Tropical reefs are shifting from coral to macroalgal dominance, with macroalgae suppressing coral... more Tropical reefs are shifting from coral to macroalgal dominance, with macroalgae suppressing coral recovery, potentially via effects on coral microbiomes. Understanding how macroalgae affect corals and their microbiomes requires comparing algae- versus coral-dominated reefs without confounding aspects of time and geography. We compared survival, settlement, and post-settlement survival of larvae, as well as the microbiomes of larvae and adults, of the Pacific coral Pocillopora damicornis between a marine protected area (MPA) dominated by corals versus an adjacent fished area dominated by macroalgae. Microbiome composition in adult coral, larval coral, and seawater did not differ between the MPA and fished area. However, microbiomes of adult coral were more variable in the fished area and Vibrionaceae bacteria, including strains most closely related to the pathogen Vibrio shilonii, were significantly enriched, but rare, in adult and larval coral from the fished area. Larvae from the macroalgae-dominated area exhibited higher pre-settlement mortality and reduced settlement compared with those from the coral-dominated area. Juveniles planted into a coral-dominated area survived better than those placed into a fished area dominated by macroalgae. Differential survival depended on whether macroalgae were immediately adjacent to juvenile coral rather than on traits of the areas per se. Contrary to our expectations, coral microbiomes were relatively uniform at the community level despite dramatic differences in macroalgal cover between the MPA (~2% cover) and fished (~90%) area. Reducing macroalgae may elicit declines in rare but potentially harmful microbes in coral and their larvae, as well as positive intergenerational effects on offspring survival.
Coral reefs are declining dramatically and losing species richness, but the impact of declining b... more Coral reefs are declining dramatically and losing species richness, but the impact of declining biodiversity on coral well-being remains inadequately understood. Here, we demonstrate that lower coral species richness alone can suppress the growth and survivorship of multiple species of corals (Porites cylindrica, Pocillopora damicornis and Acropora mil-lepora) under field conditions on a degraded, macroalgae-dominated reef. Our findings highlight the positive role of biodiversity in the function of coral reefs, and suggest that the loss of coral species richness may trigger negative feedback that causes further ecosystem decline. Understanding the role of biodiversity in ecosystem function becomes increasingly critical as natural communities are simplified or homogenized by extinctions, invasions and a host of other pressures 1. Species loss is now considered among the most serious threats to ecosystem function and integrity 2 due to the potential loss of keystone or foundation species, as well as the loss of positive interactions among potential competitors that can improve ecosystem performance 1. Such losses may be especially critical on coral reefs, which are normally complex and biodiverse, but are now becoming degraded and species poor 3,4. If we are losing both species and critical interactions that depend on biodiversity, species loss in diverse systems such as tropical reefs may initiate negative feedbacks (a biodiversity meltdown) that suppress resilience, suppress recovery and exacerbate losses of both biodiversity and ecosystem function. The function and maintenance of coral species diversity in reef ecosystems has long intrigued ecologists 5 , yet few experimental tests of biodiversity and ecosystem function have been conducted on coral reefs. As coral losses accelerate due to increasing global stressors 6,7 , there is an urgent need to understand how coral diversity influences ecosystem processes, especially as reefs transition to a new norm often characterized by reduced coral cover and increased cover of algal competitors. Investigations to date have focused mainly on relationships between coral and fish species richness 8,9 , not the impacts of coral diversity on corals themselves. Studies of the this are limited to assessments of focal coral species' performance for restoration efforts 10,11 or large-scale correlative analyses yielding mixed results 12. Manipulative experiments assessing community-level measures of ecosystem performance (for example, production and invasion resistance) for coral species in single versus multispecies settings are lacking, despite corals being the foundation taxa on which most reef species depend. Coral-coral and coral-macroalgae interactions occur on small spatial scales (mm to cm) at colony borders 13,14 , so we manipulated coral richness within 36 cm × 36 cm plots in the field. We created experimental monocultures and polycultures of three common Indo-Pacific coral species (Porites cylindrica, Pocillopora damicornis and Acropora millepora; Fig. 1a) to test the effects of coral species richness on coral growth, mortality and colonization by competing macroalgae-three key measures of reef ecosystem function-on a degraded Fijian reef (coral cover ~4% 15). Species richness in our manipulations was representative of richness at similar spatial scales in the field (median = 2 species per 36 cm × 36 cm plot; Fig. 1a, inset). Each monoculture plot held 18 implants of a single species (216 of each species total). Each polyculture held 6 implants of each of the 3 species (72 of each species in total; positions randomized on each plot; Fig. 1a,b). The experiment involved 864 corals assessed at 0, 4 and 16 months. At month 4, we consistently found a richness effect (sensu ref. 16)
Loss of larger consumers from stressed ecosystems can lead to trophic release of mid-level consum... more Loss of larger consumers from stressed ecosystems can lead to trophic release of mid-level consumers that then impact foundation species, suppressing ecosystem function and resilience. For example, in coral reef ecosystems, outbreaks of coral predators like crown-of-thorns sea stars have been associated with fishing pressure and can dramatically impact the composition and persistence of corals. However, the ecological impacts, and consequences for management, of smaller, less obvious corallivores remain inadequately understood. We investigated whether reef state (coral vs. seaweed domination) influenced densities and size frequencies of the corallivorous gastropod Coralliophila vio-lacea on its common host, the coral Porites cylindrica, within three pairs of small Marine Protected Areas (MPAs) and adjacent fished areas in Fiji. C. violacea densities were 5-35 times greater, and their size frequencies more broadly distributed, within seaweed-dominated fished areas than in adjacent MPAs dominated by corals. Tethering snails (4-9 mm in shell height) in place on their coral hosts indicated that suppression of snails in MPAs was due to predation, apparently by fishes. When tethered on the benthos (where they rarely occur), rather than on their host, mortality of larger snails (15.0-25.0 mm in shell height) was high in all areas, primarily due to hermit crabs killing them and occupying their shells. Because C. violacea is a sessile gastropod that feeds affixed to the base of corals and produces minimal visible damage, it has been considered a "prudent feeder" that minimally impacts its host coral. We assessed this over a 24-d feeding period in the field. Feeding by individual C. violacea reduced P. cylindrica growth by ~18-43% depending on snail size. Our findings highlight the considerable , but underappreciated, negative impacts of this common corallivore on degraded reefs. As reefs degrade and corals are lost, remaining corals (often species of Porites) may gain the full attention of elevated densities of coral consumers. This will further damage the remaining foundation species, suppressing the resilience of corals and enhancing the resilience of degraded, seaweed-dominated reefs.
Tropical reefs are commonly transitioning from coral to macroalgal dominance, producing abrupt, a... more Tropical reefs are commonly transitioning from coral to macroalgal dominance, producing abrupt, and often lasting, shifts in community composition and ecosystem function. Although negative effects of macroalgae on corals are well documented, whether such effects vary with spatial scale or the density of macroalgae remains inadequately understood, as does the legacy of their impact on coral growth. Using adjacent coral- versus macroalgal-dominated areas, we tested effects of macroalgal competition on 2 common Indo-Pacific coral species. When corals were transplanted to areas of: (1) macroalgal dominance, (2) macroalgal dominance but with nearby macroalgae removed, or (3) coral dominance lacking macroalgae, coral growth was equivalently high in plots without macroalgae and low (62−90% less) in plots with macroalgae, regard- less of location. In a separate experiment, we exposed corals to differing densities of the dominant macroalga Sargassum polycystum. Coral survivorship was high (≥93% after 3 mo) and did not differ among treatments, whereas the growth of both coral species decreased as a function of Sargassum density. When Sargassum was removed after 3 mo, there was no legacy effect of macroalgal density on coral growth over the next 6 mo; however, there was no compensation for previously depressed growth. In sum, macroalgal impacts were density-dependent, and occurred only if macroalgae were in close contact, and coral growth was resilient to prior macroalgal contact. The temporal and spatial constraints of these interactions suggest that corals may be surprisingly resilient to periodic macroalgal competition, which could have important implications for ecosystem trajectories that lead to reef decline or recovery.
The unanticipated impacts of consumers in fragmented habitats are frequently a challenge for ecos... more The unanticipated impacts of consumers in fragmented habitats are frequently a challenge for ecosystem management. On Indo-Pacific coral reefs, crown-of-thorns sea stars (Acanthaster spp.) are coral predators whose outbreaks cause precipitous coral decline. Across large spatial scales, Acanthaster densities are lower in large no-take Marine Protected Areas (MPAs) and reefs subject to limited human exploitation. However, using a combination of observational and manipulative experiments, we found that Acanthaster densities within a network of small, no-take MPAs on reef flats in Fiji were ~2–3.4 times greater inside MPAs than in adjacent fished areas and ~2–2.5 times greater than the upper threshold density indicative of an outbreak. This appeared to result from selective Acanthaster migration to the coral-rich MPAs from fished areas that are coral-poor and dominated by macroalgae. Small MPAs can dramatically increase the cover of foundation species like corals, but may selectively attract coral predators like Acanthaster due to greater food densities within MPAs or because the MPAs are too small to support Acanthaster enemies. As coral cover increases, their chemical and visual cues may concentrate Acanthaster to outbreak densities that cause coral demise, compromising the value of small MPAs. An understanding of predator dynamics as a function of habitat type, size, and fragmentation needs to be incorporated into MPA design and management.
Indirect biotic effects arising from multispecies interactions can alter the structure and functi... more Indirect biotic effects arising from multispecies interactions can alter the structure and function of ecological communities—often in surprising ways that can vary in direction and magnitude. On Pacific coral reefs, predation by the crown-of-thorns sea star, Acanthaster planci, is associated with broad-scale losses of coral cover and increases of macroalgal cover. Macroalgal blooms increase coral–macroalgal competition and can generate further coral decline. However, using a combination of manipulative field experiments and observations, we demonstrate that macroalgae, such as Sargassum polycystum, produce associational refuges for corals and dramatically reduce their consumption by Acanthaster. Thus, as Acanthaster densities increase, macroalgae can become coral mutualists, despite being competitors that significantly suppress coral growth. Field feeding experiments revealed that the protective effects of macroalgae were strong enough to cause Acanthaster to consume low-preference corals instead of high-preference corals surrounded by macroalgae. This highlights the context-dependent nature of coral–algal interactions when consumers are common. Macroalgal creation of associational refuges from Acanthaster predation may have important implications for the structure, function and resilience of reef communities subject to an increasing number of biotic disturbances.
No-take marine protected areas (MPAs) are commonly applied in community-based management schemes ... more No-take marine protected areas (MPAs) are commonly applied in community-based management schemes to sustain and enhance coral-reef fisheries. However, many MPAs in Fiji and the South Pacific are relatively small (≤1 km2), and few data exist regarding the effects of these MPAs on populations of exploited species. We used hook-and-line fishing surveys to assess whether 4 relatively small (<1 km2) community-based MPAs in Fiji (3 current, 1 former) were providing any commonly sought benefits to exploited reef-fish stocks. All of the MPAs had maintained no-take status for over 4 yr, although the former MPA was opened to fishing 4 mo before this study. The current MPAs exhibited significantly greater catch and biomass per unit effort, individual fish biomass, and/or percentage of reproductive-size fish than paired, adjacent fished areas, while this was not the case with the former MPA. Sites with intact MPAs also exhibited greater catch diversity than the former MPA site. Additionally, tag and recapture data from the 17 recaptured of 2650 tagged fish suggest site fidelity of these fishes, although fishes initially captured in the MPA at all 4 sites were later caught in fished areas, indicating that there is movement of fishes from the MPAs to fished areas. While the combination of these findings supports the utility of even relatively small MPAs as effective tools for the conservation of certain target species, it also suggests that MPA benefits may be quickly depleted and that even closures of extended duration may be insufficient for long-term fisheries management if the MPAs are not maintained.
Tropical reefs are shifting from coral to macroalgal dominance, with macroalgae suppressing coral... more Tropical reefs are shifting from coral to macroalgal dominance, with macroalgae suppressing coral recovery, potentially via effects on coral microbiomes. Understanding how macroalgae affect corals and their microbiomes requires comparing algae- versus coral-dominated reefs without confounding aspects of time and geography. We compared survival, settlement, and post-settlement survival of larvae, as well as the microbiomes of larvae and adults, of the Pacific coral Pocillopora damicornis between a marine protected area (MPA) dominated by corals versus an adjacent fished area dominated by macroalgae. Microbiome composition in adult coral, larval coral, and seawater did not differ between the MPA and fished area. However, microbiomes of adult coral were more variable in the fished area and Vibrionaceae bacteria, including strains most closely related to the pathogen Vibrio shilonii, were significantly enriched, but rare, in adult and larval coral from the fished area. Larvae from the macroalgae-dominated area exhibited higher pre-settlement mortality and reduced settlement compared with those from the coral-dominated area. Juveniles planted into a coral-dominated area survived better than those placed into a fished area dominated by macroalgae. Differential survival depended on whether macroalgae were immediately adjacent to juvenile coral rather than on traits of the areas per se. Contrary to our expectations, coral microbiomes were relatively uniform at the community level despite dramatic differences in macroalgal cover between the MPA (~2% cover) and fished (~90%) area. Reducing macroalgae may elicit declines in rare but potentially harmful microbes in coral and their larvae, as well as positive intergenerational effects on offspring survival.
Coral reefs are declining dramatically and losing species richness, but the impact of declining b... more Coral reefs are declining dramatically and losing species richness, but the impact of declining biodiversity on coral well-being remains inadequately understood. Here, we demonstrate that lower coral species richness alone can suppress the growth and survivorship of multiple species of corals (Porites cylindrica, Pocillopora damicornis and Acropora mil-lepora) under field conditions on a degraded, macroalgae-dominated reef. Our findings highlight the positive role of biodiversity in the function of coral reefs, and suggest that the loss of coral species richness may trigger negative feedback that causes further ecosystem decline. Understanding the role of biodiversity in ecosystem function becomes increasingly critical as natural communities are simplified or homogenized by extinctions, invasions and a host of other pressures 1. Species loss is now considered among the most serious threats to ecosystem function and integrity 2 due to the potential loss of keystone or foundation species, as well as the loss of positive interactions among potential competitors that can improve ecosystem performance 1. Such losses may be especially critical on coral reefs, which are normally complex and biodiverse, but are now becoming degraded and species poor 3,4. If we are losing both species and critical interactions that depend on biodiversity, species loss in diverse systems such as tropical reefs may initiate negative feedbacks (a biodiversity meltdown) that suppress resilience, suppress recovery and exacerbate losses of both biodiversity and ecosystem function. The function and maintenance of coral species diversity in reef ecosystems has long intrigued ecologists 5 , yet few experimental tests of biodiversity and ecosystem function have been conducted on coral reefs. As coral losses accelerate due to increasing global stressors 6,7 , there is an urgent need to understand how coral diversity influences ecosystem processes, especially as reefs transition to a new norm often characterized by reduced coral cover and increased cover of algal competitors. Investigations to date have focused mainly on relationships between coral and fish species richness 8,9 , not the impacts of coral diversity on corals themselves. Studies of the this are limited to assessments of focal coral species' performance for restoration efforts 10,11 or large-scale correlative analyses yielding mixed results 12. Manipulative experiments assessing community-level measures of ecosystem performance (for example, production and invasion resistance) for coral species in single versus multispecies settings are lacking, despite corals being the foundation taxa on which most reef species depend. Coral-coral and coral-macroalgae interactions occur on small spatial scales (mm to cm) at colony borders 13,14 , so we manipulated coral richness within 36 cm × 36 cm plots in the field. We created experimental monocultures and polycultures of three common Indo-Pacific coral species (Porites cylindrica, Pocillopora damicornis and Acropora millepora; Fig. 1a) to test the effects of coral species richness on coral growth, mortality and colonization by competing macroalgae-three key measures of reef ecosystem function-on a degraded Fijian reef (coral cover ~4% 15). Species richness in our manipulations was representative of richness at similar spatial scales in the field (median = 2 species per 36 cm × 36 cm plot; Fig. 1a, inset). Each monoculture plot held 18 implants of a single species (216 of each species total). Each polyculture held 6 implants of each of the 3 species (72 of each species in total; positions randomized on each plot; Fig. 1a,b). The experiment involved 864 corals assessed at 0, 4 and 16 months. At month 4, we consistently found a richness effect (sensu ref. 16)
Loss of larger consumers from stressed ecosystems can lead to trophic release of mid-level consum... more Loss of larger consumers from stressed ecosystems can lead to trophic release of mid-level consumers that then impact foundation species, suppressing ecosystem function and resilience. For example, in coral reef ecosystems, outbreaks of coral predators like crown-of-thorns sea stars have been associated with fishing pressure and can dramatically impact the composition and persistence of corals. However, the ecological impacts, and consequences for management, of smaller, less obvious corallivores remain inadequately understood. We investigated whether reef state (coral vs. seaweed domination) influenced densities and size frequencies of the corallivorous gastropod Coralliophila vio-lacea on its common host, the coral Porites cylindrica, within three pairs of small Marine Protected Areas (MPAs) and adjacent fished areas in Fiji. C. violacea densities were 5-35 times greater, and their size frequencies more broadly distributed, within seaweed-dominated fished areas than in adjacent MPAs dominated by corals. Tethering snails (4-9 mm in shell height) in place on their coral hosts indicated that suppression of snails in MPAs was due to predation, apparently by fishes. When tethered on the benthos (where they rarely occur), rather than on their host, mortality of larger snails (15.0-25.0 mm in shell height) was high in all areas, primarily due to hermit crabs killing them and occupying their shells. Because C. violacea is a sessile gastropod that feeds affixed to the base of corals and produces minimal visible damage, it has been considered a "prudent feeder" that minimally impacts its host coral. We assessed this over a 24-d feeding period in the field. Feeding by individual C. violacea reduced P. cylindrica growth by ~18-43% depending on snail size. Our findings highlight the considerable , but underappreciated, negative impacts of this common corallivore on degraded reefs. As reefs degrade and corals are lost, remaining corals (often species of Porites) may gain the full attention of elevated densities of coral consumers. This will further damage the remaining foundation species, suppressing the resilience of corals and enhancing the resilience of degraded, seaweed-dominated reefs.
Tropical reefs are commonly transitioning from coral to macroalgal dominance, producing abrupt, a... more Tropical reefs are commonly transitioning from coral to macroalgal dominance, producing abrupt, and often lasting, shifts in community composition and ecosystem function. Although negative effects of macroalgae on corals are well documented, whether such effects vary with spatial scale or the density of macroalgae remains inadequately understood, as does the legacy of their impact on coral growth. Using adjacent coral- versus macroalgal-dominated areas, we tested effects of macroalgal competition on 2 common Indo-Pacific coral species. When corals were transplanted to areas of: (1) macroalgal dominance, (2) macroalgal dominance but with nearby macroalgae removed, or (3) coral dominance lacking macroalgae, coral growth was equivalently high in plots without macroalgae and low (62−90% less) in plots with macroalgae, regard- less of location. In a separate experiment, we exposed corals to differing densities of the dominant macroalga Sargassum polycystum. Coral survivorship was high (≥93% after 3 mo) and did not differ among treatments, whereas the growth of both coral species decreased as a function of Sargassum density. When Sargassum was removed after 3 mo, there was no legacy effect of macroalgal density on coral growth over the next 6 mo; however, there was no compensation for previously depressed growth. In sum, macroalgal impacts were density-dependent, and occurred only if macroalgae were in close contact, and coral growth was resilient to prior macroalgal contact. The temporal and spatial constraints of these interactions suggest that corals may be surprisingly resilient to periodic macroalgal competition, which could have important implications for ecosystem trajectories that lead to reef decline or recovery.
The unanticipated impacts of consumers in fragmented habitats are frequently a challenge for ecos... more The unanticipated impacts of consumers in fragmented habitats are frequently a challenge for ecosystem management. On Indo-Pacific coral reefs, crown-of-thorns sea stars (Acanthaster spp.) are coral predators whose outbreaks cause precipitous coral decline. Across large spatial scales, Acanthaster densities are lower in large no-take Marine Protected Areas (MPAs) and reefs subject to limited human exploitation. However, using a combination of observational and manipulative experiments, we found that Acanthaster densities within a network of small, no-take MPAs on reef flats in Fiji were ~2–3.4 times greater inside MPAs than in adjacent fished areas and ~2–2.5 times greater than the upper threshold density indicative of an outbreak. This appeared to result from selective Acanthaster migration to the coral-rich MPAs from fished areas that are coral-poor and dominated by macroalgae. Small MPAs can dramatically increase the cover of foundation species like corals, but may selectively attract coral predators like Acanthaster due to greater food densities within MPAs or because the MPAs are too small to support Acanthaster enemies. As coral cover increases, their chemical and visual cues may concentrate Acanthaster to outbreak densities that cause coral demise, compromising the value of small MPAs. An understanding of predator dynamics as a function of habitat type, size, and fragmentation needs to be incorporated into MPA design and management.
Indirect biotic effects arising from multispecies interactions can alter the structure and functi... more Indirect biotic effects arising from multispecies interactions can alter the structure and function of ecological communities—often in surprising ways that can vary in direction and magnitude. On Pacific coral reefs, predation by the crown-of-thorns sea star, Acanthaster planci, is associated with broad-scale losses of coral cover and increases of macroalgal cover. Macroalgal blooms increase coral–macroalgal competition and can generate further coral decline. However, using a combination of manipulative field experiments and observations, we demonstrate that macroalgae, such as Sargassum polycystum, produce associational refuges for corals and dramatically reduce their consumption by Acanthaster. Thus, as Acanthaster densities increase, macroalgae can become coral mutualists, despite being competitors that significantly suppress coral growth. Field feeding experiments revealed that the protective effects of macroalgae were strong enough to cause Acanthaster to consume low-preference corals instead of high-preference corals surrounded by macroalgae. This highlights the context-dependent nature of coral–algal interactions when consumers are common. Macroalgal creation of associational refuges from Acanthaster predation may have important implications for the structure, function and resilience of reef communities subject to an increasing number of biotic disturbances.
No-take marine protected areas (MPAs) are commonly applied in community-based management schemes ... more No-take marine protected areas (MPAs) are commonly applied in community-based management schemes to sustain and enhance coral-reef fisheries. However, many MPAs in Fiji and the South Pacific are relatively small (≤1 km2), and few data exist regarding the effects of these MPAs on populations of exploited species. We used hook-and-line fishing surveys to assess whether 4 relatively small (<1 km2) community-based MPAs in Fiji (3 current, 1 former) were providing any commonly sought benefits to exploited reef-fish stocks. All of the MPAs had maintained no-take status for over 4 yr, although the former MPA was opened to fishing 4 mo before this study. The current MPAs exhibited significantly greater catch and biomass per unit effort, individual fish biomass, and/or percentage of reproductive-size fish than paired, adjacent fished areas, while this was not the case with the former MPA. Sites with intact MPAs also exhibited greater catch diversity than the former MPA site. Additionally, tag and recapture data from the 17 recaptured of 2650 tagged fish suggest site fidelity of these fishes, although fishes initially captured in the MPA at all 4 sites were later caught in fished areas, indicating that there is movement of fishes from the MPAs to fished areas. While the combination of these findings supports the utility of even relatively small MPAs as effective tools for the conservation of certain target species, it also suggests that MPA benefits may be quickly depleted and that even closures of extended duration may be insufficient for long-term fisheries management if the MPAs are not maintained.
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