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2018
Cyronak, T, Andersson AJ, Langdon C, Albright R, Bates NR, Caldeira K, Carlton R, Corredor JE, Dunbar RB, Enochs I, Erez J, Eyre BD, Gattuso JP, Gledhill D, Kayanne H, Kline DI, Koweek DA, Lantz C, Lazar B, Manzello D, McMahon A, Melendez M, Page HN, Santos IR, Schulz KG, Shaw E, Silverman J, Suzuki A, Teneva L, Watanabe A, Yamamoto S.  2018.  Taking the metabolic pulse of the world's coral reefs. Plos One. 13   10.1371/journal.pone.0190872   AbstractWebsite

Worldwide, coral reef ecosystems are experiencing increasing pressure from a variety of anthropogenic perturbations including ocean warming and acidification, increased sedimentation, eutrophication, and overfishing, which could shift reefs to a condition of net calcium carbonate (CaCO3) dissolution and erosion. Herein, we determine the net calcification potential and the relative balance of net organic carbon metabolism (net community production; NCP) and net inorganic carbon metabolism (net community calcification; NCC) within 23 coral reef locations across the globe. In light of these results, we consider the suitability of using these two metrics developed from total alkalinity (TA) and dissolved inorganic carbon (DIC) measurements collected on different spatiotemporal scales to monitor coral reef biogeochemistry under anthropogenic change. All reefs in this study were net calcifying for the majority of observations as inferred from alkalinity depletion relative to offshore, although occasional observations of net dissolution occurred at most locations. However, reefs with lower net calcification potential (i.e., lower TA depletion) could shift towards net dissolution sooner than reefs with a higher potential. The percent influence of organic carbon fluxes on total changes in dissolved inorganic carbon (DIC) (i.e., NCP compared to the sum of NCP and NCC) ranged from 32% to 88% and reflected inherent biogeochemical differences between reefs. Reefs with the largest relative percentage of NCP experienced the largest variability in seawater pH for a given change in DIC, which is directly related to the reefs ability to elevate or suppress local pH relative to the open ocean. This work highlights the value of measuring coral reef carbonate chemistry when evaluating their susceptibility to ongoing global environmental change and offers a baseline from which to guide future conservation efforts aimed at preserving these valuable ecosystems.

2017
Neal, BP, Khen A, Treibitz T, Beijbom O, O'Connor G, Coffroth MA, Knowlton N, Kriegman D, Mitchell BG, Kline DI.  2017.  Caribbean massive corals not recovering from repeated thermal stress events during 2005-2013. Ecology and Evolution. 7:1339-1353.   10.1002/ece3.2706   AbstractWebsite

Massive coral bleaching events associated with high sea surface temperatures are forecast to become more frequent and severe in the future due to climate change. Monitoring colony recovery from bleaching disturbances over multiyear time frames is important for improving predictions of future coral community changes. However, there are currently few multiyear studies describing long-term outcomes for coral colonies following acute bleaching events. We recorded colony pigmentation and size for bleached and unbleached groups of co-located conspecifics of three major reef-building scleractinian corals (Orbicella franksi, Siderastrea siderea, and Stephanocoenia michelini; n=198 total) in Bocas del Toro, Panama, during the major 2005 bleaching event and then monitored pigmentation status and changes live tissue colony size for 8years (2005-2013). Corals that were bleached in 2005 demonstrated markedly different response trajectories compared to unbleached colony groups, with extensive live tissue loss for bleached corals of all species following bleaching, with mean live tissue losses per colony 9 months postbleaching of 26.2% (+/- 5.4 SE) for O. franksi, 35.7% (+/- 4.7 SE) for S. michelini, and 11.2% (+/- 3.9 SE) for S. siderea. Two species, O. franksi and S. michelini, later recovered to net positive growth, which continued until a second thermal stress event in 2010. Following this event, all species again lost tissue, with previously unbleached colony species groups experiencing greater declines than conspecific sample groups, which were previously bleached, indicating a possible positive acclimative response. However, despite this beneficial effect for previously bleached corals, all groups experienced substantial net tissue loss between 2005 and 2013, indicating that many important Caribbean reef-building corals will likely suffer continued tissue loss and may be unable to maintain current benthic coverage when faced with future thermal stress forecast for the region, even with potential benefits from bleaching-related acclimation.

2015
Beijbom, O, Edmunds PJ, Roelfsema C, Smith J, Kline DI, Neal BP, Dunlap MJ, Moriarty V, Fan TY, Tan CJ, Chan S, Treibitz T, Gamst A, Mitchell BG, Kriegman D.  2015.  Towards automated annotation of benthic survey images: Variability of human experts and operational modes of automation. Plos One. 10   10.1371/journal.pone.0130312   AbstractWebsite

Global climate change and other anthropogenic stressors have heightened the need to rapidly characterize ecological changes in marine benthic communities across large scales. Digital photography enables rapid collection of survey images to meet this need, but the subsequent image annotation is typically a time consuming, manual task. We investigated the feasibility of using automated point-annotation to expedite cover estimation of the 17 dominant benthic categories from survey-images captured at four Pacific coral reefs. Inter- and intra- annotator variability among six human experts was quantified and compared to semi- and fully- automated annotation methods, which are made available at coralnet.ucsd. edu. Our results indicate high expert agreement for identification of coral genera, but lower agreement for algal functional groups, in particular between turf algae and crustose coralline algae. This indicates the need for unequivocal definitions of algal groups, careful training of multiple annotators, and enhanced imaging technology. Semi-automated annotation, where 50% of the annotation decisions were performed automatically, yielded cover estimate errors comparable to those of the human experts. Furthermore, fully-automated annotation yielded rapid, unbiased cover estimates but with increased variance. These results show that automated annotation can increase spatial coverage and decrease time and financial outlay for image-based reef surveys.

2014
Gonzalez-Rivero, M, Bongaerts P, Beijbom O, Pizarro O, Friedman A, Rodriguez-Ramirez A, Upcroft B, Laffoley D, Kline D, Bailhache C, Vevers R, Hoegh-Guldberg O.  2014.  The Catlin Seaview Survey - kilometre-scale seascape assessment, and monitoring of coral reef ecosystems. Aquatic Conservation-Marine and Freshwater Ecosystems. 24:184-198.   10.1002/aqc.2505   AbstractWebsite

Marine ecosystems provide critically important goods and services to society, and hence their accelerated degradation underpins an urgent need to take rapid, ambitious and informed decisions regarding their conservation and management.The capacity, however, to generate the detailed field data required to inform conservation planning at appropriate scales is limited by time and resource consuming methods for collecting and analysing field data at the large scales required.The Catlin Seaview Survey', described here, introduces a novel framework for large-scale monitoring of coral reefs using high-definition underwater imagery collected using customized underwater vehicles in combination with computer vision and machine learning. This enables quantitative and geo-referenced outputs of coral reef features such as habitat types, benthic composition, and structural complexity (rugosity) to be generated across multiple kilometre-scale transects with a spatial resolution ranging from 2 to 6m(2).The novel application of technology described here has enormous potential to contribute to our understanding of coral reefs and associated impacts by underpinning management decisions with kilometre-scale measurements of reef health.Imagery datasets from an initial survey of 500km of seascape are freely available through an online tool called the Catlin Global Reef Record. Outputs from the image analysis using the technologies described here will be updated on the online repository as work progresses on each dataset.Case studies illustrate the utility of outputs as well as their potential to link to information from remote sensing. The potential implications of the innovative technologies on marine resource management and conservation are also discussed, along with the accuracy and efficiency of the methodologies deployed.10.1002/(ISSN)1099-0755 Copyright (c) 2014 John Wiley & Sons, Ltd.

Neal, BP, Condit C, Liu G, dos Santos S, Kahru M, Mitchell BG, Kline DI.  2014.  When depth is no refuge: cumulative thermal stress increases with depth in Bocas del Toro, Panama. Coral Reefs. 33:193-205.   10.1007/s00338-013-1081-6   AbstractWebsite

Coral reefs are increasingly affected by high-temperature stress events and associated bleaching. Monitoring and predicting these events have largely utilized sea surface temperature data, due to the convenience of using large-scale remotely sensed satellite measurements. However, coral bleaching has been observed to vary in severity throughout the water column, and variations in coral thermal stress across depths have not yet been well investigated. In this study, in situ water temperature data from 1999 to 2011 from three depths were used to calculate thermal stress on a coral reef in Bahia Almirante, Bocas del Toro, Panama, which was compared to satellite surface temperature data and thermal stress calculations for the same area and time period from the National Oceanic and Atmospheric Administration Coral Reef Watch Satellite Bleaching Alert system. The results show similar total cumulative annual thermal stress for both the surface and depth-stratified data, but with a striking difference in the distribution of that stress among the depth strata during different high-temperature events, with the greatest thermal stress unusually recorded at the deepest measured depth during the most severe bleaching event in 2005. Temperature records indicate that a strong density-driven temperature inversion may have formed in this location in that year, contributing to the persistence and intensity of bleaching disturbance at depth. These results indicate that depth may not provide a stress refuge from high water temperature events in some situations, and in this case, the water properties at depth appear to have contributed to greater coral bleaching at depth compared to near-surface locations. This case study demonstrates the importance of incorporating depth-stratified temperature monitoring and small-scale oceanographic and hydrologic data for understanding and predicting local reef responses to elevated water temperature events.

2013
Connell, SD, Kroeker KJ, Fabricius KE, Kline DI, Russell BD.  2013.  The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance. Philosophical Transactions of the Royal Society B-Biological Sciences. 368   10.1098/rstb.2012.0442   AbstractWebsite

Predictions concerning the consequences of the oceanic uptake of increasing atmospheric carbon dioxide (CO2) have been primarily occupied with the effects of ocean acidification on calcifying organisms, particularly those critical to the formation of habitats (e. g. coral reefs) or their maintenance (e. g. grazing echinoderms). This focus overlooks direct and indirect effects of CO2 on non-calcareous taxa that play critical roles in ecosystem shifts (e. g. competitors). We present the model that future atmospheric [CO2] may act as a resource for mat-forming algae, a diverse and widespread group known to reduce the resilience of kelp forests and coral reefs. We test this hypothesis by combining laboratory and field CO2 experiments and data from 'natural' volcanic CO2 vents. We show that mats have enhanced productivity in experiments and more expansive covers in situ under projected near-future CO2 conditions both in temperate and tropical conditions. The benefits of CO2 are likely to vary among species of producers, potentially leading to shifts in species dominance in a high CO2 world. We explore how ocean acidification combines with other environmental changes across a number of scales, and raise awareness of CO2 as a resource whose change in availability could have wide-ranging community consequences beyond its direct effects.

2012
Diaz-Pulido, G, Anthony KRN, Kline DI, Dove S, Hoegh-Guldberg O.  2012.  Interactions between ocean acidification and warming on the mortality and dissolution of coralline algae. Journal of Phycology. 48:32-39.   10.1111/j.1529-8817.2011.01084.x   AbstractWebsite

Coralline algae are among the most sensitive calcifying organisms to ocean acidification as a result of increased atmospheric carbon dioxide (pCO2). Little is known, however, about the combined impacts of increased pCO2, ocean acidification, and sea surface temperature on tissue mortality and skeletal dissolution of coralline algae. To address this issue, we conducted factorial manipulative experiments of elevated CO2 and temperature and examined the consequences on tissue survival and skeletal dissolution of the crustose coralline alga (CCA) Porolithon (=Hydrolithon) onkodes (Heydr.) Foslie (Corallinaceae, Rhodophyta) on the southern Great Barrier Reef (GBR), Australia. We observed that warming amplified the negative effects of high pCO2 on the health of the algae: rates of advanced partial mortality of CCA increased from <1% to 9% under high CO2 (from 400 to 1,100 ppm) and exacerbated to 15% under warming conditions (from 26 degrees C to 29 degrees C). Furthermore, the effect of pCO2 on skeletal dissolution strongly depended on temperature. Dissolution of P. onkodes only occurred in the high-pCO2 treatment and was greater in the warm treatment. Enhanced skeletal dissolution was also associated with a significant increase in the abundance of endolithic algae. Our results demonstrate that P. onkodes is particularly sensitive to ocean acidification under warm conditions, suggesting that previous experiments focused on ocean acidification alone have underestimated the impact of future conditions on coralline algae. Given the central role that coralline algae play within coral reefs, these conclusions have serious ramifications for the integrity of coral-reef ecosystems.

Kaniewska, P, Campbell PR, Kline DI, Rodriguez-Lanetty M, Miller DJ, Dove S, Hoegh-Guldberg O.  2012.  Major cellular and physiological impacts of ocean acidification on a reef building coral. Plos One. 7   10.1371/journal.pone.0034659   AbstractWebsite

As atmospheric levels of CO2 increase, reef-building corals are under greater stress from both increased sea surface temperatures and declining sea water pH. To date, most studies have focused on either coral bleaching due to warming oceans or declining calcification due to decreasing oceanic carbonate ion concentrations. Here, through the use of physiology measurements and cDNA microarrays, we show that changes in pH and ocean chemistry consistent with two scenarios put forward by the Intergovernmental Panel on Climate Change (IPCC) drive major changes in gene expression, respiration, photosynthesis and symbiosis of the coral, Acropora millepora, before affects on biomineralisation are apparent at the phenotype level. Under high CO2 conditions corals at the phenotype level lost over half their Symbiodinium populations, and had a decrease in both photosynthesis and respiration. Changes in gene expression were consistent with metabolic suppression, an increase in oxidative stress, apoptosis and symbiont loss. Other expression patterns demonstrate upregulation of membrane transporters, as well as the regulation of genes involved in membrane cytoskeletal interactions and cytoskeletal remodeling. These widespread changes in gene expression emphasize the need to expand future studies of ocean acidification to include a wider spectrum of cellular processes, many of which may occur before impacts on calcification.

2010
Eakin, CM, Morgan JA, Heron SF, Smith TB, Liu G, Alvarez-Filip L, Baca B, Bartels E, Bastidas C, Bouchon C, Brandt M, Bruckner AW, Bunkley-Williams L, Cameron A, Causey BD, Chiappone M, Christensen TRL, Crabbe MJC, Day O, de la Guardia E, Diaz-Pulido G, DiResta D, Gil-Agudelo DL, Gilliam DS, Ginsburg RN, Gore S, Guzman HM, Hendee JC, Hernandez-Delgado EA, Husain E, Jeffrey CFG, Jones RJ, Jordan-Dahlgren E, Kaufman LS, Kline DI, Kramer PA, Lang JC, Lirman D, Mallela J, Manfrino C, Marechal JP, Marks K, Mihaly J, Miller WJ, Mueller EM, Muller EM, Toro CAO, Oxenford HA, Ponce-Taylor D, Quinn N, Ritchie KB, Rodriguez S, Ramirez AR, Romano S, Samhouri JF, Sanchez JA, Schmahl GP, Shank BV, Skirving WJ, Steiner SCC, Villamizar E, Walsh SM, Walter C, Weil E, Williams EH, Roberson KW, Yusuf Y.  2010.  Caribbean Corals in Crisis: Record Thermal Stress, Bleaching, and Mortality in 2005. Plos One. 5   10.1371/journal.pone.0013969   AbstractWebsite

Background: The rising temperature of the world's oceans has become a major threat to coral reefs globally as the severity and frequency of mass coral bleaching and mortality events increase. In 2005, high ocean temperatures in the tropical Atlantic and Caribbean resulted in the most severe bleaching event ever recorded in the basin. Methodology/Principal Findings: Satellite-based tools provided warnings for coral reef managers and scientists, guiding both the timing and location of researchers' field observations as anomalously warm conditions developed and spread across the greater Caribbean region from June to October 2005. Field surveys of bleaching and mortality exceeded prior efforts in detail and extent, and provided a new standard for documenting the effects of bleaching and for testing nowcast and forecast products. Collaborators from 22 countries undertook the most comprehensive documentation of basin-scale bleaching to date and found that over 80% of corals bleached and over 40% died at many sites. The most severe bleaching coincided with waters nearest a western Atlantic warm pool that was centered off the northern end of the Lesser Antilles. Conclusions/Significance: Thermal stress during the 2005 event exceeded any observed from the Caribbean in the prior 20 years, and regionally-averaged temperatures were the warmest in over 150 years. Comparison of satellite data against field surveys demonstrated a significant predictive relationship between accumulated heat stress (measured using NOAA Coral Reef Watch's Degree Heating Weeks) and bleaching intensity. This severe, widespread bleaching and mortality will undoubtedly have long-term consequences for reef ecosystems and suggests a troubled future for tropical marine ecosystems under a warming climate.

Mass, T, Kline DI, Roopin M, Veal CJ, Cohen S, Iluz D, Levy O.  2010.  The spectral quality of light is a key driver of photosynthesis and photoadaptation in Stylophora pistillata colonies from different depths in the Red Sea. Journal of Experimental Biology. 213:4084-4091.   10.1242/jeb.039891   AbstractWebsite

Depth zonation on coral reefs is largely driven by the amount of downwelling, photosynthetically active radiation (PAR) that is absorbed by the symbiotic algae (zooxanthellae) of corals. The minimum light requirements of zooxanthellae are related to both the total intensity of downwelling PAR and the spectral quality of the light. Here we used Stylophora pistillata colonies collected from shallow (3 m) and deep (40 m) water; colonies were placed in a respirometer under both ambient PAR irradiance and a filter that only transmits blue light. We found that the colonies exhibited a clear difference in their photosynthetic rates when illuminated under PAR and filtered blue light, with higher photosynthetic performance when deep colonies were exposed to blue light compared with full-spectrum PAR for the same light intensity and duration. By contrast, colonies from shallow water showed the opposite trend, with higher photosynthetic performances under full-spectrum PAR than under filtered blue light. These findings are supported by the absorption spectra of corals, with deeper colonies absorbing higher energy wavelengths than the shallow colonies, with different spectral signatures. Our results indicate that S. pistillata colonies are chromatically adapted to their surrounding light environment, with photoacclimation probably occurring via an increase in photosynthetic pigments rather than algal density. The spectral properties of the downwelling light are clearly a crucial component of photoacclimation that should be considered in future transplantation and photoacclimation studies.