Ilsa B. Kuffner

Effects of the benthic cyanobacterium Lyngbya majuscula on larval recruitment of the reef corals Acropora surculosa and Pocillopora damicornis

Coral reef degradation resulting from a multitude of stressors is occurring on a global scale (Hoegh-Guldberg 1999; Hughes et al. 2003). The outcome of reef degradation is often a decrease in live coral, followed by the proliferation of algae (termed a phase shift) (Hughes 1994; McCook 1999). Successful coral recruitment is critical to the regeneration of reefs, and recruitment failuremay be a major reason that reefs are not recovering from phase shifts (Hughes and Connell 1999; Hughes and Tanner 2000). When reefs become dominated by macroalgae, larval access to suitable settling habitat is decreased (McCook et al. 2001), and sediments trapped within algal turfs may reduce survival of coral spat (Sato 1985). Rates of coral recruitment are inversely correlated to algal biomass (Birkeland 1977; Rogers et al. 1984). Interactions between benthic cyanobacteria and corals have not been examined experimentally to date, but recent studies have documented cyanobacterial blooms on coral reefs in Guam (Nagle and Paul 1998; Thacker and Paul 2001), atoll islands across Micronesia and the Northwest Hawaiian Islands (especially near iron shipwrecks, J. Maragos, personal communication), and off Broward county, Florida (authors’ personal observations). Also, cyanobacteria are often dominant in the turfs that first colonize dead coral skeleton after mortality caused by coral bleaching (Diaz-Pulido and McCook 2002). The environmental factors that contribute to cyanobacterial bloom formation in the benthic marine environment have not been definitively identified, but low wave action (Thacker and Paul 2001), phosphate levels (Kuffner and Paul 2001), and iron bioavailability (J. Maragos, personal communication) may be worth examining in the field. There could be other mechanisms for reductions in coral recruitment rates besides the preemption of space by weedy primary producers. Many benthic species of algae (Hay et al. 1987; Schmitt et al. 1995) and cyanobacteria (Nagle and Paul 1998; 1999; Pennings et al. 1997) produce toxic secondary metabolites that act as anti-herbivory and anti-fouling agents (see Paul et al. 2001 for review). Lyngbya majuscula, in particular, has been shown to produce three bioactive compounds (malyngolide, malyngamide A and malyngamide B) that deter feeding in juvenile parrotfishes (Thacker et al. 1997). Given the generalized toxicity and multi-function nature of many secondary metabolites produced by marine algae and cyanobacteria (Paul et al. 2001), it would not be surprising if these or other chemicals perform allelopathic roles as well. In this study we examine the effects of Lyngbya majuscula on the larvae of two species of corals, Acropora surculosa (broadcast spawner) and Pocillopora damicornis (brooder), to test whether the presence of Lyngbya majuscula has a negative effect on coral larval survival or recruitment beyond levels that would be expected due to space preemption.

A geological perspective on the degradation and conservation of western Atlantic coral reefs

Continuing coral-reef degradation in the western Atlantic is resulting in loss of ecological and geologic functions of reefs. With the goal of assisting resource managers and stewards of reefs in setting and measuring progress toward realistic goals for coral-reef conservation and restoration, we examined reef degradation in this region from a geological perspective. The importance of ecosystem services provided by coral reefs-as breakwaters that dissipate wave energy and protect shorelines and as providers of habitat for innumerable species-cannot be overstated. However, the few coral species responsible for reef building in the western Atlantic during the last approximately 1.5 million years are not thriving in the 21st century. These species are highly sensitive to abrupt temperature extremes, prone to disease infection, and have low sexual reproductive potential. Their vulnerability and the low functional redundancy of branching corals have led to the low resilience of western Atlantic reef ecosystems. The decrease in live coral cover over the last 50 years highlights the need for study of relict (senescent) reefs, which, from the perspective of coastline protection and habitat structure, may be just as important to conserve as the living coral veneer. Research is needed to characterize the geological processes of bioerosion, reef cementation, and sediment transport as they relate to modern-day changes in reef elevation. For example, although parrotfish remove nuisance macroalgae, possibly promoting coral recruitment, they will not save Atlantic reefs from geological degradation. In fact, these fish are quickly nibbling away significant quantities of Holocene reef framework. The question of how different biota covering dead reefs affect framework resistance to biological and physical erosion needs to be addressed. Monitoring and managing reefs with respect to physical resilience, in addition to ecological resilience, could optimize the expenditure of resources in conserving Atlantic reefs and the services they provide.

Temporal Variation in Photosynthetic Pigments and UV-Absorbing Compounds in Shallow Populations of Two Hawaiian Reef Corals

ABSTRACT As we seek to understand the physiological mechanisms of coral bleaching, it is important to understand the background temporal variation in photosynthetic pigments and photoprotective compounds that corals exhibit. In this study, reef flat populations of two hermatypic coral species, Montipora capitata (Dana, 1846) and Porites compressa Dana, 1846, were sampled monthly in Kāne‘ohe Bay, Hawai‘i, from January 1998 to March 1999. Surface ultraviolet radiation (UVR) was measured continually during this time period at the same location. High-performance liquid chromatography (HPLC) analysis of photo-synthetic pigments and mycosporine-like amino acids (MAAs) revealed temporal changes in concentrations and proportions of these compounds in tissues of both species of coral. Chlorophyll a (chl a), chlorophyll c2 (chl c2), peridinin, and diadinoxanthin concentrations changed on a skeletal weight (M. capitata) or surface area (P. compressa) basis, significantly correlating with seasonal changes in solar input (number of days from the winter solstice). In P. compressa, diadinoxanthin increased in proportion to the total pigment pool during summer months, suggesting an up-regulation of a xanthophyll cycle. In M. capitata, the ratio of chl a: chl c2 decreased during winter months, suggesting photoacclimation to lower light levels. It is surprising that there was not a clear seasonal pattern in total MAA concentration for either species, with the exception of shinorine in P. compressa. The relative stability of MAA concentrations over the course of the year despite a pronounced seasonal trend in UVR suggests either that MAAs are not performing a photoprotective role in these species or that concentrations are kept at a threshold level in the presence of a dynamic light environment.

Coral Calcification and Ocean Acidification

Over 60 years ago, the discovery that light increased calcification in the coral plant-animal symbiosis triggered interest in explaining the phenomenon and understanding the mechanisms involved. Major findings along the way include the observation that carbon fixed by photosynthesis in the zooxanthellae is translocated to animal cells throughout the colony and that corals can therefore live as autotrophs in many situations. Recent research has focused on explaining the observed reduction in calcification rate with increasing ocean acidification (OA). Experiments have shown a direct correlation between declining ocean pH, declining aragonite saturation state (Ωarag), declining [CO3 2−] and coral calcification. Nearly all previous reports on OA identify Ωarag or its surrogate [CO3 2−] as the factor driving coral calcification. However, the alternate “Proton Flux Hypothesis” stated that coral calcification is controlled by diffusion limitation of net H+ transport through the boundary layer in relation to availability of dissolved inorganic carbon (DIC). The “Two Compartment Proton Flux Model” expanded this explanation and synthesized diverse observations into a universal model that explains many paradoxes of coral metabolism, morphology and plasticity of growth form in addition to observed coral skeletal growth response to OA. It is now clear that irradiance is the main driver of net photosynthesis (Pnet), which in turn drives net calcification (Gnet), and alters pH in the bulk water surrounding the coral. Pnet controls [CO3 2−] and thus Ωarag of the bulk water over the diel cycle. Changes in Ωarag and pH lag behind Gnet throughout the daily cycle by two or more hours. The flux rate Pnet, rather than concentration-based parameters (e.g., Ωarag, [CO3 2−], pH and [DIC]:[H+] ratio) is the primary driver of Gnet. Daytime coral metabolism rapidly removes DIC from the bulk seawater. Photosynthesis increases the bulk seawater pH while providing the energy that drives calcification and increases in Gnet. These relationships result in a correlation between Gnet and Ωarag, with both parameters being variables dependent on Pnet. Consequently the correlation between Gnet and Ωarag varies widely between different locations and times depending on the relative metabolic contributions of various calcifying and photosynthesizing organisms and local rates of carbonate dissolution. High rates of H+ efflux continue for several hours following the mid-day Gnet peak suggesting that corals have difficulty in shedding waste protons as described by the Proton Flux Model. DIC flux (uptake) tracks Pnet and Gnet and drops off rapidly after the photosynthesis-calcification maxima, indicating that corals can cope more effectively with the problem of limited DIC supply compared to the problem of eliminating H+. Predictive models of future global changes in coral and coral reef growth based on oceanic Ωarag must include the influence of future changes in localized Pnet on Gnet as well as changes in rates of reef carbonate dissolution. The correlation between Ωarag and Gnet over the diel cycle is simply the result of increasing pH due to photosynthesis that shifts the CO2-carbonate system equilibria to increase [CO3 2−] relative to the other DIC components of [HCO3 −] and [CO2]. Therefore Ωarag closely tracks pH as an effect of Pnet, which also drives changes in Gnet. Measurements of DIC flux and H+ flux are far more useful than concentrations in describing coral metabolism dynamics. Coral reefs are systems that exist in constant disequilibrium with the water column.

A NEW RECORD OF THE LATE PLEISTOCENE CORAL POCILLOPORA PALMATA FROM THE DRY TORTUGAS, FLORIDA REEF TRACT, USA

Abstract Pocilloporid corals dominated shallow-water environments in the Caribbean during much of the Cenozoic; however, the regional diversity of this family declined over the last 15 My, culminating with the extinction of its final member, Pocillopora palmata, during the latest Pleistocene. Here we present a new record of P. palmata from Dry Tortugas National Park in the Florida Keys and infer its likely age. Although most existing records of P. palmata are from the sub-aerial reef deposits of MIS5e (~ 125 ka), the presently submerged reef in the Dry Tortugas was too deep (> 18 m) during this period to support significant reef growth. In contrast, the maximum water depth during MIS5a (~ 82 ka) was only ~ 5.6 m, which would have been ideal for P. palmata. Diagenetic alteration prevented direct dating of the samples; however, the similarity between the depths of the Pleistocene bedrock in the Dry Tortugas and other reefs in the Florida Keys, which have been previously dated to MIS5a, support the conclusion that P. palmata likely grew in the Dry Tortugas during this period. Our study provides important new information on the history of P. palmata, but it also highlights the vital need for more comprehensive studies of the Quaternary history of Caribbean reef development. With modern reef degradation already driving yet another restructuring of Caribbean coral assemblages, insights from past extinctions may prove critical in determining the prognosis of Caribbean reefs in the future.

Fidelity of the Sr/Ca proxy in recording ocean temperature in the western Atlantic coral Siderastrea siderea

Massive corals provide a useful archive of environmental variability, but careful testing of geochemical proxies in corals is necessary to validate the relationship between each proxy and environmental parameter throughout the full range of conditions experienced by the recording organisms. Here we use samples from a coral-growth study to test the hypothesis that Sr/Ca in the coral Siderastrea siderea accurately records sea-surface temperature (SST) in the subtropics (Florida, USA) along 350 km of reef tract. We test calcification rate, measured via buoyant weight, and linear extension (LE) rate, estimated with Alizarin Red-S staining, as predictors of variance in the Sr/Ca records of 39 individual S. siderea corals grown at four outer-reef locations next to in-situ temperature loggers during two, year-long periods. We found that corals with calcification rates < 1.7 mg cm−2 d−1 or < 1.7 mm yr−1 LE returned spuriously high Sr/Ca values, leading to a cold-bias in Sr/Ca-based SST estimates. The threshold-type response curves suggest that extension rate can be used as a quality-control indicator during sample and drill-path selection when using long cores for SST paleoreconstruction. For our corals that passed this quality control step, the Sr/Ca-SST proxy performed well in estimating mean annual temperature across three sites spanning 350 km of the Florida reef tract. However, there was some evidence that extreme temperature stress in 2010 (cold snap) and 2011 (SST above coral-bleaching threshold) may have caused the corals not to record the temperature extremes. Known stress events could be avoided during modern calibrations of paleoproxies.

Underwater temperature on off-shore coral reefs of the Florida Keys, U.S.A.

The U.S. Geological Survey (USGS) Coral Reef Ecosystems Studies (CREST) project (http://coastal.er.usgs.gov/crest/) provides science that helps resource managers tasked with the stewardship of coral reef resources. Coral reef organisms are very sensitive to high and low water-temperature extremes. It is critical to precisely know water temperatures experienced by corals and associated plants and animals that live in the dynamic nearshore environment to document thresholds in temperature tolerance. This dataset provides underwater temperature data recorded every fifteen minutes from 2009 to 2015 at five off-shore coral reefs in the Florida Keys, USA. From northeast to southwest, these sites are Fowey Rocks (Biscayne National Park), Molasses Reef (Florida Keys National Marine Sanctuary, FKNMS), Crocker Reef (FKNMS), Sombrero Reef (FKNMS), and Pulaski Shoal (Dry Tortugas National Park). A portion of the dataset included here was interpreted in conjunction with coral and algal calcification rates in Kuffner et al. (2013).

Sea-level rise could overwhelm coral reefs

An assessment of the capacity of coral reefs to grow fast enough to keep up with projected rises in sea level finds that most reefs will fall behind if nothing is done to restore them.An assessment of the capacity of coral reefs to grow fast enough to keep up with projected rises in sea level finds that most reefs will fall behind if nothing is done to restore them.

Data for evaluating the Sr/Ca temperature proxy with in-situ temperature in the western Atlantic coral Siderastrea siderea

Massive corals are used as environmental recorders throughout the tropics and subtropics to study environmental variability during time periods preceding ocean-observing instrumentation. However, careful testing of paleoproxies is necessary to validate the environmental-proxy record throughout a range of conditions experienced by the recording organisms. As part of the USGS Coral Reef Ecosystems Studies project (http://coastal.er.usgs.gov/crest/), we tested the hypothesis that the coral Siderastrea siderea faithfully records sea-surface temperature (SST) in the Sr/Ca record throughout the subtropical (Florida, USA) seasonal cycle along 350 km of reef tract. The datasets included in this data release are comprised of data collected between 2009 and 2013. Coral samples were analyzed from thirty-nine corals growing in 3- to 4-meter water depths at Fowey Rocks (Biscayne National Park), Molasses Reef (Florida Keys National Marine Sanctuary, FKNMS), Sombrero Reef (FKNMS), and Pulaski Shoal (Dry Tortugas National Park). Temperatures were recorded with Onset® HOBO® Water Temp Pro V2 (U22-001) data loggers in duplicate at each site. Sr/Ca, Mg/Ca, calcification rate, and select underwater temperature data are provided here. The results of this experiment are interpreted in Kuffner et al. (in review). A larger temperature dataset, including the data provided here, is found in another data release Kuffner (2015), and a larger calcification-rate dataset is interpreted in Kuffner et al. (2013).

Investigación del USGS sobre el ecosistema de arrecifes de coral en el Atlántico

Los arrecifes de coral son estructuras sólidas, biomineralizadas que protegen comunidades costeras actuando como barreras protectoras de peligros tales como los huracanes y los tsunamis. Estos proveen arena a las playas a través de procesos naturales de erosión, fomentan la industria del turismo, las actividades recreacionales y proveen hábitats pesqueros esenciales. La continua degradación mundial de ecosistemas de arrecifes de coral está bien documentada (por ejemplo, fig. 1). Existe la necesidad de enfoque y organización de la ciencia para entender los procesos complejos físicos y biológicos e interacciones que están afectando el estado de los arrecifes coralinos y su capacidad para responder a un entorno cambiante.