Derek P. Manzello

Poorly cemented coral reefs of the eastern tropical Pacific: Possible insights into reef development in a high-CO2 world

Ocean acidification describes the progressive, global reduction in seawater pH that is currently underway because of the accelerating oceanic uptake of atmospheric CO2. Acidification is expected to reduce coral reef calcification and increase reef dissolution. Inorganic cementation in reefs describes the precipitation of CaCO3 that acts to bind framework components and occlude porosity. Little is known about the effects of ocean acidification on reef cementation and whether changes in cementation rates will affect reef resistance to erosion. Coral reefs of the eastern tropical Pacific (ETP) are poorly developed and subject to rapid bioerosion. Upwelling processes mix cool, subthermocline waters with elevated pCO2 (the partial pressure of CO2) and nutrients into the surface layers throughout the ETP. Concerns about ocean acidification have led to the suggestion that this region of naturally low pH waters may serve as a model of coral reef development in a high-CO2 world. We analyzed seawater chemistry and reef framework samples from multiple reef sites in the ETP and found that a low carbonate saturation state (Ω) and trace abundances of cement are characteristic of these reefs. These low cement abundances may be a factor in the high bioerosion rates previously reported for ETP reefs, although elevated nutrients in upwelled waters may also be limiting cementation and/or stimulating bioerosion. ETP reefs represent a real-world example of coral reef growth in low-Ω waters that provide insights into how the biological–geological interface of coral reef ecosystems will change in a high-CO2 world.

Bioerosion and Coral Reef Growth: A Dynamic Balance

Bioerosion, involving the weakening and breakdown of calcareous coral reef structures, is due to the chemical and mechanical activities of numerous and diverse biotic agents. These range in size from minute, primarily intra-skeletal organisms, the microborers (e.g., algae, fungi, bacteria) to larger and often externally-visible macroboring invertebrate (e.g., sponges, polychaete worms, sipunculans, molluscs, crustaceans, echinoids) and fish (e.g., parrotfishes, acanthurids, pufferfishes) species. Constructive coral reef growth and destructive bioerosive processes are often in close balance. Dead corals are generally subject to higher rates of bioerosion than living corals, therefore, bioerosion and reef degradation can result from disturbances that cause coral mortality, such as sedimentation, eutrophication, pollution, temperature extremes, predation, and coral diseases. The effects of intensive coral reef bioerosion, involving El Nino-Southern Oscillation, Acanthaster predation, watershed alterations, and over-fishing, are re-examined after ~20 years (early 1990s–2010). We review the evidence showing that the biologically-mediated dissolution of calcium carbonate structures by endolithic algae and clionaid sponges will be accelerated with ocean acidification. The CaCO3 budget dynamics of Caribbean and eastern tropical Pacific reefs is reviewed and provides sobering case studies on the current state of coral reefs and their future in a high-CO2 world.

Severe 2010 Cold-Water Event Caused Unprecedented Mortality to Corals of the Florida Reef Tract and Reversed Previous Survivorship Patterns

Background Coral reefs are facing increasing pressure from natural and anthropogenic stressors that have already caused significant worldwide declines. In January 2010, coral reefs of Florida, United States, were impacted by an extreme cold-water anomaly that exposed corals to temperatures well below their reported thresholds (16°C), causing rapid coral mortality unprecedented in spatial extent and severity. Methodology/Principal Findings Reef surveys were conducted from Martin County to the Lower Florida Keys within weeks of the anomaly. The impacts recorded were catastrophic and exceeded those of any previous disturbances in the region. Coral mortality patterns were directly correlated to in-situ and satellite-derived cold-temperature metrics. These impacts rival, in spatial extent and intensity, the impacts of the well-publicized warm-water bleaching events around the globe. The mean percent coral mortality recorded for all species and subregions was 11.5% in the 2010 winter, compared to 0.5% recorded in the previous five summers, including years like 2005 where warm-water bleaching was prevalent. Highest mean mortality (15%–39%) was documented for inshore habitats where temperatures were <11°C for prolonged periods. Increases in mortality from previous years were significant for 21 of 25 coral species, and were 1–2 orders of magnitude higher for most species. Conclusions/Significance The cold-water anomaly of January 2010 caused the worst coral mortality on record for the Florida Reef Tract, highlighting the potential catastrophic impacts that unusual but extreme climatic events can have on the persistence of coral reefs. Moreover, habitats and species most severely affected were those found in high-coral cover, inshore, shallow reef habitats previously considered the “oases” of the region, having escaped declining patterns observed for more offshore habitats. Thus, the 2010 cold-water anomaly not only caused widespread coral mortality but also reversed prior resistance and resilience patterns that will take decades to recover.

Hurricanes benefit bleached corals

Recent, global mass-mortalities of reef corals due to record warm sea temperatures have led researchers to consider global warming as one of the most significant threats to the persistence of coral reef ecosystems. The passage of a hurricane can alleviate thermal stress on coral reefs, highlighting the potential for hurricane-associated cooling to mitigate climate change impacts. We provide evidence that hurricane-induced cooling was responsible for the documented differences in the extent and recovery time of coral bleaching between the Florida Reef Tract and the U.S. Virgin Islands during the Caribbean-wide 2005 bleaching event. These results are the only known scenario where the effects of a hurricane can benefit a stressed marine community.

Ocean acidification refugia of the Florida Reef Tract.

Ocean acidification (OA) is expected to reduce the calcification rates of marine organisms, yet we have little understanding of how OA will manifest within dynamic, real-world systems. Natural CO2, alkalinity, and salinity gradients can significantly alter local carbonate chemistry, and thereby create a range of susceptibility for different ecosystems to OA. As such, there is a need to characterize this natural variability of seawater carbonate chemistry, especially within coastal ecosystems. Since 2009, carbonate chemistry data have been collected on the Florida Reef Tract (FRT). During periods of heightened productivity, there is a net uptake of total CO2 (TCO2) which increases aragonite saturation state (Ωarag) values on inshore patch reefs of the upper FRT. These waters can exhibit greater Ωarag than what has been modeled for the tropical surface ocean during preindustrial times, with mean (± std. error) Ωarag-values in spring = 4.69 (±0.101). Conversely, Ωarag-values on offshore reefs generally represent oceanic carbonate chemistries consistent with present day tropical surface ocean conditions. This gradient is opposite from what has been reported for other reef environments. We hypothesize this pattern is caused by the photosynthetic uptake of TCO2 mainly by seagrasses and, to a lesser extent, macroalgae in the inshore waters of the FRT. These inshore reef habitats are therefore potential acidification refugia that are defined not only in a spatial sense, but also in time; coinciding with seasonal productivity dynamics. Coral reefs located within or immediately downstream of seagrass beds may find refuge from OA.

Ocean acidification alters the otoliths of a pantropical fish species with implications for sensory function

Ocean acidification affects a wide diversity of marine organisms and is of particular concern for vulnerable larval stages critical to population replenishment and connectivity. Whereas it is well known that ocean acidification will negatively affect a range of calcareous taxa, the study of fishes is more limited in both depth of understanding and diversity of study species. We used new 3D microcomputed tomography to conduct in situ analysis of the impact of ocean acidification on otolith (ear stone) size and density of larval cobia (Rachycentron canadum), a large, economically important, pantropical fish species that shares many life history traits with a diversity of high-value, tropical pelagic fishes. We show that 2,100 μatm partial pressure of carbon dioxide (pCO2) significantly increased not only otolith size (up to 49% greater volume and 58% greater relative mass) but also otolith density (6% higher). Estimated relative mass in 800 μatm pCO2 treatments was 14% greater, and there was a similar but nonsignificant trend for otolith size. Using a modeling approach, we demonstrate that these changes could affect auditory sensitivity including a ∼50% increase in hearing range at 2,100 μatm pCO2, which may alter the perception of auditory information by larval cobia in a high-CO2 ocean. Our results indicate that ocean acidification has a graded effect on cobia otoliths, with the potential to substantially influence the dispersal, survival, and recruitment of a pelagic fish species. These results have important implications for population maintenance/replenishment, connectivity, and conservation efforts for other valuable fish stocks that are already being deleteriously impacted by overfishing.

The photosynthetic resilience of Porites furcata to salinity disturbance

Benthic habitats of Biscayne Bay, a shallow lagoon adjacent to the city of Miami, Florida, contain a limited number of coral species that represent a subset of the species found at nearby reefs of the Florida Reef Tract. The physical characteristics of this basin (i.e., variable salinity and temperature, high sedimentation) make it a marginal environment for coral growth (Lirman et al. 2003). Salinity fields of Biscayne Bay are influenced by freshwater inputs from canal, surface, and groundwater sources that create a nearshore environment with low mean salinity and high salinity fluctuation. For example, salinity fell to levels below 25 ppt in this area for 188 days in 1998 and 156 days in 1999 (Lirman et al. 2003). Siderastrea radians and Porites furcata are the most abundant coral species found in this near-shore environment (Lirman et al. 2003), suggesting their high tolerance to low and variable salinity. In this study, we test the hypothesis that a high physiological tolerance for salinity fluctuations enables P. furcata to occupy these marginal environments. Osmotic stress has long been recognized as a limiting physical parameter for marine organisms, as emphasized by the negative correlation observed between marine species and salinity levels in estuarine environments (Wells 1961). Changes in salinity are known to pose a significant metabolic drain on marine organisms, and disrupt normal cellular electrochemical processes, enzyme kinetics, and nerve conduction (Vernberg and Vernberg 1972). In corals, sudden changes in salinity are known to negatively impact reproduction (Richmond 1993), photosynthesis and respiration (Muthiga and Szmant 1987; Moberg et al. 1997; Nystrom et al. 1997; Porter et al. 1999), and survivorship (Marcus and Thourhaug 1981; Coles 1992; Krupp et al. 1998). Corals are considered to be stenohaline, with a limited ability to adapt to or survive salinity changes (Wells 1957; reviewed by Coles and Jokiel 1992). Mortality in corals is predicted to occur at salinities lower than 25 ppt (Edmondson 1928) or higher than 45 ppt (Jokiel et al. 1974). However, other studies suggest that corals can tolerate both low (17.5–28 ppt; Vaughn 1919; Edmondson 1928) and high salinities (38.5–52.5 ppt; Edmondson 1928; Wells 1957). In this study, we evaluate the photosynthetic response of P. furcata to sub-optimal salinity levels (20–45 ppt) in a series of exposure experiments of different duration (2 to 24 h).

Effects of light and elevated pCO2 on the growth and photochemical efficiency of Acropora cervicornis

The effects of light and elevated pCO2 on the growth and photochemical efficiency of the critically endangered staghorn coral, Acropora cervicornis, were examined experimentally. Corals were subjected to high and low treatments of CO2 and light in a fully crossed design and monitored using 3D scanning and buoyant weight methodologies. Calcification rates, linear extension, as well as colony surface area and volume of A. cervicornis were highly dependent on light intensity. At pCO2 levels projected to occur by the end of the century from ocean acidification (OA), A. cervicornis exhibited depressed calcification, but no change in linear extension. Photochemical efficiency (Fv/Fm) was higher at low light, but unaffected by CO2. Amelioration of OA-depressed calcification under high-light treatments was not observed, and we suggest that the high-light intensity necessary to reach saturation of photosynthesis and calcification in A. cervicornis may limit the effectiveness of this potentially protective mechanism in this species. High CO2 causes depressed skeletal density, but not linear extension, illustrating that the measurement of extension by itself is inadequate to detect CO2 impacts. The skeletal integrity of A. cervicornis will be impaired by OA, which may further reduce the resilience of the already diminished populations of this endangered species.

Enhanced macroboring and depressed calcification drive net dissolution at high-CO2 coral reefs

Ocean acidification (OA) impacts the physiology of diverse marine taxa; among them corals that create complex reef framework structures. Biological processes operating on coral reef frameworks remain largely unknown from naturally high-carbon-dioxide (CO2) ecosystems. For the first time, we independently quantified the response of multiple functional groups instrumental in the construction and erosion of these frameworks (accretion, macroboring, microboring, and grazing) along natural OA gradients. We deployed blocks of dead coral skeleton for roughly 2 years at two reefs in Papua New Guinea, each experiencing volcanically enriched CO2, and employed high-resolution micro-computed tomography (micro-CT) to create three-dimensional models of changing skeletal structure. OA conditions were correlated with decreased calcification and increased macroboring, primarily by annelids, representing a group of bioeroders not previously known to respond to OA. Incubation of these blocks, using the alkalinity anomaly methodology, revealed a switch from net calcification to net dissolution at a pH of roughly 7.8, within Intergovernmental Panel on Climate Changes (IPCC) predictions for global ocean waters by the end of the century. Together these data represent the first comprehensive experimental study of bioerosion and calcification from a naturally high-CO2 reef ecosystem, where the processes of accelerated erosion and depressed calcification have combined to alter the permanence of this essential framework habitat.

Species richness of motile cryptofauna across a gradient of reef framework erosion

Coral reef ecosystems contain exceptionally high concentrations of marine biodiversity, potentially encompassing millions of species. Similar to tropical rainforests and their insects, the majority of reef animal species are small and cryptic, living in the cracks and crevices of structural taxa (trees and corals). Although the cryptofauna make up the majority of a reef’s metazoan biodiversity, we know little about their basic ecology. We sampled motile cryptofaunal communities from both live corals and dead carbonate reef framework across a gradient of increasing erosion on a reef in Pacific Panamá. A total of 289 Operational Taxonomic Units (OTUs) from six phyla were identified. We used species-accumulation models fitted to individual- and sample-based rarefaction curves, as well as seven nonparametric richness estimators to estimate species richness among the different framework types. All procedures predicted the same trends in species richness across the differing framework types. Estimated species richness was higher in dead framework (261–370 OTUs) than in live coral substrates (112–219 OTUs). Surprisingly, richness increased as framework structure was eroded: coral rubble contained the greatest number of species (227–320 OTUs) and the lowest estimated richness of 47–115 OTUs was found in the zone where the reef framework had the greatest vertical relief. This contradicts the paradigm that abundant live coral indicates the apex of reef diversity.