1. Enochs, I.C., D.P. Manzello, P.J. Jones, C. Aguilar, K. Cohen, L. Valentino, S. Schopmeyer, G. Kolodziej, M. Jankulak, and D. Lirman. The influence of diel carbonate chemistry fluctuations on the calcification rate of Acropora cervicornis under present day and future acidification conditions. Journal of Experimental Marine Biology and Ecology, 506:15-143, doi:10.1016/j.jembe.2018.06.007 2018

    Abstract:

    Ocean acidification (OA) will result in lower calcification rates for numerous marine taxa, including many species of corals which create important reef habitat. Seawater carbonate chemistry fluctuates over cycles ranging from days to seasons, often driven by biological processes such as respiration and photosynthesis. The magnitude of diel fluctuations varies spatially and may become more pronounced in the future due to OA. Due to technical constraints, OA experiments that incorporate diel variability into treatments are few in number. As a result, the degree to which coral reef organisms are influenced by ambient daily carbonate chemistry variability is poorly understood. Here we describe an experiment conducted in a novel seawater system which can independently manipulate carbonate chemistry in 16 separate aquaria, in real time, allowing precise control of the mean and magnitude of pH oscillations while minimizing pseudoreplication. Five genotypes of the threatened Caribbean coral Acropora cervicornis were subjected to a total of five pH treatments, 7.80 ± 0.20, 7.80 ± 0.10, and 7.80 ± 0.00, as well as 8.05 ± 0.10 and 8.05 ± 0.00. Those corals exposed to variable contemporary conditions (8.05 ± 0.10) calcified faster than those in current and future static treatment levels, which did not significantly differ from each other. Variable contemporary pH also resulted in faster growth rates than highly variable future conditions (7.80 ± 0.20), but were not significantly different than future conditions with the same ±0.10 diel pH oscillation. These findings support the importance of incorporating diel variability into OA experiments and suggest that more variable natural ecosystems may yield higher calcification rates for corals.

  2. Gintert, B.E., D.P. Manzello, I.C. Enochs, G. Kolodziej, R. Carlton, A.C.R. Gleason, and N. Gracias. Marked annual coral bleaching resilience of an inshore patch reef in the Florida Keys: A nugget of hope, aberrance, or last man standing? Coral Reefs, 37(2):533-547, doi:10.1007/s00338-018-1678-x 2018

    Abstract:

    Annual coral bleaching events, which are predicted to occur as early as the next decade in the Florida Keys, are expected to cause catastrophic coral mortality. Despite this, there is little field data on how Caribbean coral communities respond to annual thermal stress events. At Cheeca Rocks, an inshore patch reef near Islamorada, Florida, the condition of 4234 coral colonies was followed over 2 years of subsequent bleaching in 2014 and 2015, the two hottest summers on record for the Florida Keys. In 2014, this site experienced 7.7 degree heating weeks (DHW) and, as a result, 38.0% of corals bleached and an additional 36.6% were pale or partially bleached. In situ temperatures in summer of 2015 were even warmer, with the site experiencing 9.5 DHW. Despite the increased thermal stress in 2015, only 12.1% of corals were bleached in 2015, which was 3.1 times less than 2014. Partial mortality dropped from 17.6% of surveyed corals to 4.3% between 2014 and 2015, and total colony mortality declined from 3.4 to 1.9% between years. Total colony mortality was low over both years of coral bleaching with 94.7% of colonies surviving from 2014 to 2016. The reduction in bleaching severity and coral mortality associated with a second stronger thermal anomaly provides evidence that the response of Caribbean coral communities to annual bleaching is not strictly temperature dose dependent and that acclimatization responses may be possible even with short recovery periods. Whether the results from Cheeca Rocks represent an aberration or a true resilience potential is the subject of ongoing research.

  3. Manzello, D.P., I.C. Enochs, G. Kolodziej, R. Carlton, and L. Valentino. Resilience in carbonate production despite three coral bleaching events in 5 years on an inshore patch reef in the Florida Keys. Marine Biology, 165(6):99, doi:10.1007/s00227-018-3354-7 2018

    Abstract:

    The persistence of coral reef frameworks requires that calcium carbonate (CaCO3) production by corals and other calcifiers outpaces CaCO3 loss via physical, chemical, and biological erosion. Coral bleaching causes declines in CaCO3 production, but this varies with bleaching severity and the species impacted. We conducted census-based CaCO3 budget surveys using the established ReefBudget approach at Cheeca Rocks, an inshore patch reef in the Florida Keys, annually from 2012 to 2016. This site experienced warm-water bleaching in 2011, 2014, and 2015. In 2017, we obtained cores of the dominant calcifying coral at this site, Orbicella faveolata, to understand how calcification rates were impacted by bleaching and how they affected the reef-wide CaCO3 budget. Bleaching depressed O. faveolata growth and the decline of this one species led to an overestimation of mean (± std. error) reef-wide CaCO3 production by + 0.68 (± 0.167) to + 1.11 (± 0.236) kg m−2 year−1 when using the static ReefBudget coral growth inputs. During non-bleaching years, the ReefBudget inputs slightly underestimated gross production by − 0.10 (± 0.022) to − 0.43 (± 0.100) kg m−2 year−1. Carbonate production declined after the first year of back-to-back bleaching in 2014, but then increased after 2015 to values greater than the initial surveys in 2012. Cheeca Rocks is an outlier in the Caribbean and Florida Keys in terms of coral cover, carbonate production, and abundance of O. faveolata, which is threatened under the Endangered Species Act. Given the resilience of this site to repeated bleaching events, it may deserve special management attention.

  4. Perry, C.T., L. Alvarez-Filip, N.A.J. Graham, P.J. Mumby, S.K. Wilson, P.S. Kench, D.P. Manzello, K.M. Morgan, A.B.A. Slangen, D.P. Thompson, F. Januchowski-Hartley, S.G. Smithers, R.S. Steneck, R. Carlton, E.N. Edinger, I.C. Enochs, N. Estrada-Saldivar, M.D.E. Haywood, G. Kolodziej, G.N. Murphy, E. Perez-Cervantes, A. Suchley, L. Valentino, R. Boenish, M. Wilson, and C. Macdonald. Loss of coral reef growth capacity to track future increases in sea level. Nature, 558(7710):396-400, doi:10.1038/s41586-018-0194-z 2018

    Abstract:

    Sea-level rise (SLR) is predicted to elevate water depths above coral reefs and to increase coastal wave exposure as ecological degradation limits vertical reef growth, but projections lack data on interactions between local rates of reef growth and sea level rise. Here we calculate the vertical growth potential of more than 200 tropical western Atlantic and Indian Ocean reefs, and compare these against recent and projected rates of SLR under different Representative Concentration Pathway (RCP) scenarios. Although many reefs retain accretion rates close to recent SLR trends, few will have the capacity to track SLR projections under RCP4.5 scenarios without sustained ecological recovery, and under RCP8.5 scenarios most reefs are predicted to experience mean water depth increases of more than 0.5 m by 2100. Coral cover strongly predicts reef capacity to track SLR, but threshold cover levels that will be necessary to prevent submergence are well above those observed on most reefs. Urgent action is thus needed to mitigate climate, sea-level and future ecological changes in order to limit the magnitude of future reef submergence.

  5. 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.

  6. 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.

  7. 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.

  8. 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.

  9. 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.

  10. 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.

  11. 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.