Spatial covariation in nutrient enrichment and fishing of herbivores in an oceanic coral reef ecosystem.
ABSTRACT: Both natural and anthropogenic stressors are increasing on coral reefs, resulting in large-scale loss of coral and potential shifts from coral- to macroalgae-dominated community states. Two factors implicated in shifts to macroalgae are nutrient enrichment and fishing of reef herbivores. Although either of these factors alone could facilitate establishment of macroalgae, reefs may be particularly vulnerable to coral-to-algae phase shifts in which strong bottom-up forcing from nutrient enrichment is accompanied by a weakening of herbivore control of macroalgae via intense fishing. We explored spatial heterogeneity and covariance in these drivers on reefs in the lagoons of Moorea, French Polynesia, where the local fishery heavily targets herbivorous fishes and there are spatially variable inputs of nutrients from agricultural fertilizers and wastewater systems. Spatial patterns of fishing and nutrient enrichment were not correlated at the two landscape scales we examined: among the 11 interconnected lagoons around the island or among major habitats (fringing reef, mid-lagoon, back reef) within a lagoon. This decoupling at the landscape scale resulted from patterns of covariation between enrichment and fishing that differed qualitatively between cross-shore and long-shore directions. At the cross-shore scale, nutrient enrichment declined but fishing increased from shore to the crest of the barrier reef. By contrast, nutrient enrichment and fishing were positively correlated in the long-shore direction, with both increasing with proximity to a pass in the barrier reef. Contrary to widespread assumptions in the scientific literature that human coastal population density correlates with impact on marine ecosystems and that fishing effort declines linearly with distance from the shore, these local stressors produced a complex spatial mosaic of reef vulnerabilities. Our findings support spatially explicit management involving the control of anthropogenic nutrients and strategic reductions in fishing pressure on herbivores by highlighting specific areas to target for management actions.
Project description: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.
Project description:Significance Ecological theory predicts that under the same environmental conditions, an ecosystem could have more than one community state that is maintained by reinforcing feedbacks. If so, a sufficiently large disturbance can flip the system to a less desired community that is difficult to reverse. Here, we demonstrate that a coral reef can become trapped in a seaweed-dominated state in the same conditions under which corals thrive. The implications are profound, particularly in light of the increasing occurrence of shifts to seaweed on coral reefs worldwide. Our results indicate that anticipatory management strategies that lessen the chance of a switch to seaweeds will be more effective than those aimed at restoring the coral community after a shift. Ecological theory predicts that ecosystems with multiple basins of attraction can get locked in an undesired state, which has profound ecological and management implications. Despite their significance, alternative attractors have proven to be challenging to detect and characterize in natural communities. On coral reefs, it has been hypothesized that persistent coral-to-macroalgae “phase shifts” that can result from overfishing of herbivores and/or nutrient enrichment may reflect a regime shift to an alternate attractor, but, to date, the evidence has been equivocal. Our field experiments in Moorea, French Polynesia, revealed the following: (i) hysteresis existed in the herbivory–macroalgae relationship, creating the potential for coral–macroalgae bistability at some levels of herbivory, and (ii) macroalgae were an alternative attractor under prevailing conditions in the lagoon but not on the fore reef, where ambient herbivory fell outside the experimentally delineated region of hysteresis. These findings help explain the different community responses to disturbances between lagoon and fore reef habitats of Moorea over the past several decades and reinforce the idea that reversing an undesired shift on coral reefs can be difficult. Our experimental framework represents a powerful diagnostic tool to probe for multiple attractors in ecological systems and, as such, can inform management strategies needed to maintain critical ecosystem functions in the face of escalating stresses.
Project description:<h4>Background</h4>The chemically-rich seaweed Galaxaura is not only highly competitive with corals, but also provides substrate for other macroalgae. Its ecology and associated epiphytes remain largely unexplored. To fill this knowledge gap, we undertook an ecological assessment to explore the spatial variation, temporal dynamics, and diversity of epiphytic macroalgae of Galaxaura divaricata on patch reefs in the lagoon of Dongsha Atoll, a shallow coral reef ecosystem in the northern South China Sea that has been repeatedly impacted by mass coral bleaching events.<h4>Methods</h4>Twelve spatially independent patch reefs in the Dongsha lagoon were first surveyed to assess benthic composition in April 2016, and then revisited to determine G. divaricata cover in September 2017, with one additional Galaxaura-dominated reef (site 9). Four surveys over a period of 17 months were then carried out on a degraded patch reef site to assess the temporal variation in G. divaricata cover. Epiphytic macroalgae associated with G. divaricata were quantified and identified through the aid of DNA barcoding at this degraded site.<h4>Results</h4>Patch reefs in the Dongsha lagoon were degraded, exhibiting relatively low coral cover (5-43%), but high proportions of macroalgae (13-58%) and other substrate (rubble and dead corals; 23-69%). The distribution of G. divaricata was heterogeneous across the lagoon, with highest abundance (16-41%) in the southeast area. Temporal surveys showed consistently high covers (mean ± SD = 16.9 ± 1.21%) of G. divaricata for 17 months. Additional photographic evidence suggested that overgrowth of G. divaricata can persist for 3.5 years. Yet, G. divaricata provides substrate to other macroalgae (e.g., Lobophora sp.) that also limit the growth of corals.<h4>Conclusions</h4>Our study demonstrates that an allelopathic seaweed, such as G. divaricata, can overgrow degraded coral reefs for extended periods of time. By providing habitat for other harmful macroalgae, a prolonged Galaxaura overgrowth could further enhance the spread of macroalgae, and strengthen negative feedback loops, decreasing the recovery potential of degraded reefs.
Project description:We quantify the relative importance of multi-scale drivers of reef fish assemblage structure on isolated coral reefs at the intersection of the Indian and Indo-Pacific biogeographical provinces. Large (>30 cm), functionally-important and commonly targeted species of fish, were surveyed on the outer reef crest/front at 38 coral reef sites spread across three oceanic coral reef systems (i.e. Christmas Island, Cocos (Keeling) Islands and the Rowley Shoals), in the tropical Indian Ocean (<i>c</i>. 1.126 x 106 km<sup>2</sup>). The effects of coral cover, exposure, fishing pressure, lagoon size and geographical context, on observed patterns of fish assemblage structure were modelled using Multivariate Regression Trees. Reef fish assemblages were clearly separated in space with geographical location explaining ~53 % of the observed variation. Lagoon size, within each isolated reef system was an equally effective proxy for explaining fish assemblage structure. Among local-scale variables, 'distance from port', a proxy for the influence of fishing, explained 5.2% of total variation and separated the four most isolated reefs from Cocos (Keeling) Island, from reefs with closer boating access. Other factors were not significant. Major divisions in assemblage structure were driven by sister taxa that displayed little geographical overlap between reef systems and low abundances of several species on Christmas Island corresponding to small lagoon habitats. Exclusion of geographical context from the analysis resulted in local processes explaining 47.3% of the variation, highlighting the importance of controlling for spatial correlation to understand the drivers of fish assemblage structure. Our results suggest reef fish assemblage structure on remote coral reef systems in the tropical eastern Indian Ocean reflects a biogeographical legacy of isolation between Indian and Pacific fish faunas and geomorphological variation within the region, more than local fishing pressure or reef condition. Our findings re-emphasise the importance that historical processes play in structuring contemporary biotic communities.
Project description:On coral reefs, fishes can facilitate coral growth via nutrient excretion; however, as coral abundance declines, these nutrients may help facilitate increases in macroalgae. By combining surveys of reef communities with bioenergetics modeling, we showed that fish excretion supplied 25 times more nitrogen to forereefs in the Florida Keys, USA, than all other biotic and abiotic sources combined. One apparent result was a positive relationship between fish excretion and macroalgal cover on these reefs. Herbivore biomass also showed a negative relationship with macroalgal cover, suggesting strong interactions of top-down and bottom-up forcing. Nutrient supply by fishes also showed a negative correlation with juvenile coral density, likely mediated by competition between macroalgae and corals, suggesting that fish excretion may hinder coral recovery following large-scale coral loss. Thus, the impact of nutrient supply by fishes may be context-dependent and reinforce either coral-dominant or coral-depauperate reef communities depending on initial community states.
Project description:Terrestrial runoff after heavy rainfall can increase nutrient concentrations in waters overlying coral reefs that otherwise experience low nutrient levels. Field measurements during a runoff event showed a sharp increase in nitrate (75-fold), phosphate (31-fold) and ammonium concentrations (3-fold) in waters overlying a fringing reef at the island of Curaçao (Southern Caribbean). To understand how benthic reef organisms make use of such nutrient pulses, we determined ammonium, nitrate and phosphate uptake rates for one abundant coral species, turf algae, six macroalgal and two benthic cyanobacterial species in a series of laboratory experiments. Nutrient uptake rates differed among benthic functional groups. The filamentous macroalga Cladophora spp., turf algae and the benthic cyanobacterium Lyngbya majuscula had the highest uptake rates per unit biomass, whereas the coral Madracis mirabilis had the lowest. Combining nutrient uptake rates with the standing biomass of each functional group on the reef, we estimated that the ammonium and phosphate delivered during runoff events is mostly taken up by turf algae and the two macroalgae Lobophora variegata and Dictyota pulchella. Our results support the often proposed, but rarely tested, assumption that turf algae and opportunistic macroalgae primarily benefit from episodic inputs of nutrients to coral reefs.
Project description:Fishing is widely considered a leading cause of biodiversity loss in marine environments, but the potential effect on ecosystem processes, such as nutrient fluxes, is less explored. Here, we test how fishing on Caribbean coral reefs influences biodiversity and ecosystem functions provided by the fish community, that is, fish-mediated nutrient capacity. Specifically, we modelled five processes of nutrient storage (in biomass) and supply (via excretion) of nutrients, as well as a measure of their multifunctionality, onto 143 species of coral reef fishes across 110 coral reef fish communities. These communities span a gradient from extreme fishing pressure to protected areas with little to no fishing. We find that in fished sites fish-mediated nutrient capacity is reduced almost 50%, despite no substantial changes in the number of species. Instead, changes in community size and trophic structure were the primary cause of shifts in ecosystem function. These findings suggest that a broader perspective that incorporates predictable impacts of fishing pressure on ecosystem function is imperative for effective coral reef conservation and management.
Project description:The diversity of coral reef and soft sediment ecosystems in the Red Sea has to date received limited scientific attention. This study investigates changes in the community composition of both reef and macrobenthic communities along a cross shelf gradient. Coral reef assemblages differed significantly in species composition and structure with location and depth. Inner shelf reefs harbored less abundant and less diverse coral assemblages with higher percentage macroalgae cover. Nutrient availability and distance from the shoreline were significantly related to changes in coral composition and structure. This study also observed a clear inshore offshore pattern for soft sediment communities. In contrast to the coral reef patterns the highest diversity and abundance of soft sediment communities were recorded at the inshore sites, which were characterized by a higher number of opportunistic polychaete species and bivalves indicative of mild disturbance. Sediment grain size and nutrient enrichment were important variables explaining the variability. This study aims to contribute to our understanding of ecosystem processes and biodiversity in the Red Sea region in an area that also has the potential to provide insight into pressing topics, such as the capacity of reef systems and benthic macrofaunal organisms to adapt to global climate change.
Project description:Fishing and pollution are chronic stressors that can prolong recovery of coral reefs and contribute to ecosystem decline. While this premise is generally accepted, management interventions are complicated because the contributions from individual stressors are difficult to distinguish. The present study examined the extent to which fishing pressure and pollution predicted progress towards the Micronesia Challenge, an international conservation strategy initiated by the political leaders of 6 nations to conserve at least 30% of marine resources by 2020. The analyses were rooted in a defined measure of coral-reef-ecosystem condition, comprised of biological metrics that described functional processes on coral reefs. We report that only 42% of the major reef habitats exceeded the ecosystem-condition threshold established by the Micronesia Challenge. Fishing pressure acting alone on outer reefs, or in combination with pollution in some lagoons, best predicted both the decline and variance in ecosystem condition. High variances among ecosystem-condition scores reflected the large gaps between the best and worst reefs, and suggested that the current scores were unlikely to remain stable through time because of low redundancy. Accounting for the presence of marine protected area (MPA) networks in statistical models did little to improve the models' predictive capabilities, suggesting limited efficacy of MPAs when grouped together across the region. Yet, localized benefits of MPAs existed and are expected to increase over time. Sensitivity analyses suggested that (i) grazing by large herbivores, (ii) high functional diversity of herbivores, and (iii) high predator biomass were most sensitive to fishing pressure, and were required for high ecosystem-condition scores. Linking comprehensive fisheries management policies with these sensitive metrics, and targeting the management of pollution, will strengthen the Micronesia Challenge and preserve ecosystem services that coral reefs provide to societies in the face of climate change.
Project description:Parts of coral reefs from New Caledonia (South Pacific) were registered at the UNESCO World Heritage list in 2008. Management strategies aiming at preserving the exceptional ecological value of these reefs in the context of climate change are currently being considered. This study evaluates the appropriateness of an exclusive fishing ban of herbivorous fish as a strategy to enhance coral reef resilience to hurricanes and bleaching in the UNESCO-registered areas of New Caledonia. A two-phase approach was developed: 1) coral, macroalgal, and herbivorous fish communities were examined in four biotopes from 14 reefs submitted to different fishing pressures in New Caledonia, and 2) results from these analyses were challenged in the context of a global synthesis of the relationship between herbivorous fish protection, coral recovery and relative macroalgal development after hurricanes and bleaching. Analyses of New Caledonia data indicated that 1) current fishing pressure only slightly affected herbivorous fish communities in the country, and 2) coral and macroalgal covers remained unrelated, and macroalgal cover was not related to the biomass, density or diversity of macroalgae feeders, whatever the biotope or level of fishing pressure considered. At a global scale, we found no relationship between reef protection status, coral recovery and relative macroalgal development after major climatic events. These results suggest that an exclusive protection of herbivorous fish in New Caledonia is unlikely to improve coral reef resilience to large-scale climatic disturbances, especially in the lightly fished UNESCO-registered areas. More efforts towards the survey and regulation of major chronic stress factors such as mining are rather recommended. In the most heavily fished areas of the country, carnivorous fish and large targeted herbivores may however be monitored as part of a precautionary approach.