Landscape-scale patterns of nutrient enrichment in a coral reef ecosystem: implications for coral to algae phase shifts.

Nutrient pollution is altering coastal ecosystems worldwide. On coral reefs, excess nutrients can favor the production of algae at the expense of reef-building corals, yet the role of nutrients in driving community changes such as shifts from coral to macroalgae is not well understood. Here we investigate the potential role of anthropogenic nutrient loading in driving recent coral-to-macroalgae phase shifts on reefs in the lagoons surrounding the Pacific island of Moorea, French Polynesia. We use nitrogen (N) tissue content and stable isotopes (δ15 N) in an abundant macroalga (Turbinaria ornata) together with empirical models of nutrient discharge to describe spatial and temporal patterns of nutrient enrichment in the lagoons. We then employ time series data to test whether recent increases in macroalgae are associated with nutrients. Our results revealed that patterns of N enrichment were linked to several factors, including rainfall, wave-driven circulation, and distance from anthropogenic nutrient sources, especially human sewage. Reefs near large watersheds, where inputs of N from sewage and agriculture are high, have been consistently enriched in N for at least the last decade. In many of these areas, corals have decreased and macroalgae have increased, while reefs with lower levels of N input have maintained high cover of coral and low cover of macroalgae. Importantly, these patchy phase shifts to macroalgae have occurred despite substantial island-wide increases in the density and biomass of herbivorous fishes over the time period. Together, these results indicate that nutrient loading may be an important driver of coral-to-macroalgae phase shifts in the lagoons of Moorea even though the reefs harbor an abundant and diverse herbivore assemblage. These results emphasize the important role that bottom-up factors can play in driving coral-to-macroalgae phase shifts and underscore the critical importance of watershed management for reducing inputs of nutrients and other land-based pollutants to coral reef ecosystems.

Stony coral populations are more sensitive to changes in vital rates in disturbed environments.

Reef-building corals, like many long-lived organisms, experience environmental change as a combination of separate but concurrent processes, some of which are gradual yet long-lasting, while others are more acute but short-lived. For corals, some chronic environmental stressors, such as rising temperature and ocean acidification, are thought to induce gradual changes in colonies' vital rates. Meanwhile, other environmental changes, such as the intensification of tropical cyclones, change the disturbance regime that corals experience. Here, we use a physiologically structured population model to explore how chronic environmental stressors that impact the vital rates of individual coral colonies interact with the intensity and magnitude of disturbance to affect coral population dynamics and cover. We find that, when disturbances are relatively benign, intraspecific density dependence driven by space competition partially buffers coral populations against gradual changes in vital rates. However, the impact of chronic stressors is amplified in more highly disturbed environments, because disturbance weakens the buffering effect of space competition. We also show that coral cover is more sensitive to changes in colony growth and mortality than to external recruitment, at least in open populations, and that space competition and size structure mediate the extent and pace of coral population recovery following a large-scale mortality event. Understanding the complex interplay among chronic environmental stressors, mass-mortality events, and population size structure sharpens our ability to manage and to restore coral-reef ecosystems in an increasingly disturbed future.

Extreme rainfall events pulse substantial nutrients and sediments from terrestrial to nearshore coastal communities: a case study from French Polynesia.

Rainfall mobilizes and transports anthropogenic sources of sediments and nutrients from terrestrial to coastal marine ecosystems, and episodic but extreme rainfall may drive high fluxes to marine communities. Between January 13th and January 22nd, 2017, the South Pacific Island of Moorea, French Polynesia experienced an extreme rainfall event. ~57 cm of rain was delivered over a 10-day storm. We quantified pulsed sediments and nutrients transported to nearshore reefs. We determined the spatial and temporal extent of the sediment pulse with estimates of water transparency. We quantified pulsed nutrients at multiple spatial and temporal scales. To determine if terrestrial nutrients were incorporated into the benthic community, we collected macroalgae over 10 days following the storm and measured tissue nutrient concentrations and δN15. Pulsed sediments impacted water clarity for 6 days following the storm, with greatest impacts closest to the river mouth. Nitrite +nitrate concentrations were >100 times the average while phosphate was >25 times average. Macroalgal tissue nutrients were elevated, and δN15 implicates sewage as the source, demonstrating transported nutrients were transferred to producer communities. Future climate change predictions suggest extreme rainfall will become more common in this system, necessitating research on these pulses and their ramifications on marine communities.

Ocean acidification effects on in situ coral reef metabolism.

The Anthropocene climate has largely been defined by a rapid increase in atmospheric CO2, causing global climate change (warming) and ocean acidification (OA, a reduction in oceanic pH). OA is of particular concern for coral reefs, as the associated reduction in carbonate ion availability impairs biogenic calcification and promotes dissolution of carbonate substrata. While these trends ultimately affect ecosystem calcification, scaling experimental analyses of the response of organisms to OA to consider the response of ecosystems to OA has proved difficult. The benchmark of ecosystem-level experiments to study the effects of OA is provided through Free Ocean CO2 Enrichment (FOCE), which we use in the present analyses for a 21-d experiment on the back reef of Mo'orea, French Polynesia. Two natural coral reef communities were incubated in situ, with one exposed to ambient pCO2 (393 µatm), and one to high pCO2 (949 µatm). Our results show a decrease in 24-h net community calcification (NCC) under high pCO2, and a reduction in nighttime NCC that attenuated and eventually reversed over 21-d. This effect was not observed in daytime NCC, and it occurred without any effect of high pCO2 on net community production (NCP). These results contribute to previous studies on ecosystem-level responses of coral reefs to the OA conditions projected for the end of the century, and they highlight potential attenuation of high pCO2 effects on nighttime net community calcification.

Contrasting responses of photosynthesis and photochemical efficiency to ocean acidification under different light environments in a calcifying alga.

Ocean acidification (OA) is predicted to enhance photosynthesis in many marine taxa. However, photophysiology has multiple components that OA may affect differently, especially under different light environments, with potentially contrasting consequences for photosynthetic performance. Furthermore, because photosynthesis affects energetic budgets and internal acid-base dynamics, changes in it due to OA or light could mediate the sensitivity of other biological processes to OA (e.g. respiration and calcification). To better understand these effects, we conducted experiments on Porolithon onkodes, a common crustose coralline alga in Pacific coral reefs, crossing pCO2 and light treatments. Results indicate OA inhibited some aspects of photophysiology (maximum photochemical efficiency), facilitated others (α, the responsiveness of photosynthesis to sub-saturating light), and had no effect on others (maximum gross photosynthesis), with the first two effects depending on treatment light level. Light also exacerbated the increase in dark-adapted respiration under OA, but did not alter the decline in calcification. Light-adapted respiration did not respond to OA, potentially due to indirect effects of photosynthesis. Combined, results indicate OA will interact with light to alter energetic budgets and potentially resource allocation among photosynthetic processes in P. onkodes, likely shifting its light tolerance, and constraining it to a narrower range of light environments.

Nitrogen enrichment offsets direct negative effects of ocean acidification on a reef-building crustose coralline alga.

Ocean acidification (OA) and nutrient enrichment threaten the persistence of near shore ecosystems, yet little is known about their combined effects on marine organisms. Here, we show that a threefold increase in nitrogen concentrations, simulating enrichment due to coastal eutrophication or consumer excretions, offset the direct negative effects of near-future OA on calcification and photophysiology of the reef-building crustose coralline alga, Porolithon onkodes Projected near-future pCO2 levels (approx. 850 µatm) decreased calcification by 30% relative to ambient conditions. Conversely, nitrogen enrichment (nitrate + nitrite and ammonium) increased calcification by 90-130% in ambient and high pCO2 treatments, respectively. pCO2 and nitrogen enrichment interactively affected instantaneous photophysiology, with highest relative electron transport rates under high pCO2 and high nitrogen. Nitrogen enrichment alone increased concentrations of the photosynthetic pigments chlorophyll a, phycocyanin and phycoerythrin by approximately 80-450%, regardless of pCO2 These results demonstrate that nutrient enrichment can mediate direct organismal responses to OA. In natural systems, however, such direct benefits may be counteracted by simultaneous increases in negative indirect effects, such as heightened competition. Experiments exploring the effects of multiple stressors are increasingly becoming important for improving our ability to understand the ramifications of local and global change stressors in near shore ecosystems.

Recruitment Drives Spatial Variation in Recovery Rates of Resilient Coral Reefs.

Tropical reefs often undergo acute disturbances that result in landscape-scale loss of coral. Due to increasing threats to coral reefs from climate change and anthropogenic perturbations, it is critical to understand mechanisms that drive recovery of these ecosystems. We explored this issue on the fore reef of Moorea, French Polynesia, following a crown-of-thorns seastar outbreak and cyclone that dramatically reduced cover of coral. During the five-years following the disturbances, the rate of re-establishment of coral cover differed systematically around the triangular-shaped island; coral cover returned most rapidly at sites where the least amount of live coral remained after the disturbances. Although sites differed greatly in the rate of return of coral, all showed at least some evidence of re-assembly to their pre-disturbance community structure in terms of relative abundance of coral taxa and other benthic space holders. The primary driver of spatial variation in recovery was recruitment of sexually-produced corals; subsequent growth and survivorship were less important in shaping the spatial pattern. Our findings suggest that, although the coral community has been resilient, some areas are unlikely to attain the coral cover and taxonomic structure they had prior to the most recent disturbances before the advent of another landscape-scale perturbation.

Framework of barrier reefs threatened by ocean acidification.

To date, studies of ocean acidification (OA) on coral reefs have focused on organisms rather than communities, and the few community effects that have been addressed have focused on shallow back reef habitats. The effects of OA on outer barrier reefs, which are the most striking of coral reef habitats and are functionally and physically different from back reefs, are unknown. Using 5-m long outdoor flumes to create treatment conditions, we constructed coral reef communities comprised of calcified algae, corals, and reef pavement that were assembled to match the community structure at 17 m depth on the outer barrier reef of Moorea, French Polynesia. Communities were maintained under ambient and 1200 µatm pCO2 for 7 weeks, and net calcification rates were measured at different flow speeds. Community net calcification was significantly affected by OA, especially at night when net calcification was depressed ~78% compared to ambient pCO2 . Flow speed (2-14 cm s(-1) ) enhanced net calcification only at night under elevated pCO2 . Reef pavement also was affected by OA, with dissolution ~86% higher under elevated pCO2 compared to ambient pCO2 . These results suggest that net accretion of outer barrier reef communities will decline under OA conditions predicted within the next 100 years, largely because of increased dissolution of reef pavement. Such extensive dissolution poses a threat to the carbonate foundation of barrier reef communities.

Kelp canopy facilitates understory algal assemblage via competitive release during early stages of secondary succession.

Kelps are conspicuous foundation species in marine ecosystems that alter the composition of understory algal assemblages. While this may be due to changes in the competitive interactions between algal species, how kelp canopies mediate propagule supply and establishment success of understory algae is not well known. In Southern California, USA, Eisenia arborea forms dense kelp canopies in shallow subtidal environments and is associated with an understory dominated by red algal species. In canopy-free areas, however, the algal assemblage is comprised of mostly brown algal species. We used a combination of mensurative and manipulative experiments to test whether Eisenia facilitates the understory assemblage by reducing competition between these different types of algae by changes in biotic interactions and/or recruitment. Our results show Eisenia facilitates a red algal assemblage via inhibition of brown algal settlement into the canopy zone, allowing recruitment to occur by vegetative means rather than establishment of new individuals. In the canopy-free zone, however, high settlement and recruitment rates suggest competitive interactions shape the community there. These results demonstrate that foundation species alter the distribution and abundance of associated organisms by affecting not only interspecific interactions but also propagule supply and recruitment limitation.

Persistence and change in community composition of reef corals through present, past, and future climates.

The reduction in coral cover on many contemporary tropical reefs suggests a different set of coral community assemblages will dominate future reefs. To evaluate the capacity of reef corals to persist over various time scales, we examined coral community dynamics in contemporary, fossil, and simulated future coral reef ecosystems. Based on studies between 1987 and 2012 at two locations in the Caribbean, and between 1981 and 2013 at five locations in the Indo-Pacific, we show that many coral genera declined in abundance, some showed no change in abundance, and a few coral genera increased in abundance. Whether the abundance of a genus declined, increased, or was conserved, was independent of coral family. An analysis of fossil-reef communities in the Caribbean revealed changes in numerical dominance and relative abundances of coral genera, and demonstrated that neither dominance nor taxon was associated with persistence. As coral family was a poor predictor of performance on contemporary reefs, a trait-based, dynamic, multi-patch model was developed to explore the phenotypic basis of ecological performance in a warmer future. Sensitivity analyses revealed that upon exposure to thermal stress, thermal tolerance, growth rate, and longevity were the most important predictors of coral persistence. Together, our results underscore the high variation in the rates and direction of change in coral abundances on contemporary and fossil reefs. Given this variation, it remains possible that coral reefs will be populated by a subset of the present coral fauna in a future that is warmer than the recent past.

Acclimatization of the crustose coralline alga Porolithon onkodes to variable pCO2.

Ocean acidification (OA) has important implications for the persistence of coral reef ecosystems, due to potentially negative effects on biomineralization. Many coral reefs are dynamic with respect to carbonate chemistry, and experience fluctuations in pCO2 that exceed OA projections for the near future. To understand the influence of dynamic pCO2 on an important reef calcifier, we tested the response of the crustose coralline alga Porolithon onkodes to oscillating pCO2. Individuals were exposed to ambient (400 µatm), high (660 µatm), or variable pCO2 (oscillating between 400/660 µatm) treatments for 14 days. To explore the potential for coralline acclimatization, we collected individuals from low and high pCO2 variability sites (upstream and downstream respectively) on a back reef characterized by unidirectional water flow in Moorea, French Polynesia. We quantified the effects of treatment on algal calcification by measuring the change in buoyant weight, and on algal metabolism by conducting sealed incubations to measure rates of photosynthesis and respiration. Net photosynthesis was higher in the ambient treatment than the variable treatment, regardless of habitat origin, and there was no effect on respiration or gross photosynthesis. Exposure to high pCO2 decreased P. onkodes calcification by >70%, regardless of the original habitat. In the variable treatment, corallines from the high variability habitat calcified 42% more than corallines from the low variability habitat. The significance of the original habitat for the coralline calcification response to variable, high pCO2 indicates that individuals existing in dynamic pCO2 habitats may be acclimatized to OA within the scope of in situ variability. These results highlight the importance of accounting for natural pCO2 variability in OA manipulations, and provide insight into the potential for plasticity in habitat and species-specific responses to changing ocean chemistry.

Herbivory, connectivity, and ecosystem resilience: response of a coral reef to a large-scale perturbation.

Coral reefs world-wide are threatened by escalating local and global impacts, and some impacted reefs have shifted from coral dominance to a state dominated by macroalgae. Therefore, there is a growing need to understand the processes that affect the capacity of these ecosystems to return to coral dominance following disturbances, including those that prevent the establishment of persistent stands of macroalgae. Unlike many reefs in the Caribbean, over the last several decades, reefs around the Indo-Pacific island of Moorea, French Polynesia have consistently returned to coral dominance following major perturbations without shifting to a macroalgae-dominated state. Here, we present evidence of a rapid increase in populations of herbivorous fishes following the most recent perturbation, and show that grazing by these herbivores has prevented the establishment of macroalgae following near complete loss of coral on offshore reefs. Importantly, we found the positive response of herbivorous fishes to increased benthic primary productivity associated with coral loss was driven largely by parrotfishes that initially recruit to stable nursery habitat within the lagoons before moving to offshore reefs later in life. These results underscore the importance of connectivity between the lagoon and offshore reefs for preventing the establishment of macroalgae following disturbances, and indicate that protecting nearshore nursery habitat of herbivorous fishes is critical for maintaining reef resilience.

Subtidal benthic heterogeneity: flow environment modification and impacts on marine algal community structure and morphology.

The shallow subtidal zone of rocky coastlines is a highly dynamic environment characterized by micro- and macroscopic benthic structures that alter the ambient flow environment, creating "flow microhabitats." We examined the impact of macroscopic benthic structure on the maximum flow speeds and the corresponding macroalgal community cover and morphological diversity observed in response to microhabitats in both exposed and sheltered near-shore sites. Flow speeds were reduced by a factor of 2 within crevices and also in the flow-shadow of protruding rock substrate when compared to neighboring unobstructed planar microhabitats. Algal communities within crevices and in the wake of protrusions were found to have greater cover of foliose red algal species compared to horizontal microhabitats in exposed sites, but reduced cover of these species in sheltered sites. The morphologies of two rhodophytes common to all microhabitats, Chondracanthus spinosus and Pterocladiella capillacea, were examined at both exposed and sheltered sites. Exposed horizontal morphotypes of both species were generally smaller and streamlined, whereas thalli from within crevices and in the wake of protrusions were larger and bushier. We conclude that algal cover and morphology is affected by the alteration in flow around both protruding bodies and crevices when compared to unobstructed sites.

Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals.

The phase change from coral to macroalgal dominance on many Caribbean reefs was exacerbated by the mortality of the echinoid Diadema antillarum in 1983-1984, and until recently, this sea urchin has remained rare on reefs throughout the western Atlantic. By the late 1990s, Diadema started to reappear in large numbers on some Jamaican reefs, and by 2000, the high densities were correlated with significantly greater abundances of juvenile corals. Here, we show that dense populations of Diadema now occur over a multi-kilometre-wide scale at six locations scattered along a 4100 km arc across the entire Caribbean. In all cases, these dense populations are found in shallow water (< 6 m depth) on outer reef communities and are associated with reduced macroalgal cover and enhanced coral recruitment. We conclude that population recovery of Diadema is occurring at both local and regional scales, and that grazing by this echinoid is creating conditions favouring the recruitment of corals.