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. 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.

  3. 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.

  4. 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.

  5. 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.

  6. 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.

  7. 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.