Robert C. Carpenter

Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef

The transition of many Caribbean reefs from coral to macroalgal dominance has been a prominent issue in coral reef ecology for more than 20 years. Alternative stable state theory predicts that these changes are reversible but, to date, there is little indication of this having occurred. Here we present evidence of the initiation of such a reversal in Jamaica, where shallow reefs at five sites along 8 km of coastline now are characterized by a sea urchin-grazed zone with a mean width of 60 m. In comparison to the seaward algal zone, macroalgae are rare in the urchin zone, where the density of Diadema antillarum is 10 times higher and the density of juvenile corals is up to 11 times higher. These densities are close to those recorded in the late 1970s and early 1980s and are in striking contrast to the decade-long recruitment failure for both Diadema and scleractinians. If these trends continue and expand spatially, reefs throughout the Caribbean may again become dominated by corals and algal turf.

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.

Mass mortality of Diadema antillarum. II : Effects on population densities and grazing intensity of parrotfishes and surgeonfishes

It has been hypothesized that herbivorous fishes and the regular echinoidDiadema antillarum Philippi compete for benthic algae as their major food resource. Mass mortality ofD. antillarum in February 1984 provided the opportunity to test the hypothesis that herbivorous fishes and sea urchins were competing previously. Visual censuses of herbivorous fishes conducted over 4 yr in four reef zones on Tague Bay Reef, St. Croix, U.S. Virgin Islands, before and after the mass mortality indicated that population densities increased approximately three-fold in backreef and shallow (2m) forereef zones and two-fold, and four-fold in mid (5m) and deep (10m) forereef zones, respectively. Juvenile parrotfishes constituted the major component of these increases, except in the shallow forereef where acanthurids became most abundant. Grazing intensity by herbivorous fishes increased in three of the four reef zones immediately following the mass mortality. These data support the hypothesis that exploitative competition for algal resources was occurring prior to the sea urchin mass-mortality, although alternative hypotheses cannot be discounted completely. Despite the increases in the abundances of, and grazing by, herbivorous fishes, the algal community continued to increase in percent cover and biomass, indicating that increased grazing by fishes does not compensate for the loss of grazing byD. antillarum in controlling algal abundance and community structure.

Coral reef calcifiers buffer their response to ocean acidification using both bicarbonate and carbonate.

Central to evaluating the effects of ocean acidification (OA) on coral reefs is understanding how calcification is affected by the dissolution of CO2 in sea water, which causes declines in carbonate ion concentration [CO32−] and increases in bicarbonate ion concentration [HCO3−]. To address this topic, we manipulated [CO32−] and [HCO3−] to test the effects on calcification of the coral Porites rus and the alga Hydrolithon onkodes, measured from the start to the end of a 15-day incubation, as well as in the day and night. [CO32−] played a significant role in light and dark calcification of P. rus, whereas [HCO3−] mainly affected calcification in the light. Both [CO32−] and [HCO3−] had a significant effect on the calcification of H. onkodes, but the strongest relationship was found with [CO32−]. Our results show that the negative effect of declining [CO32−] on the calcification of corals and algae can be partly mitigated by the use of HCO3− for calcification and perhaps photosynthesis. These results add empirical support to two conceptual models that can form a template for further research to account for the calcification response of corals and crustose coralline algae to OA.

THE EFFECTS OF MORPHOLOGY AND WATER FLOW ON PHOTOSYNTHESIS OF MARINE MACROALGAE

We present observations and experimental results supporting the view that macroalgal morphology can represent a balance between maximizing photosynthetic ability and limiting susceptibility of the thallus to mechanical damage. The relationships among morphology, water flow, and photosynthesis were examined for five algal species representing three functional forms of marine macroalgae at Santa Catalina Island, California, USA. The relationship between surface area/volume ratio (SA/V) and rates of biomass-specific net photosynthesis (NP) across functional-form groups was examined to test the hypothesis that NP is related positively to SA/V. The rate of NP increased with increasing SA/V across functional groups. This relationship then was examined within a functional group for two species, Dictyopteris undulata and Zonaria farlowii, which are morphologically variable among sites. Flow measurements and morphometric analysis of thalli of D. undulata and Z. farlowii at two wave-exposed and two wave-protected sites indicated that intraspecific morphological variation corresponded to variation in wave exposure. A field experiment that manipulated rates of flow in situ resulted in morphological changes in D. undulata and Z. farlowii, indicating that water motion was responsible for the observed morphological plasticity. To examine the interaction between morphology and water flow on algal physiology, NP was estimated for morphotypes of D. undulata and Z. farlowii from wave-exposed and wave-protected sites. At saturating photon flux densities, NP was affected significantly by flow speed, particularly for morphotypes from the wave-protected site. For these morphotypes, increased flow speeds resulted in sustained, then decreased NP as flow speeds exceeded 17 cm/s, suggesting that water flow may affect NP at low flow speeds by mitigating mass transfer limitation and at high flow speeds by changing light interception and flow within the compacted thallus. The plasticity of morphologies and the interaction of these morphotypes with flow may represent a trade-off between maximizing NP and reducing the susceptibility of the thallus to mechanical damage and/or dislodgement by hydrodynamic forces.

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.

Water flow modulates the response of coral reef communities to ocean acidification

By the end of the century coral reefs likely will be affected negatively by ocean acidification (OA), but both the effects of OA on coral communities and the crossed effects of OA with other physical environmental variables are lacking. One of the least considered physical parameters is water flow, which is surprising considering its strong role in modulating the physiology of reef organisms and communities. In the present study, the effects of flow were tested on coral reef communities maintained in outdoor flumes under ambient pCO2 and high pCO2 (1300 μatm). Net calcification of coral communities, including sediments, was affected by both flow and pCO2 with calcification correlated positively with flow under both pCO2 treatments. The effect of flow was less evident for sediments where dissolution exceeded precipitation of calcium carbonate under all flow speeds at high pCO2. For corals and calcifying algae there was a strong flow effect, particularly at high pCO2 where positive net calcification was maintained at night in the high flow treatment. Our results demonstrate the importance of water flow in modulating the coral reef community response to OA and highlight the need to consider this parameter when assessing the effects of OA on coral reefs.

Effects of physical and biological disturbances on algal turfs in Kaneohe Bay, Hawaii

Disturbance in coral reef environments commonly results in an algal community dominated by highly productive, small filamentous forms and cyanobacteria, collectively known as algal turf. Research on the types of disturbance responsible for this community structure has concentrated mainly on biological disturbance in the form of grazing, although physical and other forms of biological disturbances may be important in many coral reef areas. On the reef flat in Kaneohe Bay, Oahu, Hawaii, algal turfs grow primarily upon coral rubble that tumbles with passing swells. We manipulated the frequency of rubble tumbling in field experiments to mimic the effects of physical disturbance by abrasion and light reduction on algal biomass, canopy height, and community structure. Treatments approximated a gradient of disturbance intensities and durations that occur on the reef flat. Although sea urchins and herbivorous fishes are not widespread and abundant on the reef flat, biological disturbances to algal turf communities in the form of herbivory by small crabs and abrasion by tough macroalgae contributed significantly to the variation in algal turf biomass. Within all experiments increasing disturbance significantly reduced algal biomass and canopy heights and the community structure shifted to more disturbance-tolerant algal forms. This study shows that the chronic physical disturbances from water motion and biological disturbances other than grazing from large herbivores can control algal communities in coral reef environments.

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.

PHOTOSYNTHESIS/PHOTON FLUX DENSITY RELATIONSHIPS AMONG COMPONENTS OF CORAL REEF ALGAL TURFS1

Photosynthesis/photon flux density (PFD) relationships were compared among some of the major components of sparse algal turfs (green endoliths, red crusts, red filaments, Crouania, Sphacelaria)/ from Tague Bay forereef St. Croix, U.S. Virgin Islands. Algal turfs grazed by the sea urchin Diadema antillarum were 2–10 times more productive per unit chl a than when not grazed by sea urchins. The maximum rate of net photosynthesis (Pnetmax) and saturation PFDs, but not the slope of the light‐limited portion of the curve (α), differed significantly among the algal turf components examined. The hypothesis that increased biomass‐specific primary productivity results from shifts in algal community structure was not supported because the maximum difference in photosynthesis between algal components was only a factor of two, and the less productive components were relatively more abundant under grazing. In the understory, green endoliths exhibited higher α and lower Pnetmax, suggesting shade adaptation. Photon flux density measurements taken with a fiber optic microprobe within the algal turfs indicated that photosynthesis of basal portions of algal filaments and red crusts are light‐limited in ungrazed algal turfs. As self‐shading changes with grazer‐mediated canopy removal, algal sublayers will contribute differentially to whole turf primary productivity.