1. Kuffner, I.B., E. Bartels, A. Stathakopoulos, I.C. Enochs, G. Kolodziej, L.T. Toth, and D.P. Manzello. Plasticity in skeletal characteristics of nursery-raised staghorn coral, Acropora cervicornis. Coral Reefs, 36(3):679-684, doi:10.1007/s00338-017-1560-2 2017

    Abstract:

    Staghorn coral, Acropora cervicornis, is a threatened species and the primary focus of western Atlantic reef restoration efforts to date. We compared linear extension, calcification rate, and skeletal density of nursery-raised A. cervicornis branches reared for 6 months either on blocks attached to substratum or hanging from PVC trees in the water column. We demonstrate that branches grown on the substratum had significantly higher skeletal density, measured using computerized tomography, and lower linear extension rates compared to water-column fragments. Calcification rates determined with buoyant weighing were not statistically different between the two grow-out methods, but did vary among coral genotypes. Whereas skeletal density and extension rates were plastic traits that depended on grow-out method, calcification rate was conserved. Our results show that the two rearing methods generate the same amount of calcium carbonate skeleton but produce colonies with different skeletal characteristics and suggest that there is genetically-based variability in coral calcification performance.

  2. Camp, E.F., D.J. Smith, C. Evenhuis, I. Enochs, D. Manzello, S. Woodcock, and D.J. Suggett. Acclimatization to high-variance habitats does not enhance physiological tolerance of two key Caribbean corals to future temperature and pH. Philosophical Transactions of the Royal Society B, 283(1831):20160442, doi:10.1098/rspb.2016.0442 2016

    Abstract:

    Corals are acclimatized to populate dynamic habitats that neighbor coral reefs. Habitats such as seagrass beds exhibit broad diel changes in temperature and pH that routinely expose corals to conditions predicted for reefs over the next 50-100 years. However, whether such acclimatization effectively enhances physiological tolerance to, and hence provides refuge against, future climate scenarios remains unknown. Also, whether corals living in low-variance habitats can tolerate present-day high-variance conditions remains untested. We experimentally examined how pH and temperature predicted for the year 2100 affects the growth and physiology of two dominant Caribbean corals (Acropora palmata and Porites astreoides) native to habitats with intrinsically low (outer-reef terrace, LV) and/or high (neighboring seagrass, HV) environmental variance. Under present-day temperature and pH, growth and metabolic rates (calcification, respiration, and photosynthesis) were unchanged for HV versus LV populations. Superimposing future climate scenarios onto the HV and LV conditions did not result in any enhanced tolerance to colonies native to HV. Calcification rates were always lower for elevated temperature and/or reduced pH. Together, these results suggest that seagrass habitats may not serve as refugia against climate change if the magnitude of future temperature and pH changes is equivalent to neighboring reef habitats.

  3. Enochs, I.C., D.P. Manzello, A. Tribollet, L. Valentino, G. Kolodziej, E.M. Donham, M.D. Fitchett, R. Carlton, and N.N. Price. Elevated colonization of microborers at a volcanically acidified coral reef. PLoS ONE, 11(7):e0159818, doi:10.1371/journal.pone.0159818 2016

    Abstract:

    Experiments have demonstrated that ocean acidification (OA) conditions projected to occur by the end of the century will slow the calcification of numerous coral species and accelerate the biological erosion of reef habitats (bioerosion). Microborers, which bore holes less than 100 μm diameter, are one of the most pervasive agents of bioerosion and are present throughout all calcium carbonate substrates within the reef environment. The response of diverse reef functional groups to OA is known from real-world ecosystems but, to date, our understanding of the relationship between ocean pH and carbonate dissolution by microborers is limited to controlled laboratory experiments. Here we examine the settlement of microborers to pure mineral calcium carbonate substrates (calcite) along a natural pH gradient at a volcanically acidified reef at Maug, Commonwealth of the Northern Mariana Islands (CNMI). Colonization of pioneer microborers was higher in the lower pH waters near the vent field. Depth of microborer penetration was highly variable both among and within sites (4.2–195.5 μm) over the short duration of the study (3 mo.), and no clear relationship to increasing CO2 was observed. Calculated rates of biogenic dissolution, however, were highest at the two sites closer to the vent and were not significantly different from each other. These data represent the first evidence of OA-enhancement of microboring flora colonization in newly available substrates and provide further evidence that microborers, especially bioeroding chlorophytes, respond positively to low pH. The accelerated breakdown and dissolution of reef framework structures with OA will likely lead to declines in structural complexity and integrity, as well as possible loss of essential habitat.

  4. Enochs, I.C., D.P. Manzello, G. Kolodziej, S.H.C. Noonan, L. Valentino, and K.E. Fabricius. Enhanced macroboring and depressed calcification drive net dissolution at high CO2 coral reefs. Proceedings of the Royal Society B, 283(1842):20161742, doi:10.1098/rspb.2016.1742 2016

    Abstract:

    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 Change's (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.

  5. Enochs, I.C., D.P. Manzello, H.H. Wirshing, R. Carlton, and J. Serafy. Micro-CT analysis of the Caribbean octocoral Eunicea flexuosa subjected to elevated pCO2. ICES Journal of Marine Science, 73(3):910-919, doi:10.1093/icesjms/fsv159 2016

    Abstract:

    Rising anthropogenic carbon dioxide has resulted in a drop in ocean pH, a phenomenon known as ocean acidification (OA). These acidified waters have many ramifications for diverse marine biota, especially those species which precipitate calcium carbonate skeletons. The permanence of coral reef ecosystems is, therefore, closely related to OA stress as habitat-forming corals will exhibit reduced calcification and growth. Relatively little is known concerning the fate of other constituent taxa which may either suffer concomitant declines or be competitively favored in acidified waters. Here, we experimentally (49 d) test the effects of next century predictions for OA (pH = 7.75, pCO2 = 1081 µatm) vs. near-present-day conditions (pH = 8.01, pCO2 = 498 µatm) on the common Caribbean octocoral Eunicea flexuosa. We measure linear extension of this octocoral and use a novel technique, high-resolution micro-computed tomography, to measure potential differences in the morphology of calcified internal skeletal structures (sclerites) in a 2 mm apical section of each branch. Despite the use of highly accurate procedures, we found no significant differences between treatments in either the growth of E. flexuosa branches or the structure of their sclerites. Our results suggest a degree of resilience to OA stress and provide evidence that this octocoral species may persist on Caribbean coral reefs, despite global change.

  6. Glynn, P.W., D.P. Manzello, and I.C. Enochs (eds.). Coral Reefs of the Eastern Tropical Pacific: Persistence and Loss in a Dynamic Environment. Springer Netherlands, 657 pp., doi:10.1007/978-94-017-7499-4 2016

    Abstract:

    This book documents and examines the state of health of coral reefs in the eastern tropical Pacific region. It touches on the occurrence of coral reefs in the waters of surrounding countries, and it explores their biogeography, biodiversity, and condition relative to the El Niño-Southern Oscillation and human impacts. Additionally contained within is a field that presents information on many of the species presented in the preceding chapters.

  7. Humphreys, A.F., J. Halfar, F. Rivera, D. Manzello, C.E. Reymond, H. Westphal, and B. Riegl. Variable El Niño-Southern Oscillation influence on biofacies dynamics of eastern Pacific shallow-water carbonate systems. Geology, 44(7):571-574, doi:10.1130/G37745.1 2016

    Abstract:

    The El Niño–Southern Oscillation (ENSO) is a periodic climatic and oceanic event caused by sea-surface temperature and nutrient anomalies over the eastern tropical Pacific Ocean (ETP). Recurring ENSO events have a significant impact on climate and the ecosystems of the circum-Pacific region. In the marine realm, ENSO is known for altering temperature and nutrient patterns, affecting the pelagic food chain, and causing widespread bleaching of corals due to temperature stress. The potential impacts of ENSO on shallow benthic ecosystems as a whole, however, are poorly understood. Here, we compared biogenic sedimentary facies of ETP shallow-water carbonate systems in a strongly ENSO-influenced area (Galápagos Islands, Ecuador [GAL]) with similar systems in an area less strongly influenced by ENSO (Gulf of California, Mexico [GOC]). Carbonate assemblages in both study regions range from coral-algal–dominated (photozoan) to molluscan-dominated (heterozoan) assemblages. Linear statistical models, comparing the distribution of carbonates against prominent local oceanographic parameters, show that minimum chlorophyll-a and maximum sea-surface temperature (which are both strongly influenced by ENSO) are dominant drivers shaping carbonate sediment facies in the GAL. In contrast, GOC carbonates have a distinct mean chlorophyll-a signature that is the result of an upwelling-induced north-south nutrient gradient not significantly influenced by ENSO.

  8. Manzello, D., C.M. Eakin, and P.W. Glynn. Effects of global warming and ocean acidification on carbonate budgets of eastern Pacific coral reefs. In Coral Reefs of the Eastern Tropical Pacific: Persistence and Loss in a Dynamic Environment, P.W. Glynn, D.P. Manzello, and I. Enochs (eds.). Springer Netherlands, 517-533, doi:10.1007/978-94-017-7499-4 2016

    Abstract:

    Eastern tropical Pacific (ETP) coral reefs provide a real-world example of reef growth, development, structure, and function under the high-pCO2, low aragonite saturation state (Ωarag) conditions expected for the entire tropical surface ocean with a doubling to tripling of atmospheric CO2. This provides a unique opportunity to examine various aspects of calcium carbonate (CaCO3) budgets in low-Ωarag conditions in the present day. Unlike anywhere else in the world, the ETP displays a continuum of thermal stress and CO2 inputs up to levels at which reef building is terminated and reef structures are lost. The response of coral reef CaCO3 budgets to El Niño warming across the ETP shows that reefs can be completely lost after experiencing a 2–3°C thermal anomaly sustained in excess of two months during the warmest time of the year at Ωarag values expected for the rest of the tropics when atmospheric CO2 doubles. ETP coral reefs have persisted and shown resilience to this level of thermal stress or acidification when acting alone, but the combination of the two corresponded with the complete elimination of reef framework structures in the southern Galápagos Islands over the decade after the 1982–83 El Niño warming event. Reef carbonate degradation is exacerbated also by diverse agents of bioerosion such as sea urchins, boring bivalves, and excavating sponges, with experimental evidence demonstrating that the latter may even increase their activities during ocean warming and pH decline. This chapter reviews the CaCO3 budget of ETP coral reefs and discusses how a high-CO2 world may impact the major biotic and abiotic factors responsible for the cycling of carbonate materials. Coral reefs of the ETP serve as a model for conditions that will occur in other regions within a few decades.

  9. Enochs, I.C., D.P. Manzello, E.M. Donham, G. Kolodziej, R. Okano, L. Johnston, C. Young, J. Iguel, C.B. Edwards, M.D. Fox, L. Valentino, S. Johnson, D. Benavente, S.J. Clark, R. Carlton, T. Burton, Y. Eynaud, and N.N. Price. Shift from coral to macroalgae dominance on a volcanically acidified reef. Nature Climate Change, 5(12):1083-1088, doi:10.1038/nclimate2758 2015

    Abstract:

    Rising anthropogenic CO2 in the atmosphere is accompanied by an increase in oceanic CO2 and a concomitant decline in seawater pH. This phenomenon, known as ocean acidification (OA), has been experimentally shown to impact the biology and ecology of numerous animals and plants, most notably those that precipitate calcium carbonate skeletons, such as reef-building corals. Volcanically acidified water at Maug, Commonwealth of the Northern Mariana Islands (CNMI) is equivalent to near-future predictions for what coral reef ecosystems will experience worldwide due to OA. We provide the first chemical and ecological assessment of this unique site and show that acidification-related stress significantly influences the abundance and diversity of coral reef taxa, leading to the often-predicted shift from a coral to an algae-dominated state. This study provides field evidence that acidification can lead to macroalgae dominance on reefs.

  10. Enochs, I.C., D.P. Manzello, R.D. Carton, D.M. Graham, R. Ruzicka, and M.A Collela. Ocean acidification enhances the bioerosion of a common coral reef sponge: Implications for the persistence of the Florida Reef Tract. Bulletin of Marine Science, 91(2):271-290, doi:10.5343/bms.2014.1045 2015

    Abstract:

    The increase in anthropogenic carbon dioxide in seawater, termed ocean acidification (OA), depresses calcification rates of coral and algae, and may contribute toward reef ecosystem degradation. To test how future OA conditions will influence biologically-mediated dissolution (bioerosion) of coral by the common Caribbean boring sponge Pione lampa (de Laubenfels, 1950), we conducted a series of carefully controlled incubations and used changes in total alkalinity (TA) to calculate calcium carbonate dissolution. We present data showing a positive relationship between seawater pCO2 and chemical bioerosion that predict a 99% increase in chemical erosion before the end of the century, more than double the expected decline in coral calcification rate. To examine how OA-enhanced erosion will influence reef ecosystem persistence, we incorporated these and other data into a carbonate budget model of 37 reefs along the Florida Reef Tract (FRT). Our model showed that all FRT reefs had a positive CaCO3 budget [mean = 8.257 (SE 0.8077) kg m−2 yr−1] in preindustrial times, whereas approximately 89% of reefs presently exhibit net erosion. Present-day reef-specific calcification would need to increase by 29.4% to compensate for projected end of the century OA-enhancement of total bioerosion. These findings show that OA may accelerate Caribbean and Atlantic coral reef degradation more rapidly than previously predicted

  11. Glynn, P.W., and D.P. Manzello. Bioerosion and coral reef growth: A dynamic balance. In Coral Reefs in the Anthropocene, C. Birkeland (ed.). Springer, Dordrecht, 67-97, doi:10.1007/978-94-017-7249-5 2015

    Abstract:

    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 invertebrates (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 Niño-Southern Oscillation, Acanthaster predation, watershed alterations, and over-fishing, are re-examined after ~20 years (early 1990s-2010). We review the evidence showing that 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.

  12. Manzello, D.P. Rapid recent warming of coral reefs in the Florida Keys. Scientific Reports, 5:16762, doi:10.1038/srep16762 2015

    Abstract:

    Coral reef decline in the Florida Keys has been well-publicized, controversial, and polarizing owing to debate over the causative agent being climate change versus overfishing. The recurrence of mass bleaching in 2014, the sixth event since 1987, prompted a reanalysis of temperature data. The summer and winter of 2014 were the warmest on record. The oldest known in-situ temperature record of any coral reef is from Hens and Chickens Reef (H&C) in the Florida Keys, which showed significant warming from 1975-2014. The average number of days ≥31.5 and 32oC per year increased 2670% and 2560%, respectively, from the mid-1990s to present relative to the previous 20 years. In every year after 1992 and 1994, maximum daily average temperatures exceeded 30.5 and 31oC, respectively. From 1975-1994, temperatures were <31oC in 61% of years, and in 44% of the years prior to 1992 temperatures were <30.5oC. The measured rate of warming predicts the start of annual bleaching between 2020 and 2034, sooner than expected from climate models and satellite-based sea temperatures. These data show that thermal stress is increasing and occurring on a near-annual basis on Florida Keys reefs due to ocean warming from climate change.

  13. Manzello, D.P., I.C. Enochs, G. Kolodziej, and R. Carlton. Coral growth patterns of Montastraea cavernosa and Porites astreoides in the Florida Keys: The importance of thermal stress and inimical waters. Journal of Experimental Marine Biology and Ecology, 471:198-207, doi:10.1016/j.jembe.2015.06.010 2015

    Abstract:

    The calcification and extension rates of two species of scleractinian coral (Montastraea cavernosa, Porites astreoides) were measured in corals experimentally transplanted to paired inshore and offshore locations in the Upper, Middle, and Lower Florida Keys from 2010 to 2011. Growth rates were compared with respect to 1) shelf location, 2) species, 3) region, and 4) temperature. Transplanted corals on inshore reefs generally calcified less than those at paired offshore sites, but these differences were only significant in a few cases. This difference in growth is likely because of two thermal stress events that occurred inshore, but not offshore, as growth records from cores of P. astreoides revealed significantly higher extension and calcification inshore from 2001–2013. The core data confirmed that the years 2010–2012 were a period of depressed growth inshore. Calcification and extension rates of the experimental corals were not statistically different between M. cavernosa and P. astreoides within a given site. The only exceptions were that calcification was higher in M. cavernosa at the Middle Keys inshore site. The Middle Florida Keys sites had the lowest rates of calcification, supporting the hypothesis that the influence of Florida Bay waters in this region contributes to poor reef development. Mean calcification rates negatively correlated with metrics of cold stress in M. cavernosa and heat stress in P. astreoides. The lack of a significant correlation between heat stress and mean calcification in M. cavernosa may help explain this species persistence on today's reefs. Maximum calcification and mean extension, however, were negatively correlated with maximum running 30-day mean temperature, showing that the growth of M. cavernosa is not completely insensitive to warm water stress. The ‘weedy’ life-history strategy of P. astreoides may compensate for the sensitivity of calcification rates to heat stress reported here, allowing this species to maintain the stable populations that have been observed throughout Florida and the wider Caribbean.

  14. Manzello, D.P., I.C. Enochs, G. Kolodziej, and R. Carlton. Recent decade of growth and calcification of Orbicella faveolata in the Florida Keys: An inshore-offshore comparison. Marine Ecology Progress Series, 521:81-89, doi:10.3354/meps11085 2015

    Abstract:

    Coral reefs along the Florida Keys portion of the Florida Reef Tract (FRT) have undergone a dramatic decline since the 1980s. Since the 1997-98 El Niño event, coral cover on offshore reefs of the FRT has been ≤ 5% and continues to decline. Mortality of the framework-constructing coral in the Orbicella (formerly Montastraea) annularis species complex has driven this recent loss in overall coral cover. One exception to this decline occurred on the inshore patch reefs of the Florida Keys, where coral cover has remained relatively high. We examined the growth and calcification of Orbicella faveolata, an ecologically important subspecies of the O. annularis complex, at both an inshore and offshore reef site representing this dichotomy of present-day coral cover. The period examined (2004-2013) encompasses the Caribbean-wide 2005 mass coral bleaching, the 2009-10 catastrophic cold-water bleaching, and a warm-water bleaching event in 2011. Extension and calcification rates were higher inshore every year from 2004-2013 except when there were thermal stress events that solely impacted inshore reefs (2009-10, 2011-12). Inshore growth rates recovered quickly from cold and warm-water stress. These higher calcification rates and their quick recovery after thermal stress are likely important factors in the persistence of high coral cover inshore.

  15. Sutton, A., D. Manzello, and B. Gintert. Coupling chemical and biological monitoring to understand the impact of ocean acidification on coral reef ecosystems. Oceanography, 28(2):28-29, doi:10.5670/oceanog.2015.28 2015

    Abstract:

    No abstract.

  16. Towle, E.K., R. Carlton, C. Langdon, and D.P. Manzello. In-situ measurement of metabolic status in three coral species from the Florida Reef Tract. Regional Studies in Marine Science, 2:145-153, doi:10.1016/j.rsma.2015.09.007 2015

    Abstract:

    The goal of this study was to gain an understanding of intra- and inter-specific variation in calcification rate, lipid content, symbiont density, and chlorophyll-a of corals in the Florida Reef Tract to improve our insight of in-situ variation and resilience capacity in coral physiology. The Florida Keys are an excellent place to assess this question regarding resilience because coral cover has declined dramatically since the late 1970s, yet has remained relatively high on some inshore patch reefs. Coral lipid content has been shown to be an accurate predictor of resilience under stress; however, much of the current lipid data in the literature comes from laboratory-based studies, and previous in-situ lipid work has been highly variable. The calcification rates of three species were monitored over a seven-month period at three sites, and lipid content was quantified at two seasonal time points at each of the three sites. Montastraea cavernosa had the highest mean calcification rate (4.7 mg cm−2 day−1) and lowest mean lipid content (1.6 mg cm−2) across sites and seasons. In contrast, Orbicella faveolata and Porites astreoides had lower mean calcification rates (2.8 mg cm−2 day−1 and 2.4 mg cm−2 day−1, respectively) and higher mean lipid contents (3.5 mg cm−2  and 2.3 mg cm−2, respectively) across sites and seasons. Given the recent Endangered Species Act (ESA) listing of O. faveolata and the relative persistence of M. cavernosa and P. astreoides on a population-scale, this study suggests that the hypothesis that coral lipids are good indicators of resilience may be species-specific or more complex and interrelated with other environmental factors than previously understood. Additionally, coral lipid storage under benign thermal conditions may differ from lipid storage before, during, and after thermal stress events.

  17. Brainard, R., C. Caldow, M. Eakin, S. Gittings, D. Gledhill, R. Hill, C. Jeffrey, J. Karazsia, R. Kosaki, C. Loper, D. Manzello, M. Miller, G. Piniak, B. Schroeder, J. Schull, B. Vargas-Angel, and I. Williams. National coral reef monitoring plan. NOAA Coral Reef Conservation Program, Silver Spring, MD, 39 pp., 2014

    Abstract: No abstract.

  18. Enochs, I.C., D.P. Manzello, R. Carlton, S. Schopmeyer, R. van Hooidonk, and D. Lirman. Effects of light and elevated pCO2 on the growth and photochemical efficiency of Acropora cervicornis. Coral Reefs, 33(2):477-485, doi:10.1007/s00338-014-1132-7 2014

    Abstract:

    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 (F v/F m) 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.

  19. Manzello, D.P., I.C. Enochs, A. Bruckner, P.G. Renaud, G. Kolodziej, D.A. Budd, R. Carlton, and P.W. Glynn. Galapagos coral reef persistence after ENSO warming across an acidification gradient. Geophysical Research Letters, 41(24):9001-9008, doi:10.1002/2014GL062501 2014

    Abstract:

    Anthropogenic CO2 is causing warming and ocean acidification. Coral reefs are being severely impacted, yet confusion lingers regarding how reefs will respond to these stressors over this century. Since the 1982–1983 El Niño–Southern Oscillation warming event, the persistence of reefs around the Galápagos Islands has differed across an acidification gradient. Reefs disappeared where pH  < 8.0 and aragonite saturation state (Ωarag)  ≤ 3 and have not recovered, whereas one reef has persisted where pH  > 8.0 and Ωarag  > 3. Where upwelling is greatest, calcification by massive Porites is higher than predicted by a published relationship with temperature despite high CO2, possibly due to elevated nutrients. However, skeletal P/Ca, a proxy for phosphate exposure, negatively correlates with density (R = −0.822, p < 0.0001). We propose that elevated nutrients have the potential to exacerbate acidification by depressing coral skeletal densities and further increasing bioerosion already accelerated by low pH.

  20. van Hooidonk, R., J.A. Maynard, D. Manzello, and S. Planes. Opposite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs. Global Change Biology, 20(1):103-112, doi:10.1111/gcb.12394 2014

    Abstract:

    Coral reefs and the services they provide are seriously threatened by ocean acidification and climate change impacts like coral bleaching. Here, we present updated global projections for these key threats to coral reefs based on ensembles of IPCC AR5 climate models using the new Representative Concentration Pathway (RCP) experiments. For all tropical reef locations, we project absolute and percentage changes in aragonite saturation state (Ωarag) for the period between 2006 and the onset of annual severe bleaching (thermal stress >8 degree heating weeks); a point at which it is difficult to believe reefs can persist as we know them. Severe annual bleaching is projected to start 10–15 years later at high-latitude reefs than for reefs in low latitudes under RCP8.5. In these 10–15 years, Ωarag keeps declining and thus any benefits for high-latitude reefs of later onset of annual bleaching may be negated by the effects of acidification. There are no long-term refugia from the effects of both acidification and bleaching. Of all reef locations, 90% are projected to experience severe bleaching annually by 2055. Furthermore, 5% declines in calcification are projected for all reef locations by 2034 under RCP8.5, assuming a 15% decline in calcification per unit of Ωarag. Drastic emissions cuts, such as those represented by RCP6.0, result in an average year for the onset of annual severe bleaching that is ~20 years later (2062 vs. 2044). However, global emissions are tracking above the current worst-case scenario devised by the scientific community, as has happened in previous generations of emission scenarios. The projections here for conditions on coral reefs are dire, but provide the most up-to-date assessment of what the changing climate and ocean acidification mean for the persistence of coral reefs.

  21. Bignami, S., I.C. Enochs, D.P. Manzello, S. Sponaugle, and R.K. Cowen. Ocean acidification alters the otoliths of a pan-tropical fish species with implications for sensory function. Proceedings of the National Academy of Sciences USA, 110(18):7366-7370, doi:10.1073/pnas.1301365110 2013

    Abstract:

    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.

  22. Manzello, D.P., I.C. Enochs, S. Musielewicz, R. Carlton, and D. Gledhill. Tropical cyclones cause CaCO3 undersaturation of coral reef seawater in a high-CO2 world. Journal of Geophysical Research, 118(C10):5312-5321, doi:10.1002/jgrc.20378 2013

    Abstract:

    Ocean acidification is the global decline in seawater pH and calcium carbonate (CaCO3) saturation state (Ω) due to the uptake of anthropogenic CO2 by the world's oceans. Acidification impairs CaCO3 shell and skeleton construction by marine organisms. Coral reefs are particularly vulnerable, as they are constructed by the CaCO3 skeletons of corals and other calcifiers. We understand relatively little about how coral reefs will respond to ocean acidification in combination with other disturbances, such as tropical cyclones. Seawater carbonate chemistry data collected from two reefs in the Florida Keys before, during, and after Tropical Storm Isaac provide the most thorough data to-date on how tropical cyclones affect the seawater CO2-system of coral reefs. Tropical Storm Isaac caused both an immediate and prolonged decline in seawater pH. Aragonite saturation state was depressed by 1.0 for a full week after the storm impact. Based on current 'business-as-usual' CO2 emissions scenarios, we show that tropical cyclones with high rainfall and runoff can cause periods of undersaturation (Ω < 1.0) for high-Mg calcite and aragonite mineral phases at acidification levels before the end of this century. Week-long periods of undersaturation occur for 18 mol% high-Mg calcite after storms by the end of the century. In a high-CO2 world, CaCO3 undersaturation of coral reef seawater will occur as a result of even modest tropical cyclones. The expected increase in the strength, frequency, and rainfall of the most severe tropical cyclones with climate change in combination with ocean acidification will negatively impact the structural persistence of coral reefs over this century.

  23. McLeod, E., K.R.N. Anthony, A. Andersson, R. Beeden, Y. Golbuu, J. Kleypas, K. Kroeker, D. Manzello, R.V. Salm, H. Schuttenberg, and J.E. Smith. Preparing to manage coral reefs for ocean acidification: Lessons from coral bleaching. Frontiers in Ecology and the Environment, 11(1):20-27, doi:10.1890/110240 2013

    Abstract: Ocean acidification is a direct consequence of increasing atmospheric carbon dioxide concentrations and is predicted to compromise the structure and function of coral reefs within this century. Research into the effects of ocean acidification on coral reefs has focused primarily on measuring and predicting changes in seawater carbon (C) chemistry and the biological and geochemical responses of reef organisms to such changes. To date, few ocean acidification studies have been designed to address conservation planning and management priorities. Here, we discuss how existing marine protected area design principles developed to address coral bleaching may be modified to address ocean acidification. We also identify five research priorities needed to incorporate ocean acidification into conservation planning and management: (1) establishing an ocean C chemistry baseline; (2) establishing ecological baselines; (3) determining species/habitat/community sensitivity to ocean acidification; (4) projecting changes in seawater carbonate chemistry; and (5) identifying potentially synergistic effects of multiple stressors.

  24. Enochs, I.C., and D.P. Manzello. Responses of cryptofaunal species richness and trophic potential to coral reef habitat degradation. Diversity, 4(1):94-104, doi:10.3390/d4010094 2012

    Abstract:

    Coral reefs are declining worldwide as a result of many anthropogenic disturbances. This trend is alarming because coral reefs are hotspots of marine biodiversity and considered the 'rainforests of the sea. As in the rainforest, much of the diversity on a coral reef is cryptic, remaining hidden among the cracks and crevices of structural taxa. Although the cryptofauna make up the majority of a reef's metazoan biodiversity, we know little about their basic ecology or how these communities respond to reef degradation. Emerging research shows that the species richness of the motile cryptofauna is higher among dead (framework) vs. live coral substrates and, surprisingly, increases within successively more eroded reef framework structures, ultimately reaching a maximum in dead coral rubble. Consequently, the paradigm that abundant live coral is the apex of reef diversity needs to be clarified. This provides guarded optimism amidst alarming reports of declines in live coral cover and the impending doom of coral reefs, as motile cryptic biodiversity should persist independent of live coral cover. Granted, the maintenance of this high species richness is contingent on the presence of reef rubble, which will eventually be lost due to physical, chemical, and biological erosion if not replenished by live coral calcification and mortality. The trophic potential of a reef, as inferred from the abundance of cryptic organisms, is highest on live coral. Among dead framework substrates, however, the density of cryptofauna reaches a peak at intermediate levels of degradation. In summary, the response of the motile cryptofauna, and thus a large fraction of the reef's biodiversity, to reef degradation is more complex and nuanced than currently thought; such that species richness may be less sensitive than overall trophic function.

  25. Enochs, I.C., and D.P. Manzello. Species richness of motile cryptofauna across a gradient of reef framework erosion. Coral Reefs, 31(3):653-661, doi:10.1007/s00338-012-0886-z 2012

    Abstract: 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 Panama. 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.

  26. Manzello, D.P., I.C. Enochs, N. Melo, D.K. Gledhill, and E.M. Johns. Ocean acidification refugia of the Florida Reef track. PLoS ONE, 7(7):e41715, 10 pp., doi:10.1371/journal.pone.0041 2012

    Abstract: 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 (T CO2) which increases aragonite saturation state (Varag) values on inshore patch reefs of the upper FRT. These waters can exhibit greater Varag than what has been modeled for the tropical surface ocean during preindustrial times, with mean (6 std. error) Varag-values in spring = 4.69 (60.101). Conversely, Varag-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.

  27. van Hooidonk, R.J., D.P. Manzello, J. Moye, M.E. Brandt, J.C. Hendee, C. McCoy, and C. Manfrino. Coral bleaching at Little Cayman, Cayman Islands, 2009. Estuarine, Coastal and Shelf Science, 106:80-84, doi:10.1016/j.ecss.2012.04.021 2012

    Abstract:

    The global rise in sea temperature through anthropogenic climate change is affecting coral reef ecosystems through a phenomenon known as coral bleaching; that is, the whitening of corals due to the loss of the symbiotic zooxanthellae which impart corals with their characteristic vivid coloration. We describe aspects of the most prevalent episode of coral bleaching ever recorded at Little Cayman, Cayman Islands, during the fall of 2009. The most susceptible corals were found to be, in order, Siderastrea siderea, Montastraea annularis, and Montastraea faveolata, while Diplora strigosa and Agaricia spp. were less so, yet still showed considerable bleaching prevalence and severity. Those found to be least susceptible were Porites porites, Porites astreoides, and Montastraea cavernosa. These observations and other reported observations of coral bleaching, together with 29 years (1982-2010) of satellite-derived sea surface temperatures, were used to optimize bleaching predictions at this location. To do this a Degree Heating Weeks (DHW) and Peirce Skill Score (PSS) analysis were employed to calculate a local bleaching threshold above which bleaching was expected to occur. A threshold of 4.2 DHW had the highest skill, with a PSS of 0.70. The method outlined here could be applied to other regions to find the optimal bleaching threshold and improve bleaching predictions.

  28. Enochs, I.C., L.T. Toth, V.W. Brandtneris, J.C. Afflerbach, and D.P. Manzello. Environmental determinants of motile cryptofauna on an eastern Pacific reef. Marine Ecology Progress Series, 438:105-118, doi:10.3354/meps09259 2011

    Abstract: Coral reef cryptofauna, which live hidden within reef framework structures, are considered to be the most diverse group of coral reef metazoans. They likely comprise more biomass than all surface fauna, providing important food sources for fishes and playing important roles as predators, herbivores, detritivores, filter feeders, and scavengers. In an era of global change, it is important to determine how these communities are structured across reef habitats as well as to understand how reef framework degradation will impact the cryptofauna and, by extension, ecosystem function. Artificial reef framework (ARF) units were constructed from coral rubble to approximate framework substrates. Forty replicates were subjected to treatments of differing porosity, flow, and coral cover in a fully-crossed ANOVA design. After two months in situ, all motile cryptofauna (>2 mm) were counted, weighed, and identified to the lowest possible level. A total of 11,309 specimens were collected, comprising more than 121 species from six separate phyla. Cryptofaunal abundances and biomass were higher in low porosity crypts and biomass was greater in slow flow environments, highlighting the importance of sheltered low porosity habitats, such as backreef rubble plains. The presence of live coral was not found to have a significant effect on the motile cryptofauna occupying the dead coral framework below it, suggesting a high degree of resilience in how framework-dwelling fauna respond to coral mortality. These data support the assertion that artificial reefs are capable of facilitating the accumulation of a diverse cryptic community, independent of live coral, provided they contain suitably porous crypts.

  29. Lirman, D., S. Schopmeyer, D. Manzello, L.J. Gramer, W.F. Precht, F. Muller-Karger, K. Banks. B. Barnes, E. Bartels, A. Bourque, J. Byrne, S. Donahue, J. Duquesnel, L. Fisher, D. Gilliam, J. Hendee, M. Johnson, K. Maxwell, E. McDevitt, J. Monty, D. Rueda, R. Ruzicka, and S. Thanner. Severe 2010 cold-water event caused unprecedented mortality to corals of the Florida Reef Tract and reversed previous survivorship patterns. PLoS ONE, 6(8):E23047, doi:10.1371/journal.pone.0023047 2011

    Abstract:

    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.

  30. Brainard, R.E., S. Bainbridge, R. Brinkman, C.M. Eakin, M. Field, J.-P. Gattuso, D. Gledhill, L. Gramer, A. Green, J. Hendee, R.K. Hoeke, S.J. Holbrook, O. Hoegh-Guldberg, M. Lammers, D. Manzello, M. McManus, R. Moffitt, M. Monaco, J.A. Morgan, D. Obura, S. Planes, R.J. Schmitt, C. Steinberg, H. Sweatman, O.J. Vetter, C. Wilkinson, and K.B. Wong. An international network of coral reef ecosystem observing systems (I-CREOS). In Proceedings, OceanObs09: Sustained Ocean Observations and Information for Society (Volume 2), Venice, Italy, September 21-25, 2009, J. Hall, D.E. Harrison, and D. Stammer (eds.). ESA Publication, WPP-306, 15 pp., doi:10.5270/OceanObs09.cwp.09 2010

    Abstract: Coral reefs are complex, biologically diverse, and highly valued ecosystems that are declining worldwide due to climate change and ocean acidification, overfishing, land-based sources of pollution, and other anthropogenic threats. To assist policymakers and resource managers at international, national, and local levels in effectively implementing ecosystem approaches to sustainable management and conservation of coral reefs and their biodiversity, it is necessary to have timely, unbiased integrated ecosystem observations about the conditions of coral reefs and the complex physical and biogeochemical processes supporting them. To provide these interdisciplinary ecosystem observations, an International network of Coral Reef Ecosystem Observing Systems (I-CREOS) is proposed that will organize and build upon existing coral reef observation systems being developed around the globe. This paper uses examples of some developing observation systems to demonstrate some of the approaches and technologies available for acquiring biological, physical, and geochemical observations using combinations of visual surveys, moored instrument arrays, spatial-hydrographic and water quality surveys, satellite remote sensing, and hydrodynamic and ecosystem modeling. This fledgling, and hopefully expanding, network of observing systems represents the early stages of an integrated ecosystem observing system for coral reefs capable of providing policymakers, resource managers, researchers, and other stakeholders with essential information products needed to assess various responses of coral reef ecosystems to natural variability and anthropogenic perturbations. While significant challenges and gaps in the I-CREOS network remain, it demonstrably fulfills the requirements of an operational, integrated, interdisciplinary, coastal component of GOOS. Continued support, further development, and open expansion of this emerging network are encouraged and needed to ensure the continually increasing value of the networks observational and predictive capacity. With common goals to maximize versatility, accessibility, and robustness, the existing infrastructure and capacity provide a foundation by which increased global cooperation and coordination could naturally lead to a globally comprehensive I-CREOS.

  31. Gledhill, D.K., T. Goedeke, K. Helmle, J. Hendee, A. Hilting, E. Jewett, B. Keller, D. Manzello, M. Miller, E. Rule, B. Sunda, and R. Wanninkhof. Southeast Atlantic and Gulf of Mexico region ocean acidification research implementation plan, pp. 77-91. In NOAA Ocean and Great Lakes Acidification Research Implementation Plan, A.J. Sutton (ed.). NOAA Special Report, 143 pp., 2010

    Abstract: No abstract.

  32. Manzello, D.P. Coral growth with thermal stress and ocean acidification: Lessons from the eastern tropical Pacific. Coral Reefs, 29(3):749-758, doi:10.1007/s00338-010-0623-4 2010

    Abstract: The rapid growth of scleractinian corals is responsible for the persistence of coral reefs through time. Coral growth rates have declined over the past 30 years in the western Pacific, Indian, and North Atlantic Oceans. The spatial scale of this decline has led researchers to suggest that a global phenomenon like ocean acidification may be responsible. A multi-species inventory of coral growth from Pacific Panama confirms that declines have occurred in some, but not all species. Linear extension declined significantly in the most important reef builder of the eastern tropical Pacific, Pocillopora damicornis, by nearly one-third from 1974 to 2006. The rate of decline in skeletal extension for P. damicornis from Pacific Panama (0.9% year-1) was nearly identical to massive Porites in the Indo-Pacific over the past 20-30 years (0.89-1.23% year-1). The branching pocilloporid corals have shown an increased tolerance to recurrent thermal stress events in Panama, but appear to be susceptible to acidification. In contrast, the massive pavonid corals have shown less tolerance to thermal stress, but may be less sensitive to acidification. These differing sensitivities will be a fundamental determinant of eastern tropical Pacific coral reef community structure with accelerating climate change that has implications for the future of reef communities worldwide.

  33. Manzello, D.P. Ocean acidification hotspots: Spatiotemporal dynamics of the seawater CO2-system from eastern Pacific coral reefs. Limnology and Oceanography, 55(1):239-248, doi:10.4319/lo.2010.55.1.0239 2010

    Abstract:

    Seawater CO2 system dynamics were assessed from eastern Pacific reef sites in Panama over five consecutive years (2003-2008) and twice in the Galapagos Islands (2003 and 2009). The seawater CO2 system was highly variable in time and space, but was explained by physical forcing from meteorological (seasonal rainfall) and oceanographic (upwelling, tides) processes interacting with diurnal reef metabolism. Galapagos coral reef communities are naturally exposed to the highest ambient partial pressure of CO2 (pCO2) and lowest aragonite saturation (Ωarag) values documented for any coral reef environment to date. During upwelling in the Galapagos, mean pCO2 and mean Ωarag at five different sites ranged from 53.1 to 73.5 Pa and 2.27 to 2.86, respectively. Values of pCO2 and Ωarag ranged from 21.0 to 48.7 Pa and 2.47 to 4.18, respectively, on the Saboga Reef in the seasonally upwelling Gulf of Panama, with the highest pCO2 and lowest Ωarag values occurring during upwelling. The Uva Reef, in the nonupwelling Gulf of Chiriqui of Pacific Panama, had mean Ωarag values that were always significantly greater than those at the Saboga Reef. Diurnal changes in the seawater CO2 system from reef metabolism on the Uva Reef were magnified at low tide and highly significant differences were measured over depths as shallow as 15 m because of the shallow thermocline that is pervasive throughout the eastern Pacific. These naturally high-CO2 reefs persist near the Ωarag distributional threshold for coral reefs and are thus expected to be the first and most affected by ocean acidification.

  34. Hendee, J.C., L.J. Gramer, D. Manzello, and M. Jankulak. Ecological forecasting for coral reef ecosystems. Proceedings, 11th International Coral Reef Symposium, Ft. Lauderdale, FL, July 7-11, 2008. International Society for Reef Studies, 534-538, 2009

    Abstract: Assessment of coral reef ecosystems implies the acquisition of precision data and observations appropriate for answering questions about the response of multiple organisms to physical and other environmental stimuli. At the National Oceanic and Atmospheric Administrations Atlantic Oceanographic and Meteorological Laboratory, we model marine organismal response to the environment in terms of a Stimulus/Response Index (S/RI). S/RI is computed using an approach called heuristic programming, from parameters bounded in subjective terms, which are defined numerically by comparing historical data with expert opinion, so as to match research and our understanding of the process in question. The modeled organismal response is called an ecological forecast, or ecoforecast, and relative possibility and intensity of the response is reflected in a rising S/RI. We have had success to date in modeling coral bleaching response to high sea temperatures plus high irradiance and other parameters. The approach requires, a) highly robust instrumentation (in situ, satellite, or other) deployed for long periods and producing high quality data in near real-time, b) a basic understanding of the process, behavior and/or physiology being modeled, and, c) a knowledge of approximate threshold levels for single or synergistically acting environmental parameters that elicit the phenomenon in question.

  35. Lirman, D., and D.P. Manzello. Patterns of resistance and resilience of the stress-tolerant coral Siderastrea radians (Pallas) to sub-optimal salinity and sediment burial. Journal of Experimental Marine Biology and Ecology, 369(1):72-77, doi:10.1016/j.jembe.2008.10.024 2009

    Abstract: The coastal lagoons of south Florida, U.S., experience fluctuating levels of sedimentation and salinity and contain only a subset of the coral species found at the adjacent reefs of the Florida Reef Tract. The dominant species within these habitats is Siderastrea radians, which can reach densities of up to 68 colonies m-2 and is commonly exposed to salinity extremes (< 10 psu to > 37 psu) and chronic sediment burial. In this study, we document the patterns of resistance and resilience of S. radians to sub-optimal salinity levels and sediment burial in a series of short-term, long-term, acute, chronic, single-stressor, and sequential-stressor experiments. S. radians displayed remarkable patterns of resistance and resilience, and mortality was documented only under prolonged (> 48 h) continuous exposure to salinity extremes (15 and 45 psu) and chronic sediment burial. A reduction in photosynthetic rates was documented for all salinity exposures and the decrease in photosynthesis was linearly related to exposure time. Negative impacts on photosynthetic rates were more severe under low salinity (15 psu) than under high salinity (45 psu). Corals exposed to intermediate, low-salinity levels (25 psu) exhibited initial declines in photosynthesis that were followed by temporary increases that may represent transient acclimatization patterns. The impacts of sediment burial were influenced by the duration of the burial period and ranged from a temporary reduction in photosynthesis to significant reductions in growth and tissue mortality. The maintenance of P/R ratios >1 and the rapid (<24 h) recovery of photosynthetic rates after burial periods of 2-24 h indicates that S. radians is able to resist short-term burial periods with minor physiological consequences. However, as burial periods increase and colonies become covered at multiple chronic intervals, sediment burial resulted in extended photosynthetic recovery periods, reduced growth, and mortality. Under normal conditions (i.e., no salinity stress), S. radians was very effective at clearing sediments, and >50% of the colonies surface area was cleared within 1 h. However, clearing rates were influenced by physiological status, and prior exposure to sub-optimal salinity significantly reduced the clearing rates of stressed colonies. The response of S. radians to disturbance documented in this study characterizes this species as highly stress-tolerant and provides an explanation for its present high abundance in both reef and marginal environments. Moreover, the key life-history attributes of S. radians, such as brooding reproductive strategy, small colony size, high stress-tolerance, and high recruitment rates, suggest the potential for this species to replace reef-building taxa under increased disturbance scenarios in Florida and elsewhere in the region.

  36. Manzello, D.P. Reef development and resilience to acute (El Niño warming) and chronic (high-CO2) disturbances in the eastern tropical Pacific: A real-world climate change model. Proceedings, 11th International Coral Reef Symposium, Ft. Lauderdale, FL, July 7-11, 2008. International Society for Reef Studies, 1299-1304, 2009

    Abstract:

    It has been recently recognized that eastern tropical Pacific (ETP) coral reefs exist under naturally occurring high-CO2, low carbonate saturation (OMEGA) conditions that encompass the range of expected changes for the entire tropical surface ocean with a doubling and tripling of atmospheric CO2. Holocene reef development positively and linearly tracks OMEGA in the ETP; illustrating the real-world importance of this variable on reef building. Galapagos reef communities have been subject to the most extreme thermal anomalies associated with the El Niño-Southern Oscillation (ENSO) and also experience the lowest OMEGA levels in the ETP. Reef resilience has been so poor in Galapagos that reef structures were completely bioeroded in 2 waters throughout the ETP. These combined acute (ENSO) and chronic (high-CO2) disturbances may help explain why coral reefs are scant and many genera of corals went extinct in the ETP during the late Cenozoic; thus providing a real-world example of the combined thermal and chemical ramifications of climate change on coral reef structure, function, and resilience to disturbance over geologic time.

  37. Manzello, D.P. M. Warner, E. Stabenau, J. Hendee, M. Lesser, and M. Jankulak. Remote monitoring of chlorophyll fluorescence in two reef corals during the 2005 bleaching event at Lee Stocking Island, Bahamas. Coral Reefs, 28(1):209-214, doi:10.1007/s00338-008-0455-7 2009

    Abstract: Zooxanthellae fluorescence was measured in situ, remotely, and in near real-time with a pulse amplitude modulated (PAM) fluorometer for a colony of Siderastrea siderea and Agaricia tenuifolia at Lee Stocking Island, Bahamas during the Caribbean-wide 2005 bleaching event. These colonies displayed evidence of photosystem II (PS II) inactivation coincident with thermal stress and seasonally high doses of solar radiation. Hurricane-associated declines in temperature and light appear to have facilitated the recovery of maximum quantum yield of PS II within these two colonies, although both corals responded differently to individual storms. PAM fluorometry, coupled with long-term measurement of in situ light and temperature, provides much more detail of coral photobiology on a seasonal time scale and during possible bleaching conditions than sporadic, subjective, and qualitative observations. S. siderea displayed evidence of PS II inactivation over a month prior to the issuing of a satellite-based, sea surface temperature (SST) bleaching alert by the National Oceanic and Atmospheric Administration (NOAA). In fact, recovery had already begun in S. siderea when the bleaching alert was issued. Fluorescence data for A. tenuifolia were difficult to interpret because the shaded parts of a colony were monitored and thus did not perfectly coincide with thermal stress and seasonally high doses of solar radiation as in S. siderea. These results further emphasize the limitations of solely monitoring SST (satellite or in situ) as a bleaching indicator without considering the physiological status of coral-zooxanthellae symbioses.

  38. Manzello, D.P., and J.A. Kleypas. Reef development in a high-CO2 world: Coral reefs of the eastern tropical Pacific. Global Change Newsletter, 73:24, 2009

    Abstract: No abstract.

  39. Hendee, J.C., L. Gramer, D.P. Manzello, and M. Jankulak. Integrating near real-time data for coral reef ecological forecasting. Proceedings of the Gulf and Caribbean Fisheries Institute, 59:525-528, 2008

    Abstract: The National Oceanic and Atmospheric Administration (NOAA) has committed to integrating ocean data from a variety of sources into an Integrated Ocean Observing System, and to work towards operational ecological forecasting as part of its Ecosystem Approach to Management. Consistent with this, NOAA's Coral Reef Conservation Program has committed to integrating coral data from a variety of sources for the specific benefit of coral reef researchers and Marine Protected Area (MPA) managers; and NOAA's Atlantic Oceanographic and Meteorological Laboratory, together with its NOAA and University of Miami partners, are contributing to this goal through their Integrated Coral Observing Network (ICON) project. ICON provides Web-based software to integrate satellite, monitoring station (in situ), and radar data sources in near real-time; and utilizes an inference engine (artificial intelligence software) to provide ecological forecasts using some or all of these data. The capabilities of ICON software are currently being focused upon one area in particular, Molasses Reef in the Florida Keys National Marine Sanctuary, to provide proof-of-concept, and to provide a "discovery prototype" for consideration by the MPA managers assembled at the GCFI conference. Feedback to ICON developers from MPA managers--based upon their own specific management requirements and priorities, and knowledge of the prototype capabilities--is essential to set priorities and enable additional ICON software engineering specifically tailored to MPA managers' needs. Featured in the prototype are several levels of user access: layperson, researcher, site maintainer, MPA manager, and software developer colleague. Depending upon user access, information products can include recent and historical single-source and integrated data output, custom graphics output, and ecological forecasts for coral bleaching, coral spawning, upwelling, pollution impacts and larval drift.

  40. Hendee, J.C., L. Gramer, J.A. Kleypas, D.P. Manzello, M. Jankulak, and C. Langdon. The Integrated Coral Observing Network (ICON): Sensor solutions for sensitive sites. Proceedings, Third International Conference on Intelligent Sensors, Sensor Networks, and Information Processing, Melbourne, Australia, December 3-6, 2007. Institute of Electrical and Electronics Engineers (IEEE), 669-673, doi:10.1109/ISSNIP.2007.4496923 2008

    Abstract:

    The National Oceanic and Atmospheric Administration's (NOAA) Integrated Coral Observing Network (ICON) has been operational since 2000 and works closely with most U.S. Government and many international environmental partners involved in coral reef research. The ICON program has pioneered the use of artificial intelligence techniques to assess near real-time data streams from environment sensor networks such as the SEAKEYS Network (Florida Keys), the Australia Institute of Marine Science Weather Network, NOAA's Coral Reef Ecosystem Division network in the Pacific, and its own Integrated Coral Observing Network (ICON) of stations in the Caribbean. Besides its innovative approach to coral monitoring station deployments, the ICON program recently pioneered techniques for the near real-time integration of satellite, in situ, and radar data sources for purposes of ecological forecasting of such events as coral bleaching, coral spawning, upwelling, and other marine behavioral or physical oceanographic events. The ICON program has also ushered in the use of Pulse-Amplitude-Modulating fluorometry to measure near real-time physiological recording of response to environmental stress during coral bleaching, thus providing even better ecological forecasting capabilities through artificial intelligence and data integrative techniques. Herewith, we describe these techniques, along with a report on new coral calcification instrumentation augmenting the ICON Network sensor array.

  41. Manzello, D.P. Short and long-term ramifications of climate change upon coral reef ecosystems: Case studies across two oceans. Ph.D. thesis, University of Miami, Rosenstiel School of Marine and Atmospheric Science, 82 pp. , 2008

    Abstract:

    World-wide coral reefs are in a state of decline as a result of many local and regional factors. 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 over the next 100 years. It is well established that elevated sea temperatures cause widespread coral bleaching, yet confusion lingers as to what facet of extreme temperatures is most important. Utilizing long-term in situ datasets, nine thermal stress indices were calculated and their effectiveness at segregating bleaching years a posteriori for multiple reefs on the Florida Reef Tract was tested. Simple bleaching thresholds based on deviations above the climatological maximum monthly sea temperature were just as effective at identifying bleaching years as complex thermal stress indices. Near real-time bleaching alerts issued by NOAA's Integrated Coral Observing Network (ICON) are now based upon a running 30-day average SST, such that alerts are only issued when the running 30-day average SST exceeds the estimated bleaching threshold for a particular site. In addition to three widespread, mass-coral bleaching events, the Florida Reef Tract was impacted by three tropical storms and 12 hurricanes from 1997-2005. Sea surface cooling associated with the high frequency of hurricanes that impacted Florida in 2005 likely acted to ameliorate the severity and duration of bleaching. Nonetheless, hurricane-associated cooling is not expected to nullify the proposed effects of climate change on coral reefs. The role of thermal stress in coral bleaching has been extensively studied for eastern tropical Pacific (ETP) coral reefs. However, the ETP presents a unique opportunity as this region has sub-optimal conditions for coral reef development because of upwelling of carbon dioxide-enriched water along the shallow thermocline. This upwelling results in a depressed aragonite saturation state, which is likely an additional factor in the poor reef development throughout the ETP. The highest aragonite saturation states documented in this study occur in the Gulf of Chiriquí, which corresponds with the greatest reef development of the entire ETP. Seasonal upwelling had a significant effect on the carbonate chemistry of surface waters in Pacific Panama. This regionally-depressed aragonite saturation of the ETP appears to result in corals with a less dense skeleton. Density values of poritid corals from the Galapagos, where aragonite saturation was the lowest documented in this study, were significantly less dense relative to those from Panama and the Great Barrier Reef. The density of non-living pocilloporid framework components were no different across the ETP carbonate saturation gradients. This could be a result of the activity of boring sponges removing the primary carbonate material within the dead coral skeleton, thus lowering density, albeit physical-chemical dissolution cannot be ruled out. These studies provide real-world examples of the ramifications of global climate change upon coral reef ecosystems.

  42. Manzello, D.P., J.A. Kleypas, D.A. Budd, C.M. Eakin, P.W. Glynn, and C. Langdon. Poorly cemented coral reefs of the eastern tropical Pacific: Possible insights into reef development in a high-CO2 world. Proceedings of the National Academy of Sciences, 105(30):10,450-10,455, doi:10.1073/pnas.0712167105 2008

    Abstract: 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 (Omega) 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-Omega waters that provide insights into how the biological-geological interface of coral reef ecosystems will change in a high-CO2 world.

  43. Manzello, D.P., M. Brandt, T.B. Smith, D. Lirman, J.C. Hendee, and R.S. Nemeth. Hurricanes benefit bleached corals. Proceedings of the National Academy of Sciences, 104(29):12,035-12,039, doi:10.1073/pnas.0701194104 2007

    Abstract:

    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.

  44. Manzello, D.P., R. Berkelmans, and J.C. Hendee. Coral bleaching indices and thresholds for the Florida Reef Tract, Bahamas, and St. Croix, U.S. Virgin Islands. Marine Pollution Bulletin, 54(12):1923-1931, doi:10.1016/j.marpolbul.2007.08.009 2007

    Abstract: It is well established that elevated sea temperatures cause widespread coral bleaching, yet confusion lingers as to what facet of extreme temperatures is most important. Utilizing long-term in situ datasets, we calculated nine thermal stress indices and tested their effectiveness at segregating bleaching years a posteriori for multiple reefs on the Florida Reef Tract. The indices examined represent three aspects of thermal stress: (1) short-term, acute temperature stress; (2) cumulative temperature stress; and (3) temperature variability. Maximum monthly sea surface temperature (SST) and the number of days >30.5°C were the most significant; indicating that cumulative exposure to temperature extremes characterized bleaching years. Bleaching thresholds were warmer for Florida than the Bahamas and St. Croix, U.S. Virgin Islands reflecting differences in seasonal maximum SST. Hindcasts showed that monthly mean SST above a local threshold explained all bleaching years in Florida, the Bahamas, and U.S. Virgin Islands.

  45. Hendee, J.C., E.R. Stabenau, L. Florit, D. Manzello, and C. Jeffris. Infrastructure and capabilities of a near real-time meteorological and oceanographic in situ instrumented array and its role in marine environmental decision support. In Remote Sensing of Aquatic Coastal Ecosystem Processes, L.L. Richardson and E.F. LeDrew (eds.). Springer Verlag, 9:135-156, 2006

    Abstract:

    No abstract.

  46. Manzello, D., J.C. Hendee, D. Ward, and Z. Hillis-Starr. An evaluation of environmental parameters coincident with the partial bleaching event in St. Croix, U.S. Virgin Islands (2003). Proceedings, 10th International Coral Reef Symposium, Okinawa, Japan, June 28-July 2, 2004. International Society for Coral Reef Studies, 709-717, 2006

    Abstract:

    A partial bleaching event was reported in September and October 2003 in St. Croix, yet no bleaching alert was produced by the expert system software dubbed the Coral Reef Early Warning System (CREWS). This presents an opportunity for refining the modeling and predictive success of the CREWS software specifically for the St. Croix site by examination of the pertinent environmental parameters (sea temperature, wind speeds, irradiance) associated with the 2003 bleaching event. Elevated sea temperatures were likely the primary catalyst of bleaching and were coincident with dampened wind speeds. The least attenuation (greatest penetration) of UVB occurred during October when bleaching was most severe, but was variable. A nearly parallel trend with wind speed and UVB penetration was found and supports the hypothesis that the attenuation of UVB into the water column is controlled by CDOM concentrations, which are elevated due to wind-driven mixing.

  47. Manzello, D. A decade of SEAKEYS data: SST trends and patterns, pp. 35-36. In The Effects of Combined Sea Temperature, Light, and Carbon Dioxide on Coral Bleaching, Settlement, and Growth, J.C. Hendee (ed.). NOAA Research Special Report, Silver Spring, MD, 126 pp., 2004

    Abstract:

    No abstract.

  48. Lirman, D., B. Orlando, S. Macia, D. Manzello, L. Kaufman, P. Biber, and T. Jones. Coral communities of Biscayne Bay, Florida and adjacent offshore areas: Diversity, abundance, distribution, and environmental correlates. Aquatic Conservation: Marine and Freshwater Ecosystems, 13(2):121-135, doi:10.1002/aqc.552 2003

    Abstract:

    Hardbottom habitats of Biscayne Bay, a shallow lagoon adjacent to the city of Miami, Florida, contain a limited number of coral species that represent a small subset of the species found at nearby offshore hardbottom and reef habitats of the Florida Reef Tract. Although the physical characteristics of this basin make it a marginal environment for coral growth, the presence of dense populations of Siderastrea radians and Porites furcata indicate that these, as well as other corals that are found at lower densities, are able to tolerate extreme and fluctuating conditions. Three factors, temperature, sedimentation, and salinity, appear to limit coral abundance, diversity, and distribution within Biscayne Bay. Temperatures exhibit high frequencies of extreme high and low values known to cause coral stress and mortality elsewhere. Similarly, sedimentation rates are very high and sediment resuspension caused by currents, storms, and boating activities commonly bury corals under sediment layers. Sediment burial was shown experimentally to influence growth and mortality of S. radians. The salinity of Biscayne Bay is influenced by freshwater inputs from canal, sheetflow, and groundwater sources that create a near-shore environment with low mean salinity and high salinity fluctuation. Coral communities along this western margin have the lowest coral density and species richness. Chronic exposure to low salinity was shown experimentally to cause a decrease in the growth of S. radians. The location of Biscayne Bay, downstream of a large restoration effort planned for the Everglades watershed, highlights the need to understand the relationship between the physical environment and the health of benthic communities. The data presented here provide the type of scientific information needed so that management decisions can take into account the potential impacts of human activities on the health of coral populations that are already near their tolerance limits for temperature, salinity, and sedimentation.

  49. Manzello, D., and D. Lirman. The photosynthetic resilience of Porites furcata to salinity disturbance. Coral Reefs, 22(4):537-540, doi:10.1007/s00338-003-0327-0 2003

    Abstract:

    No abstract.

  50. Lirman, D., D. Manzello, and S. Macia. Back from the dead: The resilence of Siderastrea radians to severe stress. Coral Reefs, 21(3):291-292, doi:10.1007/s00338-002-0244-7 2002

    Abstract:

    No abstract.