumber removal increased tissue mortality ofAcropora pulchraby ~370% and colony mortality by ~1500%. Additionally, farmerfish that killAcropora pulchrabases to culture their algal gardens further suppress disease by separating corals from contact with the disease-causing sediment—functioning as mutualists rather than parasites despite killing coral bases. Historic overharvesting of sea cucumbers increases coral disease and threatens the persistence of tropical reefs. Enhancing sea cucumbers may enhance reef resilience by suppressing disease.more » « less
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Abstract Coral bleaching is a well-documented and increasingly widespread phenomenon in reefs across the globe, yet there has been relatively little research on the implications for reef water column microbiology and biogeochemistry. A mesocosm heating experiment and bottle incubation compared how unbleached and bleached corals alter dissolved organic matter (DOM) exudation in response to thermal stress and subsequent effects on microbial growth and community structure in the water column. Thermal stress of healthy corals tripled DOM flux relative to ambient corals. DOM exudates from stressed corals (heated and/or previously bleached) were compositionally distinct from healthy corals and significantly increased growth of bacterioplankton, enriching copiotrophs and putative pathogens. Together these results demonstrate how the impacts of both short-term thermal stress and long-term bleaching may extend into the water column, with altered coral DOM exudation driving microbial feedbacks that influence how coral reefs respond to and recover from mass bleaching events.more » « less
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Abstract Cryptic species (evolutionarily distinct lineages that do not align with morphologically defined species) are being increasingly discovered but are poorly integrated into ecological theory. In particular, we still lack a useful understanding of if and how cryptic species differ in ways that affect community recovery from disturbances and responses to anthropogenic stressors, such as the removal of consumers and pollution from nutrients. On coral reefs, nutrient pollution increases the growth of macroalgae that displace corals. Reductions in herbivorous fishes reduce the suppression of macroalgae, while reductions in coralivorous fishes reduce predation on corals. An unresolved question is if and how cryptic coral species respond differently to these impacts, thereby differing in their ability to influence coral community dynamics and maintain coral dominance. Therefore, we assessed how the response of crypticPocilloporaspecies over a period of three years following a simulated disturbance from a cyclone depended on the experimental reduction of fish consumer pressure and nutrient addition. After three years, five morphologically cryptic, but genetically distinct,Pocilloporaspecies recruited to the reef. However, recruitment was dominated by two species:Pocillopora tuahiniensis(46%) andPocillopora meandrina(43%). Under ambient conditions, recruitment ofP. tuahiniensisandP. meandrinawas similar, but experimentally reducing consumer pressure increased recruitment ofP. tuahiniensisby up to 73% and reduced recruitment ofP. meandrinaby up to 49%. In both species, nutrient enrichment increased recruitment and colony growth rates equally, but colonies ofP. tuahiniensisgrew faster and were up to 25% larger after three years than those ofP. meandrina,and growth was unaffected by reduced consumer pressure. Predation by excavating corallivorous fish was higher forP. meandrinathan forP. tuahiniensis, especially under nutrient enrichment. In contrast, polyp extension (an indicator of elevated heterotrophic feeding as well as susceptibility and attractiveness to corallivores) was lower forP. meandrinathan forP. tuahiniensis, especially under low to medium consumer pressure. Overall, we uncovered ecological differences in the response of morphologically cryptic foundation species to two pervasive stressors on coral reefs. Our results demonstrate how cryptic species respond differently to key anthropogenic stressors, which may contribute to response diversity that can support ecological resilience or increase extinction risk.more » « less
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Abstract Climate change is intensifying extreme weather events, including marine heatwaves, which are prolonged periods of anomalously high sea surface temperature that pose a novel threat to aquatic animals. Tropical animals may be especially vulnerable to marine heatwaves because they are adapted to a narrow temperature range. If these animals cannot acclimate to marine heatwaves, the extreme heat could impair their behavior and fitness. Here, we investigated how marine heatwave conditions affected the performance and thermal tolerance of a tropical predatory fish, arceye hawkfish (Paracirrhites arcatus), across two seasons in Moorea, French Polynesia. We found that the fish’s daily activities, including recovery from burst swimming and digestion, were more energetically costly in fish exposed to marine heatwave conditions across both seasons, while their aerobic capacity remained the same. Given their constrained energy budget, these rising costs associated with warming may impact how hawkfish prioritize activities. Additionally, hawkfish that were exposed to hotter temperatures exhibited cardiac plasticity by increasing their maximum heart rate but were still operating within a few degrees of their thermal limits. With more frequent and intense heatwaves, hawkfish, and other tropical fishes must rapidly acclimate, or they may suffer physiological consequences that alter their role in the ecosystem.more » « less
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Abstract Marine heatwaves are increasing in frequency and duration, threatening tropical reef ecosystems through intensified coral bleaching events. We examined a strikingly variable spatial pattern of bleaching in Moorea, French Polynesia following a heatwave that lasted from November 2018 to July 2019. In July 2019, four months after the onset of bleaching, we surveyed > 5000 individual colonies of the two dominant coral genera,PocilloporaandAcropora, at 10 m and 17 m water depths, at six forereef sites around the island where temperature was measured. We found severe bleaching increased with colony size for both coral genera, butAcroporableached more severely thanPocilloporaoverall. Acroporableached more at 10 m than 17 m, likely due to higher light availability at 10 m compared to 17 m, or greater daily temperature fluctuation at depth. Bleaching inPocilloporacorals did not differ with depth but instead varied with the interaction of colony size and Accumulated Heat Stress (AHS), in that larger colonies (> 30 cm) were more sensitive to AHS than mid-size (10–29 cm) or small colonies (5–9 cm). Our findings provide insight into complex interactions among coral taxa, colony size, and water depth that produce high spatial variation in bleaching and related coral mortality.more » « less
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