Simultaneous top-down and bottom-up forces control macroalgal blooms on coral reefs (Reply to the comment by Hughes et al.) (original) (raw)
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Marine Ecology Progress Series, 2009
Coral reefs are in global decline, with seaweeds replacing corals as spatial dominants. Overfishing of herbivores, anthropogenic eutrophication, and interactions between these factors have been postulated as causes, but long-term tests of these factors are uncommon. We factorially manipulated herbivorous fishes and nutrients at a depth of 16 to 18 m for 7 to 10 mo in 2 experiments over 2 yr. Herbivore exclusion increased algal cover by about 4 to 10 ×, algal biomass by 4 to 6 ×, and suppressed cover of crustose coralline algae by 80 to 100%. Nutrient enrichment had no effect on the cover or mass of upright algae, but altered species composition by suppressing cyanobacteria and facilitating red macroalgae in the absence of herbivores. Nutrient addition increased macroalgal species richness in the absence, but not the presence of herbivores. Feeding by herbivorous fishes increased by 3 to 13 × on nutrient-enriched vs. control plots. This herbivory facilitated cover of crustose coralline algae, demonstrated that herbivores selectively target more nutritional prey, and suggested that herbivores could suppress macrophyte accumulation at sites with increased nutrient availability. Effects of fishes and nutrients on corals varied as a function of coral species. For the branching coral Porites porites, 56% of individuals exposed to fishes were completely consumed; however, individuals that survived grew 60 to 80% more in the presence of fishes. For Porites astreoides, exposure to fishes did not affect mortality, but increased net growth by 3 to 4 times. For this coral, nutrient addition decreased growth when exposed to fishes but not when protected from fishes, suggesting that fishes may have fed more on nutrient-enriched corals.
Bulletin of Marine Science, 2013
Populations of Diadema antillarum (Philippi, 1845) have been slow to recover after their 1983 Caribbean-wide massive mortality. The continued absence of this important coral reef herbivore as well as further impacts on local and regional-scales have severely threatened the health of coral reefs. From 2008 to 2011, the population of D. antillarum and structure of the benthic community were monitored within Akumal Bay, Mexico, a heavily impacted ecosystem. Across the 4 yrs of the study, densities of adult D. antillarum did not significantly change and were highest on backreef sites (mean 1.30 and 1.44 m −2). Coral cover was low at all sites (maximum 14%) and decreased during the 4 yrs of the study. Changes in crustose coralline algae (CCA) cover varied by year but was significantly higher on forereef sites, while cover by turf-algal-sediment (TAS) increased at all four sites. Diadema antillarum densities correlated positively with coral and CCA cover in the backreef sites where sea urchin densities were higher but no correlation occurred with TAS and turf. Where Echinometra lucunter (Linnaeus, 1758) sea urchins were more prevalent, their densities correlated negatively with coral and positively with CCA. Although densities of adult D. antillarum were comparable to other regions of the Caribbean, increases in TAS over the 4 yrs of this study may be evidence that even an important herbivore cannot prevent continued decline of a reef in an impacted ecosystem. Coral reefs in the Caribbean have experienced major disturbances over the past few decades and continue to be under a combination of stressors including bleaching, overexploitation of herbivores, coral diseases, and declining water quality, which has resulted in an increase in macroalgae cover (Knowlton 1992, Aronson and Precht 2001, Hughes et al. 2003, Bellwood et al. 2004). The importance of long-spined sea urchin, Diadema antillarum (Philippi, 1845), in removing macroalgae cover became evident after their massive mortality in 1983, when algal biomass abruptly increased (de Ruyter van Steveninck and Bak 1986, Carpenter 1988, Hughes 1994). As the populations of D. antillarum recover after their 1983 Caribbean-wide massive mortality (Lessios et al. 1984b, Lessios 2005), it remains unclear if grazing by this herbivore provides a suitable driver from which to expect a decrease in macroalgal cover on impacted coral reefs. Modeled scenarios indicate that sea urchins impart significant resilience to Caribbean reefs such that continued decline is inevitable when sea urchins are scarce (Mumby et al. 2006). However, abundant literature indicates it is a combination of factors which impacts the benthic dynamics on coral reefs and the propensity for shifts between dominant states [e.g., competition for space (Sandin and McNamara 2012), herbivore diversity (Cheal et al. 2010), biotic histories (Aronson et al. 2004), global climate change and marine diseases (Aronson and Precht 2006)].
Turf algae are multispecies communities of small marine macrophytes that are becoming a dominant component of coral reef communities around the world. To assess the impact of turf algae on corals, we investigated the effects of increased nutrients (eutrophication) on the interaction between the Caribbean coral Montastraea annularis and turf algae at their growth boundary. We also assessed whether herbivores are capable of reducing the abundance of turf algae at coral-algae boundaries. We found that turf algae cause visible (overgrowth) and invisible negative effects (reduced fitness) on neighbouring corals. Corals can overgrow neighbouring turf algae very slowly (at a rate of 0.12 mm 3 wk 21 ) at ambient nutrient concentrations, but turf algae overgrew corals (at a rate of 0.34 mm 3 wk 21 ) when nutrients were experimentally increased. Exclusion of herbivores had no measurable effect on the rate turf algae overgrew corals. We also used PAM fluorometry (a common approach for measuring of a colony's ''fitness'') to detect the effects of turf algae on the photophysiology of neighboring corals. Turf algae always reduced the effective photochemical efficiency of neighbouring corals, regardless of nutrient and/or herbivore conditions. The findings that herbivores are not capable of controlling the abundance of turf algae and that nutrient enrichment gives turf algae an overall competitive advantage over corals together have serious implications for the health of Caribbean coral reef systems. At ambient nutrient levels, traditional conservation measures aimed at reversing coral-to-algae phase shifts by reducing algal abundance (i.e., increasing herbivore populations by establishing Marine Protected Areas or tightening fishing regulations) will not necessarily reduce the negative impact of turf algae on local coral communities. Because turf algae have become the most abundant benthic group on Curaçao (and likely elsewhere in the Caribbean), new conservation strategies are required to mitigate their negative impact on coral communities. Citation: Vermeij MJA, van Moorselaar I, Engelhard S, Hö rnlein C, Vonk SM, et al. (2010) The Effects of Nutrient Enrichment and Herbivore Abundance on the Ability of Turf Algae to Overgrow Coral in the Caribbean. PLoS ONE 5(12): e14312.
Scientific Reports, 2013
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. SUBJECT AREAS: COMMUNITY ECOLOGY ECOSYSTEM ECOLOGY ICHTHYOLOGY CORAL REEFS
Limnology and Oceanography, 1997
During the past two decades coral reefs in the greater Caribbean area have been altered by phase shifts away from corals and toward macroalgae or algal turfs. This study tested the hypothesis that because the phase shift on reefs in Jamaica and southeast Florida involved frondose macroalgae, bottom-up control via nutrient enrichment must be a causal factor. The approach was multifaceted and included measurement of near-bottom nutrient concentrations, salinity, nutrient enrichment bioassays, alkaline phosphatase assays, tissue C : N : P ratios, and tissue 15N : 14N (6"N) ratios. In both locations, concentrations of dissolved inorganic nitrogen (DIN) and soluble reactive phosphorus (SRP) exceeded nutrient thresholds (-1 .O PM DIN, 0.1 PM SRP) noted to sustain macroalgal blooms on Caribbean coral reefs. High seawater DIN : SRP ratios, alkaline phosphatase activity, and tissue C : P and N : P ratios of macroalgae on the carbonate-rich Jamaican reef suggested SRP limitation of productivity compared to lower values of these variables on siliciclastic reefs in Florida that suggested DIN limitation. This pattern was corroborated experimentally when SRP enrichment increased P,,,, (photosynthetic capacity at light saturation) of the chlorophyte Chaetomorpha Zinum in Jamaica compared to DIN enrichment that increased (x (the photosynthetic efficiency under low irradiance) of the deeper growing chlorophyte Codium isthmocladum in southeast Florida. Increased DIN concentrations were associated with reduced salinity on both reefs, indicating submarine groundwatcr discharge was a significant source of DIN. Elevated S15N values of C. isthmocladum tissue further pointed to wastewater DIN as a source of nitrogen contributing to the blooms in southeast Florida.
Coral Reefs, 2009
We conducted a 20-week manipulative field experiment on shallow forereefs of the Florida Keys to assess the separate and interactive effects of herbivory and nutrient enrichment on the development of macroalgal communities and the fitness of the corals Porites porites and Siderastrea siderea. Excluding large herbivorous fishes produced macrophyte blooms both with and without nutrient enrichment. In contrast, there were no direct effects of nutrient enrichment. There were, however, small, but significant, interactive effects of herbivory and enrichment on macroalgal cover. Following nutrient enrichment, total macroalgae and the common seaweeds Dictyota spp. were suppressed in the presence, but not in the absence, of large herbivorous fishes-suggesting that fishes were selectively feeding on nutrient-enriched macrophytes. Access by large herbivores prevented algal overgrowth of corals, but these large fishes also directly grazed both corals. Excluding fishes did not alter survivorship of either coral species, but did decrease parrotfish grazing scars on both corals and increased the net growth of P. porites. Nutrient additions had no direct effects on the survivorship of corals, but there was a trend (P = 0.097) for nutrients to stimulate the growth of P. porites. The preponderance of experiments available to date indicates that loss of key herbivores is a major factor driving macroalgal blooms on coral reefs; anthropogenic nutrient pollution generally plays a more minor role.
Smithsonian Contributions to the Marine Sciences, 2009
Threshold levels (i.e., tipping points where the probability of community phase shifts is increased and the potential for recoverability is reduced) for critical bottomup interactions of productivity (e.g., nutrients) and those for top-down disturbances (e.g., herbivory) must be known to manage the competitive interactions determining the health of coral-dominated reefs. We further posit that latent trajectories (reduced resiliencies/ recoverability from phase shifts) are often activated or accelerated by large-scale stochastic disturbances such as tropical storms, cold fronts, warming events, diseases, and predator outbreaks. In highly diverse and productive reef ecosystems, much of the overall diversity at the benthic primary producer level is afforded by the interaction of opposing nutrient-limiting/nutrient-enhancing and herbivory controls with the local physical and spatial variability, such that a mosaic of environmental conditions typically occur in close proximity. Although the relative dominance model (RDM) appears straightforwardly simple, because of the nature of direct/indirect and stimulating/limiting factors and their interactions it is extremely complex. For example, insuffi cient nutrients may act directly to limit fl eshy algal domination (via physiological stress); conversely, abundant nutrients enhance fl eshy algal growth, with the opposite effect on reef-building corals (via toxic inhibition or increased diseases). Furthermore, the effects of controls can be indirect, by infl uencing competition. Even this seemingly indirect control can have further levels of complexity because competition between algae and corals can be direct (e.g., overgrowth) or indirect (e.g., preemption of substrate). High herbivory (via physical removal) also acts indirectly on fl eshy algae through reduced competitive ability, whereas lowered herbivory and elevated nutrients also indirectly inhibit or control corals and coralline algae by enhancing fl eshy algal competition. Other ecologically important bottom-up factors, such as reduced light, abrasion, allelopathy, disease vectoring, and sediment smothering, also result from indirect side effects of fl eshy algal competition. These factors tend to selectively eliminate the long-lived organisms in favor of weedy fast-growing species, thereby reducing desirable complexity and biodiversity.
Coral Reefs, 2001
Macroalgae were experimentally reduced by approximately 2.5 kg/m 2 on eight similar-sized patch reefs of Glovers Reef Atoll, Belize, in September 1998. Four of these reefs were in a protected``no-take'' zone and four were in a``general use'' ®shing zone. Eight adjacent reefs (four in each management zone) were also studied as unmanipulated controls to determine the interactive eect of algal reduction and ®sheries management on algae, coral, ®sh, and rates of herbivory. The 16 reefs were sampled ®ve times for 1 year after the manipulation. We found that the no-®shing zone had greater population densities for 13 of 30 species of ®sh, including four herbivorous species, but lower herbivory levels by sea urchins. However, there was lower stony coral cover and higher macroalgal cover in the``no-take'' zone, both prior to and after the experiment. There were no signi®cant eects of management on the percent cover of¯eshy macroalgae. The algal reduction resulted in an increase in six ®sh species, including four herbivores and two which feed on invertebrates. One species, Lutjanus griseus, declined in experimental reefs. Macroalgal biomass quickly recovered from the reduction in both management areas within a few months, and by species-level community measures within 1 year, while stony coral was reduced in all treatments. Coral bleaching and Hurricane Mitch disturbed the site at the beginning of the study period and may explain the loss of stony coral and rapid increase in erect algae. We suggest that reducing macroalgae, as a technique to restore turf and encrusting coralline algae and stony corals, may work best after reefs have been fully protected from ®shing for a period long enough to allow herbivorous ®sh to recover (i.e. >5 years). Further ecological studies on Glovers Reef are required to understand the shift from coral to algal dominance that has occurred on this reef in the last 25 years.
Impact of herbivore identity on algal succession and coral growth on a Caribbean reef
PLoS One, 2010
Background: Herbivory is an important top-down force on coral reefs that regulates macroalgal abundance, mediates competitive interactions between macroalgae and corals, and provides resilience following disturbances such as hurricanes and coral bleaching. However, reductions in herbivore diversity and abundance via disease or over-fishing may harm corals directly and may indirectly increase coral susceptibility to other disturbances.